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Genistein: a promising molecule modulating tumour growth and wound healing?


Authors: Petra Mitrengová;  Pavel Mučaji;  Vlasta Peržeľová;  Erik Dosedla;  Peter Gál
Published in the journal: Čes. slov. Farm., 2018; 67, 3-13
Category: Review Articles

Summary

Although it has been shown that oestrogen replacement therapy is able to improve wound healing, several side effects of this replacement therapy have precluded its common use in clinical practice. On the other hand, the phytoestrogen genistein (the selective oestrogen receptor modulator belonging to the group of isoflavones) has been introduced into several clinical trials to improve cancer treatment efficiency and experiments suggest its positive effect on wound healing. The main mechanisms of action, which have been elucidated so far, include induction of apoptosis, cell cycle arrest, inhibition of angiogenesis and tyrosine kinase activity as well as cancer chemoprevention and reduction of climacteric symptoms. Unfortunately, all underlying mechanism in the modulation of biological processes involved in wound healing and tumour growth are not yet fully understood. Therefore, the present review summarizes the effects of genistein on biological processes in different wound healing models and selected tumours.

Key words:

genistein • tissue repair and regeneration • carcinoma • skin


Zdroje

  1.   Ososki A. L., Kennelly E. J. Phytoestrogens: a review of the Present State of Research. Phytother. Res. 2003; 17, 845–869.

  2.   Brzezinski A., Debi A. Phytoestrogens: the “natural” selective estrogen receptor modulators? Eur J. Obstet. Gynecol. Reprod. Biol. 1999; 85, 47–51.

  3.   Kelly P. M., Keely N. O., Bright S. A., Yassin B., Ana G., Fayne D., Zisterer D. M., Meegan M. J. Novel selective estrogen receptor ligand conjugates incorporating endoxifen-combretastatin and cyclofenil-combretastatin hybrid scaffolds: Synthesis and biochemical evaluation. Molecules 2017; 22, 1440.

  4.   Lee I. R., Dawson S. A., Watherall J. D., Hahnel R. Sex hormone-binding globulin secretion by human hepatocarcinoma cells is increased by estrogens and androgens. J. Clin. Endocrinol. Metab. 1987; 64, 825–831.

  5.   Cassidy A. Potential risks and benefits of phytoestrogen-rich diets. Int. J. Vitam. Nutr. Res. 2003; 73, 120–126.

  6.   Mezei O., Banz W. J., Steger R. W., Peluso M. R., Winters T. A., Shay N. Soy isoflavones exert antidiabetic and hypolipidemic effects through the PPAR pathways in obese Zucker rats and murine RAW 264.7 cells. J. Nutr. 2003; 133, 1238–1243.

  7.   Chemical Book. © 2016 citované 2017-01-27). Dostupné na: http://www.chemicalbook.com/ChemicalProductProperty_EN_CB6163787.htm

  8.   Roland W. S., Vincken J. P., Gouka R. J., van Buren L., Gruppen H., Smit G. Soy Isoflavones and Other Isoflavonoids Activate the Human Bitter Taste Receptors hTAS2R14 and hTAS2R39. J. Agric. Food Chem. 2011; 59, 11764–11771.

  9.   Yang Z., Kulkarni K., Zhu W., Hu M. Bioavailability and Pharmacokinetics of Genistein: Mechanistic Studies on its ADME. Anticancer Agents Med. Chem. 2012; 12, 1264–1280.

10.   Wu J. G., Ge J., Zhang Y. P., Yu Y., Zhang X. Y. Solubility of Genistein in Water, Methanol, Ethanol, Propan-2-ol, 1-Butanol, and Ethyl Acetate from (280 to 333) K. J. Chem. Eng. Data 2010; 55, 5286–5288.

11.   Fukutake M., Takahashi M., Ishida K., Kawamura H., Sugimura T., Wakabayashi K. Quantification of Genistein and Genistin in Soybean and Soybean products. Food Chem. Toxicol. 1996; 34, 457–461.

12.   Dalu A., Haskell J. F., Coward L., Lamartiniere C. A. Genistein, a Component of Soy, Inhibits the Expression of the EGF and ErbB2/Neu Receptors in the Rat Dorsolateral Prostate. Prostate. 1998; 37, 36–43.

13.   Banerjee S., Li Y., Wang Z., Sarkar F. H. Multi-targeted therapy of cancer by genistein. Cancer Lett. 2008; 269, 226–242.

14.   Kim Y. S., Choi K. C., Hwang K. A. Genistein suppressed epithelial-mesenchymal transition and migration efficacies of BG-1 ovarian cancer cells activated by estrogenic chemicals via estrogen receptor pathway and down-regulation of TGF-β signaling pathway. Phytomedicine 2015; 22, 993–999.

15.   Kuiper G. G., Lemmen J. G., Carlsson B., Corton J. C., Safe S. H., van der Saag P. T., van der Burg B., Gustafsson J. A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998; 139, 4252–4263.

16.   Polkowski K., Popiołkiewicz J., Krzeczyński P., Ramza J., Pucko W., Zegrocka-Stendel O., Boryski J., Skierski J. S., Mazurek A. P., Grynkiewicz G. Cytostatic and cytotoxic activity of synthetic genistein glycosides against human cancer cell lines. Cancer Lett. 2004; 203, 59–69.

17.   Popiołkiewicz J., Polkowski K., Skierski J.S., Mazurek A. P. In vitro toxicity evaluation in the development of new anticancer drugs – genistein glycosides. Cancer Lett. 2005; 229, 67–75.

18.   Kwon S. H., Kang M. J., Huh J. S., Ha K. W., Lee J. R., Lee S. K., Lee B. S., Han I. H., Lee M. S., Lee M. W., Lee J., Choi Y. W. Comparison of oral bioavailability of genistein and genistin in rats. Int. J. Pharm. 2007; 337, 148–154.

19.   Steensma A., Faassen-Peters M. A., Noteborn H. P., Rietjens I. M. Bioavailability of Genistein and Its Glycoside Genistin As Measured in the Portal Vein of Freely Moving Unanesthetized Rats. J. Agric. Food Chem. 2006; 54, 8006–8012.

20.   Pasqualini J. R. Breast Cancer: Prognosis, Treatment, and Prevention. New York, Basel: CRC Press 2002.

21.   Liu B., Edgerton S., Yang X., Kim A., Ordonez-Ercan D., Mason T., Alvarez K., McKimmey C., Liu N., Thor A. Low-dose dietary phytoestrogen abrogates tamoxifen-associated mammary tumor prevention. Cancer Res. 2005; 65, 879–886.

22.   Kapiotis S., Hermann M., Held I., Seelos C., Ehringer H., Gmeiner B. M. Genistein, the dietary-derived angiogenesis inhibitor, prevents LDL oxidation and protects endothelial cells from damage by atherogenic LDL. Arterioscler. Thromb. Vasc. Biol. 1997; 17, 2868–2874.

23.   Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 1987; 262, 5592–5595.

24.   Stahl S., Chun T. Y., Gray W. G. Phytoestrogens act as estrogen agonists in an estrogen-responsive pituitary cell line. Toxicol. Appl. Pharmacol. 1998; 152, 41–48.

25.   Jurzak M., Ramos P., Pilawa B. The influence of genistein on free radicals in normal dermal fibroblasts and keloid fibroblasts examined by EPR spectroscopy. Med. Chem. Res. 2017; 26, 1297–1305.

26.   Zhang Z., Wang C. Z., Du G. J., Qi L. W., Calway T., He T. C., Du W., Yuan C. S. Genistein induces G2/M cell cycle arrest and apoptosis via ATM/p53- dependent pathway in human colon cancer cells. Int. J. Oncol. 2013; 43, 289–296.

27.   Varinská L., Gál P., Mojžišová G., Mirossay L., Mojžiš J. Soy and breast cancer: focus on angiogenesis. Int. J. Mol. Sci. 2015; 16, 11728–11749.

28.   Su S. J., Yeh T. M., Chuang W. J., Ho C. L., Chang K. L., Cheng H. L., Liu H. S., Cheng H. L., Hsu P. Y., Chow N. H. The novel targets for anti-angiogenesis of genistein on human cancer cells. Biochem. Pharmacol. 2005; 69, 307–318.

29.   Guo Y., Wang S., Hoot D. R., Clinton S. K. Suppression of VEGF-mediated autocrine and paracrine interactions between prostate cancer cells and vascular endothelial cells by soy isoflavones. J. Nutr. Biochem. 2007; 18, 408–417.

30.   Zhou J. R., Gugger E. T., Tanaka T., Guo Y., Blackburn G. L., Clinton S. K. Soybean phytochemicals inhibit the growth of transplantable human prostate carcinoma and tumor angiogenesis in mice. J. Nutr. 1999; 129, 1628–1635.

31.   Bakkiyanathan A., Joseph A. M., Tharani L., Malathi R. Genistein, the phytoestrogen induces heart-and-soul (has) phenotypes in zebrafish embryo. J. Dev. Biol. Tissue Eng. 2010; 2, 18–22.

32.   Mukhopadhyay S., Ballard B. R., Mukherjee S., Kabir S. M., Das S. K. Beneficial effects of soy protein in the initiation and progression against dimethylbenz(a) anthracene-induced breast tumors in female rats. Mol. Cell Biochem. 2006; 290: 169–176.

33.   Farina H. G., Pomies M., Alonso D. F., Gomez D. E. Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol. Rep. 2006; 16, 885–891.

34.   Lamartiniere, C. A. Protection against breast cancer with genistein: a component of soy. Am. J. Clin. Nutr. 2000; 71, 1705–1707.

35.   Allred C. D., Allred K. F., Ju Y. H., Virant S. M., Helferich W. G. Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependent (MCF-7) tumors in a dose-dependent manner. Cancer Res. 2001; 61, 5045–5050.

36.   Hsieh C. Y., Santell R. C., Haslam S. Z., Helferich W. G. Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res. 1998; 58, 3833–3838.

37.   Chang E. C., Charn T. H., Park S. H., Helferich W. G., Komm B., Katzenellenbogen J. A., Katzenellenbogen B. S. Estrogen receptors α and β as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol. Endocrinol. 2008; 22, 1032–1043.

38.   Li Z., Li J., Mo B., Hu C., Liu H., Qi H., Wang X., Xu J. Genistein induces G2/M cell cycle arrest via stable activation of ERK1/2 pathway in MDA-MB-231 breast cancer cells. Cell Biol. Toxicol. 2008; 24, 401–409.

39.   Wang T. T. Y., Sathyamoorthy N., Phang J. M. Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis 1996; 17, 271–275.

40.   Leung L. K., Wang T. T. Bcl-2 is not reduced in the death of MCF-7 cells at low genistein concentration. J. Nutr. 2000; 130, 2922–2926.

41.   Pagliacci M. C., Smacchia M., Migliorati G., Grignani F., Riccardi C., Nicoletti I. Growth-inhibitory effects of the natural phytoestrogen genistein in MCF-7 human breast cancer cells. Eur. J. Cancer. 1994; 30, 1675–1682.

42.   Paruthiyil S., Parmar H., Kerekatte V., Cunha G. R., Firestone G. L., Leitman D. C. Estrogen receptor β inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Res. 2004; 64, 423–428.

43.   Jiang Y., Gong P., Madak-Erdogan Z., Martin T., Jeyakumar M., Carlson K., Khan I., Smillie T. J., Chittiboyina A. G., Rotte S. C. K., Helferich W. G., Katzenellenbogen J. A., Katzenellenbogen B. S. Mechanisms enforcing the estrogen receptor β selectivity of botanical estrogens. FASEB J. 2013; 27, 4406–4418.

44.   Gong L., Li Y., Nedeljkovic-Kurepa A., Sarkar F. H. Inactivation of NF-κB by genistein is mediated via Akt signaling pathway in breast cancer cells. Oncogene 2003; 22, 4702–4709.

45.   Mai Z., Blackburn G. L., Zhou J. R. Genistein sensitizes inhibitory effect of tamoxifen on the growth of estrogen receptor-positive and HER2-overexpressing human breast cancer cells. Mol. Carcinog. 2007; 46, 534–542.

46.   Li Y., Ahmed F., Ali S., Philip P. A., Kucuk O., Sarkar F. H. Inactivation of nuclear factor KB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells. Cancer Res. 2005; 65, 6934–6942.

47.   Seo H. S., DeNardo D. G., Jacquot Y., Laïos I., Vidal D. S., Zambrana C. R., Leclercq G., Brown P. H. Stimulatory eect of genistein and apigenin on the growth of breast cancer cells correlates with their ability to activate ER alpha. Breast Cancer Res. Treat. 2006; 99, 121–134.

48.   Pan H., Zhou W., He W., Liu X., Ding Q., Ling L., Zha X., Wang S. Genistein inhibits MDA-MB-231 triple-negative breast cancer cell growth by inhibiting NF-κB activity via the Notch-1 pathway. Int. J. Mol. Med. 2012; 30, 337–343.

49.   Shim H. Y., Park J. H., Paik H. D., Nah S. Y., Kim D. S., Han Y. S. Genistein-induced apoptosis of human breast cancer MCF-7 cells involves calpain-caspase and apoptosis signaling kinase 1–p38 mitogen-activated protein kinase activation Cascades. Anticancer Drugs 2007; 18, 649–657.

50.   Prietsch R. F., Monte L. G., da Silva F. A., Beira F. T., Del Pino F. A., Campos V. F., Collares T., Pinto L. S., Spanevello R. M., Gamaro G. D., Braganhol E. Genistein induces apoptosis and autophagy in human breast MCF-7 cells by modulating the expression of proapoptotic factors and oxidative stress enzymes. Mol. Cell. Biochem. 2014; 390, 235–242.

51.   Ovarian Cancer Research Fund Alliance © 2016 citované 2017-11-22). Dostupné na: https://ocrfa.org/patients/about-ovarian-cancer/statistics/

52.   Luo H., Jiang B. H., King S. M., Chen Y. C. Inhibition of Cell Growth and VEGF Expression in Ovarian Cancer Cells by Flavonoids. Nutr. Cancer 2008; 60, 800–809.

53.   Ouyang G., Yao L., Ruan K., Song G., Mao Y., Bao S. Genistein induces G2/M cell cycle arrest and apoptosis of human ovarian cancer cells via activation of DNA damage checkpoint pathways. Cell. Biol. Int. 2009; 33, 1237–1244.

54.   Antosiak A., Milowska K., Maczynska K., Rozalska S., Gabryelak T. Cytotoxic activity of genistein-8-C-glucoside form Lupinus luteus L. and genistein against human SK-OV-3 ovarian carcinoma cell line. Med. Chem. Res. 2016; 26, 64–73.

55.   American Cancer Society. Colorectal Cancer Facts & Figures 2014–2016. Atlanta: American Cancer Society © 2014 citované 2017-11-23). Dostupné na: https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/colorectal-cancer-facts-and-figures/colorectal-cancer-facts-and-figures-2014-2016.pdf

56.   Raju J., Bielecki A., Caldwell D., Lok E., Taylor M., Kapal K., Curran I., Cooke G. M., Bird R. P., Mehta R. Soy isoflavones modulate azoxymethane-induced rat colon carcinogenesis exposed pre- and postnatally and inhibit growth of DLD-1 human colon adenocarcinoma cells by increasing the expression of estrogen receptor-b 1–3. J. Nutr. 2009; 139, 474–481.

57.   Qi W., Weber C. R., Wasland K., Savkovic S. D. Genistein inhibits proliferation of colon cancer cells by attenuating a negative effect of epidermal growth factor on tumor suppressor FOXO3 activity. BMC Cancer 2011; 11, 219.

58.   Pool-Zobel B. L., Adlercreutz H., Glei M., Liegibel U. M., Sittlingon J., Rowland I., Wähälä K., Rechkemmer G. Isoflavonoids and lignans have different potentials to modulate oxidative genetic damage in human colon cells. Carcinogenesis 2000; 21, 1247–1252.

59.   American Cancer Society © 2016 citované 2017-11-27). Dostupné na: https://www.cancer.org/cancer/prostate-cancer.html

60.   Normanno N., De Luca A., Bianco C., Strizzi L., Mancino M., Maiello M. R., Carotenuto A., De Feo G., Caponigro F., Salomon D. S. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 2006; 366, 2–16.

61.   Raffoul J. J., Wang Y., Kucuk O., Forman J. D., Sarkar F. H., Hillman G. G. Genistein inhibits radiation-induced activation of NF-κB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 2006; 6, 107.

62.   Suzuki K., Koike H., Matsui H., Ono Y., Hasumi M., Nakazato H., Okugi H., Sekine Y., Oki K., Ito K., Yamamoto T., Fukabori Y., Kurokawa K., Yamanaka H. Genistein, a soy isoflavone, induces glutathione peroxidase in the human prostate cancer cell lines LNCaP a PC-3. Int. J. Cancer 2002; 99, 846–852.

63.   Kumi-Diaka J. Chemosensitivity of human prostate cancer cells PC3 and LNCaP to genistein isoflavone and β-lapachone. Biol. Cell. 2002; 94, 37–44.

64.   Hörmann V., Kumi-Diaka J., Durity M., Rathinavelu A. Anticancer activities of genistein-topotecan combination in prostate cancer cells. J. Cell. Mol. Med. 2012; 16, 2631–2636.

65.   Gu Y., Zhu C. F., Dai Y. L., Zhong Q., Sun B. Inhibitory effects of genistein on metastasis of human hepatocellular carcinoma. World J. Gastroenterol. 2009; 15, 4952–4957.

66.   Gu Y., Zhu C. F., Iwamoto H., Chen J. S. Genistein inhibits invasive potential of human hepatocellular carcinoma by altering cell cycle, apoptosis, and angiogenesis. World J. Gastroenterol. 2005; 11, 6512–6517.

67.   Mansoor T. A., Ramalho R. M., Luo X., Ramalhete C., Rodrigues C. M., Ferreira M. J. Isoflavones as apoptosis inducers in human hepatoma HuH‐7 cells. Phytother. Res. 2011; 25, 1819–1824.

68.   Yeh T. C., Chiang P. C., Li T. K., Hsu J. L., Lin C. J., Wang S. W., Peng C. Y., Guh J. H. Genistein induces apoptosis in human hepatocellular carcinomas via interaction of endoplasmic reticulum stress and mitochondrial insult. Biochem. Pharmacol. 2007; 73, 782–792.

69.   Chodon D., Ramamurty N., Sakthisekaran D. Preliminary studies on induction of apoptosis by genistein on HepG2 cell line. Toxicol. In Vitro 2007; 21, 887–891.

70.   Wang S. D., Chen B. C., Kao S. T., Liu C. J., Yeh C. C. Genistein inhibits tumor invasion by suppressing multiple signal transduction pathways in human hepatocellular carcinoma cells. BMC Complement. Altern. Med. 2014; 14, 26.

71.   Dai W., Wang F., He L., Lin C., Wu S., Chen P., Zhang Y., Shen M., Wu D., Wang C., Lu J., Zhou Y., Xu X., Xu L., Guo C. Genistein inhibits hepatocellular carcinoma cell migration by reversing the epithelial-mesenchymal transition: partial mediation by the transcription factor NFAT1. Mol. Carcinog. 2015; 54, 301–311.

72.   Huang W., Wan C., Luo Q., Huang Z., Luo Q. Genistein-inhibited cancer stem cell-like properties and reduced chemoresistance of gastric cancer. Int. J. Mol. Sci. 2014; 15, 3432–3443.

73.   Yu D., Shin H. S., Lee Y. S., Lee D., Kim S., Lee Y. C. Genistein attenuates cancer stem cell characteristics in gastric cancer through the down-regulation of Gli1. Oncol. Rep. 2014; 31, 673–678.

74.   Zhou H. B., Chen J. J., Wang W. X., Cai J. T., Du Q. Apoptosis of human primary gastric carcinoma cells induced by genistein. World J. Gastroenterol. 2004; 10, 1822–1825.

75.   Li Y. S., Wu L. P., Li K. H., Liu Y. P., Xiang R., Zhang S. B., Zhu L. Y., Zhang L. Y. Involvement of nuclear factor kappa B (NF-κB) in the down-regulation of cyclooxygenase-2 (COX-2) by genistein in gastric cancer cells. J. Int. Med. Res. 2011; 39, 2141–2150.

76.   Tatsuta M., Iishi H., Baba M., Yano H., Uehara H., Nakaizumi A. Attenuation by genistein of sodium-chloride-enhanced gastric carcinogenesis induced by N-methyl-N’-nitro-N-nitrosoguanidine in Wistar rats. Int. J. Cancer 1999; 80, 396–399.

77.   American Cancer Society © 2016 citované 2017-11-25). Dostupné na: https://www.cancer.org/cancer/pancreatic-cancer/detection-diagnosis-staging/survival-rates.html

78.   Büchler P., Reber H. A., Büchler M. W., Friess H., Lavey R. S., Hines O. J. Antiangiogenic activity of genistein in pancreatic carcinoma cells is mediated by the inhibition of hypoxia-inducible factor-1 and the down-regulation of VEGF gene expression. Cancer 2004; 100, 201–210.

79.   Suzuki R., Kang Y., Li X., Roife D., Zhang R., Fleming J. B. Genistein potentiates the antitumor effect of 5-fluorouracil by inducing apoptosis and autophagy in human pancreatic cancer cells. Anticancer Res. 2014; 34, 4685–4692.

80.   El-Rayes B. F, Ali S., Ali I.F., Philip P. A, Abbruzzese J., Sarkar F. H. Potentiation of the effect of erlotinib by genistein in pancreatic cancer: the role of akt and nuclear factor-KB. Cancer Res. 2006; 66, 10553–10559.

81.   Li Y., Ellis K. L., Ali S., El-Rayes B. F., Nedeljkovic-Kurepa A., Kucuk O., Philip P. A., Sarkar F. H. Apoptosis-inducing effect of chemotherapeutic agents is potentiated by soy isoflavone genistein, a natural inhibitor of NF-kB in BxPC-3 pancreatic cancer cell line. Pancreas 2004; 28, 90–95.

82.   Ma J., Zeng F., Ma C., Pang H., Fang B., Lian C., Yin B., Zhang X., Wang Z., Xia J. Synergistic reversal effect of epithelial-to-mesenchymal transition by miR-223 inhibitor and genistein in gemcitabine-resistant pancreatic cancer cells. Am. J. Cancer Res. 2016; 6, 1384–1395.

83.   Tian T., Li J., Li B., Wang Y., Li M., Ma D., Wang X. Genistein exhibits anti-cancer effects via down-regulating FoxM1 in H446 small- cell lung cancer cells. Tumour Biol. 2014; 35, 4137–4145.

84.   Yang Y., Zang A., Jia Y., Shang Y., Zhang Z., Ge K., Zhang J., Fan W., Wang B. Genistein inhibits A549 human lung cancer cell proliferation via miR-27a and MET signaling. Oncol. Lett. 2016; 12: 2189–2193.

85.   Shiau, R. J., Chen K. Y., Wen Y. D., Chuang C. H., Yeh S. L. Genistein and β-carotene enhance the growth-inhibitory effect of trichostatin A in A549 cells. Eur. J. Nutr. 2010; 49, 19–25.

86.   Cheng J., Qi J., Li X. T., Zhou K., Xu J. H., Zhou Y., Zhang G. Q., Xu J. P., Zhou R. J. ATRA and Genistein synergistically inhibit the metastatic potential of human lung adenocarcinoma cells. Int. J. Clin. Exp. Med. 2015; 8, 4220–4227.

87.   Zhu H., Cheng H., Ren Y., Liu Z. G., Zhang Y. F., De Luo B. Synergistic inhibitory effects by the combination of gefitinib and genistein on NSCLC with acquired drug-resistance in vitro and in vivo. Mol. Biol. Rep. 2012; 39, 4971–4979.

88.   Stupp R., Mason W. P., van den Bent M. J., Weller M., Fisher B., Taphoorn M. J., Belanger K., Brandes A. A., Marosi C., Bogdahn U., Curschmann J., Janzer R. C., Ludwin S. K., Gorlia T., Allgeier A., Lacombe D., Cairncross J. G., Eisenhauer E., Mirimanoff R. O., European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005; 352, 987–996.

89.   Khaw A. K., Yong J. W., Kalthur G., Hande M. P. Genistein Induces Growth Arrest and Suppresses Telomerase Activity in Brain Tumor Cells. Genes Chromosomes Cancer 2012; 51, 961–974.

90.   Belcher S. M., Burton C. C., Cookman C. J., Kirby M., Miranda G. L., Saeed F. O., Wray K. E. Estrogen and soy isoflavonoids decrease sensitivity of medulloblastoma and central nervous system primitive neuroectodermal tumor cells to chemotherapeutic cytotoxicity. BMC Pharmacol. Toxicol. 2017; 18, 63.

91.   Klauser E., Gülden M., Maser E., Seibert S., Seibert H. Additivity, antagonism, and synergy in arsenic trioxide- induced growth inhibition of C6 glioma cells: Effects of genistein, quercetin and buthionine-sulfoximine. Food Chem. Toxicol. 2014; 67, 212–221.

92.   Jeng Y. J., Watson C. S. Proliferative and anti-proliferative effects of dietary levels of phytoestrogens in rat pituitary GH3/B6/F10 cells – the involvement of rapidly activated kinases and caspases. BMC Cancer 2009; 9, 334.

93.   Dvorak H. F. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 1986; 315, 1650–1659.

94.   Dvořánková B., Szabo P., Lacina L., Gál P., Uhrová J., Zima T., Kaltner H., André S., Gabius H. J., Syková E., Smetana Jr. K. Human galectins induce conversion of dermal fibroblasts into myofibroblasts and production of extracellular matrix: Potential application in tissue engineering and wound repair. Cells Tissues Organs 2011; 194, 469–480.

95.   Kolář M., Szabo P., Dvořánková B., Lacina L., Gabius H. J., Strnad H., Sáchová J., Vlček C., Plzák J., Chovanec M., Cada Z., Betka J., Fík Z., Pačes J., Kovářová H., Motlík J., Jarkovská K., Smetana Jr. K. Up-regulation of il-6, il-8 and cxcl-1 production in dermal fibroblasts by normal/malignant epithelial cells in vitro: Immunohistochemical and transcriptomic analyses. Biol. Cell 2012; 104, 738–751.

96.   Lacina L., Plzák J., Kodet O., Szabo P., Chovanec M., Dvořánková B., Smetana Jr. K. Cancer microenvironment: What can we learn from the stem cell niche. Int. J. Mol. Sci. 2015; 16, 24094–24110.

97.   Emmerson E., Campbell L., Ashcroft G. S., Hardman M. J. The phytoestrogen genistein promotes wound healing by multiple independent mechanisms. Mol. Cell Endocrinol. 2010; 321, 184–193.

98.   Ashcroft G. S., Dodsworth J., van Boxtel E., Tarnuzzer R. W., Horan M. A., Schultz G. S., Ferguson M. W. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat. Med. 1997; 3, 1209–1215.

99.   Marini H., Polito F., Altavilla D., Irrera N., Minutoli L., Calò M., Adamo E. B., Vaccaro M., Squadrito F., Bitto A. Genistein aglycone improves skin repair in an incisional model of wound healing: a comparison with raloxifene and oestradiol in ovariectomized rats. Br. J. Pharmacol. 2010; 160, 1185–1194.

100. Renda G., Yalçın F. N., Nemutlu E., Akkol E. K., Süntar I., Keleş H., Ina H., Çalış I., Ersöz T. Comparative assessment of dermal wound healing potentials of various Trifolium L. extracts and determination of their isoflavone contents as potential active ingredients. J. Ethnopharmacol. 2013; 148, 423–432.

101. Jurzak M., Adamczyk K., Antończak P., Garncarczyk A., Kuśmierz D., Latocha M. Evaluation of genistein ability to modulate CTGF mRNA/protein expression, genes expression of TGFβ isoforms and expression of selected genes regulating cell cycle in keloid fibroblasts in vitro. Acta Pol. Pharm. 2014; 71, 972–986.

102. Cao C., Li S., Dai X., Chen Y., Feng Z., Zhao Y., Wu J. Genistein inhibits proliferation and functions of hypertrophic scar fibroblasts. Burns 2009; 35, 89–97.

103. Park E., Lee S. M., Jung I. K., Lim Y., Kim J. H. Effects of genistein on early-stage cutaneous wound healing. Biochem. Biophys. Res. Commun. 2011; 410, 514–519.

104. Eo H., Lee H. J., Lim Y. Ameliorative effect of dietary genistein on diabetes induced hyper- inflammation and oxidative stress during early stage of wound healing in alloxan induced diabetic mice. Biochem. Biophys. Res. Commun. 2016; 478, 1021–1027.

105. van der Veldt A. A., Lammertsma A. A., Smit E. F. Scheduling of anticancer drugs: Timing may be everything. Cell Cycle 2012; 11, 4339–4343.

106. Park J. W., Hwang S. R., Yoon I. S. Advanced growth factor delivery systems in wound management and skin regeneration. Molecules 2017; 22, 1259.

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Pharmacy Clinical pharmacology
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