ERβ-dependent neuroglobin up-regulation impairs 17β-estradiol-induced apoptosis in DLD-1 colon cancer cells upon oxidative stress injury

Journal of Steroid Biochemistry and Molecular Biology

Volumn 149, Issue , 2015, Pages 128-137

  Fiocchetti, Marco ^a   Camilli, Giulia ^a   Acconcia, Filippo ^a   Leone, Stefano ^a   Ascenzi, Paolo ^a   Marino, Maria ^a  

^a ROMA TRE UNIVERSITY   (Italy)

Author keywords

17 Estradiol; Apoptosis; Colon cancer cell line; Estrogen receptor ; Neuroglobin; Oxidative stress

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYTOCHROME C; ESTRADIOL; ESTROGEN RECEPTOR BETA; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROGLOBIN; GLOBIN; MESSENGER RNA; NERVE PROTEIN;

ADENOCARCINOMA CELL LINE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL FRACTIONATION; CELL VIABILITY; COLORECTAL CARCINOMA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; CYTOSOLIC FRACTION; ENDOSOME; ENZYME ACTIVATION; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LYSOSOME; MITOCHONDRION; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING; COLON; COLON TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; COLON; COLONIC NEOPLASMS; CYTOCHROMES C; ESTRADIOL; ESTROGEN RECEPTOR BETA; GENE EXPRESSION REGULATION, NEOPLASTIC; GLOBINS; HUMANS; MITOCHONDRIA; NERVE TISSUE PROTEINS; OXIDATIVE STRESS; RNA, MESSENGER; UP-REGULATION;

EID: 84923313812     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2015.02.005     Document Type: Article

References (62)

1. F. Acconcia, and M. Marino The effects of 17β-estradiol in cancer are mediated by estrogen receptor signaling at the plasma membrane Front Physiol. 2 2011 30
2. F. Acconcia, P. Totta, S. Ogawa, I. Cardillo, S. Inoue, S. Leone, A. Trentalance, M. Muramatsu, and M. Marino Survival versus apoptotic 17β-estradiol effect: role of ERα and ERβ activated non-genomic signaling J. Cell. Physiol. 203 2005 193 201
3. P. Ascenzi, A. Bocedi, and M. Marino Structure-function relationship of estrogen receptor α and β: impact on human health Mol. Aspects Med. 27 2006 299 402
4. P. Ascenzi, S. Gustincich, and M. Marino Mammalian nerve globins in search of functions IUBMB Life 66 2014 268 276
5. D. Behrens, J.H. Gill, and I. Fichtner Loss of tumourigenicity of stably ERβ-transfected MCF-7 breast cancer cells Mol. Cell. Endocrinol. 274 2007 19 29
6. S. Borgquist, C. Holm, M. Stendahl, L. Anagnostaki, G. Landberg, and K. Jirstrom Oestrogen receptors α and β show different associations to clinicopathological parameters and their co-expression might predict a better response to endocrine treatment in breast cancer J. Clin. Pathol. 61 2008 197 203
7. T. Brittain, J. Skommer, K. Henty, N. Birch, and S. Raychaudhuri A role for human neuroglobin in apoptosis IUBMB Life 62 2010 878 885
8. T. Brittain, and J. Skommer Does a redox cycle provide a mechanism for setting the capacity of neuroglobin to protect cells from apoptosis? IUBMB Life 64 2010 419 422
9. T. Burmester, B. Ebner, B. Weich, and T. Hankeln Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues Mol. Biol. Evol. 19 2002 416 421
10. T. Burmester, B. Weich, S. Reinhardt, and T. Hankeln A vertebrate globin expressed in the brain Nature 407 2000 520 523
11. K.A. Burns, and K.S. Korach Estrogen receptors and human disease: an update Arch. Toxicol. 86 2012 1491 1504
12. F. Caiazza, P. Galluzzo, S. Lorenzetti, and M. Marino 17β-estradiol induces ERβ up-regulation via p38/MAPK activation in colon cancer cells Biochem. Biophys. Res. Commun. 359 2007 102 107
13. M. Campbell-Thompson, I.J. Lynch, and B. Bhardwaj Expression of estrogen receptor (ER) subtypes and ERβ isoforms in colon cancer Cancer Res. 61 2001 632 640
14. cx isoforms in non-neoplastic endometrium and in endometrioid carcinoma Int. J. Gynecol. Cancer 17 2007 905 913
15. E. De Marinis, E. Acaz-Fonseca, M.A. Arevalo, P. Ascenzi, M. Fiocchetti, M. Marino, and L.M. Garcia-Segura 17β-Oestradiol anti-inflammatory effects in primary astrocytes require oestrogen receptor β-mediated neuroglobin up-regulation J. Neuroendocrinol. 25 2013 260 270
16. 2-induced toxicity Neurosignals 18 2010 223 235
17. 2-induced apoptosis of neuroblastoma Cell Death Dis. 4 2013 e508
18. J.J. DeCosse, S.S. Ngoi, J.S. Jacobson, and W.J. Cennerazzo Gender and colorectal cancer Eur. J. Cancer Prev. 2 1993 105 115
19. B.J. Deroo, and K.S. Korach Estrogen receptors and human disease J. Clin. Invest. 116 2006 561 570
20. M. Emara, A.R. Turner, and J. Allalunis-Turner Hypoxic regulation of cytoglobin and neuroglobin expression in human normal and tumor tissues Cancer Cell Int. 10 2010 33
21. A. Fago, A.J. Mathews, S. Dewilde, L. Moens, and T. Brittain The reactions of neuroglobin with CO: evidence for two forms of the ferrous protein J. Inorg. Biochem. 100 2006 1339 1343
22. M. Fiocchetti, P. Ascenzi, and M. Marino Neuroprotective effects of 17β-estradiol rely on estrogen receptor membrane initiated signals Front. Physiol. 3 2012 73
23. M. Fiocchetti, E. De Marinis, P. Ascenzi, and M. Marino Neuroglobin and neuronal survival Biochim. Biophys. Acta 1834 2013 1744 1749
24. M. Fiocchetti, M.T. Nuzzo, P. Totta, F. Acconcia, P. Ascenzi, and M. Marino Neuroglobin, a pro-survival player in estrogen receptor α-positive cancer cells Cell Death Dis. 5 2014 e1449
25. E.F. Foley, A.A. Jazaeri, M.A. Shupnik, O. Jazaeri, and L.W. Rice Selective loss of estrogen receptor β in malignant human colon Cancer Res. 60 2000 245 248
26. E.M. Fox, J. Andrade, and M.A. Shupnik Novel actions of estrogen to promote proliferation: integration of cytoplasmic and nuclear pathways Steroids 74 2009 622 627
27. P. Galluzzo, F. Caiazza, S. Moreno, and M. Marino Role of ERβ palmitoylation in the inhibition of human colon cancer cell proliferation Endocr. Relat. Cancer 14 2007 153 167
28. T.A. Gorr, D. Wichmann, C. Pilarsky, J.P. Theurillat, A. Fabrizius, T. Laufs, T. Bauer, M. Koslowski, S. Horn, T. Burmester, T. Hankeln, and G. Kristiansen Old proteins-new locations: myoglobin, haemoglobin, neuroglobin and cytoglobin in solid tumours and cancer cells Acta Physiol. 202 2011 563 581
29. D.A. Greenberg, K. Jin, and A.A. Curr Neuroglobin: an endogenous neuroprotectant Curr. Opin. Pharmacol. 8 2008 20 24
30. F. Grodstein, P.A. Newcomb, and M.J. Stampfer Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis Am. J. Med. 106 1999 574 582
31. J. Hartman, K. Edvardsson, K. Lindberg, C. Zhao, C. Williams, A. Ström, and J.-A. Gustafsson Tumor repressive functions of estrogen receptor β in SW480 colon cancer cells Cancer Res. 69 2009 6100 6106
32. N. Heldring, A. Pike, S. Andersson, J. Matthews, G. Cheng, J. Hartman, M. Tujague, A. Ström, E. Treuter, M. Warner, and J.-A. Gustafsson Estrogen receptors: how do they signal and what are their targets Physiol. Rev. 87 2007 905 931
33. O. Imamov, G.J. Shim, M. Warner, and J.-A. Gustafsson Estrogen receptor β in health and disease Biol. Reprod. 73 2005 866 871
34. J.P. Issa, Y.L. Ottaviano, P. Celano, S.R. Hamilton, N.E. Davidson, and S.B. Baylin Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon Nat. Genet. 7 1994 536 540
35. R. Kennelly, D.O. Kavanagh, A.M. Hogan, and D.C. Winter Oestrogen and the colon: potential mechanisms for cancer prevention Lancet Oncol. 9 2008 385 391
36. A.A. Khan, Y. Wang, Y. Sun, X.O. Mao, L. Xie, E. Miles, J. Graboski, S. Chen, L.M. Ellerby, K. Jin, and D.A. Greenberg Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia Proc. Natl. Acad. Sci. U. S. A. 103 2006 17944 17948
37. P.A. Konstantinopoulos, A. Kominea, G. Vandoros, G.P. Sykiotis, P. Andricopoulos, Varakis I. Sotiropoulou-Bonikou, and A.G. Papavassiliou Oestrogen receptor β (ERβ) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation Eur. J. Cancer 39 2003 1251 1258
38. C.Y. Lin, A. Ström, S. Li Kong, S. Kietz, J.S. Thomsen, J.B. Tee, V.B. Vega, L.D. Miller, J. Smeds, J. Bergh, J.-A. Gustafsson, and E.T. Liu Inhibitory effects of estrogen receptor β on specific hormone-responsive gene expression and association with disease outcome in primary breast cancer Breast Cancer Res 9 2007 R25
39. M. Macaluso, M. Montanari, P.B. Noto, V. Gregorio, C. Bronner, and A. Giordano Epigenetic modulation of estrogen receptor-α by pRb family proteins: a novel mechanism in breast cancer Cancer Res. 67 2007 7731 7737
40. M. Marino, P. Galluzzo, S. Leone, F. Acconcia, and P. Ascenzi Nitric oxide impairs the 17β-estradiol-induced apoptosis in human colon adenocarcinoma cells Endocr. Relat. Cancer 13 2006 559 569
41. M. Marino Xenoestrogens challenge 17β-estradiol protective effects in colon cancer World J. Gastrointest. Oncol. 6 2014 67 73
42. J. Matthews, and J.-A. Gustafsson Estrogen signaling: a subtle balance between ERα and ERβ Mol. Interv. 3 2003 281 292
43. S. Ogawa, S. Inoue, T. Watanabe, H. Hiroi, A. Orimo, T. Hosoi, Y. Ouchi, and M. Muramatsu The complete primary structure of human estrogen receptor β (hERβ) and its heterodimerization with ERα in vivo and in vitro Biochem. Biophys. Res. Commun. 243 1998 122 126
44. U. Oleksiewicz, N. Daskoulidou, T. Liloglou, K. Tasopoulou, J. Bryan, J.R. Gosney, J.K. Field, and G. Xinarianos Neuroglobin and myoglobin in non-small cell lung cancer: expression, regulation and prognosis Lung Cancer 74 2011 411 418
45. D. Peroni, A. Negro, M. Bahr, and G.P. Dietz Intracellular delivery of Neuroglobin using HIV-1 TAT protein transduction domain fails to protect against oxygen and glucose deprivation Neurosci. Lett. 421 2007 110 114
46. Y. Qiu, C.E. Waters, A.E. Lewis, M.J. Langman, and M.C. Eggo Oestrogen-induced apoptosis in colonocytes expressing oestrogen receptor β J. Endocrinol. 174 2002 369 377
47. S. Raychaudhuri, J. Skommer, K. Henty, N. Birch, and T. Brittain Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death Apoptosis 15 2010 401 411
48. S. Reuss, S. Saaler-Reinhardt, B. Weich, S. Wystub, M.H. Reuss, T. Burmester, and T. Hankeln Expression analysis of neuroglobin mRNA in rodent tissues Neuroscience 115 2002 645 656
49. M. Schmidt, A. Giessl, T. Laufs, T. Hankeln, U. Wolfrum, and T. Burmester How does the eye breathe? Evidence for neuroglobin-mediated oxygen supply in the mammalian retina J. Biol. Chem. 278 2003 1932 1935
50. cx/beta2 is correlated with better prognosis in breast cancer Jpn. J. Clin. Oncol. 37 2007 820 828
51. Y. Sun, K. Jin, X.O. Mao, Y. Zhu, and D.A. Greenberg Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury Proc. Natl. Acad. Sci. U. S. A. 98 2001 15306 15311
52. Y. Sun, K. Jin, A. Peel, X.O. Mao, L. Xie, and D.A. Greenberg Neuroglobin protects the brain from experimental stroke in vivo Proc. Natl. Acad. Sci. U. S. A. 100 2003 3497 3500
53. C. Thomas, and J.-A. Gustafsson The different roles of ER subtypes in cancer biology and therapy Nat. Rev. Cancer 11 2011 597 608
54. P. Totta, V. Pesiri, M. Marino, and F. Acconcia Lysosomal function is involved in 17β-estradiol-induced estrogen receptor α degradation and cell proliferation PLoS One 9 2014 e94880
55. O. Wada-Hiraike, O. Imamov, H. Hiraike, K. Hultenby, T. Schwend, Y. Omoto, M. Warner, and J-Å. Gustafsson Role of estrogen receptor β in colonic epithelium Proc. Natl. Acad. Sci. U. S. A. 103 2006 2959 2964
56. N.A. Wong, R.D. Malcomson, D.I. Jodrell, N.P. Groome, D.J. Harrison, and P.T. Saunders ERβ isoform expression in colorectal carcinoma: an in vivo and in vitro study of clinicopathological and molecular correlates J. Pathol. 207 2005 53 60
57. S. Wystub, T. Laufs, M. Schmidt, T. Burmester, U. Maas, S. Saaler-Reinhardt, T. Hankeln, and S. Reuss Localization of neuroglobin protein in the mouse brain Neurosci. Lett. 346 2003 114 116
58. Z. Yu, J. Xu, N. Liu, Y. Wang, X. Li, S. Pallast, K. Leyen, and X. Wang Mitochondrial distribution of neuroglobin and its response to oxygen-glucose deprivation in primary-cultured mouse cortical neurons Neuroscience 218 2012 235 242
59. C. Zhang, C. Wang, M. Deng, L. Li, H. Wang, M. Fan, W. Xu, F. Meng, L. Qian, and F. He Full-length cDNA cloning of human neuroglobin and tissue expression of rat neuroglobin Biochem. Biophys. Res. Commun. 290 2002 1411 1419
60. J. Zhang, S.J. Lan, Q.R. Liu, J.M. Liu, and X.Q. Chen Neuroglobin, a novel intracellular hexa-coordinated globin, functions as a tumor suppressor in hepatocellular carcinoma via Raf/MAPK/Erk Mol. Pharmacol. 83 2013 1109 1119
61. G.Y. Zhou, S.N. Zhou, Z.Y. Lou, C.S. Zhu, X.P. Zheng, and X.Q. Hu Translocation and neuroprotective properties of transactivator of transcription protein transduction domain neuroglobin fusion protein in primary cultured cortical neurons Biotechnol. Appl. Biochem. 49 2008 25 33
62. A.S. Varner, C.E. Ducker, Z. Xia, Y. Zhuang, M.L. De Vos, and C.D. Smith Characterization of human palmitoyl-acyl transferase activity using peptides that mimic distinct palmitoylation motifs Biochem. J. 373 2003 91 99