HtrA1 is induced by oxidative stress and enhances cell senescence through p38 MAPK pathway

Experimental Eye Research

Volumn 112, Issue , 2013, Pages 79-92

  Supanji, ^a,b   Shimomachi, Mari ^a   Hasan, Md Zobaer ^a   Kawaichi, Masashi ^a   Oka, Chio ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b GADJAH MADA UNIVERSITY   (Indonesia)

Author keywords

Age related macular degeneration; AMD; HtrA1; Oxidative stress; P38 MAPK; Retinal pigment epithelium; Senescence

Indexed keywords

BETA GALACTOSIDASE; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; HTRA1 ENZYME; HYDROGEN PEROXIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL AGING; CELL DEATH; CONTROLLED STUDY; EMBRYONIC FIBROBLAST; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FIBROBLAST; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL AGING; FEMALE; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NIH 3T3 CELLS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLASMIDS; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; TRANSFECTION; UP-REGULATION;

EID: 84877912239     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.04.013     Document Type: Article

References (78)

1. Risk factors associated with age-related macular degeneration. A case-control study in the age-related eye disease study: age-related eye disease study report number 3. Ophthalmology 2000, 107:2224-2232. Age-Related Eye Disease Study Research Group.
2. Ajayi F., Kongoasa N., Gaffey T., Asmann Y.W., Watson W.J., Baldi A., Lala P., Shridhar V., Brost B., Chien J. Elevated expression of serine protease HtrA1 in preeclampsia and its role in trophoblast cell migration and invasion. Am. J. Obstet. Gynecol. 2008, 199:557. e1-557.10.
3. Alba B.M., Gross C.A. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 2004, 52:613-619.
4. An E., Sen S., Park S.K., Gordish-Dressman H., Hathout Y. Identification of novel substrates for the serine protease HTRA1 in the human RPE secretome. Invest. Ophthalmol. Vis. Sci. 2010, 51:3379-3386.
5. Austin B.A., Liu B., Li Z., Nussenblatt R.B. Biologically active fibronectin fragments stimulate release of MCP-1 and catabolic cytokines from murine retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 2009, 50:2896-2902.
6. Baldi A., De Luca A., Morini M., Battista T., Felsani A., Baldi F., Catricala C., Amantea A., Noonan D.M., Albini A., Natali P.G., Lombardi D., Paggi M.G. The HtrA1 serine protease is down-regulated during human melanoma progression and represses growth of metastatic melanoma cells. Oncogene 2002, 21:6684-6688.
7. Bartholomew J.N., Volonte D., Galbiati F. Caveolin-1 regulates the antagonistic pleiotropic properties of cellular senescence through a novel Mdm2/p53-mediated pathway. Cancer Res. 2009, 69:2878-2886.
8. Bulavin D.V., Phillips C., Nannenga B., Timofeev O., Donehower L.A., Anderson C.W., Appella E., Fornace A.J. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat. Genet. 2004, 36:343-350.
9. Cai W., Rudolph J.L., Harrison S.M., Jin L., Frantz A.L., Harrison D.A., Andres D.A. An evolutionarily conserved Rit GTPase-p38 MAPK signaling pathway mediates oxidative stress resistance. Mol. Biol. Cell 2011, 22:3231-3241.
10. Chien J., Ota T., Aletti G., Shridhar R., Boccellino M., Quagliuolo L., Baldi A., Shridhar V. Serine protease HtrA1 associates with microtubules and inhibits cell migration. Mol. Cell. Biol. 2009, 29:4177-4187.
11. Chien J., Staub J., Hu S.I., Erickson-Johnson M.R., Couch F.J., Smith D.I., Crowl R.M., Kaufmann S.H., Shridhar V. Acandidate tumor suppressor HtrA1 is downregulated in ovarian cancer. Oncogene 2004, 23:1636-1644.
12. Chowers I., Meir T., Lederman M., Goldenberg-Cohen N., Cohen Y., Banin E., Averbukh E., Hemo I., Pollack A., Axer-Siegel R., Weinstein O., Hoh J., Zack D.J., Galbinur T. Sequence variants in HTRA1 and LOC387715/ARMS2 and phenotype and response to photodynamic therapy in neovascular age-related macular degeneration in populations from Israel. Mol. Vis. 2008, 14:2263-2271.
13. Clausen T., Kaiser M., Huber R., Ehrmann M. HTRA proteases: regulated proteolysis in protein quality control. Nat. Rev. Mol. Cell. Biol. 2011, 12:152-162.
14. Clausen T., Southan C., Ehrmann M. The HtrA family of proteases: implications for protein composition and cell fate. Mol. Cell. 2002, 10:443-455.
15. Coleman H.R., Chan C.C., Ferris F.L., Chew E.Y. Age-related macular degeneration. Lancet 2008, 372:1835-1845.
16. Cong R., Zhou B., Sun Q., Gu H., Tang N., Wang B. Smoking and the risk of age-related macular degeneration: a meta-analysis. Ann. Epidemiol. 2008, 18:647-656.
17. Congdon N., O'Colmain B., Klaver C.C., Klein R., Munoz B., Friedman D.S., Kempen J., Taylor H.R., Mitchell P. Causes and prevalence of visual impairment among adults in the United States. Arch. Ophthalmol. 2004, 122:477-485. Eye Diseases Prevalence Research Group.
18. Cruickshanks K.J., Klein R., Klein B.E. Sunlight and age-related macular degeneration. The Beaver Dam Eye Study. Arch. Ophthalmol. 1993, 111:514-518.
19. DeWan A., Bracken M.B., Hoh J. Two genetic pathways for age-related macular degeneration. Curr. Opin. Genet. Dev. 2007, 17:228-233.
20. Dewan A., Liu M., Hartman S., Zhang S.S., Liu D.T., Zhao C., Tam P.O., Chan W.M., Lam D.S., Snyder M., Barnstable C., Pang C.P., Hoh J. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science 2006, 314:989-992.
21. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O. Abiomarker that identifies senescent human cells in culture and in aging skin invivo. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9363-9367.
22. Dong A., Xie B., Shen J., Yoshida T., Yokoi K., Hackett S.F., Campochiaro P.A. Oxidative stress promotes ocular neovascularization. J.Cell. Physiol. 2009, 219:544-552.
23. Dunn K.C., Aotaki-Keen A.E., Putkey F.R., Hjelmeland L.M. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 1996, 62:155-169.
24. Evans J.R. Risk factors for age-related macular degeneration. Prog. Retin. Eye Res. 2001, 20:227-253.
25. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
26. Foucaud-Scheunemann C., Poquet I. HtrA is a key factor in the response to specific stress conditions in Lactococcus lactis. FEMS Microbiol. Lett. 2003, 224:53-59.
27. Gao H., Hollyfield J.G. Aging of the human retina. Differential loss of neurons and retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 1992, 33:1-17.
28. Gehrs K.M., Anderson D.H., Johnson L.V., Hageman G.S. Age-related macular degeneration-emerging pathogenetic and therapeutic concepts. Ann. Med. 2006, 38:450-471.
29. Gemba T., Valbracht J., Alsalameh S., Lotz M. Focal adhesion kinase and mitogen-activated protein kinases are involved in chondrocyte activation by the 29-kDa amino-terminal fibronectin fragment. J.Biol. Chem. 2002, 277:907-911.
30. Gil J., Peters G. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat. Rev. Mol. Cell. Biol. 2006, 7:667-677.
31. Grau S., Richards P.J., Kerr B., Hughes C., Caterson B., Williams A.S., Junker U., Jones S.A., Clausen T., Ehrmann M. The role of human HtrA1 in arthritic disease. J.Biol. Chem. 2006, 281:6124-6129.
32. Gutierrez-Uzquiza A., Arechederra M., Molina I., Banos R., Maia V., Benito M., Guerrero C., Porras A. C3G down-regulates p38 MAPK activity in response to stress by Rap-1 independent mechanisms: involvement in cell death. Cell. Signal. 2010, 22:533-542.
33. Hadfield K.D., Rock C.F., Inkson C.A., Dallas S.L., Sudre L., Wallis G.A., Boot-Handford R.P., Canfield A.E. HtrA1 inhibits mineral deposition by osteoblasts: requirement for the protease and PDZ domains. J.Biol. Chem. 2008, 283:5928-5938.
34. Harlow E., Lane D. Antibodies. A Laboratory Manual 1988, Cold Spring Harbor Laboratory.
35. Hara K., Shiga A., Fukutake T., Nozaki H., Miyashita A., Yokoseki A., Kawata H., Koyama A., Arima K., Takahashi T., Ikeda M., Shiota H., Tamura M., Shimoe Y., Hirayama M., Arisato T., Yanagawa S., Tanaka A., Nakano I., Ikeda S., Yoshida Y., Yamamoto T., Ikeuchi T., Kuwano R., Nishizawa M., Tsuji S., Onodera O. Association of HTRA1 mutations and familial ischemic cerebral small-vessel disease. N.Engl. J. Med. 2009, 360:1729-1739.
36. He X., Khurana A., Maguire J.L., Chien J., Shridhar V. HtrA1 sensitizes ovarian cancer cells to cisplatin-induced cytotoxicity by targeting XIAP for degradation. Int. J. Cancer 2012, 130:1029-1035.
37. Hu S.I., Carozza M., Klein M., Nantermet P., Luk D., Crowl R.M. Human HtrA, an evolutionarily conserved serine protease identified as a differentially expressed gene product in osteoarthritic cartilage. J.Biol. Chem. 1998, 273:34406-34412.
38. Iwasa H., Han J., Ishikawa F. Mitogen-activated protein kinase p38 defines the common senescence-signalling pathway. Genes Cells 2003, 8:131-144.
39. Jones A., Kumar S., Zhang N., Tong Z., Yang J.H., Watt C., Anderson J., Amrita, Fillerup H., McCloskey M., Luo L., Yang Z., Ambati B., Marc R., Oka C., Zhang K., Fu Y. Increased expression of multifunctional serine protease, HTRA1, in retinal pigment epithelium induces polypoidal choroidal vasculopathy in mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14578-14583.
40. Justilien V., Pang J.J., Renganathan K., Zhan X., Crabb J.W., Kim S.R., Sparrow J.R., Hauswirth W.W., Lewin A.S. SOD2 knockdown mouse model of early AMD. Invest. Ophthalmol. Vis. Sci. 2007, 48:4407-4420.
41. Kasahara E., Lin L.R., Ho Y.S., Reddy V.N. SOD2 protects against oxidation-induced apoptosis in mouse retinal pigment epithelium: implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2005, 46:3426-3434.
42. Kim G.Y., Mercer S.E., Ewton D.Z., Yan Z., Jin K., Friedman E. The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation. J.Biol. Chem. 2002, 277:29792-29802.
43. Klein R., Klein B.E., Linton K.L., DeMets D.L. The Beaver Dam Eye Study: the relation of age-related maculopathy to smoking. Am. J. Epidemiol. 1993, 137:190-200.
44. Kurz T., Karlsson M., Brunk U.T., Nilsson S.E., Frennesson C. ARPE-19 retinal pigment epithelial cells are highly resistant to oxidative stress and exercise strict control over their lysosomal redox-active iron. Autophagy 2009, 5:494-501.
45. Larsson L.G. Oncogene- and tumor suppressor gene-mediated suppression of cellular senescence. Semin. Cancer Biol. 2011, 21:367-376.
46. Lin K.L., Chou C.H., Hsieh S.C., Hwa S.Y., Lee M.T., Wang F.F. Transcriptional upregulation of DDR2 by ATF4 facilitates osteoblastic differentiation through p38 MAPK-mediated Runx2 activation. J.Bone Miner. Res. 2010, 25:2489-2503.
47. Loosmore S.M., Yang Y.P., Oomen R., Shortreed J.M., Coleman D.C., Klein M.H. The Haemophilus influenzae HtrA protein is a protective antigen. Infect. Immun. 1998, 66:899-906.
48. MacLaren A., Black E.J., Clark W., Gillespie D.A. c-Jun-deficient cells undergo premature senescence as a result of spontaneous DNA damage accumulation. Mol. Cell. Biol. 2004, 24:9006-9018.
49. Martindale J.L., Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J.Cell. Physiol. 2002, 192:1-15.
50. Matsuzawa A., Ichijo H. Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim. Biophys. Acta 2008, 1780:1325-1336.
51. Mullany S.A., Moslemi-Kebria M., Rattan R., Khurana A., Clayton A., Ota T., Mariani A., Podratz K.C., Chien J., Shridhar V. Expression and functional significance of HtrA1 loss in endometrial cancer. Clin. Cancer Res. 2011, 17:427-436.
52. Murwantoko, Yano M., Ueta Y., Murasaki A., Kanda H., Oka C., Kawaichi M. Binding of proteins to the PDZ domain regulates proteolytic activity of HtrA1 serine protease. Biochem. J. 2004, 381:895-904.
53. Ng T.K., Yam G.H., Chen W.Q., Lee V.Y., Chen H., Chen L.J., Choy K.W., Yang Z., Pang C.P. Interactive expressions of HtrA1 and VEGF in human vitreous humors and fetal RPE cells. Invest. Ophthalmol. Vis. Sci. 2011, 52:3706-3712.
54. Nie G.Y., Hampton A., Li Y., Findlay J.K., Salamonsen L.A. Identification and cloning of two isoforms of human high-temperature requirement factor A3 (HtrA3), characterization of its genomic structure and comparison of its tissue distribution with HtrA1 and HtrA2. Biochem. J. 2003, 371:39-48.
55. Oka C., Tsujimoto R., Kajikawa M., Koshiba-Takeuchi K., Ina J., Yano M., Tsuchiya A., Ueta Y., Soma A., Kanda H., Matsumoto M., Kawaichi M. HtrA1 serine protease inhibits signaling mediated by Tgfbeta family proteins. Development 2004, 131:1041-1053.
56. Onder O., Turkarslan S., Sun D., Daldal F. Overproduction or absence of the periplasmic protease DegP severely compromises bacterial growth in the absence of the dithiol: disulfide oxidoreductase DsbA. Mol. Cell. Proteomics 2008, 7:875-890.
57. Pocrnich C.E., Liu H., Feng M., Peng T., Feng Q., Hutnik C.M. P38 mitogen-activated protein kinase protects human retinal pigment epithelial cells exposed to oxidative stress. Can. J. Ophthalmol. 2009, 44:431-436.
58. Polur I., Lee P.L., Servais J.M., Xu L., Li Y. Role of HTRA1, a serine protease, in the progression of articular cartilage degeneration. Histol. Histopathol. 2010, 25:599-608.
59. Serrano M., Lin A.W., McCurrach M.E., Beach D., Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997, 88:593-602.
60. Shaw P.X., Zhang L., Zhang M., Du H., Zhao L., Lee C., Grob S., Lim S.L., Hughes G., Lee J., Bedell M., Nelson M.H., Lu F., Krupa M., Luo J., Ouyang H., Tu Z., Su Z., Zhu J., Wei X., Feng Z., Duan Y., Yang Z., Ferreyra H., Bartsch D.U., Kozak I., Zhang L., Lin F., Sun H., Feng H., Zhang K. Complement factor H genotypes impact risk of age-related macular degeneration by interaction with oxidized phospholipids. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(34):13757-13762.
61. Skorko-Glonek J., Zurawa D., Kuczwara E., Wozniak M., Wypych Z., Lipinska B. The Escherichia coli heat shock protease HtrA participates in defense against oxidative stress. Mol. Gen. Genet. 1999, 262:342-350.
62. Smeds A., Varmanen P., Palva A. Molecular characterization of a stress-inducible gene from Lactobacillus helveticus. J.Bacteriol. 1998, 180:6148-6153.
63. Thornton J., Edwards R., Mitchell P., Harrison R.A., Buchan I., Kelly S.P. Smoking and age-related macular degeneration: a review of association. Eye (Lond.) 2005, 19:935-944.
64. Timmers C., Sharma N., Opavsky R., Maiti B., Wu L., Wu J., Orringer D., Trikha P., Saavedra H.I., Leone G. E2f1, E2f2, and E2f3 control E2F target expression and cellular proliferation via a p53-dependent negative feedback loop. Mol. Cell. Biol. 2007, 27:65-78.
65. Tocharus J., Tsuchiya A., Kajikawa M., Ueta Y., Oka C., Kawaichi M. Developmentally regulated expression of mouse HtrA3 and its role as an inhibitor of TGF-beta signaling. Dev. Growth Differ. 2004, 46:257-274.
66. Tsuchiya A., Yano M., Tocharus J., Kojima H., Fukumoto M., Kawaichi M., Oka C. Expression of mouse HtrA1 serine protease in normal bone and cartilage and its upregulation in joint cartilage damaged by experimental arthritis. Bone 2005, 37:323-336.
67. Tuo J., Ross R.J., Reed G.F., Yan Q., Wang J.J., Bojanowski C.M., Chew E.Y., Feng X., Olsen T.W., Ferris F.L., Mitchell P., Chan C.C. The HtrA1 promoter polymorphism, smoking, and age-related macular degeneration in multiple case-control samples. Ophthalmology 2008, 115:1891-1898.
68. Vierkotten S., Muether P.S., Fauser S. Overexpression of HTRA1 leads to ultrastructural changes in the elastic layer of Bruch's membrane via cleavage of extracellular matrix components. PLoS One 2011, 6:e22959.
69. Wada T., Stepniak E., Hui L., Leibbrandt A., Katada T., Nishina H., Wagner E.F., Penninger J.M. Antagonistic control of cell fates by JNK and p38-MAPK signaling. Cell. Death Differ. 2008, 15:89-93.
70. Wang E. Senescent human fibroblasts resist programmed cell death, and failure to suppress bcl2 is involved. Cancer Res. 1995, 55:2284-2292.
71. Weismann D., Hartvigsen K., Lauer N., Bennett K.L., Scholl H.P., Charbel Issa P., Cano M., Brandstatter H., Tsimikas S., Skerka C., Superti-Furga G., Handa J.T., Zipfel P.F., Witztum J.L., Binder C.J. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature 2011, 478:76-81.
72. Winkler B.S., Boulton M.E., Gottsch J.D., Sternberg P. Oxidative damage and age-related macular degeneration. Mol. Vis. 1999, 5:32.
73. Yang Z., Camp N.J., Sun H., Tong Z., Gibbs D., Cameron D.J., Chen H., Zhao Y., Pearson E., Li X., Chien J., Dewan A., Harmon J., Bernstein P.S., Shridhar V., Zabriskie N.A., Hoh J., Howes K., Zhang K. Avariant of the HTRA1 gene increases susceptibility to age-related macular degeneration. Science 2006, 314:992-993.
74. Yang Z., Tong Z., Chen Y., Zeng J., Lu F., Sun X., Zhao C., Wang K., Davey L., Chen H., London N., Muramatsu D., Salasar F., Carmona R., Kasuga D., Wang X., Bedell M., Dixie M., Zhao P., Yang R., Gibbs D., Liu X., Li Y., Li C., Li Y., Campochiaro B., Constantine R., Zack D.J., Campochiaro P., Fu Y., Li D.Y., Katsanis N., Zhang K. Genetic and functional dissection of HTRA1 and LOC387715 in age-related macular degeneration. PLoS Genet. 2010, 6:e1000836.
75. Young R.W. Pathophysiology of age-related macular degeneration. Surv. Ophthalmol. 1987, 31:291-306.
76. Zhou J.Y., Liu Y., Wu G.S. The role of mitogen-activated protein kinase phosphatase-1 in oxidative damage-induced cell death. Cancer Res. 2006, 66:4888-4894.
77. Zhu D., Wu J., Spee C., Ryan S.J., Hinton D.R. BMP4 mediates oxidative stress-induced retinal pigment epithelial cell senescence and is overexpressed in age-related macular degeneration. J.Biol. Chem. 2009, 284:9529-9539.
78. Zurawa-Janicka D., Kobiela J., Stefaniak T., Wozniak A., Narkiewicz J., Wozniak M., Limon J., Lipinska B. Changes in expression of serine proteases HtrA1 and HtrA2 during estrogen-induced oxidative stress and nephrocarcinogenesis in male Syrian hamster. Acta Biochim. Pol. 2008, 55:9-19.