Research Article
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The Senescence Program is Reduced in Proteasome Inhibitor Bortezomib-Resistant PC3 Prostate Cancer Cell Line

Year 2023, Volume: 82 Issue: 1, 49 - 58, 26.06.2023

Abstract

Objective: Senescence may act as an antitumor mechanism by preventing the proliferation of cancer cells. Here we investigated the hypothesis that PC3 prostate cancer cells resistant to bortezomib respond differently to proteasomal inhibition with respect to induction of the senescence program as compared to the parental cells.
Materials and Methods: The degree of senescence was measured by 𝛽-galactosidase activity and the level of senescenceassociated p16 INK4a by Western blotting after treatment of cells with varying concentrations of bortezomib. In addition, the senescence-associated secretory phenotype was analyzed by Human Cytokine Antibody Array.
Results: It is reported that the basal level of senescence was lower in resistant cells compared to non-resistant cells. It was found that the basal level of the senescence marker p16 INK4a was lower in bortezomib-resistant cells than in parent non-resistant cells. Moreover, p16 INK4a was significantly reduced in both cells under conditions of 100 nM bortezomib treatment, a finding suggesting that the reduced senescence after proteasomal inhibition was likely due to the reduced levels of p16 INK4a. Finally, it is reported here for the first time that basal levels of the proteins NAP2, FGF-6, MIP-3𝛼, and PARC are significantly increased in the resistant cells compared to the parental cells.
Conclusion: Overall, the results suggest that inhibition of senescence may play an important function in the development of resistance to bortezomib.

Supporting Institution

The Scientific Research Projects Coordination Unit of Kutahya Health Sciences University

Project Number

TSA-2021-56

Thanks

We would like to acknowledge the financial support by the Scientific Research Projects Coordination Unit of Kutahya Health Sciences University with Grant No. TSA-2021-56.

References

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  • Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, et al. Oncogene-induced senescence re-layed by an interleukin-dependent inflammatory network. Cell. 2008;133(6):1019-1031. google scholar Sapochnik M, Fuertes M, Arzt E. Programmed cell senescence: role of IL-6 in the pituitary. J Mol Endocrinol. 2017;58(4):241-253. google scholar
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  • McDermott M, Eustace AJ, Busschots S, Breen L, Crown J, Clynes M, et al. In vitro development of chemotherapy and targeted therapy drug-resistant cancer cell lines: a prac-tical guide with case studies. Front Oncol. 2014;4:40. doi: 10.3389/fonc.2014.00040. google scholar
  • Yerlikaya A, Erin N. Differential sensitivity of breast cancer and melanoma cells to proteasome inhibitor Velcade. Int J Mol Med. 2008;22(6):817-823. google scholar
  • Kanbur E, Baykal AT, Yerlikaya A. Molecular analysis of cell survival and death pathways in the proteasome inhibitor bortezomib-resistant PC3 prostate cancer cell line. Medical On-col. 2021;38(9):112. doi: 10.1007/s12032-021-01563-1. google scholar
  • Yerlikaya A, Dokudur H. Investigation of the eIF2alpha phos-phorylation mechanism in response to proteasome inhibi-tion in melanoma and breast cancer cells. Mol Biol (Mosk). 2010;44(5):859-866. google scholar
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254. google scholar
  • Park HH, Kim H, Park SY, Hwang SM, Hong SM, Park S, et al. RIPK3 activation induces TRIM28 derepression in cancer cells and enhances the anti-tumor microenvironment. Mol Cancer. 2021;20(1):107. doi: 10.1186/s12943-021-01399-3. google scholar
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  • Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, et al. Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes Dis. 2014;1(1):87-105. google scholar
  • Kim J, Kim YS, Ko J. CKbeta8/CCL23 and its isoform CKbeta8-1 induce up-regulation of cyclins via the G(i)/G(o) pro-tein/PLC/PKCdelta/ERK leading to cell-cycle progression. Cy- tokine. 2010;50(1):42-49. google scholar
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  • Rodriguez P, Pelletier J, Price GB, Zannis-Hadjopoulos M. NAP-2: Histone chaperone function and phosphorylation state though the cell cycle. J Mol Biol. 2000;298(2):225-238. google scholar
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  • Rani A, Dasgupta P, Murphy JJ. Prostate cancer: the role of inflam-mation and chemokines. Am J Patho.l 2019;189(11):2119-2137. google scholar
  • Salazar N, Castellan M, Shirodkar SS, Lokeshwar BL. Chemokines and chemokine receptors as promoters of prostate cancer growth and progression. Crit Rev Eukaryot Gene Expr. 2013; 23(1): 77-91. google scholar
  • Coutu DL, Galipeau J. Roles of FGF signaling in stem cell self-renewal, senescence and aging. Aging (Albany NY). 2011;3(10):920-933. google scholar
  • Shang D, Sun D, Shi C, Xu J, Shen M, HuX, et al. Activation of epidermal growth factor receptor signaling mediates cellular senescence induced by certain pro-inflammatory cytokines. Aging Cell 2020;19(5):e13145. doi: 10.1111/acel.13145 google scholar
  • Struyf S, Schutyser E, Gouwy M, Gijsbers K, Proost P, Benoit Y, et al. PARC/CCL18 is a plasma CC chemokine with increased levels in childhood acute lymphoblastic leukemia. Am J Pathol 2003;163(5):2065-2075. google scholar
Year 2023, Volume: 82 Issue: 1, 49 - 58, 26.06.2023

Abstract

Project Number

TSA-2021-56

References

  • Herranz N, Gil J. Mechanisms and functions of cellular senes-cence. J Clin Invest. 2018;128(4):1238-1246. google scholar
  • Kumari R, Jat P. Mechanisms of cellular senescence: cell cycle arrest and senescence associated secretory phenotype.Front Cell Dev Biol. 2021 9:645593. doi: 10.3389/fcell.2021.645593 google scholar
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next gener-ation. Cell. 2011;144(5):646-674. google scholar
  • Bolden JE, Lowe SW. Cellular Senescence. In: The Molecular Ba-sis of Cancer. 4th edn. Edited by Mendelsohn J, Gray JW, Howley PM, Israel MA, Thompson CB. Philadelphia, PA: Elsevier Inc. 2014;229-238. google scholar
  • Liu XL, Ding J, Meng LH. Oncogene-induced senescence: a double edged sword in cancer. Acta Pharmacol Sin. 2018;39(10):1553-1558. google scholar
  • Schwarze SR, Shi Y, Fu VX, Watson PA, Jarrard DF. Role of cyclin-dependent kinase inhibitors in the growth arrest at senes-cence in human prostate epithelial and uroepithelial cells. Onco-gene. 2001;20(57):8184-8192. google scholar
  • Land H, Parada LF, Weinberg RA. Tumorigenic conversion of pri-mary embryo fibroblasts requires at least two cooperating onco-genes. Nature. 1983;304(5927): 596-602. google scholar
  • Shay JW, Pereira-Smith OM, Wright WE. A role for both RB and p53 in the regulation of human cellular senescence. Exp Cell Res. 1991;196(1):33-39. google scholar
  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Onco-genic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88(5):593-602 google scholar
  • Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, Lowe SW. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 1998;12(19):3008-3019. google scholar
  • Deschenes-Simard X, Gaumont-Leclerc MF, Bourdeau V, Lessard F, Moiseeva O, Forest V, et al. Tumor suppressor ac-tivity of the ERK/MAPK pathway by promoting selective protein degradation. Genes Dev. 2013;27(8):900-915. google scholar
  • Deschenes-Simard X, Lessard F, Gaumont-Leclerc MF, Bardeesy N, Ferbeyre G. Cellular senescence and protein degradation: breaking down cancer. Cell Cycle. 2014;13(12):1840-1858. google scholar
  • Hilt W, Wolf DH. Proteasomes: Destruction as a programme. Trends Biochem Sc. 1996;21(3):96-102. google scholar
  • Leestemaker Y, Ovaa H. Tools to investigate the ubiquitin protea-some system. Discov Today Technol. 2017;26:25-31. google scholar
  • Wu WK, Cho CH, Lee CW, Wu K, Fan D, Yu J, et al. Proteasome inhibition: a new therapeutic strategy to cancer treatment. Cancer Lett. 2010;293(1):15-22. google scholar
  • Robak P, Robak T. Bortezomib for the treatment of hematologic malignancies: 15 Years Later. Drugs R D. 2019;19(2):73-92. google scholar
  • Yerlikaya A, Yontem M. The significance of ubiquitin proteasome pathway in cancer development. Recent Pat Anticancer Drug Dis-cov. 2013;8(3):298-309. google scholar
  • Aras B, Yerlikaya A. Bortezomib and etoposide combinations exert synergistic effects on the human prostate cancer cell line PC-3. Oncol Lett. 2016;11(5):3179-3184. google scholar
  • Yerlikaya A, Altikat S, Irmak R, Cavga FZ, Kocacan SA, Boyaci I. Effect of bortezomib in combination with cisplatin and 5-fluorouracil on 4T1 breast cancer cells. Mol Med Rep. 2013;8(1):277-281. google scholar
  • Yerlikaya A, Kanbur E. The ubiquitin-proteasome pathway and re-sistance mechanisms developed against the proteasomal inhibitors in cancer cells.Curr Drug Targets. 2020;21(13):1313-1325. google scholar
  • Yerlikaya A, Okur E. An investigation of the mechanisms un-derlying the proteasome inhibitor bortezomib resistance in PC3 prostate cancer cell line. Cytotechnology. 2020;72(1):121-130. google scholar
  • Guillon J, Petit C, Toutain B, Guette C, Lelievre E, Co-queret O. Chemotherapy-induced senescence, an adaptive mech-anism driving resistance and tumor heterogeneity. Cell Cycle .2019;18(19):2385-2397. google scholar
  • Wyld L, Bellantuono I, Tchkonia T, Morgan J, Turner O, Foss F, et al. Senescence and cancer: a review of clinical implica-tions of senescence and senotherapies. Cancers. 2020;12(8). doi: 10.3390/cancers12082134 google scholar
  • Coppe JP, Patil CK, Rodier F, Krtolica A, Beausejour CM, Par-rinello S, et al. A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physio-logical oxygen. PloS One. 2010;5(2):e9188. doi: 10.1371/jour-nal.pone.0009188. google scholar
  • Hinds P, Pietruska J. Senescence and tumor suppression. F1000Res. 2017;6:2121. doi: 10.12688/f1000research.11671.1. google scholar
  • Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, et al. Oncogene-induced senescence re-layed by an interleukin-dependent inflammatory network. Cell. 2008;133(6):1019-1031. google scholar Sapochnik M, Fuertes M, Arzt E. Programmed cell senescence: role of IL-6 in the pituitary. J Mol Endocrinol. 2017;58(4):241-253. google scholar
  • Bairoch A. The cellosaurus, a cell-line knowledge resource. J Biomol Tech. 2018;29(2):25-38. google scholar
  • McDermott M, Eustace AJ, Busschots S, Breen L, Crown J, Clynes M, et al. In vitro development of chemotherapy and targeted therapy drug-resistant cancer cell lines: a prac-tical guide with case studies. Front Oncol. 2014;4:40. doi: 10.3389/fonc.2014.00040. google scholar
  • Yerlikaya A, Erin N. Differential sensitivity of breast cancer and melanoma cells to proteasome inhibitor Velcade. Int J Mol Med. 2008;22(6):817-823. google scholar
  • Kanbur E, Baykal AT, Yerlikaya A. Molecular analysis of cell survival and death pathways in the proteasome inhibitor bortezomib-resistant PC3 prostate cancer cell line. Medical On-col. 2021;38(9):112. doi: 10.1007/s12032-021-01563-1. google scholar
  • Yerlikaya A, Dokudur H. Investigation of the eIF2alpha phos-phorylation mechanism in response to proteasome inhibi-tion in melanoma and breast cancer cells. Mol Biol (Mosk). 2010;44(5):859-866. google scholar
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254. google scholar
  • Park HH, Kim H, Park SY, Hwang SM, Hong SM, Park S, et al. RIPK3 activation induces TRIM28 derepression in cancer cells and enhances the anti-tumor microenvironment. Mol Cancer. 2021;20(1):107. doi: 10.1186/s12943-021-01399-3. google scholar
  • Yang L, Fang J, Chen J. Tumor cell senescence response pro-duces aggressive variants. Cell Death Discov. 2017;3:17049. doi: 10.1038/cddiscovery.2017.49. google scholar Dasgupta J, Kar S, Liu R, Joseph J, Kalyanaraman B, Remington SJ, et al. Reactive oxygen species control senescence-associated matrix metalloproteinase-1 though c-Jun-N- terminal kinase. J Cell Physiol. 2010;225(1):52-62. google scholar
  • Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, et al. Bone Morphogenetic Protein (BMP) signaling in development and human diseases. Genes Dis. 2014;1(1):87-105. google scholar
  • Kim J, Kim YS, Ko J. CKbeta8/CCL23 and its isoform CKbeta8-1 induce up-regulation of cyclins via the G(i)/G(o) pro-tein/PLC/PKCdelta/ERK leading to cell-cycle progression. Cy- tokine. 2010;50(1):42-49. google scholar
  • Gu JJ, Kaufman GP, Mavis C, Czuczman MS, Hernandez-Ilizaliturri FJ. Mitotic catastrophe and cell cycle arrest are alter-native cell death pathways executed by bortezomib in rituximab resistant B-cell lymphoma cells. Oncotarget. 2017;8(8):12741-12753. google scholar
  • Kretowski R, Borzym-Kluczyk M, Cechowska-Pasko M. Hy-poxia enhances the senescence effect of bortezomib-the pro-teasome inhibitor-on human skin fibroblasts. Biomed Res Int. 2014;196249. doi: 10.1155/2014/196249. google scholar
  • Marcoux S, Le ON, Langlois-Pelletier C, Laverdiere C, Hatami A, Robaey P, et al. Expression of the senescence marker p16INK4a in skin biopsies of acute lymphoblastic leukemia survivors: a pilot study. Radiat Oncol. 2013;8:252. doi: 10.1186/1748-717X-8-252. google scholar
  • Buckley S, Shi W, Driscoll B, Ferrario A, Anderson K, Warbur-ton D. BMP4 signaling induces senescence and modulates the oncogenic phenotype of A549 lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol. 2004;286(1):81-86. google scholar
  • Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature. 2013;494(7437):361-365. google scholar
  • Rodriguez P, Pelletier J, Price GB, Zannis-Hadjopoulos M. NAP-2: Histone chaperone function and phosphorylation state though the cell cycle. J Mol Biol. 2000;298(2):225-238. google scholar
  • Guo F, Long L, Wang J, Wang Y, Liu Y, Wang L, et al. Insights on CXC chemokine receptor 2 in breast cancer: An emerging target for oncotherapy. Oncology Lett. 2019;18(6):5699-5708. google scholar
  • Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast cancer stem cells are regulated by mesenchymal stem cells though cytokine networks. Cancer Res 2011;71(2):614-624. google scholar
  • Liu Q, Li A, Tian Y, Wu JD, Liu Y, Li T, et al. The CXCL8-CXCR1/2 pathways in cancer. Cytokine Growth Factor Rev. 2016;31:61-71. google scholar
  • Rani A, Dasgupta P, Murphy JJ. Prostate cancer: the role of inflam-mation and chemokines. Am J Patho.l 2019;189(11):2119-2137. google scholar
  • Salazar N, Castellan M, Shirodkar SS, Lokeshwar BL. Chemokines and chemokine receptors as promoters of prostate cancer growth and progression. Crit Rev Eukaryot Gene Expr. 2013; 23(1): 77-91. google scholar
  • Coutu DL, Galipeau J. Roles of FGF signaling in stem cell self-renewal, senescence and aging. Aging (Albany NY). 2011;3(10):920-933. google scholar
  • Shang D, Sun D, Shi C, Xu J, Shen M, HuX, et al. Activation of epidermal growth factor receptor signaling mediates cellular senescence induced by certain pro-inflammatory cytokines. Aging Cell 2020;19(5):e13145. doi: 10.1111/acel.13145 google scholar
  • Struyf S, Schutyser E, Gouwy M, Gijsbers K, Proost P, Benoit Y, et al. PARC/CCL18 is a plasma CC chemokine with increased levels in childhood acute lymphoblastic leukemia. Am J Pathol 2003;163(5):2065-2075. google scholar
There are 50 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Ertan Kanbur 0000-0001-8399-8942

Semih Şeker 0000-0002-8957-2050

Ferah Budak 0000-0001-7625-9148

Azmi Yerlikaya 0000-0002-0678-0701

Project Number TSA-2021-56
Publication Date June 26, 2023
Submission Date January 21, 2023
Published in Issue Year 2023 Volume: 82 Issue: 1

Cite

AMA Kanbur E, Şeker S, Budak F, Yerlikaya A. The Senescence Program is Reduced in Proteasome Inhibitor Bortezomib-Resistant PC3 Prostate Cancer Cell Line. Eur J Biol. June 2023;82(1):49-58. doi:10.18478/iufsjb.1240253