Deficiency of Prdx6 in lens epithelial cells induces ER stress response-mediated impaired homeostasis and apoptosis

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 4, 2011, Pages

  Fatma, Nigar ^a   Singh, Prerna ^a   Chhunchha, Bhavana ^a   Kubo, Eri ^b   Shinohara, T ^a   Bhargavan, Biju ^a   Singh, Dhirendra P ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Antioxidant; Endoplasmic reticulum; Peroxiredoxin 6; Reactive oxygen species; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CALNEXIN; CALRETICULIN; CASPASE 12; CASPASE 3; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2ALPHA; PEROXIREDOXIN 6; PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; TUNICAMYCIN;

AGING; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL HYPOXIA; CELL MEMBRANE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; LENS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA INTERFERENCE; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HOMEOSTASIS; LENS, CRYSTALLINE; MICE; MICE, KNOCKOUT; PEROXIREDOXIN VI; STRESS, PHYSIOLOGICAL;

EID: 80053189509     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00061.2011     Document Type: Article

References (87)

1. Azfer A, Niu J, Rogers LM, Adamski FM, Kolattukudy PE. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am J Physiol Heart Circ Physiol 291: H1411-H1420, 2006.
2. Barbazetto IA, Liang J, Chang S, Zheng L, Spector A, Dillon JP. Oxygen tension in the rabbit lens and vitreous before and after vitrectomy. Exp Eye Res 78: 917-924, 2004.
3. Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev 78: 547-581, 1998.
4. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332, 2000.
5. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol 33: 1897-1918, 2001.
6. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307: 935-939, 2005.
7. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxiainduced transcription. Proc Natl Acad Sci USA 95: 11715-11720, 1998.
8. Chen JW, Dodia C, Feinstein SI, Jain MK, Fisher AB. 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J Biol Chem 275: 28421-28427, 2000.
9. Chong ZZ, Li F, Maiese K. Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75: 207-246, 2005.
10. Corley KM, Taylor CJ, Lilly B. Hypoxia-inducible factor 1alpha modulates adhesion, migration, and FAK phosphorylation in vascular smooth muscle cells. J Cell Biochem 96: 971-985, 2005.
11. DeGracia DJ, Kumar R, Owen CR, Krause GS, White BC. Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J Cereb Blood Flow Metab 22: 127-141, 2002.
12. Eismann T, Huber N, Shin T, Kuboki S, Galloway E, Wyder M, Edwards MJ, Greis KD, Shertzer HG, Fisher AB, Lentsch AB. Peroxiredoxin-6 protects against mitochondrial dysfunction and liver injury during ischemia-reperfusion in mice. Am J Physiol Gastrointest Liver Physiol 296: G266-G274, 2009.
13. 2+ homeostasis. Brain Res 1233: 63-78, 2008.
14. Fatma N, Kubo E, Sharma P, Beier DR, Singh DP. Impaired homeostasis and phenotypic abnormalities in Prdx6_/_ mice lens epithelial cells by reactive oxygen species: increased expression and activation of TGFbeta. Cell Death Differ 12: 734-750, 2005.
15. Fatma N, Kubo E, Takamura Y, Ishihara K, Garcia C, Beebe DC, Singh DP. Loss of NF-kappaB control and repression of Prdx6 gene transcription by reactive oxygen species-driven SMAD3-mediated transforming growth factor beta signaling. J Biol Chem 284: 22758-22772, 2009.
16. Fatma N, Kubo E, Toris CB, Stamer WD, Camras CB, Singh DP. PRDX6 attenuates oxidative stress-and TGFbeta-induced abnormalities of human trabecular meshwork cells. Free Radic Res 43: 783-795, 2009.
17. Fatma N, Singh DP, Shinohara T, Chylack LT Jr. Transcriptional regulation of the antioxidant protein 2 gene, a thiol-specific antioxidant, by lens epithelium-derived growth factor to protect cells from oxidative stress. J Biol Chem 276: 48899-48907, 2001.
18. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247, 2000.
19. Fisher AB, Beers MF. Letter to the editor: Hyperoxia and acute lung injury. Am J Physiol Lung Cell Mol Physiol 295: L1066, 2008. Author reply L1067, 2008.
20. Fisher AB, Dodia C, Feinstein SI, Ho YS. Altered lung phospholipid metabolism in mice with targeted deletion of lysosomal-type phospholipase A2. J Lipid Res 46: 1248-1256, 2005.
21. Fitch CL, Swedberg SH, Livesey JC. Measurement and manipulation of the partial pressure of oxygen in the rat anterior chamber. Curr Eye Res 20: 121-126, 2000.
22. Gardian G, Browne SE, Choi DK, Klivenyi P, Gregorio J, Kubilus JK, Ryu H, Langley B, Ratan RR, Ferrante RJ, Beal MF. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J Biol Chem 280: 556-563, 2005.
23. Gething MJ, Sambrook J. Protein folding in the cell. Nature 355: 33-45, 1992.
24. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115: 500-508, 2005.
25. Gong B, Zhang LY, Lam DS, Pang CP, Yam GH. Sodium 4-phenylbutyrate ameliorates the effects of cataract-causing mutant gammaDcrystallin in cultured cells. Mol Vis 16: 997-1003, 2010.
26. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408, 2005.
27. Han C, Nam MK, Park HJ, Seong YM, Kang S, Rhim H. Tunicamycininduced ER stress upregulates the expression of mitochondrial HtrA2 and promotes apoptosis through the cytosolic release of HtrA2. J Microbiol Biotechnol 18: 1197-1202, 2008.
28. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633, 2003.
29. Helbig H, Hinz JP, Kellner U, Foerster MH. Oxygen in the anterior chamber of the human eye. Ger J Ophthalmol 2: 161-164, 1993.
30. Helenius A, Marquardt T, Braakman I. The endoplasmic reticulum as a protein-folding compartment. Trends Cell Biol 2: 227-231, 1992.
31. Holekamp NM, Shui YB, Beebe DC. Vitrectomy surgery increases oxygen exposure to the lens: a possible mechanism for nuclear cataract formation. Am J Ophthalmol 139: 302-310, 2005.
32. Hotokezaka Y, van Leyen K, Lo EH, Beatrix B, Katayama I, Jin G, Nakamura T. alphaNAC depletion as an initiator of ER stress-induced apoptosis in hypoxia. Cell Death Differ 16: 1505-1514, 2009.
33. Immenschuh S, Baumgart-Vogt E. Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid Redox Signal 7: 768-777, 2005.
34. Kalai M, Lamkanfi M, Denecker G, Boogmans M, Lippens S, Meeus A, Declercq W, Vandenabeele P. Regulation of the expression and processing of caspase-12. J Cell Biol 162: 457-467, 2003.
35. Kang JH, Shin I, Han JS. Changes of phospholipase D activity in TNF-alpha and anti-Fas/Apo1 monoclonal antibody induced apoptosis in HL-60 and A20 cells. Exp Mol Med 30: 21-27, 1998.
36. Kang SW, Baines IC, Rhee SG. Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J Biol Chem 273: 6303-6311, 1998.
37. Kim KS, Sengupta S, Berk M, Kwak YG, Escobar PF, Belinson J, Mok SC, Xu Y. Hypoxia enhances lysophosphatidic acid responsiveness in ovarian cancer cells and lysophosphatidic acid induces ovarian tumor metastasis in vivo. Cancer Res 66: 7983-7990, 2006.
38. Kubo E, Fatma N, Akagi Y, Beier DR, Singh SP, Singh DP. TATmediated PRDX6 protein transduction protects against eye lens epithelial cell death and delays lens opacity. Am J Physiol Cell Physiol 294: C842-C855, 2008.
39. Kubo E, Miyazawa T, Fatma N, Akagi Y, Singh DP. Development-and age-associated expression pattern of peroxiredoxin 6, and its regulation in murine ocular lens. Mech Ageing Dev 127: 249-256, 2006.
40. Kubo E, Singh DP, Fatma N, Akagi Y. TAT-mediated peroxiredoxin 5 and 6 protein transduction protects against high-glucose-induced cytotoxicity in retinal pericytes. Life Sci 84: 857-864, 2009.
41. Lamkanfi M, Kalai M, Vandenabeele P. Caspase-12: an overview. Cell Death Differ 11: 365-368, 2004.
42. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 15: 1460-1471, 2008.
43. Liu CY, Schroder M, Kaufman RJ. Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 275: 24881-24885, 2000.
44. Liu H, Baliga R. Endoplasmic reticulum stress-associated caspase 12 mediates cisplatin-induced LLC-PK1 cell apoptosis. J Am Soc Nephrol 16: 1985-1992, 2005.
45. Liu J, Hales AM, Chamberlain CG, McAvoy JW. Induction of cataractlike changes in rat lens epithelial explants by transforming growth factor beta. Invest Ophthalmol Vis Sci 35: 388-401, 1994.
46. Liu L, Ning X, Sun L, Zhang H, Shi Y, Guo C, Han S, Liu J, Sun S, Han Z, Wu K, Fan D. Hypoxia-inducible factor-1 alpha contributes to hypoxia-induced chemoresistance in gastric cancer. Cancer Sci 99: 121-128, 2008.
47. Loor G, Schumacker PT. Role of hypoxia-inducible factor in cell survival during myocardial ischemia-reperfusion. Cell Death Differ 15: 686-690, 2008.
48. Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18: 716-731, 2007.
49. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293, 2007.
50. Malhotra JD, Miao H, Zhang K, Wolfson A, Pennathur S, Pipe SW, Kaufman RJ. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 105: 18525-18530, 2008.
51. Mandic A, Hansson J, Linder S, Shoshan MC. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J Biol Chem 278: 9100-9106, 2003.
52. Manevich Y, Fisher AB. Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipid metabolism. Free Radic Biol Med 38: 1422-1432, 2005.
53. Manevich Y, Shuvaeva T, Dodia C, Kazi A, Feinstein SI, Fisher AB. Binding of peroxiredoxin 6 to substrate determines differential phospholipid hydroperoxide peroxidase and phospholipase A(2) activities. Arch Biochem Biophys 485: 139-149, 2009.
54. Manevich Y, Sweitzer T, Pak JH, Feinstein SI, Muzykantov V, Fisher AB. 1-Cys peroxiredoxin overexpression protects cells against phospholipid peroxidation-mediated membrane damage. Proc Natl Acad Sci USA 99: 11599-11604, 2002.
55. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schumacker PT, Simon MC. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 1: 393-399, 2005.
56. Mates JM, Perez-Gomez C, Nunez de Castro I. Antioxidant enzymes and human diseases. Clin Biochem 32: 595-603, 1999.
57. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21: 1249-1259, 2001.
58. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
59. Nagineni CN, Bhat SP. Alpha B-crystallin is expressed in kidney epithelial cell lines and not in fibroblasts. FEBS Lett 249: 89-94, 1989.
60. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103, 2000.
61. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389, 2004.
62. Park BJ, Lim YS, Lee HJ, Eum WS, Park J, Han KH, Choi SY, Lee KS. Anti-oxidative effects of Phellinus linteus and red ginseng extracts on oxidative stress-induced DNA damage. BMB Rep 42: 500-505, 2009.
63. Patenaude A, Ven Murthy MR, Mirault ME. Mitochondrial thioredoxin system: effects of TrxR2 overexpression on redox balance, cell growth, and apoptosis. J Biol Chem 279: 27302-27314, 2004.
64. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 514: 122-128, 2002.
65. Salminen A, Kaarniranta K. ER stress and hormetic regulation of the aging process. Ageing Res Rev 9: 211-217, 2010.
66. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3: 99-111, 2002.
67. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L, Wek RC. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18: 7499-7509, 1998.
68. Singh DP, Ohguro N, Chylack LT Jr, Shinohara T. Lens epitheliumderived growth factor: increased resistance to thermal and oxidative stresses. Invest Ophthalmol Vis Sci 40: 1444-1451, 1999.
69. Szegezdi E, Fitzgerald U, Samali A. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann NY Acad Sci 1010: 186-194, 2003.
70. Tu BP, Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164: 341-346, 2004.
71. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84, 2007.
72. Wang X, Phelan SA, Forsman-Semb K, Taylor EF, Petros C, Brown A, Lerner CP, Paigen B. Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J Biol Chem 278: 25179-25190, 2003.
73. Wang X, Phelan SA, Petros C, Taylor EF, Ledinski G, Jurgens G, Forsman-Semb K, Paigen B. Peroxiredoxin 6 deficiency and atherosclerosis susceptibility in mice: significance of genetic background for assessing atherosclerosis. Atherosclerosis 177: 61-70, 2004.
74. Wang Y, Feinstein SI, Manevich Y, Ho YS, Fisher AB. Peroxiredoxin 6 gene-targeted mice show increased lung injury with paraquat-induced oxidative stress. Antioxid Redox Signal 8: 229-237, 2006.
75. Wang Y, Lu Q, Sheldon FS, Ho YS, Phelan SA, Beers MF, Fisher AB. [Antioxidative role of peroxiredoxin 6 in acute lung injury]. Zhonghua Er Ke Za Zhi 46: 739-744, 2008.
76. Wang Y, Phelan SA, Manevich Y, Feinstein SI, Fisher AB. Transgenic mice overexpressing peroxiredoxin 6 show increased resistance to lung injury in hyperoxia. Am J Respir Cell Mol Biol 34: 481-486, 2006.
77. Wu W, Platoshyn O, Firth AL, Yuan JX. Hypoxia divergently regulates production of reactive oxygen species in human pulmonary and coronary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 293: L952-L959, 2007.
78. Wu Y, Feinstein SI, Manevich Y, Chowdhury I, Pak JH, Kazi A, Dodia C, Speicher DW, Fisher AB. Mitogen-activated protein kinasemediated phosphorylation of peroxiredoxin 6 regulates its phospholipase A(2) activity. Biochem J 419: 669-679, 2009.
79. Wu YZ, Manevich Y, Baldwin JL, Dodia C, Yu K, Feinstein SI, Fisher AB. Interaction of surfactant protein A with peroxiredoxin 6 regulates phospholipase A2 activity. J Biol Chem 281: 7515-7525, 2006.
80. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, Yoffe B. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 36: 592-601, 2002.
81. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115: 2656-2664, 2005.
82. Xue X, Piao JH, Nakajima A, Sakon-Komazawa S, Kojima Y, Mori K, Yagita H, Okumura K, Harding H, Nakano H. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem 280: 33917-33925, 2005.
83. Yam GH, Gaplovska-Kysela K, Zuber C, Roth J. Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Invest Ophthalmol Vis Sci 48: 1683-1690, 2007.
84. Yang WW, Shu B, Zhu Y, Yang HT. E2F6 inhibits cobalt chloridemimetic hypoxia-induced apoptosis through E2F1. Mol Biol Cell 19: 3691-3700, 2008.
85. Yokouchi M, Hiramatsu N, Hayakawa K, Okamura M, Du S, Kasai A, Takano Y, Shitamura A, Shimada T, Yao J, Kitamura M. Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem 283: 4252-4260, 2008.
86. Yoshida H, Oku M, Suzuki M, Mori K. pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172: 565-575, 2006.
87. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12: 982-995, 1998