The Potential of Gallic Acid as a Radiosensitizer on Human Prostate Cancer: A Systematic Review of Preclinical Studies
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Abstract
Prostate adenocarcinoma accounts for majority of prostate cancer cases, and it was found to be highly radioresistant. Gallic acid is a phenolic acid naturally occurring in many plants, reported to exhibit biological activities in eliminat- ing cancer cell lines and xenografts. The purpose of this study is to review gallic acid as a potential radiosensitizer agent in prostate cancer treatment. Article search was conducted in PubMed, EBSCO, and Scopus. 11 studies using different cell lines including DU145, PC-3, LNCaP, and 22Rv1 xenograft of human prostate cancer were reviewed in this paper. Gallic acid acts as a radiosensitizer mainly by increasing caspase-3 and caspase-9 activation resulting in apoptosis, while also reducing intracellular CDKs, cyclins, and cdc25 phosphatases ultimately causing G2-M cell cycle arrest. Gallic acid has a potential to be a new radiosensitizer compound in prostate cancer treatment. Addi- tional clinical studies using gallic acid derivatives with lower hydrophilicity are needed.
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Athankar KK, Wasewar KL, Varma MN, Shende DZ. Reactive extraction of gallic acid with tri-n-caprylylamine. New J Chem. 2016 Mar 8;40(3):2413–7.
Kim D-O, Lee KW, Lee HJ, Lee CY. Vitamin C Equivalent Antioxidant Capacity (VCEAC) of Phenolic Phytochemicals. J Agric Food Chem. 2002 Jun 1;50(13):3713–7.
Yen G-C, Duh P-D, Tsai H-Ls. Antioxidant and pro-oxidant properties of ascorbic acid and gallic acid. Food Chem. 2002 Nov 1;79(3):307–13.
Rusell LH, Mazzio E, Badisa RB, Zhu Z-P, Agharahimi M, Millington DJ, et al. Differential Cytotoxicity of Triphala and its Phenolic Constituent Gallic acid on Human Prostate Cancer LNCap and Normal Cells. Anticancer Res. 2011 Nov;31(11):3739–45.
Kaur M, Velmurugan B, Rajamanickam S, Agarwal R, Agarwal C. Gallic Acid, an Active Constituent of Grape Seed Extract, Exhibits Anti-proliferative, Pro- apoptotic and Anti-tumourigenic Effects Against Prostate Carcinoma Xenograft Growth in Nude Mice. Pharm Res. 2009 Sep;26(9):2133–40.
Eghbaliferiz S, Iranshahi M. Prooxidant Activity of Polyphenols, Flavonoids, Anthocyanins and Carotenoids: Updated Review of Mechanisms and Catalyzing Metals. Phytother Res. 2016;30(9):1379–91.
Dorniani D, Bullo S, Barahuie F, Arulselvan P, Hussein M, Fakurazi S, et al. Graphene Oxide- Gallic Acid Nanodelivery System for Cancer Therapy. Nanoscale Res Lett. 2016 Nov 1;11.
Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: a Review. Ann Bot. 2003 Jan 2;91(2):179–94.
Noctor G, Arisi A-CM, Jouanin L, Foyer CH. Manipulation of Glutathione and Amino Acid Biosynthesis in the Chloroplast. Plant Physiol. 1998 Oct;118(2):471–82.
Strlic M, Radovic T, Kolar J, Pihlar B. Anti- and Prooxidative Properties of Gallic Acid in Fenton- Type Systems. J Agric Food Chem. 2002 Nov 1;50:6313–7.
Pernar CH, Ebot EM, Wilson KM, Mucci LA. The Epidemiology of Prostate Cancer. Cold Spring Harb Perspect Med. 2018 Dec 1;8(12):a030361.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.
Ward MC, Tendulkar RD, Videtic GMM. Essentials of Clinical Radiation Oncology. Springer Publishing Company; 2017.
Ahlering Thomas E., Lieskovsky Gary, Skinner Donald G. Salvage Surgery Plus Androgen Deprivation for Radioresistant Prostatic Adenocarcinoma. J Urol. 1992 Mar 1;147(3 Part 2):900–2.
Crawford ED. Understanding the Epidemiology, Natural History, and Key Pathways Involved in Prostate Cancer. Urology. 2009 May 1;73(5, Supplement):S4–10.
Kim YS, Kang MJ, Cho YM. Low Production of Reactive Oxygen Species and High DNA Repair: Mechanism of Radioresistance of Prostate Cancer Stem Cells. Anticancer Res. 2013 Oct 1;33(10):4469–74.
Yajun C, Yuan T, Zhong W, Bin X. Investigation of the molecular mechanisms underlying postoperative recurrence in prostate cancer by gene expression profiling. Exp Ther Med. 2017 Dec 31;15(1):761–8.
Liu S-G, Li H-C, Zhao B-S, Cao F. Expression of activin A in tissue and serum of patients with esophageal squamous cell carcinoma and its clinical significance. Chin J Oncol. 2013 Nov 1;35(11):843–7.
Mehta PB, Jenkins BL, McCarthy L, Thilak L, Robson CN, Neal DE, et al. MEK5 overexpression is associated with metastatic prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. Oncogene. 2003 Mar;22(9):1381–9.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group TP. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLOS Med. 2009 Jul 21;6(7):e1000097.
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009 Dec 4;339(jul21 1):b2700–b2700.
Perez-Cornago A, Travis RC, Appleby PN, Tsilidis KK, Tjønneland A, Olsen A, et al. Fruit and vegetable intake and prostate cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Int J Cancer. 2017;141(2):287–97.
Tang HM, Cheung PCK. Gallic Acid Triggers Iron- Dependent Cell Death with Apoptotic, Ferroptotic, and Necroptotic Features. Toxins. 2019 26;11(9).
Agarwal C, Tyagi A, Agarwal R. Gallic acid causes inactivating phosphorylation of cdc25A/cdc25C- cdc2 via ATM-Chk2 activation, leading to cell cycle arrest, and induces apoptosis in human prostate carcinoma DU145 cells. Mol Cancer Ther. 2006 Dec 1;5(12):3294–302.
Chen H-M, Wu Y-C, Chia Y-C, Chang F-R, Hsu H-K, Hsieh Y-C, et al. Gallic acid, a major component of Toona sinensis leaf extracts, contains a ROS- mediated anti-cancer activity in human prostate cancer cells. Cancer Lett. 2009 Dec;286(2):161– 71.
Heidarian E, Keloushadi M, Ghatreh-Samani K, Jafari-Dehkordi E. Gallic Acid Inhibits Invasion and Reduces IL-6 Gene Expression, pSTAT3, pERK1/2, and pAKT Cellular Signaling Proteins in Human Prostate Cancer DU-145 Cells. Int J Cancer Manag. 2017;10(11).
Meng M. Gallic acid suppresses the migration and invasion of PC-3 human prostate cancer cells via inhibition of matrix metalloproteinase-2 and -9 signaling pathways. Oncol Rep. 2011;26:177–84
Heidarian E, Keloushadi M, Ghatreh-Samani K, Valipour P. The reduction of IL-6 gene expression, pAKT, pERK1/2, pSTAT3 signaling pathways and invasion activity by gallic acid in prostate cancer PC3 cells. Biomed Pharmacother. 2016 Dec;84:264–9.
Liu K-C, Ho H-C, Huang A-C, Ji B-C, Lin H-Y, Chueh F-S, et al. Gallic acid provokes DNA damage and suppresses DNA repair gene expression in human prostate cancer PC-3 cells: GA Affects DNA Damage and Repair Gene in PC-3 Cells. Environ Toxicol. 2013 Oct;28(10):579–87.
Saffari-Chaleshtori J, Heidari-Sureshjani E, Moradi F, Jazi HM, Heidarian E. The Study of Apoptosis- inducing Effects of Three Pre-apoptotic Factors by Gallic Acid, Using Simulation Analysis and the Comet Assay Technique on the Prostatic Cancer Cell Line PC3. Malays J Med Sci. 2017;24(4):18– 29.
Veluri R, Singh RP, Liu Z, Thompson JA, Agarwal R, Agarwal C. Fractionation of grape seed extract and identification of gallic acid as one of the major active constituents causing growth inhibition and apoptotic death of DU145 human prostate carcinoma cells. Carcinogenesis. 2006 Jul 1;27(7):1445–53. .
Russell LH, Mazzio E, Badisa RB, Zhu Z-P, Agharahimi M, Oriaku ET, et al. Autoxidation of Gallic acid Induces ROS-dependant Death in Human Prostate Cancer LNCaP Cells. Anticancer Res. 2012 May;32(5):1595–602.
McArthur K, Kile BT. Apoptotic Caspases: Multiple or Mistaken Identities? Trends Cell Biol. 2018 Jun 1;28(6):475–93.
Santos NFGD, Silva RF, Pinto MMPL, Silva EBD, Tasat DR, Amaral A, et al. Active caspase-3 expression levels as bioindicator of individual radiosensitivity. An Acad Bras Ciênc. 2017 May;89(1):649–59.
Zhao P-J, Song S-C, Du L-W, Zhou G-H, Ma S-L, Li J-H, et al. Paris Saponins enhance radiosensitivity in a gefitinib-resistant lung adenocarcinoma cell line by inducing apoptosis and G2/M cell cycle phase arrest. Mol Med Rep. 2016 Mar 1;13(3):2878–84.
Chetty C, Bhoopathi P, Rao JS, Lakka SS. Inhibition of matrix metalloproteinase-2 enhances radiosensitivity by abrogating radiation-induced FoxM1-mediated G2/M arrest in A549 lung cancer cells. Int J Cancer. 2009;124(10):2468–77.
Otto T, Sicinski P. Cell cycle proteins as promising targets in cancer therapy. Nat Rev Cancer. 2017 Feb;17(2):93–115.
Göttgens E-L, Bussink J, Leszczynska KB, Peters H, Span PN, Hammond EM. Inhibition of CDK4/ CDK6 Enhances Radiosensitivity of HPV Negative Head and Neck Squamous Cell Carcinomas. Int J Radiat Oncol. 2019 Nov 1;105(3):548–58.
Ding F-N, Gao B-H, Wu X, Gong C-W, Wang W-Q, Zhang S-M. miR-122-5p modulates the radiosensitivity of cervical cancer cells by regulating cell division cycle 25A (CDC25A). FEBS Open Bio. 2019;9(11):1869–79.
Sur S, Agrawal DK. Phosphatases and kinases regulating CDC25 activity in the cell cycle: clinical implications of CDC25 overexpression and potential treatment strategies. Mol Cell Biochem. 2016 May 1;416(1):33–46.
Liu L, Guo K, Liang Z, Li F, Wang H. Identification of candidate genes that may contribute to the metastasis of prostate cancer by bioinformatics analysis. Oncol Lett. 2018 Jan 1;15(1):1220–8.
Zhang X, Peng L, Liu A, Ji J, Zhao L, Zhai G. The enhanced effect of tetrahydrocurcumin on radiosensitivity of glioma cells. J Pharm Pharmacol. 2018;70(6):749–59.
Sha J, Li J, Wang W, Pan L, Cheng J, Li L, et al. Curcumin induces G0/G1 arrest and apoptosis in hormone independent prostate cancer DU-145 cells by down regulating Notch signaling. Biomed Pharmacother. 2016 Dec 1;84:177–84.
Gondhowiardjo S. Apoptosis, angiogenesis and radiation treatment. Acta Medica Indones. 2004 Jun;36(2):100–8.
Kuwana T, King L, Cosentino K, Suess J, Garcia- Saez A, Gilmore AP, et al. Bax mitochondrial residency is more critical than Bax oligomerization for apoptosis. bioRxiv. 2019 Apr 29;618868.
Adams JM, Cory S. The BCL-2 arbiters of apoptosis and their growing role as cancer targets. Cell Death Differ. 2018 Jan;25(1):27–36.
Kuwana T, Newmeyer DD. Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol. 2003 Dec;15(6):691–9.
Choi S, Chen Z, Tang LH, Fang Y, Shin SJ, Panarelli NC, et al. Bcl-xL promotes metastasis independent of its anti-apoptotic activity. Nat Commun. 2016 Jan 20;7(1):10384.
Zhang Z, Jin F, Lian X, Li M, Wang G, Lan B, et al. Genistein promotes ionizing radiation-induced cell death by reducing cytoplasmic Bcl-xL levels in non-small cell lung cancer. Sci Rep. 2018 Jan 10;8(1):328.
Qin C, Chen X, Bai Q, Davis MR, Fang Y. Factors associated with radiosensitivity of cervical cancer. Anticancer Res. 2014 Sep;34(9):4649–56.
Azimian H, Dayyani M, Toossi MTB, Mahmoudi M. Bax/Bcl-2 expression ratio in prediction of response to breast cancer radiotherapy. Iran J Basic Med Sci. 2018 Mar;21(3):325–32.
Li H, Qiu Z, Li F, Wang C. The relationship between MMP-2 and MMP-9 expression levels with breast cancer incidence and prognosis. Oncol Lett. 2017 Oct 31;14(5):5865–70.
Zhang W, Wang F, Xu P, Miao C, Zeng X, Cui X, et al. Perfluorooctanoic acid stimulates breast cancer cells invasion and up-regulates matrix metalloproteinase-2/-9 expression mediated by activating NF-κB. Toxicol Lett. 2014 Aug 17;229(1):118–25.
Ko YS, Jin H, Lee JS, Park SW, Chang KC, Kang KM, et al. Radioresistant breast cancer cells exhibit increased resistance to chemotherapy and enhanced invasive properties due to cancer stem cells. Oncol Rep. 2018 Dec 1;40(6):3752–62.
Hennessy BT, Gonzalez-Angulo A-M, Stemke- Hale K, Gilcrease MZ, Krishnamurthy S, Lee J-S, et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res. 2009 May 15;69(10):4116–24.
Sugano H, Shirai Y, Horiuchi T, Saito N, Shimada Y, Eto K, et al. Nafamostat Mesilate Enhances the Radiosensitivity and Reduces the Radiation- Induced Invasive Ability of Colorectal Cancer Cells. Cancers. 2018 Oct;10(10):386.
Permata TBM, Hagiwara Y, Sato H, Yasuhara T, Oike T, Gondhowiardjo S, et al. Base excision repair regulates PD-L1 expression in cancer cells. Oncogene. 2019 Jun;38(23):4452–66.
Lavin MF. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene. 2007 Dec 10;26(56):7749–58.
Koh HK, Seo SY, Kim JH, Kim HJ, Chie EK, Kim S-K, et al. Disulfiram, a Re-positioned Aldehyde Dehydrogenase Inhibitor, Enhances Radiosensitivity of Human Glioblastoma Cells In Vitro. Cancer Res Treat Off J Korean Cancer Assoc. 2019 Apr;51(2):696–705.
Timme CR, Rath BH, O’Neill JW, Camphausen K, Tofilon PJ. The DNA-PK Inhibitor VX-984 Enhances the Radiosensitivity of Glioblastoma Cells Grown In Vitro and as Orthotopic Xenografts. Mol Cancer Ther. 2018 Jun 1;17(6):1207–16.
Chun JY, Tummala R, Nadiminty N, Lou W, Liu C, Yang J, et al. Andrographolide, an Herbal Medicine, Inhibits Interleukin-6 Expression and Suppresses Prostate Cancer Cell Growth. Genes Cancer. 2010 Aug;1(8):868–76.
Matsuoka Y, Nakayama H, Yoshida R, Hirosue A, Nagata M, Tanaka T, et al. IL-6 controls resistance to radiation by suppressing oxidative stress via the Nrf2-antioxidant pathway in oral squamous cell carcinoma. Br J Cancer. 2016 Nov;115(10):1234– 44.
Geiger JL, Grandis JR, Bauman JE. The STAT3 pathway as a therapeutic target in head and neck cancer: Barriers and innovations. Oral Oncol. 2016 May 1;56:84–92.
Das TP, Suman S, Papu John AMS, Pal D, Edwards A, Alatassi H, et al. Activation of AKT negatively regulates the pro-apoptotic function of death- associated protein kinase 3 (DAPK3) in prostate cancer. Cancer Lett. 2016 Jul 28;377(2):134–9.
Oeck S, Al-Refae K, Riffkin H, Wiel G, Handrick R, Klein D, et al. Activating Akt1 mutations alter DNA double strand break repair and radiosensitivity. Sci Rep. 2017 Feb 17;7(1):42700.
Kuwahara Y, Tomita K, Urushihara Y, Sato T, Kurimasa A, Fukumoto M. Association between radiation-induced cell death and clinically relevant radioresistance. Histochem Cell Biol. 2018 Dec 1;150(6):649–59.
Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell. 2011 Nov 11;147(4):742–58.
Golden EB, Pellicciotta I, Demaria S, Barcellos-Hoff MH, Formenti SC. The convergence of radiation and immunogenic cell death signaling pathways. Front Oncol. 2012;2:88.
Gudkov AV, Komarova EA. The role of p53 in determining sensitivity to radiotherapy. Nat Rev Cancer. 2003 Feb;3(2):117–29.
Dornan D, Shimizu H, Perkins ND, Hupp TR. DNA-dependent acetylation of p53 by the transcription coactivator p300. J Biol Chem. 2003 Apr 11;278(15):13431–41
Kuribayashi K, Finnberg N, Jeffers JR, Zambetti GP, El-Deiry WS. The relative contribution of pro-apoptotic p53-target genes in the triggering of apoptosis following DNA damage in vitro and in vivo. Cell Cycle Georget Tex. 2011 Jul 15;10(14):2380–9.
Ridolfi R. Study of the track reconstruction in the FOOT experiment for Hadrontherapy. 2018.
Brandsma I, Gent DC. Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integr. 2012 Nov 27;3:9.
Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004 Jul 15;59(4):928–42.
Brown JM, Carlson DJ, Brenner DJ. The Tumour Radiobiology of SRS and SBRT: Are More Than the 5 Rs Involved? Int J Radiat Oncol. 2014 Feb 1;88(2):254–62.
Lesueur P, Chevalier F, Austry J-B, Waissi W, Burckel H, Noël G, et al. Poly-(ADP-ribose)-polymerase inhibitors as radiosensitizers: a systematic review of pre-clinical and clinical human studies. Oncotarget. 2017 Jul 7;8(40):69105–24.
Paramita RI, Arsianti A, Radji M. Synthesis and Cytotoxic Activities of Hexyl Esters Derivatives of Gallic Acid Against MCF-7 Cell line. Orient J Chem. 2018 Feb 19;34(1):295–300.
Ulfa DM, Arsianti A, Radji M. In Silico Docking Studies of Gallic Acid Structural Analogues as Bcl- xL Inhibitor in Cancer. Asian J Pharm Clin Res. 2017 Apr 1;10(4):119.