Biomedical Science Letters (대한의생명과학회지)

The Korean Society for Biomedical Laboratory Sciences (대한의생명과학회)
권호 표지
DOI QR코드

DOI QR Code

Estrogen Induces CK2α Activation via Generation of Reactive Oxygen Species

  • Jeong, Soo-Yeon (Department of Biological Sciences, College of Natural Sciences, Chonnam National University) ;
  • Im, Suhn-Young (Department of Biological Sciences, College of Natural Sciences, Chonnam National University)
  • Received : 2018.10.22
  • Accepted : 2019.02.12
  • Published : 2019.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

The protein kinase $CK2{\alpha}$ (formerly Casein Kinase II) is implicated in tumorigenesis and transformation. However, the mechanisms of $CK2{\alpha}$ activation in breast cancer have yet to be elucidated. This study investigated the mechanisms of $CK2{\alpha}$ activation in estrogen signaling. Estrogen increased reactive oxygen species (ROS) production, $CK2{\alpha}$ activity, and protein expression in estrogen receptor positive ($ER^+$) MCF-7 human breast cancer cells, which were inhibited by the antioxidant N-acetyl-L-cysteine. $H_2O_2$ enhanced $CK2{\alpha}$ activity and protein expression. Human epidermal growth factor (EGF) increased ROS production, $CK2{\alpha}$ activity and protein expression in EGF receptor 2 (HER2)-overexpressing MCF-7 (MCF-7 HER2) cells, but not in MCF-7 cells. Estrogen induced the phosphorylation of p38 mitogen-activated protein kinase (MAPK). The p38 inhibitor, SB202190, blocked estrogen-induced increases in ROS production, $CK2{\alpha}$ activity and $CK2{\alpha}$ protein expression. The data suggest that ROS/p38 MAPK is the key inducer of $CK2{\alpha}$ activation in response to estrogen or EGF.

Keywords

References

  1. Allende JE, Allende CC. Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB Journal. 1995. 9: 313-323. https://doi.org/10.1096/fasebj.9.5.7896000
  2. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, Rhee SG. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. Journal of Biological Chemistry. 1997. 272: 217-221. https://doi.org/10.1074/jbc.272.1.217
  3. Brennan JP, Bardswell SC, Burgoyne JR, Fuller W, Schroder E, Wait R, Begum S, Kentish JC, Eaton P. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. Journal of Biological Chemistry. 2006. 281: 21827-21836. https://doi.org/10.1074/jbc.M603952200
  4. Burness ML, Grushko TA, Olopade OI. Epidermal growth factor receptor in triplenegative and basal-like breast cancer: promising clinical target or only a marker? Cancer Journal. 2010. 16: 23-32. https://doi.org/10.1097/PPO.0b013e3181d24fc1
  5. Carew JS, Huang P. Mitochondrial defects in cancer. Molecular Cancer. 2002. 1: 15.
  6. Chua MM, Ortega CE, Sheikh A, Lee M, Abdul-Rassoul H, Hartshorn KL, Dominguez I. CK2 in Cancer: Cellular and biochemical mechanisms and potential therapeutic target. Pharmaceuticals (Basel). 2017. 10: 30. https://doi.org/10.3390/ph10010030
  7. Clemons M, Goss P. Estrogen and the risk of breast cancer. New England Journal of Medicine. 2001. 344: 276-285. https://doi.org/10.1056/NEJM200101253440407
  8. Duncan JS, Litchfield DW. Too much of a good thing: the role of protein kinase CK2 in tumorigenesis and prospects for therapeutic inhibition of CK2. Biochimica et Biophysica Acta. 2008. 1784: 33-47. https://doi.org/10.1016/j.bbapap.2007.08.017
  9. Felty Q. Singh, KP, Roy D. Estrogen-induced G1/S transition of G0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling. Oncogene. 2005. 24: 4883-4893. https://doi.org/10.1038/sj.onc.1208667
  10. Felty Q, Xiong WC, Sun D, Sarkar S, Singh KP, Parkash J, Roy D. Estrogen induced mitochondrial reactive oxygen species as signal-transducing messengers, Biochemistry. 2005. 44: 6900-6909. https://doi.org/10.1021/bi047629p
  11. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International Journal of Cancer. 2010. 127: 2893-2917. https://doi.org/10.1002/ijc.25516
  12. Filhol O, Giacosa S, Wallez Y, Cochet C. Protein kinase CK2 in breast cancer: the $CK2{\beta}$ regulatory subunit takes center stage in epithelial plasticity. Cellular and Molecular Life Sciences. 2015. 72: 3305-3322. https://doi.org/10.1007/s00018-015-1929-8
  13. Fujino G, Noguchi T, Matsuzawa A, Yamauchi S, Saitoh M, Takeda K, Ichijo H. Thioredoxin and TRAF Family Proteins Regulate Reactive Oxygen Species-Dependent Activation of ASK1 through Reciprocal Modulation of the N Terminal Homophilic Interaction of ASK1. Molecular and Cellular Biology. 2007. 27: 8152-8163. https://doi.org/10.1128/MCB.00227-07
  14. Giorgi C, Agnoletto C, Baldini C, Bononi A, Bonora M, Marchi S, Missiroli S, Patergnani S, Poletti F, Rimessi A, Zavan B, Pinton P. Redox control of protein kinase C: Cell-and disease-specific aspects. Antioxidants & Redox Signaling. 2010. 13: 1051-1085. https://doi.org/10.1089/ars.2009.2825
  15. Giusiano S, Cochet C, Filhol O, Duchemin-Pelletier E, Secq V, Bonnier P, Carcopino X, Boubli L, Birnbaum D, Garcia S, Iovanna J, Charpin C. Protein kinase $CK2{\alpha}$ subunit overexpression correlates with metastatic risk in breast carcinomas: quantitative immunohistochemistry in tissue microarrays. European Journal of Cancer. 2011. 47: 792-801. https://doi.org/10.1016/j.ejca.2010.11.028
  16. Groenen LC, Nice E, Burgess AW. Structure-function relationships for the EGF/TGF-alpha family of mitogens. Growth Factors. 1994. 11: 235-257. https://doi.org/10.3109/08977199409010997
  17. Hofmann F, Feil R, Kleppisch T, Schlossmann J. Function of cGMP Dependent Protein Kinases as Revealed by Gene Deletion. Physiological Review. 2006. 86: 1-23. https://doi.org/10.1152/physrev.00015.2005
  18. Kim KJ, Cho KD, Jang KY, Kim HA, Kim HK, Lee HK, Im SY. Platelet-activating factor enhances tumor metastasis via the reactive oxygen species-dependent protein kinase casein kinase 2-mediated nuclear factor-${\kappa}B$ activation. Immunology. 2014. 143: 21-32. https://doi.org/10.1111/imm.12283
  19. Lemke G. Neuregulins in development. Molecular and Cellular Neuroscience. 1996. 7: 247-262. https://doi.org/10.1006/mcne.1996.0019
  20. Li Z, Zhang G, Feil R, Han J, Du X. Sequential activation of p38 and ERK pathways by cGMP-dependent protein kinase leading to activation of the platelet integrin ${\alpha}IIb{\beta}3$. Blood. 2006. 107: 965-972. https://doi.org/10.1182/blood-2005-03-1308
  21. Litchfield DW. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochemical Journal. 2003. 369: 1-15. https://doi.org/10.1042/bj20021469
  22. Mahadev K, Zilbering A, Zhu L, Goldstein BJ. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. Journal of Biological Chemistry. 2001. 276: 21938-21942. https://doi.org/10.1074/jbc.C100109200
  23. Me'nard S, Pupa SM, Campiglio M, Tagliabue E. Biologic and therapeutic role of HER2 in cancer. Oncogene. 2003. 22: 6570-6578. https://doi.org/10.1038/sj.onc.1206779
  24. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. Journal of Clinical Oncology. 2003. 21: 2787-2799. https://doi.org/10.1200/JCO.2003.01.504
  25. Ohba M, Shibanuma M, Kuroki T, Nose K. Production of hydrogen peroxide by transforming growth factor-beta 1 and its involvement in induction of egr-1 in mouse osteoblastic cells. Journal of Cell Biology. 1994. 126: 1079-1088. https://doi.org/10.1083/jcb.126.4.1079
  26. Okoh V, Deoraj A, Roy D. Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta. 2011. 1815: 115-133.
  27. Parkash J, Felty Q, Roy D. Estrogen exerts a spatial and temporal influence on reactive oxygen species generation that precedes calcium uptake in high-capacity mitochondria: implications for rapid nongenomic signaling of cell growth. Biochemistry. 2006. 45: 2872-2881. https://doi.org/10.1021/bi051855x
  28. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jefrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature. 2000. 406: 747-752. https://doi.org/10.1038/35021093
  29. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. Prognostic markers in triple-negative breast cancer. Cancer. 2007. 109: 25-32. https://doi.org/10.1002/cncr.22381
  30. Roy D, Cai Q, Felty Q, Narayan S. Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. Journal of Toxicology and Environmental Health Part B Critical Reviews. 2007. 10: 235-257. https://doi.org/10.1080/15287390600974924
  31. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO Journal. 1998. 17: 2596-2606. https://doi.org/10.1093/emboj/17.9.2596
  32. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cellular Physiology and Biochemistry. 2001. 11: 173-186. https://doi.org/10.1159/000047804
  33. Seo HS, Choi HS, Kim SR, Choi YK, Woo SM, Shin I, Woo JK, Park SY, Shin YC, Ko SG. Apigenin induces apoptosis via extrinsic pathway, inducing p53 and inhibiting STAT3 and $NF{\kappa}B$ signaling in HER2-overexpressing breast cancer cells. Molecular Cellular Biochemistry. 2012. 366: 319-334. https://doi.org/10.1007/s11010-012-1310-2
  34. Singh NN, Ramji DP. Protein kinase CK2, an important regulator of the inflammatory response? Journal of Molecular Medicine (Berl). 2008. 86: 887-897. https://doi.org/10.1007/s00109-008-0352-0
  35. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987. 235: 177-182. https://doi.org/10.1126/science.3798106
  36. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lnning PE, Brown PO, Brresen-Dale AL, Botstein D. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proceedings of the National Academy of Sciences of the USA. 2003. 100: 8418-8423. https://doi.org/10.1073/pnas.0932692100
  37. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of $H_2O_2$ for platelet-derived growth factor signal transduction. Science. 1995. 270: 296-299. https://doi.org/10.1126/science.270.5234.296
  38. Thannickal VJ, Fanburg BL. Activation of an $H_2O_2$-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta 1. Journal of Biological Chemistry. 1995. 270: 30334-30338. https://doi.org/10.1074/jbc.270.51.30334
  39. Toikkanen S, Helin H, Isola J, Joensuu H. Prognostic significance of HER-2 oncoprotein expression in breast cancer: a 30-tear follow-up. Journal of Clinical Oncology. 1992. 10: 1044-1048. https://doi.org/10.1200/JCO.1992.10.7.1044
  40. Yager JD, Liehr JG. Molecular mechanisms of estrogen carcinogenesis. Annual Review of Pharmacology and Toxicology. 1996. 36: 203-232. https://doi.org/10.1146/annurev.pa.36.040196.001223
  41. Zhang J, Shen B, Lin A. Novel strategies for inhibition of the p38 MAPK pathway. Trends Pharmacological Sciences. 2007. 28: 286-295. https://doi.org/10.1016/j.tips.2007.04.008