Role of GDF15 in methylseleninic acid-mediated inhibition of cell proliferation and induction of apoptosis in prostate cancer cells
Autoři:
Wenbo Zhang aff001; Cheng Hu aff001; Xiaojie Wang aff001; Shanshan Bai aff001; Subing Cao aff002; Margaret Kobelski aff002; James R. Lambert aff003; Jingkai Gu aff001; Yang Zhan aff001
Působiště autorů:
National Engineering Laboratory for AIDS Vaccine, School of Life Sciences, Jilin University, Changchun, Jilin, China
aff001; Department of Structural and Cellular Biology, Tulane Cancer Center, School of Medicine, Tulane University, New Orleans, Louisiana, United States of America
aff002; Department of Pathology, University of Colorado School of Medicine, Aurora, Colorado, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222812
Souhrn
The growth inhibitory efficacy of methylseleninic acid (MSA) in prostate cancer cells has been documented extensively. However, our understanding of the immediate targets that are key to the growth inhibitory effects of MSA remains limited. Here, using multiple preclinical prostate cancer models, we demonstrated in vitro and in vivo that GDF15 is a most highly induced, immediate target of MSA. We further showed that knockdown of GDF15 mitigates MSA inhibition of cell proliferation and induction of apoptosis. Analysis of gene expression data from over 1000 primary and 200 metastatic prostate cancer samples revealed that GDF15 expression is decreased in metastatic prostate cancers compared to primary tumors and that lower GDF15 levels in primary tumors are associated with higher Gleason scores and shorter survival of the patients. Additionally, pathways that are negatively correlated with GDF15 levels in clinical samples are also negatively correlated with MSA treatment in cultured cells. Since most, if not all, of these pathways have been implicated in prostate cancer progression, suppressing their activities by inducing GDF15 is consistent with the anticancer effects of MSA in prostate cancer. Overall, this study provides support for GDF15 as an immediate target of MSA in prostate cancer cells.
Klíčová slova:
Biology and life sciences – Cell biology – Physical sciences – Chemistry – Research and analysis methods – Cell processes – Anatomy – Medicine and health sciences – Urology – Oncology – Cancer treatment – Cancers and neoplasms – Cell death – Chemical elements – Immunologic techniques – Immunoassays – Enzyme-linked immunoassays – Apoptosis – Bioassays and physiological analysis – Microarrays – Exocrine glands – Cell proliferation – Genitourinary tract tumors – Prostate cancer – Prostate diseases – Prostate gland – Selenium
Zdroje
1. Knudsen KE, Scher HI. Starving the addiction: new opportunities for durable suppression of AR signaling in prostate cancer. ClinCancer Res. 2009;15(15):4792–8.
2. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus Prednisone or Mitoxantrone plus Prednisone for Advanced Prostate Cancer. New England Journal of Medicine. 2004;351(15):1502–12. doi: 10.1056/NEJMoa040720 15470213
3. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet. 2010;376(9747):1147–54. doi: 10.1016/S0140-6736(10)61389-X 20888992
4. Fizazi K, Scher HI, Molina A, Logothetis CJ, Chi KN, Jones RJ, et al. Abiraterone acetate for treatment of metastatic castration-resistant prostate cancer: final overall survival analysis of the COU-AA-301 randomised, double-blind, placebo-controlled phase 3 study. Lancet Oncol. 2012;13(10):983–92. doi: 10.1016/S1470-2045(12)70379-0 22995653
5. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. NEnglJMed. 2012;367(13):1187–97.
6. Cho SD, Jiang C, Malewicz B, Dong Y, Young CY, Kang KS, et al. Methyl selenium metabolites decrease prostate-specific antigen expression by inducing protein degradation and suppressing androgen-stimulated transcription. MolCancer Ther. 2004;3(5):605–11.
7. Dong Y, Lee SO, Zhang H, Marshall J, Gao AC, Ip C. Prostate specific antigen expression is down-regulated by selenium through disruption of androgen receptor signaling. Cancer Res. 2004;64(1):19–22. 14729601
8. Dong Y, Zhang H, Hawthorn L, Ganther HE, Ip C. Delineation of the Molecular Basis for Selenium-induced Growth Arrest in Human Prostate Cancer Cells by Oligonucleotide Array. Cancer Research. 2003;63(1):52–9. 12517777
9. Gasparian AV, Yao YJ, Lu J, Yemelyanov AY, Lyakh LA, Slaga TJ, et al. Selenium compounds inhibit I kappa B kinase (IKK) and nuclear factor-kappa B (NF-kappa B) in prostate cancer cells. MolCancer Ther. 2002;1(12):1079–87.
10. Gundimeda U, Schiffman JE, Chhabra D, Wong J, Wu A, Gopalakrishna R. Locally generated methylseleninic acid induces specific inactivation of protein kinase C isoenzymes: relevance to selenium-induced apoptosis in prostate cancer cells. J Biol Chem. 2008;283(50):34519–31. doi: 10.1074/jbc.M807007200 18922790.
11. Jiang C, Wang Z, Ganther H, Lu J. Caspases as key executors of methyl selenium-induced apoptosis (anoikis) of DU-145 prostate cancer cells. Cancer Res. 2001;61(7):3062–70. 11306488
12. Lee SO, Yeon CJ, Nadiminty N, Trump DL, Ip C, Dong Y, et al. Monomethylated selenium inhibits growth of LNCaP human prostate cancer xenograft accompanied by a decrease in the expression of androgen receptor and prostate-specific antigen (PSA). The Prostate. 2006;66(10):1070–5. doi: 10.1002/pros.20329 16637076
13. Li GX, Lee HJ, Wang Z, Hu H, Liao JD, Watts JC, et al. Superior in vivo inhibitory efficacy of methylseleninic acid against human prostate cancer over selenomethionine or selenite. Carcinogenesis. 2008;29(5):1005–12. doi: 10.1093/carcin/bgn007 18310093
14. Liu Y, Liu X, Guo Y, Liang Z, Tian Y, Lu L, et al. Methylselenocysteine preventing castration-resistant progression of prostate cancer. Prostate. 2015;75(9):1001–8. doi: 10.1002/pros.22987 25754033.
15. Pinto JT, Sinha R, Papp K, Facompre ND, Desai D, El-Bayoumy K. Differential effects of naturally occurring and synthetic organoselenium compounds on biomarkers in androgen responsive and androgen independent human prostate carcinoma cells. Int J Cancer. 2007;120(7):1410–7. doi: 10.1002/ijc.22500 17205524.
16. Wang L, Bonorden MJ, Li GX, Lee HJ, Hu H, Zhang Y, et al. Methyl-selenium compounds inhibit prostate carcinogenesis in the transgenic adenocarcinoma of mouse prostate model with survival benefit. Cancer PrevRes(Phila Pa). 2009;2(5):484–95.
17. Wang L, Guo X, Wang J, Jiang C, Bosland MC, Lu J, et al. Methylseleninic Acid Superactivates p53-Senescence Cancer Progression Barrier in Prostate Lesions of Pten-Knockout Mouse. Cancer Prev Res (Phila). 2016;9(1):35–42. doi: 10.1158/1940-6207.CAPR-15-0236 26511486.
18. Wang L, Zhang J, Zhang Y, Nkhata K, Quealy E, Liao JD, et al. Lobe-specific lineages of carcinogenesis in the transgenic adenocarcinoma of mouse prostate and their responses to chemopreventive selenium. Prostate. 2011;71(13):1429–40. doi: 10.1002/pros.21360 21360561.
19. Wu Y, Zhang H, Dong Y, Park YM, Ip C. Endoplasmic reticulum stress signal mediators are targets of selenium action. Cancer Res. 2005;65(19):9073–9. doi: 10.1158/0008-5472.CAN-05-2016 16204082
20. Zhan Y, Cao B, Qi Y, Liu S, Zhang Q, Zhou W, et al. Methylselenol prodrug enhances MDV3100 efficacy for treatment of castration-resistant prostate cancer. Int J Cancer. 2013;133(9):2225–33. doi: 10.1002/ijc.28202 23575870
21. Zhang H, Dong Y, Zhao H, Brooks JD, Hawthorn L, Nowak N, et al. Microarray data mining for potential selenium targets in chemoprevention of prostate cancer. Cancer Genomics and Proteomics. 2005;2:97–114. 18548127
22. Zhao H, Whitfield ML, Xu T, Botstein D, Brooks JD. Diverse effects of methylseleninic acid on the transcriptional program of human prostate cancer cells. MolBiolCell. 2004;15(2):506–19.
23. Sinha I, Allen JE, Pinto JT, Sinha R. Methylseleninic acid elevates REDD1 and inhibits prostate cancer cell growth despite AKT activation and mTOR dysregulation in hypoxia. Cancer Med. 2014;3(2):252–64. doi: 10.1002/cam4.198 24515947.
24. Sinha I, Null K, Wolter W, Suckow MA, King T, Pinto JT, et al. Methylseleninic acid downregulates hypoxia-inducible factor-1alpha in invasive prostate cancer. Int J Cancer. 2012;130(6):1430–9. doi: 10.1002/ijc.26141 21500193.
25. Marshall JR, Burk RF, Payne Ondracek R, Hill KE, Perloff M, Davis W, et al. Selenomethionine and methyl selenocysteine: multiple-dose pharmacokinetics in selenium-replete men. Oncotarget. 2017;8(16):26312–22. doi: 10.18632/oncotarget.15460 28412747.
26. Ip C, Thompson HJ, Zhu Z, Ganther HE. In vitro and in vivo studies of methylseleninic acid: evidence that a monomethylated selenium metabolite is critical for cancer chemoprevention. Cancer Res. 2000;60(11):2882–6. 10850432
27. Ip C. Lessons from basic research in selenium and cancer prevention. J Nutr. 1998;128(11):1845–54. doi: 10.1093/jn/128.11.1845 9808633
28. Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, et al. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA. 2009;301(1):39–51. doi: 10.1001/jama.2008.864 19066370
29. Ohta Y, Kobayashi Y, Konishi S, Hirano S. Speciation analysis of selenium metabolites in urine and breath by HPLC- and GC-inductively coupled plasma-MS after administration of selenomethionine and methylselenocysteine to rats. ChemRes Toxicol. 2009;22(11):1795–801.
30. Wang X, Baek SJ, Eling TE. The diverse roles of nonsteroidal anti-inflammatory drug activated gene (NAG-1/GDF15) in cancer. Biochem Pharmacol. 2013;85(5):597–606. doi: 10.1016/j.bcp.2012.11.025 23220538.
31. Klein KA, Reiter RE, Redula J, Moradi H, Zhu XL, Brothman AR, et al. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. NatMed. 1997;3(4):402–8.
32. Robinson D, Van Allen EM, Wu YM, Schultz N, Lonigro RJ, Mosquera JM, et al. Integrative clinical genomics of advanced prostate cancer. Cell. 2015;161(5):1215–28. doi: 10.1016/j.cell.2015.05.001 26000489
33. Wang L, Dehm SM, Hillman DW, Sicotte H, Tan W, Gormley M, et al. A prospective genome-wide study of prostate cancer metastases reveals association of wnt pathway activation and increased cell cycle proliferation with primary resistance to abiraterone acetate-prednisone. Ann Oncol. 2018;29(2):352–60. doi: 10.1093/annonc/mdx689 29069303.
34. Beltran H, Prandi D, Mosquera JM, Benelli M, Puca L, Cyrta J, et al. Divergent clonal evolution of castration-resistant neuroendocrine prostate cancer. Nat Med. 2016;22(3):298–305. doi: 10.1038/nm.4045 26855148.
35. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMCBioinformatics. 2011;12:323.
36. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature. 2012;487(7406):239–43. doi: 10.1038/nature11125 22722839
37. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell. 2010;18(1):11–22. doi: 10.1016/j.ccr.2010.05.026 20579941
38. Erho N, Crisan A, Vergara IA, Mitra AP, Ghadessi M, Buerki C, et al. Discovery and validation of a prostate cancer genomic classifier that predicts early metastasis following radical prostatectomy. PLoS One. 2013;8(6):e66855. doi: 10.1371/journal.pone.0066855 23826159.
39. Piccolo SR, Sun Y, Campbell JD, Lenburg ME, Bild AH, Johnson WE. A single-sample microarray normalization method to facilitate personalized-medicine workflows. Genomics. 2012;100(6):337–44. doi: 10.1016/j.ygeno.2012.08.003 22959562.
40. Latonen L, Afyounian E, Jylha A, Nattinen J, Aapola U, Annala M, et al. Integrative proteomics in prostate cancer uncovers robustness against genomic and transcriptomic aberrations during disease progression. Nat Commun. 2018;9(1):1176. doi: 10.1038/s41467-018-03573-6 29563510.
41. Appierto V, Villani MG, Cavadini E, Gariboldi M, De Cecco L, Pierotti MA, et al. Analysis of gene expression identifies PLAB as a mediator of the apoptotic activity of fenretinide in human ovarian cancer cells. Oncogene. 2007;26(27):3952–62. doi: 10.1038/sj.onc.1210171 17213814.
42. Min KW, Liggett JL, Silva G, Wu WW, Wang R, Shen RF, et al. NAG-1/GDF15 accumulates in the nucleus and modulates transcriptional regulation of the Smad pathway. Oncogene. 2016;35(3):377–88. doi: 10.1038/onc.2015.95 25893289.
43. Emmerson PJ, Wang F, Du Y, Liu Q, Pickard RT, Gonciarz MD, et al. The metabolic effects of GDF15 are mediated by the orphan receptor GFRAL. Nat Med. 2017;23(10):1215–9. doi: 10.1038/nm.4393 28846098.
44. Vanhara P, Hampl A, Kozubik A, Soucek K. Growth/differentiation factor-15: prostate cancer suppressor or promoter? Prostate Cancer Prostatic Dis. 2012;15(4):320–8. doi: 10.1038/pcan.2012.6 22370725.
45. Cheng JC, Chang HM, Leung PC. Wild-type p53 attenuates cancer cell motility by inducing growth differentiation factor-15 expression. Endocrinology. 2011;152(8):2987–95. doi: 10.1210/en.2011-0059 21586550.
46. Kelly JA, Lucia MS, Lambert JR. p53 controls prostate-derived factor/macrophage inhibitory cytokine/NSAID-activated gene expression in response to cell density, DNA damage and hypoxia through diverse mechanisms. Cancer Lett. 2009;277(1):38–47. doi: 10.1016/j.canlet.2008.11.013 19100681.
47. Kakehi Y, Segawa T, Wu XX, Kulkarni P, Dhir R, Getzenberg RH. Down-regulation of macrophage inhibitory cytokine-1/prostate derived factor in benign prostatic hyperplasia. Prostate. 2004;59(4):351–6. doi: 10.1002/pros.10365 15065082.
48. Smith ML, Lancia JK, Mercer TI, Ip C. Selenium compounds regulate p53 by common and distinctive mechanisms. Anticancer Res. 2004;24(3a):1401–8. 15274301
49. Park SH, Choi HJ, Yang H, Do KH, Kim J, Kim HH, et al. Two in-and-out modulation strategies for endoplasmic reticulum stress-linked gene expression of pro-apoptotic macrophage-inhibitory cytokine 1. J Biol Chem. 2012;287(24):19841–55. doi: 10.1074/jbc.M111.330639 22511768.
50. Lambert JR, Whitson RJ, Iczkowski KA, La Rosa FG, Smith ML, Wilson RS, et al. Reduced expression of GDF-15 is associated with atrophic inflammatory lesions of the prostate. Prostate. 2015;75(3):255–65. doi: 10.1002/pros.22911 25327758.
51. Husaini Y, Lockwood GP, Nguyen TV, Tsai VW, Mohammad MG, Russell PJ, et al. Macrophage inhibitory cytokine-1 (MIC-1/GDF15) gene deletion promotes cancer growth in TRAMP prostate cancer prone mice. PLoS One. 2015;10(2):e0115189. doi: 10.1371/journal.pone.0115189 25695521.
52. Cheung PK, Woolcock B, Adomat H, Sutcliffe M, Bainbridge TC, Jones EC, et al. Protein profiling of microdissected prostate tissue links growth differentiation factor 15 to prostate carcinogenesis. Cancer Res. 2004;64(17):5929–33. doi: 10.1158/0008-5472.CAN-04-1216 15342369.
53. Li J, Veltri RW, Yuan Z, Christudass CS, Mandecki W. Macrophage inhibitory cytokine 1 biomarker serum immunoassay in combination with PSA is a more specific diagnostic tool for detection of prostate cancer. PLoS One. 2015;10(4):e0122249. doi: 10.1371/journal.pone.0122249 25853582.
54. Hood BL, Darfler MM, Guiel TG, Furusato B, Lucas DA, Ringeisen BR, et al. Proteomic analysis of formalin-fixed prostate cancer tissue. Mol Cell Proteomics. 2005;4(11):1741–53. doi: 10.1074/mcp.M500102-MCP200 16091476.
55. Lambert JR, Kelly JA, Shim M, Huffer WE, Nordeen SK, Baek SJ, et al. Prostate derived factor in human prostate cancer cells: gene induction by vitamin D via a p53-dependent mechanism and inhibition of prostate cancer cell growth. J Cell Physiol. 2006;208(3):566–74. doi: 10.1002/jcp.20692 16741990.
56. Liu T, Bauskin AR, Zaunders J, Brown DA, Pankhurst S, Russell PJ, et al. Macrophage inhibitory cytokine 1 reduces cell adhesion and induces apoptosis in prostate cancer cells. Cancer Res. 2003;63(16):5034–40. 12941831.
57. Senapati S, Rachagani S, Chaudhary K, Johansson SL, Singh RK, Batra SK. Overexpression of macrophage inhibitory cytokine-1 induces metastasis of human prostate cancer cells through the FAK-RhoA signaling pathway. Oncogene. 2010;29(9):1293–302. doi: 10.1038/onc.2009.420 19946339.
58. Chen SJ, Karan D, Johansson SL, Lin FF, Zeckser J, Singh AP, et al. Prostate-derived factor as a paracrine and autocrine factor for the proliferation of androgen receptor-positive human prostate cancer cells. Prostate. 2007;67(5):557–71. doi: 10.1002/pros.20551 17221842.
59. Tsui KH, Chang YL, Feng TH, Chung LC, Lee TY, Chang PL, et al. Growth differentiation factor-15 upregulates interleukin-6 to promote tumorigenesis of prostate carcinoma PC-3 cells. J Mol Endocrinol. 2012;49(2):153–63. doi: 10.1530/JME-11-0149 22872134.
60. Rasiah KK, Kench JG, Gardiner-Garden M, Biankin AV, Golovsky D, Brenner PC, et al. Aberrant neuropeptide Y and macrophage inhibitory cytokine-1 expression are early events in prostate cancer development and are associated with poor prognosis. Cancer Epidemiol Biomarkers Prev. 2006;15(4):711–6. doi: 10.1158/1055-9965.EPI-05-0752 16614113.
61. Kawahara T, Ishiguro H, Hoshino K, Teranishi J, Miyoshi Y, Kubota Y, et al. Analysis of NSAID-activated gene 1 expression in prostate cancer. Urol Int. 2010;84(2):198–202. doi: 10.1159/000277599 20215826.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania