Research Article
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Proteasomal System Related Stress Response in Different Cancer Cell Lines

Year 2021, Volume: 11 Issue: 1, 28 - 33, 31.03.2021

Ayse Tarbin Jannuzzı , Sema Arslan Buket Alpertunga , Betül Karademir Yılmaz

https://doi.org/10.33808/clinexphealthsci.802815

Abstract

Objective: Proteasomal system is the primary protein degradation mechanism and important for cellular homeostasis. On the other hand, increased proteasome activity protects cancer cells from cell death. The objective of this preliminary study was to determine the response of the proteasomal system to oxidative stress in human cancer cell lines including K562 chronic myelogenous leukemia, U251 glioblastoma, DU145 prostate cancer, HepG2C3A hepatoma, and MCF7 breast cancer.

Methods: Cells were exposed to hydrogen peroxide (H2O2) as a stressor. 20S and 26S proteasome activities and K48-linked protein ubiquitination levels were determined immediately and 3 hours after exposure.

Results: As an immediate response, 20S proteasome activities decreased in only K562 and U251 cells and 20S+26S proteasome activities decreased only in K562 cells. Following 3h of incubation, all cells showed a significant decrease in both 20S and 20S+26S proteasome activities. K48-linked protein ubiquitination levels increased immediately in K562 and DU145 cells. After 3h of incubation, ubiquitination levels increased in all cell lines except MCF7 cells.

Conclusion: The difference in the response of the proteasomal system to stress could be the reason for differential adaptation to oxidative
stress in different cancer types.

Keywords

proteasome activity 20S proteasome 26S proteasome Oxidative stress cancer

Supporting Institution

Marmara University Research Fund

Project Number

SAG-B-130319-0089

References

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  • 2. Epstein T, Gatenby RA, Brown JS. The Warburg effect as an adaptation of cancer cells to rapid fluctuations in energy demand. PLoS One 2017; 12: e0185085.
  • 3. Liberti M V., Locasale JW. The Warburg Effect: How Does it Benefit Cancer Cells? Trends Biochem Sci 2016; 41:211–218.
  • 4. Sena LA, Chandel NS. Physiological Roles of Mitochondrial Reactive Oxygen Species. Mol Cell 2012; 48: 158–167.
  • 5. Locasale JW, Cantley LC. Metabolic flux and the regulation of mammalian cell growth. Cell Metab 2011; 14(4):443–451.
  • 6. Sullivan LB, Chandel NS. Mitochondrial reactive oxygen species and cancer. Cancer Metab 2014; 2(1):17.
  • 7. Davies KJA. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001; 83(3–4):301–310.
  • 8. Breusing N, Grune T. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol Chem 2008; 389(3):203–209.
  • 9. Grune T, Reinheckel T, Davies KJ. Degradation of oxidized proteins in mammalian cells. FASEB J 1997; 11(7):526–534.
  • 10. Jung T, Catalgol B, Grune T. The proteasomal system. Molecular Aspects of Medicine 2009; 30:191–296.
  • 11. Jung T, Grune T. The proteasome and the degradation of oxidized proteins: part I—structure of proteasomes. Redox Biol 2013; 1(1):178–182.
  • 12. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82(2):373–428.
  • 13. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J, et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009; 137(1):133–145.
  • 14. Strickland E, Hakala K, Thomas PJ, DeMartino GN. Recognition of misfolding proteins by PA700, the regulatory subcomplex of the 26 S proteasome. J Biol Chem 2000; 275(8):5565–5572.
  • 15. Shang F, Taylor A. Ubiquitin–proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 2011; 51(1):5–16.
  • 16. Schmidt M, Finley D. Regulation of proteasome activity in health and disease. Biochim Biophys Acta (BBA)-Molecular Cell Res 2014; 1843(1):13–25.
  • 17. Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012; 482(7384):186.
  • 18. Sitte N, Merker K, Grune T. Proteasome-dependent degradation of oxidized proteins in MRC-5 fibroblasts. FEBS Lett 1998; 440:399–402.
  • 19. Grune T, Catalgol B, Licht A, Ermak G, Pickering AM, Ngo JK, et al. HSP70 mediates dissociation and reassociation of the 26S proteasome during adaptation to oxidative stress. Free Radic Biol Med 2011; 51(7):1355–1364.
  • 20. Chen L, Madura K. Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Res 2005; 65(13):5599–5606.
  • 21. Arlt A, Bauer I, Schafmayer C, Tepel J, Müerköster SS, Brosch M, et al. Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an enhanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene 2009; 28:3983–3996.
  • 22. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994; 15(1):7–10.
  • 23. Boldyrev AA. Discrimination between apoptosis and necrosis of neurons under oxidative stress. Biochem C/C BIOKHIMIIA 2000; 65(7):834–842.
  • 24. Adams J. The proteasome: structure, function, and role in the cell. Cancer Treat Rev 2003; 29:3–9.
  • 25. Ertel A, Verghese A, Byers SW, Ochs M, Tozeren A. Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer 2006; 5(1):55.
  • 26. Ikeda F, Dikic I. Atypical ubiquitin chains: new molecular signals. “Protein Modifications: Beyond the Usual Suspects” review series. EMBO Rep 2008; 9:536–542.
  • 27. Launay N, Ruiz M, Fourcade S, Schlüter A, Guilera C, Ferrer I, et al. Oxidative stress regulates the ubiquitin–proteasome system and immunoproteasome functioning in a mouse model of X-adrenoleukodystrophy. Brain 2013; 136(3):891–904.
  • 28. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373–399.
  • 29. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39(1):44–84.
  • 30. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292(5521):1552–1555.
  • 31. Tyedmers J, Mogk A, Bukau B. Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 2010; 11(11):777–788.
  • 32. Lefaki M, Papaevgeniou N, Chondrogianni N. Redox regulation of proteasome function. Redox Biol 2017; 13:452–458.
  • 33. Livnat-Levanon N, Kevei É, Kleifeld O, Krutauz D, Segref A, Rinaldi T, et al. Reversible 26S proteasome disassembly upon mitochondrial stress. Cell Rep 2014; 7:1371–1380.
  • 34. Wang X, Yen J, Kaiser P, Huang L. Regulation of the 26S proteasome complex during oxidative stress. Sci Signal 2010; 3(151):ra88–ra88.
  • 35. Reinheckel T, Ullrich O, Sitte N, Grune T. Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch Biochem Biophys 2000; 377: 65–68.
  • 36. Grice GL, Nathan JA. The recognition of ubiquitinated proteins by the proteasome. Cell Mol Life Sci 2016; 73(18):3497–3506.
  • 37. Li D, Dong Q, Tao Q, Gu J, Cui Y, Jiang X, et al. c-Abl regulates proteasome abundance by controlling the ubiquitin-proteasomal degradation of PSMA7 subunit. Cell Rep 2015; 10(4):484–496.
  • 38. Tsvetkov P, Adler J, Myers N, Biran A, Reuven N, Shaul Y. Oncogenic addiction to high 26S proteasome level. Cell Death Dis 2018;9(7):1–14.
  • 39. Kästle M, Reeg S, Rogowska-Wrzesinska A, Grune T. Chaperones, but not oxidized proteins, are ubiquitinated after oxidative stress. Free Radic Biol Med 2012; 53(7):1468–1477.
  • 40. Aiken CT, Kaake RM, Wang X, Huang L. Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics 2011; 10(5):R110-006924.
  • 41. Zhang X, Zhou J, Fernandes AF, Sparrow JR, Pereira P, Taylor A, et al. The Proteasome: A Target of Oxidative Damage in Cultured Human Retina Pigment Epithelial Cells. Investig Opthalmology Vis Sci 2008; 49:3622–3630.
  • 42. Deshaies RJ. Proteotoxic crisis, the ubiquitin-proteasome system, and cancer therapy. BMC Biol 2014; 12(1):1–14.

Year 2021, Volume: 11 Issue: 1, 28 - 33, 31.03.2021

Ayse Tarbin Jannuzzı , Sema Arslan Buket Alpertunga , Betül Karademir Yılmaz

https://doi.org/10.33808/clinexphealthsci.802815

Abstract

Project Number

SAG-B-130319-0089

References

  • 1. Wang X, Liang Z, Huang H, Liang W. Principles of ethics review on traditional medicine and the practice of institute review board in China. Chin J Integr Med 2011; 17:631–634.
  • 2. Epstein T, Gatenby RA, Brown JS. The Warburg effect as an adaptation of cancer cells to rapid fluctuations in energy demand. PLoS One 2017; 12: e0185085.
  • 3. Liberti M V., Locasale JW. The Warburg Effect: How Does it Benefit Cancer Cells? Trends Biochem Sci 2016; 41:211–218.
  • 4. Sena LA, Chandel NS. Physiological Roles of Mitochondrial Reactive Oxygen Species. Mol Cell 2012; 48: 158–167.
  • 5. Locasale JW, Cantley LC. Metabolic flux and the regulation of mammalian cell growth. Cell Metab 2011; 14(4):443–451.
  • 6. Sullivan LB, Chandel NS. Mitochondrial reactive oxygen species and cancer. Cancer Metab 2014; 2(1):17.
  • 7. Davies KJA. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001; 83(3–4):301–310.
  • 8. Breusing N, Grune T. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol Chem 2008; 389(3):203–209.
  • 9. Grune T, Reinheckel T, Davies KJ. Degradation of oxidized proteins in mammalian cells. FASEB J 1997; 11(7):526–534.
  • 10. Jung T, Catalgol B, Grune T. The proteasomal system. Molecular Aspects of Medicine 2009; 30:191–296.
  • 11. Jung T, Grune T. The proteasome and the degradation of oxidized proteins: part I—structure of proteasomes. Redox Biol 2013; 1(1):178–182.
  • 12. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82(2):373–428.
  • 13. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J, et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009; 137(1):133–145.
  • 14. Strickland E, Hakala K, Thomas PJ, DeMartino GN. Recognition of misfolding proteins by PA700, the regulatory subcomplex of the 26 S proteasome. J Biol Chem 2000; 275(8):5565–5572.
  • 15. Shang F, Taylor A. Ubiquitin–proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 2011; 51(1):5–16.
  • 16. Schmidt M, Finley D. Regulation of proteasome activity in health and disease. Biochim Biophys Acta (BBA)-Molecular Cell Res 2014; 1843(1):13–25.
  • 17. Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012; 482(7384):186.
  • 18. Sitte N, Merker K, Grune T. Proteasome-dependent degradation of oxidized proteins in MRC-5 fibroblasts. FEBS Lett 1998; 440:399–402.
  • 19. Grune T, Catalgol B, Licht A, Ermak G, Pickering AM, Ngo JK, et al. HSP70 mediates dissociation and reassociation of the 26S proteasome during adaptation to oxidative stress. Free Radic Biol Med 2011; 51(7):1355–1364.
  • 20. Chen L, Madura K. Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Res 2005; 65(13):5599–5606.
  • 21. Arlt A, Bauer I, Schafmayer C, Tepel J, Müerköster SS, Brosch M, et al. Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an enhanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene 2009; 28:3983–3996.
  • 22. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994; 15(1):7–10.
  • 23. Boldyrev AA. Discrimination between apoptosis and necrosis of neurons under oxidative stress. Biochem C/C BIOKHIMIIA 2000; 65(7):834–842.
  • 24. Adams J. The proteasome: structure, function, and role in the cell. Cancer Treat Rev 2003; 29:3–9.
  • 25. Ertel A, Verghese A, Byers SW, Ochs M, Tozeren A. Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer 2006; 5(1):55.
  • 26. Ikeda F, Dikic I. Atypical ubiquitin chains: new molecular signals. “Protein Modifications: Beyond the Usual Suspects” review series. EMBO Rep 2008; 9:536–542.
  • 27. Launay N, Ruiz M, Fourcade S, Schlüter A, Guilera C, Ferrer I, et al. Oxidative stress regulates the ubiquitin–proteasome system and immunoproteasome functioning in a mouse model of X-adrenoleukodystrophy. Brain 2013; 136(3):891–904.
  • 28. Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373–399.
  • 29. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39(1):44–84.
  • 30. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292(5521):1552–1555.
  • 31. Tyedmers J, Mogk A, Bukau B. Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 2010; 11(11):777–788.
  • 32. Lefaki M, Papaevgeniou N, Chondrogianni N. Redox regulation of proteasome function. Redox Biol 2017; 13:452–458.
  • 33. Livnat-Levanon N, Kevei É, Kleifeld O, Krutauz D, Segref A, Rinaldi T, et al. Reversible 26S proteasome disassembly upon mitochondrial stress. Cell Rep 2014; 7:1371–1380.
  • 34. Wang X, Yen J, Kaiser P, Huang L. Regulation of the 26S proteasome complex during oxidative stress. Sci Signal 2010; 3(151):ra88–ra88.
  • 35. Reinheckel T, Ullrich O, Sitte N, Grune T. Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch Biochem Biophys 2000; 377: 65–68.
  • 36. Grice GL, Nathan JA. The recognition of ubiquitinated proteins by the proteasome. Cell Mol Life Sci 2016; 73(18):3497–3506.
  • 37. Li D, Dong Q, Tao Q, Gu J, Cui Y, Jiang X, et al. c-Abl regulates proteasome abundance by controlling the ubiquitin-proteasomal degradation of PSMA7 subunit. Cell Rep 2015; 10(4):484–496.
  • 38. Tsvetkov P, Adler J, Myers N, Biran A, Reuven N, Shaul Y. Oncogenic addiction to high 26S proteasome level. Cell Death Dis 2018;9(7):1–14.
  • 39. Kästle M, Reeg S, Rogowska-Wrzesinska A, Grune T. Chaperones, but not oxidized proteins, are ubiquitinated after oxidative stress. Free Radic Biol Med 2012; 53(7):1468–1477.
  • 40. Aiken CT, Kaake RM, Wang X, Huang L. Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics 2011; 10(5):R110-006924.
  • 41. Zhang X, Zhou J, Fernandes AF, Sparrow JR, Pereira P, Taylor A, et al. The Proteasome: A Target of Oxidative Damage in Cultured Human Retina Pigment Epithelial Cells. Investig Opthalmology Vis Sci 2008; 49:3622–3630.
  • 42. Deshaies RJ. Proteotoxic crisis, the ubiquitin-proteasome system, and cancer therapy. BMC Biol 2014; 12(1):1–14.
There are 42 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Ayse Tarbin Jannuzzı 0000-0003-0578-6893

Sema Arslan This is me 0000-0003-2205-0415

Buket Alpertunga 0000-0001-6043-7560

Betül Karademir Yılmaz 0000-0003-1762-0284

Project Number SAG-B-130319-0089
Publication Date March 31, 2021
Submission Date September 30, 2020
Published in Issue Year 2021 Volume: 11 Issue: 1

Cite

APA Jannuzzı, A. T., Arslan, S., Alpertunga, B., Karademir Yılmaz, B. (2021). Proteasomal System Related Stress Response in Different Cancer Cell Lines. Clinical and Experimental Health Sciences, 11(1), 28-33. https://doi.org/10.33808/clinexphealthsci.802815
AMA Jannuzzı AT, Arslan S, Alpertunga B, Karademir Yılmaz B. Proteasomal System Related Stress Response in Different Cancer Cell Lines. Clinical and Experimental Health Sciences. March 2021;11(1):28-33. doi:10.33808/clinexphealthsci.802815
Chicago Jannuzzı, Ayse Tarbin, Sema Arslan, Buket Alpertunga, and Betül Karademir Yılmaz. “Proteasomal System Related Stress Response in Different Cancer Cell Lines”. Clinical and Experimental Health Sciences 11, no. 1 (March 2021): 28-33. https://doi.org/10.33808/clinexphealthsci.802815.
EndNote Jannuzzı AT, Arslan S, Alpertunga B, Karademir Yılmaz B (March 1, 2021) Proteasomal System Related Stress Response in Different Cancer Cell Lines. Clinical and Experimental Health Sciences 11 1 28–33.
IEEE A. T. Jannuzzı, S. Arslan, B. Alpertunga, and B. Karademir Yılmaz, “Proteasomal System Related Stress Response in Different Cancer Cell Lines”, Clinical and Experimental Health Sciences, vol. 11, no. 1, pp. 28–33, 2021, doi: 10.33808/clinexphealthsci.802815.
ISNAD Jannuzzı, Ayse Tarbin et al. “Proteasomal System Related Stress Response in Different Cancer Cell Lines”. Clinical and Experimental Health Sciences 11/1 (March 2021), 28-33. https://doi.org/10.33808/clinexphealthsci.802815.
JAMA Jannuzzı AT, Arslan S, Alpertunga B, Karademir Yılmaz B. Proteasomal System Related Stress Response in Different Cancer Cell Lines. Clinical and Experimental Health Sciences. 2021;11:28–33.
MLA Jannuzzı, Ayse Tarbin et al. “Proteasomal System Related Stress Response in Different Cancer Cell Lines”. Clinical and Experimental Health Sciences, vol. 11, no. 1, 2021, pp. 28-33, doi:10.33808/clinexphealthsci.802815.
Vancouver Jannuzzı AT, Arslan S, Alpertunga B, Karademir Yılmaz B. Proteasomal System Related Stress Response in Different Cancer Cell Lines. Clinical and Experimental Health Sciences. 2021;11(1):28-33.
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