|
| |
 |
|
| REVIEW ARTICLE |
|
| Year : 2018 | Volume
: 11
| Issue : 9 | Page : 501-509 |
|
Role of dietary phytochemicals in modulation of miRNA expression: Natural swords combating breast cancer
Banzeer Ahsan Abbasi1, Javed Iqbal1, Tariq Mahmood1, Ali Talha Khalil2, Barkat Ali1, Sobia Kanwal3, Sayed Afzal Shah1, Riaz Ahmad4
1 Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan
2 Nanosciences African Network (NANOAFNET), iThemba LABS-National Research Foundation Somerset West, Western Cape 7129, South Africa; Department of Zoology, University of Gujrat, Sub Campus Rawalpindi 46000; Department of Eastern Medicine and Surgery, Qarshi University, Lahore 56000, Pakistan
3 UNESCO UNISA Africa Chair in Nanoscience and Nanotechnology, College of Graduate Studies, University of South Africa, Pretoria 0002, South Africa
4 College of Life Sciences, Shaanxi Normal University, Xi’an 710119, China
| Date of Submission | 21-Jan-2018 |
| Date of Decision | 28-Mar-2018 |
| Date of Acceptance | 16-Apr-2018 |
| Date of Web Publication | 27-Sep-2018 |
Correspondence Address:
Javed Iqbal
Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320
Pakistan
Tariq Mahmood
Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320
Pakistan
 Source of Support: None, Conflict of Interest: None  | 39 |
DOI: 10.4103/1995-7645.242314
The National Cancer Institute had projected breast cancer (BC) as one of the topmost prevalent malignancies around the globe. In many cases, BC becomes resistant to chemotherapy, radiation and hormonal therapies. Traditional BC therapies are associated with adverse side effects, drug resistance and recurrence. Extensive research work has shown that these dietary phytochemicals (DPs) may exert therapeutic effects by regulating the miRNA expression. A large number of DPs have been researched as miRNA regulatory agents against BC and some other DPs have not yet been tested against BC. We have discussed the effects of curcumin, diallyl disulphide, 3,3′ diindolylmethane, ellagic acid, genistein, indole-3-carbinol, quercetin, resveratrol, and sulforaphane on regulation of expression of BC miRNAs in a wide range of in vitro and in vivo models. We have also shown some of the possible DPs (Oleanolic acid, capsaicin, benzyl isothiocyanate, epigallocatechin gallate, phenethyl isothiocyanate and ursolic acid) that have shown miRNA regulatory activities and have not yet been tested against BC miRNAs. Finally, current limitations, challenges, future perspectives of DPs and BC research are also critically discussed. Keywords: Breast cancer, miRNAs, Dietary phytochemicals, In vitro, In vivo
How to cite this article:
Abbasi BA, Iqbal J, Mahmood T, Khalil AT, Ali B, Kanwal S, Shah SA, Ahmad R. Role of dietary phytochemicals in modulation of miRNA expression: Natural swords combating breast cancer. Asian Pac J Trop Med 2018;11:501-9 |
How to cite this URL:
Abbasi BA, Iqbal J, Mahmood T, Khalil AT, Ali B, Kanwal S, Shah SA, Ahmad R. Role of dietary phytochemicals in modulation of miRNA expression: Natural swords combating breast cancer. Asian Pac J Trop Med [serial online] 2018 [cited 2023 Jun 7];11:501-9. Available from: https://www.apjtm.org/text.asp?2018/11/9/501/242314 |
| 1. Introduction | |  |
Breast cancer (BC) is a serious global health concern in both developed and developing countries. It is one of the major causes of cancer associated death among women across the world accounting for 25% of all new cancer cases and 15% of all new cancer deaths[1],[2]. BC is not only restricted to women, it also affects men[3], transgender individuals and people from all racial and ethnic backgrounds[4]. At present, large number of treatment methods are available for BC including surgical treatment, adjuvant chemotherapy, radiotherapy, hormonal therapy, targeted therapies together with immunotherapy, monoclonal antibody therapy and surgery [lumpectomy (breast-conserving surgical treatment) or mastectomy (surgical removal of breast tissues)][5]. But, the development of drug resistance and their side effects has weakened the potentials of these treatment strategies on cancer cells[6]. As a result, development of novel and potent drugs with no/less side effects is crucial to control the incidence of BC.
Recently, dietary phytochemicals (DPs) have appeared as chemo-preventive and chemotherapeutic agents for BC because they have no/less side effects and low toxicity compared to synthetic drugs. Additionally, they are inexpensive and readily available. Growing evidences indicates that these phytochemicals could be used as a chemo-preventive and chemo-therapeutic agent in wide range of cancer including BC[7],[8]. Emerging evidences suggested that miRNAs have played important role in the initiation, promotion and progression of various types of cancers including BC. They control the expression level of different genes and proteins related to cell growth, metastasis, proliferation and apoptosis[9],[10]. Due to their significant roles in cancer initiation and proliferation, targeting miRNAs has been considered as an effective treatment option for cancer. Recent evidences indicate that DPs may inhibit BC progression through the modulation of miRNA expression[11],[12].
A large number of DPs such as sulforaphane, ellagic acid (EA), genistein, curcumin, indole-3-carbinol (I3C), resveratrol (RV), diallyl disulphide (DADS), 3,3’-diindolylmethane (DIM), and quercetin have been tested as potent agents for regulating miRNAs against BC and a large number of DPs are still under clinical trials for their potential role against miRNAs regulation in BC. This review article focuses on some potential DPs which has shown promising results while targeting miRNAs in BC.
| 2. miRNAs involved in BC regulation | | |
miRNAs are playing a vital role in regulating BC, and it is clear from large number of evidences that disturbance in the regulation of these miRNAs are mainly involved in the initiation promotion and progression of BC. An extensive research work has been carried out to identify large number of these dysregulated miRNAs in BC. These dysregulated miRNAs play a significant role in the regulation of a wide range of different molecular processes such as invasion, proliferation, metastasis, caspase mediated cell death, self-renewal, and epithelial to mesenchymal transition. miRNAs can perform dual functions as oncogenes (biological accelerators) and tumor suppressor genes (biological breaks). Onco-miRNAs expression is up-regulated [Figure 1]; whereas, tumor-suppressor miRNAs expression [Figure 2] is downregulated in BC. Some important miRNAs along with their molecular mechanism of actions are given in [Table 1] and [Table 2]. | Table 1: Different kinds of onco-miRNAs along with their molecular mechanism of actions involved in initiation, promotion and progression of breast cancer.
Click here to view |
 | Table 2: Different kinds of tumor suppressor miRNAs along with their molecular mechanism of actions involved in suppression of breast cancer.
Click here to view |
 | Figure 1: Effect of some dietary phytochemicals against breast cancer while up-regulating expression of large number of miRNAs in order to inhibit breast cancer.
Blue arrow indicates that the mentioned dietary phytochemicals up-regulate the expression of different miRNAs involved in breast cancer control.
Click here to view |
 | Figure 2: Effect of some dietary phytochemicals against breast cancer while down-regulating expression of large number of miRNAs in order to cope up with breast cancer.
Red arrow indicates that the mentioned dietary phytochemicals down-regulate the expression of different miRNAs involved in breast cancer control.
Click here to view |
| 3. Dietary phytochemicals as potential miRNA regulatory agents | | |
DPs are found in large number of dietary supplements such as vegetables, fruits, grains, beans, and other plants. Some DPs have been tested against BC miRNAs [Table 3]. Here we discussed the effects of some DPs on BC miRNAs expression. They are chemically diverse and can regulate the miRNA expression through different strategies [Figure 3]. | Table 3: In vitro and in vivo effects of dietary phytochemicals against breast cancer while up-regulating and down-regulating the expression of different miRNAs.
Click here to view |
 | Figure 3: Effects of dietary phytochemicals on miRNA processing and expression.
These dietary phytochemicals are involved in regulating the expression of different miRNAs genes: some are up-regulated while others are down-regulated.
Click here to view |
3.1.I3C
I3C are strong phytochemicals widely distributed in the cruciferous vegetables such as kohlrabi, cauliflower (Brassica oleracea var. botrytis), broccoli (Brassica oleracea var. italica), horseradish (Armoracia rusticana), cabbage (Brassica oleracea var. capitata), collard greens (Brassica oleracea var. acephala), mustard (Brassica spp.), brussels sprouts (Brassica oleracea var. gemmifera), kale (Brassica oleracea var. acephala), rutabaga (Brassica napobrassica), turnips (Brassica rapa var. rapa), bok choy (Brassica rapa var. chinensis), wasabi (Wasabia japonica), Chinese cabbage (Brassica rapa var. chinensis), arugula (Eruca sativa), radish (Raphanus sativus) and watercress (Nasturtium officinale)[58],[59],[60].
I3C has been shown to modulate miRNA expression in BC cells. I3C up-regulate miR-34a expression level in MCF-7 BC cells as a result of miR-34a expression, and I3C treatment increases the expression of p21, p53, and p53ser15 genes, eventually inducing apoptosis and inhibiting cell growth[48]. Hence, I3C may inhibit BC progression by modulating miRNA expression. These I3C may need further research and investigations to unfold their biological potentials.
3.2. EA
EA is an anti-BC flavonoid polyphenol present in grapes (Vitis vinifera), cloudberry (Rubus chamaemorus), wolfberry (Lycium barbarum), pomegranates (Punica granatum), strawberries (Fragaria spp.), raspberries (Rubus spp.), blackberries (Rubus spp.), pecans (Carya spp.) and walnuts (Juglans spp.)[61].
Female ACI rats were treated with estrogen to induce mammary tumorigenesis and the efficacy of EA on the miRNAs expression was observed. EA treatment up-regulated the synthesis of miR-182, miR-375, miR-183, miR-34c, miR-196c, and miR-429, and down- regulated the expression of miR122, miR-127, miR-335, miR-205, and miR-206 in tumors cells. EA also reduced the expression of their targets ERa (miR-206), cyclin D1 (miR-206), cyclin G1 (miR- 182, -122), Bcl-w (miR-122), Bcl-2 (miR-122), and increased the expression of their targets RASD1 (miR-182), FoxO3a (miR-182), FoxO1 (miR-182, -183), and thereby caused the inhibition of tumor growth[52]. This finding indicates that EA has the capability of inhibiting BC progression by regulating miRNA expression; thereby, this phytochemical can be a potent anti-BC agent and needs further studies.
3.3. Pomegranate polyphenols
Pomegranate (Punica granatum L.) has been consumed for different medicinal purposes and is defined as “nature’s power fruit”. Pomegranate extract has been shown to inhibit cell survival and inflammation by modulating the expression of miRNA in BT- 474 and MDA-MB-231 BC cells. It decreased miR-155 expression, contributing to inhibition of pAkt, pPI3K, and Akt expression, and eventually caused the induction of phosphatidylinositol- 3, 4, 5-trisphosphate 5-phosphatase 1 (SHIP-1) expression in BT- 474 and MDA-MB-231 cells. Moreover, it was also noticed that pomegranate extract down-regulated miR-27a expression, resulting in transcriptional repressor ZBTB10 upregulation, and subsequently caused the downregulation of Sp (specificity protein)-1, -3, -4, VEGF, VEGF receptor-1, survivin, and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-jB) p65 expression in cancer cells. Thus, pomegranate extract inhibited cell survival and inflammation[51]. Furthermore, pomegranate extract also regulated miRNA expression in BT-474 xenografts in vivo study. Pomegranate extract reduced miR-155 expression, induced SHIP-1 expression, and inhibited pAkt and pPI3K expression. Moreover, it decreased miR-27a expression, increased ZBTB10 expression, and decreased Sp1, Sp3, Sp4 expression as well as VEGF, survivin, and NFκB p65 expression[51]. Therefore, the potential impact of pomegranate extract against BC miRNAs may be warranted for future exploration.
3.4. Sulforaphane
Sulforaphane, an isothiocyanate, is found in higher concentration in cauliflower (Brassica oleracea var. botrytis), Chinese cabbage (Brassica rapa var. chinensis), brussels sprouts (Brassica oleracea var. gemmifera), arugula (Eruca sativa), radish (Raphanus sativus), broccoli (Brassica oleracea var. italica), kohlrabi (Brassica oleracea Gongylodes Group), turnips (Brassica rapa var. rapa), bok choy (Brassica rapa var. chinensis), horseradish (Armoracia rusticana), mustard (Brassica spp.), rutabaga (Brassica napobrassica), collard greens (Brassica oleracea var. acephala) and watercress (Nasturtium officinale)[61]. Sulforaphane has been researched to regulate miRNA expression in BC cells. Sulforaphane treatment was found to increase the expression level of exosomal miR-140 and decrease the expression of exosomal miR-29a and miR-21 in CD49f+/ CD24 and ALDH1+MCF10DCIS stem-like cells. Moreover, sulforaphane decreased cancer stem cell marker ALDH1 expression and mammosphere formation in these cells. These results indicated that sulforaphane may inhibit cancer stem-like cells by regulating the expression level of miRNA[50]. Furthermore, researchers found that sulforaphane treatment up-regulated miR-140 expression in MCF10DCIS cells in vitro. Moreover, sulforaphane treatment also increased the expression of miR-140 and decreased ALDH1 and SOX9 expression in CD44+/CD24 and ALDH1+ MCF10DCIS cells in vivo. These results suggested that sulforaphane targets SOX9 and ALDH1 by regulating the expression of miR-140 and eventually suppress BC stem-like cells[50]. These findings would gain further attention for the investigations of sulforaphane as a chemo-prevention and chemo-therapeutic agent for BC.
3.5. DADS
DADS is an organosulphur compound present in garlic[7],[62]. It has been researched that DADS has shown to modulate miRNA expression in BC cells. Investigators reported that DADS treatment up-regulated the expression level of miR-34a in MDA-MB-231 cells. By up-regulating miR-34a expression, DADS treatment down-regulated sarcoma (SRC, a proto-oncogene) protein levels, and caused the suppression of Ras-GTP, leading to inhibition of extracellular signal-regulated kinase1/2 (ERK1/2) phosphorylation. These effects indicate that DADS inhibits BC cell proliferation and invasion via miR-34a mediated SRC/Ras/ERK inhibition[57]. DADS plus miR-34a treatment reduced tumor volume (as compare to control) in rats implanted with MDA-MB-231 BC cells, indicating miR-34a increases antitumor effect of DADS[57]. Hence, DADS could be a promising anticancer phytochemical against BC by targeting miRNAs and needs further research work in future.
3.6. DIM
DIM is widely distributed in cruciferous vegetables including brussels sprouts (Brassica oleracea var. gemmifera), cauliflower (Brassica oleracea var. botrytis), kale, broccoli (Brassica oleracea var. italica), kohlrabi (Brassica oleracea Gongylodes Group), watercress (Nasturtium officinale), cabbage (Brassica rapa var. chinensis), arugula (Eruca sativa), daikon (Raphanus sativus), bok choy (Brassica rapa var. chinensis), turnips (Brassica rapa var. rapa), collard greens (Brassica oleracea var. acephala), mustard greens (Brassica juncea) and radishes (Raphanus sativus)[63],[58].
DIM has been shown to regulate miRNA expression. It has been researched that DIM increased the expression level of miR-212/132 cluster and down-regulated the expression of SOX4 in T47D and MDA-MB-231 BC cells in vitro and in vivo in an aryl hydrocarbon receptor-dependent fashion. This study indicates that DIM inhibits BC metastasis via miR-212/132 mediated SOX4 downregulation[11]. Study also reported that treatment of BC SKBR-3 and MDA-MB-468 cells with DIM up-regulated miR-200a and miR-200b expression and down-regulated oncogenic forkhead box M1 (FoxMl) and pAkt expression. This in turn resulted in the arrest of cell growth[53]. These results indicated that DIM can be a potent BC miRNA regulatory agent and need further research studies.
3.7. Curcumin
Curcumin is a natural polyphenolic compound with potent anti-BC potential. And high concentration of curcumin was found in the rhizomes of turmeric[64]. It has been proven from different scientific evidences that curcumin can regulate BC miRNAs expression. Curcumin has been shown to alter bisphenolA-induced upregulation of miR-19a and miR-19b and dysregulation of tumor suppressor-PTEN, phospho serine/threonine-specific protein kinase (p-Akt), p-MDM2, p53, and proliferating cell nuclear antigen (PCNA) in BC MCF-7 cells, which lead to suppression of cell proliferation[54]. It has also been researched that curcumin inhibit metastasis in BC MDA-MB-231 cells. This effect was related with down-regulation of pro-inflammatory c-x-c motif chemokine ligand (CXCL)-1 and -2 cytokines expression through up-regulation of miR-181b expression[65]. Curcumin alone or in combination with emodin up-regulated miR-34a expression in MDA-MB-231 and MDA-MB-435 BC cells via downregulating the expression of anti-apoptotic gene B-cell lymphoma 2 (Bcl-2) and oncogene BMI-1, which finally suppressed cell proliferation and invasion in the surrounding cells[55]. Curcumin also increased the expression of miR-15a and miR-16, translated into a decrease expression of Bcl-2 and finally induced caspase mediated cell death in MCF-7 cells[66]. These scientific studies have shown that curcumin has the potential to inhibit BC progression via modulating miRNA expression; therefore, curcumin can be a potential anti-BC agent and needs further research.
3.8. Genistein
Genistein is an isoflavone widely distributed in lupine (Lupinus sp.), kudzu (Pueraria sp.), fava beans (Vicia faba), soybeans (Glycine max) and psoralea (Psoralea corylifolia)[67]. It has also been researched and proven that genistein regulated miRNA expression in BC cells. Genistein down-regulated miR-155 expression and altered miR-155 targets Foxo3, PTEN, and casein kinase 1a (CK1a), b-catenin and p27 expression in MDA MB-435 and Hs578t cells. As a consequence, genistein inhibited cancer cell survival and proliferation, and induced caspase mediated cell death[56]. This study indicates that genistein can be useful for targeting BC miRNAs. Further investigations are needed.
3.9. Quercetin
Quercetin is a flavonoid found in onions (Allium spp.), apples (Malus spp.), red wine, tea (Camellia sinensis), lemon (Citrus spp.), tomato (Solanum lycopersicum), honey, broccoli (Brassica oleracea var. italica), kale, and beans[68],[69]. Quercetin exhibited effect on BC cell growth by regulating miRNA expression. Quercetin increased the expression level of pro-apoptotic-Bax (Bcl-2 associated X), caspase-3, and decreased oncogenic-EGFR expression in MCF-7 and MDA-MB-231 cells via increasing the expression level of miR-146a expression. Quercetin induced apoptosis through Bax and caspase-3 activation by up-regulating miR-146a expression and inhibited invasion through EGFR downregulation[70]. Quercetin also up-regulated the expression of miR-146a in xenografted cells and reduced tumor volume in mice[70]. Based on this study, quercetin could be a promising anti-BC agent and needs further investigations.
3.10. RV
RV is a polyphenol found in grapes (Vitis vinifera), berries, tomato (Solanum lycopersicum), peanuts (Arachis spp.), and red wine[61]. RV down-regulated the expression of different miRNAs such as, miR- 125b-5p, miR-214-3p, miR-512-5p and miR-542-3p in MCF-7 BC cells and induces apoptosis. Moreover, it also down-regulated the expression of miRNAs as for example miR-32-5p, miR-134, miR- 200c-3p and miR-542-3p in MDA-MB-231 BC cells resulting in BC arrest. Furthermore, RV also increased the expression of apoptosis-related miR-409-3p and miR-122-5p in MCF-7 and MDA-MB-231BC cell lines respectively[12]. Moreover, RV down-regulated the expression of 18 miRNAs including miR-125b-1-3p and miR-93-5p in MCF-7 cells as well as 9 miRNAs such as miR-20a-5p and 125b-1-3p in MDA-MB-231 cells. In both cell lines, RV decreased Bcl-2, X-linked inhibitor of apoptosis protein (XIAP), cyclin-dependent kinase (CDK)-2, 4 and 6 protein expression and up-regulated caspase-8 and 9 protein expression. These results indicated RV induces apoptosis in BC cells via regulating miRNA expression[12]. According to a research study performed by Qin et al., RV also increased the expression of miR-21, miR-129, miR-204, and miR- 489 and down-regulated the expression of DNA methyltransferase 3b (DNMT3b) in in vivo rat tumors[71]. Additionally, RV increased the expression of miR-663 and miR-744 by down-regulating eukaryotic translation elongation factor 1A2 (eEEF1A2) expression in MCF-7 cells resulting in the inhibition of invasion and cell proliferation[72]. Study revealed that RV treatment increases tumor suppressive miR-16, miR-141, miR-143 and miR-200c expression in MDAMB- 231-luc-D3H2LN, MCF-7, and MCF-7-ADR cells. In addition, miR-26a, miR-34a, miR-125a-3p, miR-126, miR-128, miR-185, miR-193b, miR-195, miR-196a, miR-335, miR-340, and miR-497 expression and argonaute2 (Ago2) expression were also up-regulated in RV treated MDA-MB-231-luc-D3H2LN cells. This study indicates that RV increases Ago2 activity by upregulating tumor suppressive miRNAs, leading to suppression of tumor growth[73]. RV also suppressed tumor formation in mice injected with MB-231-luc-D3H2LN cells[73]. Clearly, RV has the potential to inhibit BC progression by regulating miRNA expression. All these studies suggested that RV needs further research to develop more anti-BC treatment agents.
| 4. Current challenges and emerging alternatives | | |
Although DPs have been recognized as BC miRNA regulatory weapons, in this literature review much more attention is given to cope up with the following limitations.
(1) Low bioavailability and poor potency of DPs are some of the limitations associated with their in vivo use. However, these problems can be resolved by developing semi-synthetic analogs of them. For example, synthetic curcumin analog 5-bis (4-hydroxy-3-methoxybenzyli dene)-N-methyl-4-piperidone has shown higher bioavailability than curcumin in mice[74] and RV analog 4,4’-dihydroxy-trans-stilbene inhibited BC cell proliferation and invasion with higher efficiency than RV[75].
The development of nanoparticle encapsulated phytochemical formulations is another solution for these bioavailability and potency limitations[2]. For example, nano-encapsulated curcumin and quercetin have shown higher bioavailability than free compounds in rats and nano-encapsulated quercetin has improved in vivo anti-BC effects compared to the free forms[61].
Another study found that nanoparticles encapsulated with both quercetin and doxorubicin significantly suppressed doxorubicin-resistant MCF-7 cells in vivo[76]. Combinations of two or more DPs may also be beneficial for bioavailability and greater potency. For example, combination of genistein and capsaicin exhibited higher anti-inflammatory and anticarcinogenic effects in MCF-7 and tissuetype plasminogen activator-induced rat mammary tumor cells than either agent alone[77].
(2) Regulation of different signaling pathways by DPs may result in some undesirable changes. For instance, the antiangiogenic characteristic of RV is not only associated with pathological angiogenesis but it also disturbs the physiological angiogenesis inside the cells[78].
(3) It is largely unknown whether advantageous effects of DPs will be seen in humans since many DP potentials have been examined only in pre-clinical trials. Based on the above evidences, it is crystal clear that a much better understanding of the efficacy of DPs in BC prevention is needed. Future research work should emphasis on: (a) Perfect characterization of these DPs, (b) Better elucidation and explanation of the molecular mechanisms actions of these DPs, (c) Confirmation of their efficacy by in vivo studies using proper animal models of BC, (d) Demonstration of their effectiveness in clinical trials and (e) Demonstration of their safety.
| 5. Concluding remarks | | |
BC is a serious concern and miRNAs are dysregulated in BC playing critical roles in regulating different stages of carcinogenesis such as tumor initiation, promotion, progression and chemoresistance. Therefore, miRNAs are gaining more attraction and are novel targets for BC treatment. Different research studies have suggested that DPs can potentially modulate the expression level of different miRNAs involved in cancer. In the present review, we have discussed some DPs that have shown promising role for targeting BC miRNAs and we have also suggested some potential DPs that can be tested against BC miRNAs for possible molecular mechanism of actions. RV, sulforaphane, genistein, curcumin, DADS, DIM, EA, I3C and quercetin exhibit promising anti- BC results inhibiting BC progression through regulating miRNA expression and it has shown efficacy to regulate miRNAs in both in vitro and in vivo studies. Among these different DPs, RV has been tested against more miRNAs than the rest of the phytochemicals. Besides, there are some other DPs (benzyl isothiocyanate, capsaicin, EGCG, oleanolic acid, phenethyl isothiocyanate, ursolic acid, etc.,) which have anti-BC potentials but yet they have not been tested and researched against miRNAs involved in BC. Importantly, further studies of these potential bioactive compounds might lead to development of strategies for BC control. Recently, different miRNAs along with their molecular targets have been identified in BC and have been recognized as therapeutic targets as well. To the best of our knowledge and after careful literature survey, DPs have been tested against only a limited number of BC miRNAs and a large number of miRNAs still need extensive research work in order to unfold their molecular mechanism of action.
Conflict of interest statement
The authors declare that they have no conflicts of interest.
Acknowledgments
All authors listed have made substantial, direct and intellectual contribution to the work. Banzeer Ahsan Abbasi and Javed Iqbal summarized the literature, wrote the manuscript and drew the figures. Barkat Ali, Sayed Afzal Shah, Sobia Kanwal Ali Talha Khalil and Riaz Ahmad revised the manuscript. TM helped in interpretation by reviewing several draft of the manuscript.
| References | | |
| 1. | Iqbal J, Abbasi BA, Batool R, Mahmood T, Ali B, Khalil AT, et al. Potential phytocompounds for developing breast cancer therapeutics: Nature’s healing touch. Eur J Pharmacol 2018; 827: 125-148.  |
| 2. | Iqbal J, Abbasi BA, Mahmood T, Kanwal S, Ali B, Shah SA, et al. Plant-derived anticancer agents: A green anticancer approach. Asian Pac J Trop Biomed 2017; 7(12): 1129-1150. |
| 3. | Grundy A, Harris SA, Demers PA, Johnson KC, Agnew DA, Canadian Cancer Registries Epidemiology Research Group, et al. Occupational exposure to magnetic fields and breast cancer among Canadian men. Cancer Med 2016; 5: 586-596. |
| 4. | Brown GR. Breast cancerin transgender veterans: A ten-case series. LGBT Health 2015; 2: 77-80. |
| 5. | Moulder S, Hortobagyi GN. Advances in the treatment of breast cancer. Clin Pharmacol Ther 2008; 83; 26-36. |
| 6. | DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics, 2013. CA Cancer J Clin 2014; 64(1): 52-62. |
| 7. | Iqbal J, Abbasi BA, Khalil AT, Ali B, Mahmood T, Kanwal S, et al. Dietary isoflavones, the modulator of breast carcinogenesis: Current landscape and future perspectives. Asian Pac J Trop Med 2018; 11(3), 186-193. |
| 8. | Kim SH, Singh SV. The role of polycomb group protein Bmi-1 and Notch4 in breast cancer stem cell inhibition by benzyl isothiocyanate. Breast Cancer Res Treat 2015; 149(3): 681-692. |
| 9. | Crippa E, Folini M, Pennati M, Zaffaroni N, Pierotti MA, Gariboldi M. miR-342 overexpression results in a synthetic lethal phenotype in BRCA1-mutant HCC1937 breast cancer cells. Oncotarget 2016; 7(14): 18594. |
| 10. | Hou LK, Yu Y, Xie YG, Wang J, Mao JF, Zhang B, et al. miR-340 and ZEB1 negative feedback loop regulates TGF-ß-mediated breast cancer progression. Oncotarget 2016; 7(18): 26016. |
| 11. | Hanieh H. Aryl hydrocarbon receptor-microRNA-212/132 axis in human breast cancer suppresses metastasis by targeting SOX4. Mol Cancer 2015; 14(1): 172. |
| 12. | Venkatadri R, Muni T, Iyer AK, Yakisich JS, Azad N. Role of apoptosis-related miRNAs in resveratrol-induced breast cancer cell death. Cell Death Dis 2016; 7(2): e2104. |
| 13. | Taylor MA, Sossey-Alaoui K, Thompson CL, Danielpour D, Schiemann WP. TGF-β upregulates miR-181a expression to promote breast cancer metastasis. J Clin Invest 2013; 123(1): 150. |
| 14. | Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nature Cell Biol 2010; 12(3): 247-256. |
| 15. | Kong W, He L, Coppola M, Guo J, Esposito NN, Coppola D, et al. MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting Foxo3a in breast cancer. J Biol Chem 2010; 285(23): 17869-17879. |
| 16. | Huang Q, Gumireddy K, Schrier M, Le Sage C, Nagel R, Nair S, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nature Cell Biol 2008; 10(2): 202-210. |
| 17. | Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449(7163): 682-688. |
| 18. | Bahena-Ocampo I, Espinosa M, Ceballos-Cancino G, Lizarraga F, Campos-Arroyo D, Schwarz A, et al. miR-10b expression in breast cancer stem cells supports self-renewal through negative PTEN regulation and sustained Akt activation. EMBO Rep 2016; 17(5): 648-658. |
| 19. | Mitra A, Rostas JW, Dyess DL, Shevde LA, Samant RS. Micro-RNA- 632 downregulates DNAJB6 in breast cancer. Lab Invest 2012; 92(9): 1310-1317. |
| 20. | Wang F, Li L, Chen Z, Zhu M, Gu Y. MicroRNA-214 acts as a potential oncogene in breast cancer by targeting the PTEN-PI3K/Akt signaling pathway. Int J Mol Med 2016; 37(5): 1421-1428. |
| 21. | Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 2008; 18(3): 350-359. |
| 22. | Song B, Wang C, Liu J, Wang X, Lv L, Wei L, et al. MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J Exp Clin Cancer Res 2010; 29(1): 29. |
| 23. | Shi W, Bruce J, Lee M, Yue S, Rowe M, Pintilie M, et al. MiR-449a promotes breast cancer progression by targeting CRIP2. Oncotarget 2016; 7(14): 18906. |
| 24. | Zhan Y, Liang X, Li L, Wang B, Ding F, Li Y, et al. MicroRNA-548j functions as a metastasis promoter in human breast cancer by targeting Tensin1. Mol Oncol 2016; 10(6): 838-849. |
| 25. | Lei R, Tang J, Zhuang X, Deng R, Li G, Yu J, et al. Suppression of MIM by microRNA-182 activates RhoA and promotes breast cancer metastasis. Oncogene 2014; 33(10): 1287-1296. |
| 26. | Simonini PDSR, Breiling A, Gupta N, Malekpour M, Youns M, Omranipour R, et al. Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor in breast cancer cells. Cancer Res 2010; 70(22): 9175-9184. |
| 27. | Chiang CH, Hou MF, Hung WC. Up-regulation of miR-182 by ß-catenin in breast cancer increases tumorigenicity and invasiveness by targeting the matrix metalloproteinase inhibitor RECK. Biochim Biophys Acta 2013; 1830(4): 3067-3076. |
| 28. | Song SJ, Poliseno L, Song MS, Ala U, Webster K, Ng C, et al. MicroRNA-antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling. Cell 2013; 154(2): 311-324. |
| 29. | Matamala N, Vargas MT, González-Cámpora R, Arias JI, Menéndez P, Andrés-Leon E, et al. MicroRNA deregulation in triple negative breast cancer reveals a role of miR-498 in regulating BRCA1 expression. Oncotarget 2016; 7(15): 20068. |
| 30. | Cai J, Guan H, Fang L, Yang Y, Zhu X, Yuan J, et al. MicroRNA-374a activates Wnt/ß-catenin signaling to promote breast cancer metastasis. J Clin Invest 2013; 123(2): 566. |
| 31. | Mertens-Talcott SU, Chintharlapalli S, Li X, Safe S. The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G 2-M checkpoint in MDA-MB-231 breast cancer cells. Cancer Res 2007; 67(22): 11001-11011. |
| 32. | Tang W, Yu F, Yao H, Cui X, Jiao Y, Lin L, et al. miR-27a regulates endothelial differentiation of breast cancer stem like cells. Oncogene 2014; 33(20): 2629-2638. |
| 33. | Tavazoie SF, Alarcón C, Oskarsson T, Padua D, Wang Q, Bos PD, et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008; 451(7175): 147-152. |
| 34. | Kumaraswamy E, Wendt KL, Augustine LA, Stecklein SR, Sibala EC, Li D, et al. BRCA1 regulation of epidermal growth factor receptor (EGFR) expression in human breast cancer cells involves microRNA-146a and is critical for its tumor suppressor function. Oncogene 2015; 34(33): 4333-4346. |
| 35. | Goldberger N, Walker RC, Kim CH, Winter S, Hunter KW. Inherited variation in miR-290 expression suppresses breast cancer progression by targeting the metastasis susceptibility gene Arid4b. Cancer Res 2013; 73(8): 2671-2681. |
| 36. | Jiang CF, Li DM, Shi ZM, Wang L, Liu MM, Ge X, et al. Estrogen regulates miRNA expression: implication of estrogen receptor and miR- 124/AKT2 in tumor growth and angiogenesis. Oncotarget 2016; 7(24): 36940. |
| 37. | Yu Z, Willmarth NE, Zhou J, Katiyar S, Wang M, Liu Y, et al. microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci U S A 2010; 107(18): 8231-8236. |
| 38. | Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature Cell Biol 2008; 10(5): 593-601. |
| 39. | Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009; 138(3): 592-603. |
| 40. | Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. Let-7 regulates self-renewal and tumorigenicity of breast cancer cells. Cell 2007; 131(6): 1109-1123. |
| 41. | Yu J, Wang JG, Zhang L, Yang HP, Wang L, Ding D, et al. MicroRNA- 320a inhibits breast cancer metastasis by targeting metadherin. Oncotarget 2016; 7(25): 38612. |
| 42. | Yin K, Yin W, Wang Y, Zhou L, Liu Y, Yang G, et al. MiR-206 suppresses epithelial mesenchymal transition by targeting TGF-ß signaling in estrogen receptor positive breast cancer cells. Oncotarget 2016; 7(17): 24537. |
| 43. | Yu F, Deng H, Yao H, Liu Q, Su F, Song E. Mir-30 reduction maintains self-renewal and inhibits apoptosis in breast tumor-initiating cells. Oncogene 2010; 29(29): 4194-4204. |
| 44. | Patel Y, Shah N, Lee JS, Markoutsa E, Jie C, Liu S, et al. A novel doublenegative feedback loop between miR-489 and the HER2-SHP2-MAPK signaling axis regulates breast cancer cell proliferation and tumor growth. Oncotarget 2016; 7(14): 18295. |
| 45. | Zhu S, Sachdeva M, Wu F, Lu Z, Mo YY. Ubc9 promotes breast cell invasion and metastasis in a sumoylation-independent manner. Oncogene 2010; 29(12): 1763-1772. |
| 46. | Yang S, Li Y, Gao J, Zhang T, Li S, Luo A, et al. MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Oncogene 2013; 32(36): 4294-4303. |
| 47. | Xu X, Zhang Y, Jasper J, Lykken E, Alexander PB, Markowitz GJ, et al. MiR-148a functions to suppress metastasis and serves as a prognostic indicator in triple-negative breast cancer. Oncotarget 2016; 7(15): 20381. |
| 48. | Hargraves KG, He L, Firestone GL. Phytochemical regulation of the tumor suppressive microRNA, miR-34a, by p53-dependent and independent responses in human breast cancer cells. Mol Carcinog 2016; 55(5): 486-498. |
| 49. | Li Q, Yao Y, Eades G, Liu Z, Zhang Y, Zhou Q. Downregulation of miR- 140 promotes cancer stem cell formation in basal-like early stage breast cancer. Oncogene, 2014; 33(20): 2589-2600. |
| 50. | Li Q, Eades G, Yao Y, Zhang Y, Zhou Q. Characterization of a stem-like subpopulation in basal-like ductal carcinoma in situ (DCIS) lesions. J Biol Chem 2014; 289(3): 1303-1312. |
| 51. | Banerjee N, Talcott S, Safe S, Mertens-Talcott SU. Cytotoxicity of pomegranate polyphenolics in breast cancer cells in vitro and vivo: Potential role of miRNA-27a and miRNA-155 in cell survival and inflammation. Breast Cancer Res Treat 2012; 136(1): 21-34. |
| 52. | Munagala R, Aqil F, Vadhanam MV, Gupta RC. MicroRNA ‘signature’during estrogen-mediated mammary carcinogenesis and its reversal by ellagic acid intervention. Cancer Lett 2013; 339(2): 175-184. |
| 53. | Ahmad A, Ali S, Ahmed A, Ali AS, Raz A, Sakr WA, et al. 3, 3’- Diindolylmethane enhances the effectiveness of herceptin against HER-2/neu-expressing breast cancer cells. PLoS One 2013; 8(1): e54657. |
| 54. | Li X, Xie W, Xie C, Huang C, Zhu J, Liang Z, et al. Curcumin modulates miR-19/PTEN/Akt/p53 axis to suppress bisphenol A-induced MCF-7 breast cancer cell proliferation. Phytother Res 2014; 28(10): 1553-1560. |
| 55. | Guo J, Li W, Shi H, Xie X, Li L, Tang H, et al. Synergistic effects of curcumin with emodin against the proliferation and invasion of breast cancer cells through upregulation of miR-34a. Mol Cell Biochem 2013; 382(1-2): 103-111. |
| 56. | de la Parra C, Castillo-Pichardo L, Cruz-Collazo A, Cubano L, Redis R, Calin GA, et al. Soy isoflavone genistein-mediated downregulation of miR-155 contributes to the anticancer effects of genistein. Nutr Cancer 2016; 68(1): 154-164. |
| 57. | Xiao X, Chen B, Liu X, Liu P, Zheng G, Ye F, et al. Diallyl disulfide suppresses SRC/Ras/ERK signaling-mediated proliferation and metastasis in human breast cancer by up-regulating miR-34a. PLoS One 2014; 9(11): e112720. |
| 58. | Higdon JV, Delage B, Williams DE, Dashwood RH. Cruciferous vegetables and human cancer risk: Epidemiologic evidence and mechanistic basis. Pharmacol Res 2007 55(3): 224-236. |
| 59. | Marconett CN, Sundar SN, Tseng M, Tin AS, Tran KQ, Mahuron KM, et al. Indole-3-carbinol downregulation of telomerase gene expression requires the inhibition of estrogen receptor-alpha and Sp1 transcription factor interactions within the hTERT promoter and mediates the G 1 cell cycle arrest of human breast cancer cells. Carcinogenesis 2011; 32(9): 1315-1323. |
| 60. | McNaughton SA, Marks GC. Development of a food composition database for the estimation of dietary intakes of glucosinolates, the biologically active constituents of cruciferous vegetables. Br J Nutr 2003; 90(3): 687-697. |
| 61. | Sayeed MA, Bracci M, Lazzarini R, Tomasetti M, Amati M, Lucarini G, et al. Use of potential dietary phytochemicals to target miRNA: Promising option for breast cancer prevention and treatment? J Funct Foods 2017; 28: 177-193. |
| 62. | Wang X, Liu R, Yang Y, Zhang M. Isolation, purification and identification of antioxidants in an aqueous aged garlic extract. Food Chem 2015; 187: 37-43. |
| 63. | Gong Y, Sohn H, Xue L, Firestone GL, Bjeldanes LF. 3, 3’- Diindolylmethane is a novel mitochondrial H +-ATP synthase inhibitor that can induce p21Cip1/Waf1 expression by induction of oxidative stress in human breast cancer cells. Cancer Res 2006; 66(9): 4880-4887. |
| 64. | Anderson AM, Mitchell MS, Mohan RS. Isolation of curcumin from turmeric. J Chem Educ 2000; 77(3): 359-360. |
| 65. | Kronski E, Fiori ME, Barbieri O, Astigiano S, Mirisola V, Killian PH, et al. miR181b is induced by the chemopreventive polyphenol curcumin and inhibits breast cancer metastasis via down-regulation of the inflammatory cytokines CXCL1 and-2. Mol Oncol 2014; 8(3): 581-595. |
| 66. | Yang J, Cao Y, Sun J, Zhang Y. Curcumin reduces the expression of Bcl-2 by upregulating miR-15a and miR-16 in MCF-7 cells. Med Oncol 2010; 27(4): 1114-1118. |
| 67. | Kaufman PB, Duke JA, Brielmann H, Boik J, Hoyt JE. A comparative survey of leguminous plants as sources of the isoflavones, genistein and daidzein: implications for human nutrition and health. J Alter Compl Med 1997; 3(1): 7-12. |
| 68. | Petrus K, Schwartz H, Sontag G. Analysis of flavonoids in honey by HPLC coupled with coulometric electrode array detection and electrospray ionization mass spectrometry. Anal Bioanal Chem 2011; 400(8): 2555-2563. |
| 69. | Lee J, Mitchell AE. Pharmacokinetics of quercetin absorption from apples and onions in healthy humans. J Agri Food Chem 2012; 60(15); 3874-3881. |
| 70. | Tao SF, He HF, Chen Q. Quercetin inhibits proliferation and invasion acts by up-regulating miR-146a in human breast cancer cells. Mol Cell Biochem 2105; 402(1-2): 93-100. |
| 71. | Qin W, Zhang K, Clarke K, Weiland T, Sauter ER. Methylation and miRNA effects of resveratrol on mammary tumors vs. normal tissue. Nutr Cancer 2014; 66(2): 270-277. |
| 72. | Vislovukh A, Kratassiouk G, Porto E, Gralievska N, Beldiman C, Pinna G, et al. Proto-oncogenic isoform A2 of eukaryotic translation elongation factor eEF1 is a target of miR-663 and miR-744. Br J Cancer 2013 108(11): 2304-2311. |
| 73. | Hagiwara K, Kosaka N, Yoshioka Y, Takahashi RU, Takeshita F, Ochiya T. Stilbene derivatives promote Ago2-dependent tumour-suppressive microRNA activity. Sci Rep 2012; 2: 314. |
| 74. | Al-Hujaily EM, Mohamed AG, Al-Sharif I, Youssef KM, Manogaran PS, Al-Otaibi B, et al. PAC, a novel curcumin analogue, has anti-breast cancer properties with higher efficiency on ER-negative cells. Breast Cancer Res Treat 2001; 128(1): 97-107. |
| 75. | Maccario C, Savio M, Ferraro D, Bianchi L, Pizzala R, Pretali L, et al. The resveratrol analog 4, 4’-dihydroxy-trans-stilbene suppresses transformation in normal mouse fibroblasts and inhibits proliferation and invasion of human breast cancer cells. Carcinogenesis 2012; 33(11): 2172-2180. |
| 76. | Lv L, Liu C, Chen C, Yu X, Chen G, Shi Y, et al. Quercetin and doxorubicin co-encapsulated biotin receptor-targeting nanoparticles for minimizing drug resistance in breast cancer. Oncotarget 2016; 7(22): 32184. |
| 77. | Hwang JT, Lee YK, Shin JI, Park OJ. Anti-inflammatory and anticarcinogenic effect of genistein alone or in combination with capsaicin in TPA-treated rat mammary glands or mammary cancer cell line. Ann N Y Acad Sci 2009; 1171(1): 415-420. |
| 78. | Brakenhielm E, Cao R, Cao Y. Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J 2001; 15(10): 1798-1800. |
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]
| This article has been cited by | | 1 |
Docking and Molecular Dynamics Simulation Revealed the Potential Inhibitory Activity of Amygdalin in Triple-Negative Breast Cancer Therapeutics Targeting the BRCT Domain of BARD1 Receptor |
|
| Prarthana Chatterjee, Rohit Karn, I. Arnold Emerson, Satarupa Banerjee | | Molecular Biotechnology. 2023; | | [Pubmed] | [DOI] | | | 2 |
An overview of natural products that modulate the expression of non-coding RNAs involved in oxidative stress and inflammation-associated disorders |
|
| Jubilate Afuoti Ngum, Fabrice Junior Tatang, Michelle Hako Toumeni, Sarah Ngate Nguengo, Ulrich Stephane Fotso Simo, Cybelle Fodieu Mezajou, Charleine Kameni, Natacha Njike Ngongang, Maxwell Fofou Tchinda, Fabrice Fabien Dongho Dongmo, Mazarin Akami, Annie Rosalie Ngane Ngono, Ousman Tamgue | | Frontiers in Pharmacology. 2023; 14 | | [Pubmed] | [DOI] | | | 3 |
Green Synthesis of Zinc Oxide Nanoparticles Using Nostoc sp. and Their Multiple Biomedical Properties |
|
| Lubna Anjum Minhas, Abdul Samad Mumtaz, Muhammad Kaleem, Dunia Al Farraj, Khalid Kamal, Malik Aamer Hassan Minhas, Rooma Waqar, Rania M. Mahmoud | | Catalysts. 2023; 13(3): 549 | | [Pubmed] | [DOI] | | | 4 |
Antioxidant, Anticancer, and PXR-Dependent CYP3A4 Attributes of Schweinfurthia papilionacea (Burm.f.) Boiss., Tricholepis glaberrima DC. and Viola stocksii Boiss |
|
| Amir Shahbaz, Javed Iqbal, Banzeer Ahsan Abbasi, Wasim Akhtar, Iram Fatima, Syeda Anber Zahra, Sobia Kanwal, Javad Sharifi-Rad, Hassan Sher, Tariq Mahmood, William C. Cho, Lei Chen | | Oxidative Medicine and Cellular Longevity. 2022; 2022: 1 | | [Pubmed] | [DOI] | | | 5 |
Therapeutic potential of chrysin nanoparticle-mediation inhibition of succinate dehydrogenase and ubiquinone oxidoreductase in pancreatic and lung adenocarcinoma |
|
| Eman M. Ragab, Doaa M. El Gamal, Tarek M. Mohamed, Abeer A. Khamis | | European Journal of Medical Research. 2022; 27(1) | | [Pubmed] | [DOI] | | | 6 |
Deciphering Chemical Profiling, Pharmacological Responses and Potential Bioactive Constituents of Saussurea lappa Decne. extracts through In Vitro Approaches |
|
| Sana Naseer, Javed Iqbal, Abeel Naseer, Sobia Kanwal, Ishtiaq Hussain, Yong Tan, Liliana Aguilar-Marcelino, Raquel Cossio-Bayugar, Zbigniew Zajac, Yousef A. Bin Jardan, Tariq Mahmood | | Saudi Journal of Biological Sciences. 2022; | | [Pubmed] | [DOI] | | | 7 |
Biosynthesis of NiO nanoparticles using Spirogyra sp. cell-free extract and their potential biological applications |
|
| Yadvinder Singh, Ramandeep Singh Sodhi, Prit Pal Singh, Sandeep Kaushal | | Materials Advances. 2022; | | [Pubmed] | [DOI] | | | 8 |
Rhamnella gilgitica
functionalized green synthesis of
ZnONPs
and their multiple therapeutic properties
|
|
| Banzeer Ahsan Abbasi, Javed Iqbal, Muhammad Israr, Tabassum Yaseen, Syeda Anber Zahra, Amir Shahbaz, Abbas Rahdar, Blqees Raouf, Shahid Ullah Khan, Sobia Kanwal, Tariq Mahmood | | Microscopy Research and Technique. 2022; | | [Pubmed] | [DOI] | | | 9 |
Phytochemistry, biological activities and in silico molecular docking studies of Oxalis pes-caprae L. compounds against SARS-CoV-2 |
|
| Farhat Gul, Ilham Khan, Javed Iqbal, Banzeer Ahsan Abbasi, Amir Shahbaz, Raffaele Capasso, Itzel Amaro-Estrada, Yousef A. Bin Jardang, Raquel Cossio-Bayugar, Tariq Mahmood | | Journal of King Saud University - Science. 2022; : 102136 | | [Pubmed] | [DOI] | | | 10 |
Phytochemical and pharmacological uses of medicinal plants to treat cancer: A case study from Khyber Pakhtunkhwa, North Pakistan |
|
| Asif Khan,Sajid Ali,Waheed Murad,Khizar Hayat,Shumaila Siraj,Muhammad Jawad,Rashid Abbas Khan,Jalal Uddin,Ahmed Al-Harrasi,Ajmal Khan | | Journal of Ethnopharmacology. 2021; : 114437 | | [Pubmed] | [DOI] | | | 11 |
Phytochemicals mediated modulation of
microRNAs
and long non-coding
RNAs
in cancer prevention and therapy
|
|
| Luis M. Ruiz-Manriquez, Carolina Estrada-Meza, Javier A. Benavides-Aguilar, S. Janin Ledesma-Pacheco, Andrea Torres-Copado, Francisco I. Serrano-Cano, Anindya Bandyopadhyay, Surajit Pathak, Samik Chakraborty, Aashish Srivastava, Ashutosh Sharma, Sujay Paul | | Phytotherapy Research. 2021; | | [Pubmed] | [DOI] | | | 12 |
Antimicrobial, cytotoxic, antioxidants, enzyme inhibition activities, and scanning electron microscopy of
Lactuca orientalis
(Boiss.) Boiss. seeds |
|
| Syeda Anber Zahra,Javed Iqbal,Banzeer Ahsan Abbasi,Amir Shahbaz,Sobia Kanwal,Syed Lal Shah,Parvaiz Ahmad,Tariq Mahmood | | Microscopy Research and Technique. 2021; | | [Pubmed] | [DOI] | | | 13 |
Scanning electron microscopy of
Sophora alopecuroides
L. seeds and their cytotoxic, antimicrobial, antioxidant, and enzyme inhibition potentials |
|
| Syeda Anber Zahra,Javed Iqbal,Banzeer Ahsan Abbasi,Tabassum Yaseen,Ayesha Hameed,Amir Shahbaz,Sobia Kanwal,Tariq Mahmood,Parvaiz Ahmad | | Microscopy Research and Technique. 2021; | | [Pubmed] | [DOI] | | | 14 |
Precursor effects on the physical, biological, and catalytic properties of
Fagonia indica
Burm.f. mediated zinc oxide nanoparticles |
|
| Safia Hameed,Ali Talha Khalil,Muhammad Ali,Javed Iqbal,Lubna Rahman,Muhammad Numan,Saleh Khamlich,Malik Maaza,Ikram Ullah,Banzeer Ahsan Abbasi,Fawaz Alasmari,Zabta Khan Shinwari | | Microscopy Research and Technique. 2021; | | [Pubmed] | [DOI] | | | 15 |
Chemical composition and pharmacological bio-efficacy of Parrotiopsis jacquemontiana (Decne) Rehder for anticancer activity |
|
| Saima Ali,Muhammad Rashid Khan,Javed Iqbal,Riffat Batool,Irum Naz,Tabassum Yaseen,Banzeer Ahsan Abbasi,Jamal Abdul Nasir,Hamed A. El-Serehy | | Saudi Journal of Biological Sciences. 2021; | | [Pubmed] | [DOI] | | | 16 |
Characterization and phytochemical constituents of Periploca hydaspidis Falc crude extract and its anticancer activities |
|
| Saima Ali,Muhammad Rashid Khan,Riffat Batool,Sayed Afzal Shah,Javed Iqbal,Banzeer Ahsan Abbasi,Tabassum Yaseen,Nida Zahra,Adil Aldhahrani,Fayez Althobaiti | | Saudi Journal of Biological Sciences. 2021; | | [Pubmed] | [DOI] | | | 17 |
Bioinspired synthesis and activity characterization of iron oxide nanoparticles made using Rhamnus Triquetra leaf extract |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Syeda Anber Zahra,Amir Shahbaz,Sobia Kanwal,Atiya Rabbani,Tariq Mahmood | | Materials Research Express. 2020; 6(12): 1250e7 | | [Pubmed] | [DOI] | | | 18 |
Green Synthesis and Characterization of Silver NPs Using Oyster Mushroom Extract For Antibacterial Efficacy |
|
| Akhtar Ram Naraian,Abhishek Kumar Bhardwaj Abhishek | | Journal of Chemistry, Environmental Sciences and its Applications. 2020; 7(1) | | [Pubmed] | [DOI] | | | 19 |
Regulation of Breast Cancer Progression by Noncoding RNAs |
|
| Ravishkumar L. Akshaya,Muthukumar Rohini,Nagarajan Selvamurugan | | Current Cancer Drug Targets. 2020; 20(10): 757 | | [Pubmed] | [DOI] | | | 20 |
Anti-Angiogenic Effects of Phytochemicals on miRNA Regulating Breast Cancer Progression |
|
| Elizabeth Varghese,Alena Liskova,Peter Kubatka,Samson Mathews Samuel,Dietrich Büsselberg | | Biomolecules. 2020; 10(2): 191 | | [Pubmed] | [DOI] | | | 21 |
Phytogenic Synthesis of Nickel Oxide Nanoparticles (NiO) Using Fresh Leaves Extract of Rhamnus triquetra (Wall.) and Investigation of Its Multiple In Vitro Biological Potentials |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Riaz Ahmad,Mahboobeh Mahmoodi,Akhtar Munir,Syeda Anber Zahra,Amir Shahbaz,Muzzafar Shaukat,Sobia Kanwal,Siraj Uddin,Tariq Mahmood,Raffaele Capasso | | Biomedicines. 2020; 8(5): 117 | | [Pubmed] | [DOI] | | | 22 |
Facile green synthesis approach for the production of chromium oxide nanoparticles and their different in vitro biological activities |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Akhtar Munir,Siraj Uddin,Sobia Kanwal,Tariq Mahmood | | Microscopy Research and Technique. 2020; | | [Pubmed] | [DOI] | | | 23 |
Environmentally friendly green approach for the fabrication of silver oxide nanoparticles: Characterization and diverse biomedical applications |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Jamal Abdul Nasir,Syeda Anber Zahra,Amir Shahbaz,Siraj Uddin,Safia Hameed,Farhat Gul,Sobia Kanwal,Tariq Mahmood | | Microscopy Research and Technique. 2020; | | [Pubmed] | [DOI] | | | 24 |
Phytofabrication of cobalt oxide nanoparticles from
Rhamnus virgata
leaves extract and investigation of different bioactivities |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Zaibunisa Khan,Riaz Ahmad,Siraj Uddin,Amir Shahbaz,Syeda Anber Zahra,Muzzafar Shaukat,Farmeen Kiran,Sobia Kanwal,Tariq Mahmood | | Microscopy Research and Technique. 2020; | | [Pubmed] | [DOI] | | | 25 |
Comparison of polyphenol-rich wine grape seed flour-regulated fecal and blood microRNAs in high-fat, high-fructose diet-induced obese mice |
|
| Kun-Ho Seo,Wallace Yokoyama,Hyunsook Kim | | Journal of Functional Foods. 2020; 73: 104147 | | [Pubmed] | [DOI] | | | 26 |
Green formulation and chemical characterizations of Rhamnella gilgitica aqueous leaves extract conjugated NiONPs and their multiple therapeutic properties |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Farmeen Kiran,Riaz Ahmad,Sobia Kanwal,Akhtar Munir,Siraj Uddin,Jamal Abdul Nasir,Wadie Chalgham,Tariq Mahmood | | Journal of Molecular Structure. 2020; : 128490 | | [Pubmed] | [DOI] | | | 27 |
Potential phytochemicals in the prevention and treatment of esophagus cancer: A green therapeutic approach |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Riaz Ahmad,Sitara Bibi,Tariq Mahmood,Sobia Kanwal,Sheeza Bashir,Farhat Gul,Safia Hameed | | Pharmacological Reports. 2019; | | [Pubmed] | [DOI] | | | 28 |
Synthesis and Characterization of Reishi Mushroom-mediated Green Synthesis of Silver Nanoparticles for the Biochemical Applications |
|
| Aysenur Aygün,Sadin Özdemir,Mehmet Gülcan,Kemal Cellat,Fatih Sen | | Journal of Pharmaceutical and Biomedical Analysis. 2019; : 112970 | | [Pubmed] | [DOI] | | | 29 |
Plant-extract mediated green approach for the synthesis of ZnONPs: Characterization and evaluation of cytotoxic, antimicrobial and antioxidant potentials |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Tariq Mahmood,Sobia Kanwal,Riaz Ahmad,Muhammad Ashraf | | Journal of Molecular Structure. 2019; 1189: 315 | | [Pubmed] | [DOI] | | | 30 |
FBiogenic synthesis of green and cost effective iron nanoparticles and evaluation of their potential biomedical properties |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Riaz Ahmad,Amir Shahbaz,Syeda Anber Zahra,Sobia Kanwal,Akhtar Munir,Atiya Rabbani,Tariq Mahmood | | Journal of Molecular Structure. 2019; : 126979 | | [Pubmed] | [DOI] | | | 31 |
The role of dietary phytochemicals in the carcinogenesis via the modulation of miRNA expression |
|
| Marek Samec,Alena Liskova,Peter Kubatka,Sona Uramova,Pavol Zubor,Samson Mathews Samuel,Anthony Zulli,Martin Pec,Tibor Bielik,Kamil Biringer,Erik Kudela,Jozef Benacka,Mariusz Adamek,Luis Rodrigo,Rachele Ciccocioppo,Taeg Kyu Kwon,Denis Baranenko,Peter Kruzliak,Dietrich Büsselberg | | Journal of Cancer Research and Clinical Oncology. 2019; | | [Pubmed] | [DOI] | | | 32 |
Potential phytochemicals in the fight against skin cancer: Current landscape and future perspectives |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Riaz Ahmad,Riffat Batool,Tariq Mahmood,Barkat Ali,Ali Talha Khalil,Sobia Kanwal,Sayed Afzal Shah,Muhammad Maqsood Alam,Sheeza Bashir,Hussain Badshah,Akhtar Munir | | Biomedicine & Pharmacotherapy. 2019; 109: 1381 | | [Pubmed] | [DOI] | | | 33 |
Bioactivities of Geranium wallichianum Leaf Extracts Conjugated with Zinc Oxide Nanoparticles |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Riaz Ahmad,Layiq Zia,Sobia Kanwal,Tariq Mahmood,Canran Wang,Jen-Tsung Chen | | Biomolecules. 2019; 10(1): 38 | | [Pubmed] | [DOI] | | | 34 |
Biofabrication of iron oxide nanoparticles by leaf extract of
Rhamnus virgata
: Characterization and evaluation of cytotoxic, antimicrobial and antioxidant potentials |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Tariq Mahmood,Abdul Qyyum,Sobia Kanwal | | Applied Organometallic Chemistry. 2019; : e4947 | | [Pubmed] | [DOI] | | | 35 |
Plant-mediated synthesis of nickel oxide nanoparticles (NiO) via Geranium wallichianum: characterization and different biological applications |
|
| Banzeer Ahsan Abbasi,Javed Iqbal,Tariq Mahmood,Riaz Ahmad,Sobia Kanwal,Shakeeb Afridi | | Materials Research Express. 2019; 6(8): 0850a7 | | [Pubmed] | [DOI] | | | 36 |
Green synthesis of zinc nanoparticles through plant extracts: establishing a novel era in cancer theranostics |
|
| Safia Hameed,Javed Iqbal,Muhammad Ali,Ali Talha Khalil,Banzeer Ahsan Abbasi,Muhammad Numan,Zabta Khan Shinwari | | Materials Research Express. 2019; 6(10): 102005 | | [Pubmed] | [DOI] | | | 37 |
Biogenic synthesis of green and cost effective cobalt oxide nanoparticles using Geranium wallichianum leaves extract and evaluation of in vitro antioxidant, antimicrobial, cytotoxic and enzyme inhibition properties |
|
| Javed Iqbal,Banzeer Ahsan Abbasi,Riffat Batool,Ali Talha Khalil,Safia Hameed,Sobia Kanwal,Ikram Ullah,Tariq Mahmood | | Materials Research Express. 2019; 6(11): 115407 | | [Pubmed] | [DOI] | |
|
 |
|
|
|
Search Pubmed for