Role of PTHrP in human intestinal Caco-2 cell response to oxidative stress

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 2834-2843

  Lezcano, Virginia ^a   Gentili, Claudia ^a   De Boland, Ana Russo ^a  

^a UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

AKT; Apoptosis; Caco 2 cell; MAPK; PTHrP

Indexed keywords

HEAT SHOCK PROTEIN 27; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PARATHYROID HORMONE; PARATHYROID HORMONE RELATED PROTEIN; PROTEIN BAX; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE 1;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN CACO 2; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

EID: 84882755902     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.06.029     Document Type: Article

References (73)

1. Jermal A., Siegel R., Ward E., Murray T., Xu J., Thun M.J. Cancer statistics, 2007. CA Cancer J. Clin. 2007, 57:43-66.
2. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55:74-108.
3. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
4. Kopfstein L., Christofori G. Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment. Cell. Mol. Life Sci. 2006, 63:449-468.
5. Kohn E.C., Liotta L.A. Molecular insights into cancer invasion: strategies for prevention and intervention. Cancer Res. 1995, 55:1856-1862.
6. Ozanne B.W., Spence H.J., McGarry L.C., Hennigan R.F. Invasion is a genetic program regulated by transcription factors. Curr. Opin. Genet. Dev. 2006, 16:65-70.
7. Nishihara M., Ito M., Tomioka T., Ohtsuru A., Tagashi T., Kanematsu T. Clinicopathological implications of parathyroid hormone-related protein in human colorectal tumours. J. Pathol. 1999, 187:217-222.
8. Suva L.J., Winslow G.A., Wettenhall R.E., Hammonds R.G., Moseley J.M., Diefenbach-Jagger H., Rodda C.P., Kemp B.E., Rodriguez H., Chen E.Y., et al. A parathyroid hormone-related protein implicated in malignant hypercalcemia: cloning and expression. Science 1987, 237:893-896.
9. Gentili C., Morelli S., Russo de Boland A. Characterization of PTH/PTHrP receptor in rat duodenum: effects of ageing. J. Cell. Biochem. 2003, 88:1157-1167.
10. Urena P., Kong X.F., Abou-Samra A.B., Juppner H., Kronenberg H.M., Potts J.T., Segre G.V. Parathyroid hormone (PTH)/PTH-related peptide receptor messenger ribonucleic acids are widely distributed in rat tissues. Endocrinology 1993, 133:617-623.
11. Maioli E., Fortino V. The complexity of parathyroid hormone-related protein signaling. Cell. Mol. Life Sci. 2004, 61:257-262.
12. Strewler G.I. Mechanisms of disease: the physiology of parathyroid hormone-related protein. N. Engl. J. Med. 2000, 342:177-185.
13. Guise T.A. Molecular mechanisms of osteolytic bone metastases. Cancer 2000, 88:2892-2898.
14. Rabbani S.A., Gladu J., Harakidas P., Jamison B., Goltzman D. Over-production of parathyroid hormone-related peptide results in increased osteolytic metastasis by prostate cancer cells in vivo. Int. J. Cancer 1999, 80:257-264.
15. Hoey R.P., Sanderson C., Iddon J., Brady G., Bundred N.J., Anderson N.G. The parathyroid hormone-related protein receptor is expressed in breast cancer bone metastases and promotes autocrine proliferation in breast carcinoma cells. Br. J. Cancer 2003, 88:567-573.
16. Weilbaecher K.N., Guise T.A., McCauley L.K. Cancer to bone: a fatal attraction. Nat. Rev. Cancer 2011, 11:411-425.
17. Li X., Loberg R.D., Liao J., Ying C., Snyder L.A., Pienta K.J., McCauley L.K. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res. 2009, 69:1685-1692.
18. Deftos L.J., Barken I., Burton D.W., Hoffman R.M., Geller J. Direct evidence that PTHrP expression promotes prostate cancer progression in bone. Biochem. Biophys. Res. Commun. 2005, 327:468-472.
19. Sourbier C., Massfelder T. Parathyroid hormone-related protein in human renal cell carcinoma. Cancer Lett. 2006, 240:170-182.
20. Shu S.T., Dirksen W.P., Lanigan L.G., Martin C.K., Thudi N.K., Werbeck J.L., Fernandez S.A., Hildreth B.E., Rosol T.J. Effects of parathyroid hormone-related protein and macrophage inflammatory protein-1a in Jurkat T-cells on tumor formation in vivo and expression of apoptosis regulatory genes in vitro. Leuk. Lymphoma 2012, 53:688-698.
21. Ramachandran A., Madesh M., Balasubramanian K.A. Apoptosis in the intestinal epithelium: its relevance in normal and pathophysiological conditions. J. Gastroenterol. Hepatol. 2000, 15:109-120.
22. Butler L.M., Hewett P.J., Fitridge R.A., Cowled P.A. Deregulation of apoptosis in colorectal carcinoma: theoretical and therapeutics implications. Aust. NZ J. Surg. 1999, 69:88-94.
23. Calvo N., German O., Russo de Boland A., Gentili C. Pro-apoptotic effects of parathyroid hormone in intestinal cells. Biochem. Cell Biol. 2009, 87:389-400.
24. Zerega B., Cermelli S., Bianco P., Cancedda R., Cancedda F.D. Parathyroid hormone [PTH(1-34)] and parathyroid hormone related protein [PTHrP(1-34)] promote reversion of hypertrophic chondrocytes to a prehypertrophic proliferating phenotype and prevent terminal differentiation of osteoblast-like cells. J. Miner. Res. 1999, 14:1281-1289.
25. Turner P.R., Mefford S., Christakos S., Nissenson R.A. Apoptosis mediated by activation of the G protein-coupled receptor for parathyroid hormone (PTH)/PTH-related protein (PTHrP). Mol. Endocrinol. 2000, 14:241-254.
26. Chen H., Demiralp B., Schneider A., Koh A., Silve C., Wang C., McCauley L.K. Parathyroid hormone and parathyroid hormone-related protein exert both pro- and anti-apoptotic effects in mesenchymal cells. J. Biol. Chem. 2002, 277:19374-19381.
27. Bradford M.M. A rapid and sensitive method for quantification of microgram quantities of proteins utilizing the principle of protein binding. Anal. Biochem. 1976, 72:248-254.
28. Minamikawa T., Sriratana A., Williams D.A., Bowser D.N., Hill J.S., Nagley P.J. Chloromethyl-X-rosamine (MitoTracker Red) photosensitises mitochondria and induces apoptosis in intact human cells. Cell Sci. 1999, 112:2419-2430.
29. Snedecor G.W., Cochran W.G. Statistical Methods 1967, Iowa State University Press, Ames, Iowa. 6th edition.
30. Adams J.M., Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 2001, 26:61-66.
31. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, Bax, lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 2002, 111:331-342.
32. Karczewski J.M., Jurgen M. Oxidative stress and cytotoxicity in intestinal epithelium. Department of Toxicology 1999, University of Nijmegen, The Netherlands.
33. Mannstadt M., Juppner H., Gardella T.J. Receptors for PTH and PTHrP: their biological importance and functional properties. Am. J. Physiol. 1999, 277:665-675.
34. Mahon M.J., Donowitz M., Yun C.C., Segre G.V. Na(+)/H(+) exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 2002, 417:858-861.
35. Mahon M.J., Segre G.V. Stimulation by parathyroid hormone of a NHERF-1-assembled complex consisting of the parathyroid hormone I receptor, phospholipase C beta, and actin increases intracellular calcium in opossum kidney cells. J. Biol. Chem. 2004, 279:23550-23558.
36. Gesty-Palmer D., Chen M., Reiter E., Ahn S., Nelson C.D., Wang S., Eckhardt A.E., Cowan C.L., Spurney R.F., Luttrell L.M., Lefkowitz R.J. Distinct β-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 2006, 281:10856-10864.
37. Baker J.G., Halland I.P., Hill S.J. Agonist and inverse agonist actions of 'β-blockers' at the human β2-adrenoceptor provide evidence for agonist directed signalling. Mol. Pharmacol. 2003, 64:1357-1369.
38. Seta K., Nanamori M., Modrall J.G., Neubig R.R., Sadoshima J. AT1 receptor mutant lacking heterotrimeric G protein coupling activates the Src-Ras-ERK pathway without nuclear translocation of ERKs. J. Biol. Chem. 2002, 277:9268-9277.
39. Azzi M., Charest P.G., Angers S., Rousseau G., Kohout T., Bouvier M., Piñeyro G. Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein coupled receptors. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11406-11411.
40. Wei H., Ahn S., Shenoy S.K., Karnik S.S., Hunyady L., Luttrell L.M., Lefkowitz R.J. Independent β-arrestin2 and G-protein-mediated pathways for angiotensin II activation of extracellular signal regulated kinases 1 and 2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10782-10787.
41. Terrillon S., Bouvier M. Receptor-activity-independent recruitment of β-arrestin2 reveals specific signalling modes. EMBO J. 2004, 23:3950-3961.
42. Shenoy S.K., Drake M.T., Nelson C.D., Houtz D.A., Xiao K., Madabushi S., Reiter E., Premont R.T., Lichtarges O., Lefkowitz R.J. β-arrestin-dependent, G protein-independent ERK1/2 activation by the β2 adrenergic receptor. J. Biol. Chem. 2006, 281:1261-1273.
43. Charest P.G., Oligny-Longpré G., Bonin H., Azzi M., Bouvier M. The V2 vasopressin receptor stimulates ERK 1/2 activity independently of heterotrimeric G protein signalling. Cell. Signal. 2007, 19:32-41.
44. Häcker G. The morphology of apoptosis. Cell Tissue Res. 2000, 301:5-17.
45. Leist M., Single B., Castoldi A.F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 1997, 185:1481-1486.
46. Matteucci C., Grelli S., De Smaele E., Fontana C., Mastino A. Identification of nuclei from apoptotic, necrotic, and viable lymphoid cells by using multiparameter flow cytometry. Cytometry 1999, 35:145-153.
47. Ricchi P., Di Palma A., Di Matola T., Apicella A., Fortunato R., Zarrilli R., Acquaviva A.M. Aspirin protects Caco-2 cells from apoptosis after serum deprivation through the activation of a phosphatidylinositol 3-kinase/AKT/p21Cip/WAF1 pathway. Mol. Pharmacol. 2003, 64:407-414.
48. Wang X., Martindale J.L., Liu Y., Holbrook N.J. The cellular response to oxidative stress: influences of mitogen-activated protein kinase signaling pathways on cell survival. Biochem. J. 1998, 333:291-300.
49. Dalton T.P., Shertzer H.G., Puga A. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 1999, 39:67-101.
50. Schreck R., Rieber P., Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991, 10:2247-2258.
51. Griendling K.K., Harrison D.G. Dual role of reactive oxygen species in vascular growth. Circ. Res. 1999, 85:562-563.
52. Fruehauf J.P., Meyskens F.L. Reactive oxygen species: a breath of life or death?. Clin. Cancer Res. 2007, 13:789-794.
53. Storz P. Reactive oxygen species in tumor progression. Front. Biosci. 2005, 10:1881-1896.
54. Tandon R., Khanna H.D., Dorababu M., Goel R.K. Oxidative stress and antioxidant status in peptic ulcer and gastric carcinoma. Indian J. Physiol. Pharmacol. 2004, 48:115-118.
55. Thomson A., Hemphill D., Jeejeebhoy K.N. Oxidative stress and antioxidants in intestinal disease. Dig. Dis. 1998, 16:152-158.
56. Wijeratne S.K., Cuppett S.L., Schlegel V. Hydrogen peroxide induced oxidative stress damage and antioxidant enzyme response in Caco-2 human colon cells. J. Agric. Food Chem. 2005, 53:8768-8774.
57. Zhou Y., Wang Q., Mark Evers B., Chung D.H. Signal transduction pathways involved in oxidative stress-induced intestinal epithelial cell apoptosis. Pediatr. Res. 2005, 58:1192-1197.
58. 2 in C2C12 skeletal muscle cells through the apoptotic intrinsic pathway. J. Endocrinol. 2012, 212:371-381.
59. Hastings R.H., Quintana R.A., Sandoval R., Duey D., Yvette R., Burton D.W., Deftos L.J. Proapoptotic effects of parathyroid hormone-related protein in type II pneumocytes. Am. J. Respir. Cell Mol. Biol. 2003, 29:733-742.
60. Henderson J.E., Amizuka N., Warshawsky H., Bisotto D., Lanske B.M., Goltzman D., Karaplis A.C. Nucleolar localization of parathyroid hormone-related peptide enhances survival of chondrocytes under conditions that promote apoptotic cell death. Mol. Cell. Biol. 1995, 15:4064-4075.
61. Brines M.L., Ling Z., Broadus A.E. Parathyroid hormone-related protein protects against kainic acid excitotoxicity in rat cerebellar granule cells by regulating L-type channel calcium flux. Neurosci. Lett. 1999, 274:13-16.
62. Dougherty K.M., Blomme E.A., Koh A.J., Henderson J.E., Pienta K.J., Rosol T.J., McCauley L.K. Parathyroid hormone-related protein as a growth regulator of prostate carcinoma. Cancer Res. 1999, 59:6015-6022.
63. Hochane M., Raison D., Coquard C., Imhoff O., Massfelder T., Moulin B., Helwig J.J., Barthelmebs M. Parathyroid hormone-related protein is a mitogenic and a survival factor of mesangial cells from male mice: role of intracrine and paracrine pathways. Endocrinology 2013, 154:853-864.
64. Vasconsuelo A., Milanesi L., Boland R. Participation of HSP27 in the antiapoptotic action of 17β-estradiol in skeletal muscle cells. Cell Stress Chaperones 2010, 15:183-192.
65. Mehlen P., Schulze-Osthoff K., Arrigo A.P. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J. Biol. Chem. 1996, 271:16510-16514.
66. Samali A., Cotter T.G. Heat shock proteins increase resistance to apoptosis. Exp. Cell Res. 1996, 223:163-170.
67. Huot J., Houle F., Spitz D.R., Landry J. Hsp27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res. 1996, 56:273-279.
68. Bornman L., Steinmann C.M., Gericke G.S., Polla B.S. In vivo heat shock protects rat myocardial mitochondria. Biochem. Biophys. Res. Commun. 1998, 246:836-840.
69. 2+ disturbances, and cell death in renal epithelial cells. J. Biol. Chem. 1997, 272:21751-21759.
70. Musch M.W., Sugi K., Straus D., Chang E.B. Heat shock protein 72 protects against oxidant-induced injury of barrier function of human colonic epithelial Caco2/bbecells. Gastroenterology 1999, 117:115-122.
71. Carlson R.M., Vavricka S.R., Eloranta J.J., Musch M.W., Arvans D.L., Kles K.A., Walsh-Reitz M.M., Kullak-Ublick G.A., Chang E.B. fMLP induces Hsp27 expression, attenuates NF-κB activation, and confers intestinal epithelial cell protection. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:1070-1078.
72. Havasi A., Li Z., Wang Z., Martin J.L., Botla V., Ruchalski K., Schwartz J.H., Borkan S.C. Hsp27 inhibits Bax activation and apoptosis via a phosphatidylinositol 3-kinase-dependent mechanism. J. Biol. Chem. 2008, 283:12305-12313.
73. Fang X., Yu S., Eder A., Mao M., Bast R.C., Boyd D., Mills G.B. Regulation of BAD phosphorylation at serine 112 by the Ras-mitogen-activated protein kinase pathway. Oncogene 1999, 18:6635-6640.