Reductive potential - A savior turns stressor in protein aggregation cardiomyopathy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 1, 2015, Pages 53-60

  Narasimhan, Madhusudhanan ^c   Rajasekaran, Namakkal S ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiomyopathy; GSH; HR120GCryAB; Nrf2; Protein aggregation; Reductive stress

Indexed keywords

CARDIOMYOPATHY; CELL PROTECTION; CELL STRESS; ENDOPLASMIC RETICULUM STRESS; EXERCISE; HEART DISEASE; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; IN VITRO STUDY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN AGGREGATION; PROTEIN AGGREGATION CARDIOMYOPATHY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REDOX STRESS; REDUCTIVE STRESS; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; HOMEOSTASIS; METABOLISM; MOUSE;

MUSCLE PROTEIN;

ANIMALS; CARDIOMYOPATHIES; HOMEOSTASIS; HUMANS; MICE; MUSCLE PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 84912106672     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.11.010     Document Type: Review

References (80)

1. Wang K., Zhang T., Dong Q., Nice E.C., Huang C., Wei Y. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis. 2013, 4:e537.
2. Sunggip C., Kitajima N., Nishida M. Redox control of cardiovascular homeostasis by angiotensin II. Curr. Pharm. Des. 2013, 19:3022-3032.
3. Ray P.D., Huang B.W., Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 2012, 24:981-990.
4. Haddad J.J. Oxygen homeostasis, thiol equilibrium and redox regulation of signalling transcription factors in the alveolar epithelium. Cell. Signal. 2002, 14:799-810.
5. Griendling K.K., FitzGerald G.A. Oxidative stress and cardiovascular injury: part I: basic mechanisms and in vivo monitoring of ROS. Circulation 2003, 108:1912-1916.
6. Griendling K.K., FitzGerald G.A. Oxidative stress and cardiovascular injury: part II: animal and human studies. Circulation 2003, 108:2034-2040.
7. Jay D., Hitomi H., Griendling K.K. Oxidative stress and diabetic cardiovascular complications. Free Radic. Biol. Med. 2006, 40:183-192.
8. Schnabel R., Blankenberg S. Oxidative stress in cardiovascular disease: successful translation from bench to bedside?. Circulation 2007, 116:1338-1340.
9. Takano H., Zou Y., Hasegawa H., Akazawa H., Nagai T., Komuro I. Oxidative stress-induced signal transduction pathways in cardiac myocytes: involvement of ROS in heart diseases. Antioxid. Redox Signal. 2003, 5:789-794.
10. Reuter S., Gupta S.C., Chaturvedi M.M., Aggarwal B.B. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 2010, 49:1603-1616.
11. Popolo A., Autore G., Pinto A., Marzocco S. Oxidative stress in patients with cardiovascular disease and chronic renal failure. Free Radic. Res. 2013, 47:346-356.
12. Griendling K.K., Alexander R.W. Oxidative stress and cardiovascular disease. Circulation 1997, 96:3264-3265.
13. Halliwell B. Oxidative stress and cancer: have we moved forward?. Biochem. J. 2007, 401:1-11.
14. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 2005, 115:500-508.
15. Wendel A. Measurement of in vivo lipid peroxidation and toxicological significance. Free Radic. Biol. Med. 1987, 3:355-358.
16. Ghyczy M., Boros M. Electrophilic methyl groups present in the diet ameliorate pathological states induced by reductive and oxidative stress: a hypothesis. Br. J. Nutr. 2001, 85:409-414.
17. Jaeschke H., Kleinwaechter C., Wendel A. NADH-dependent reductive stress and ferritin-bound iron in allyl alcohol-induced lipid peroxidation in vivo: the protective effect of vitamin E. Chem. Biol. Interact. 1992, 81:57-68.
18. Rajasekaran N.S., Connell P., Christians E.S., Yan L.J., Taylor R.P., Orosz A., Zhang X.Q., Stevenson T.J., Peshock R.M., Leopold J.A., Barry W.H., Loscalzo J., Odelberg S.J., Benjamin I.J. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130:427-439.
19. Torreggiani A., Chatgilialoglu C., Ferreri C., Melchiorre M., Atrian S., Capdevila M. Non-enzymatic modifications in metallothioneins connected to lipid membrane damages: structural and biomimetic studies under reductive radical stress. J. Proteome 2013, 92:204-215.
20. He Q., Wang M., Petucci C., Gardell S.J., Han X. Rotenone induces reductive stress and triacylglycerol deposition in C2C12 cells. Int. J. Biochem. Cell Biol. 2013, 45:2749-2755.
21. Zhang H., Rajasekaran N.S., Orosz A., Xiao X., Rechsteiner M., Benjamin I.J. Selective degradation of aggregate-prone CryAB mutants by HSPB1 is mediated by ubiquitin-proteasome pathways. J. Mol. Cell. Cardiol. 2012, 49:918-930.
22. Yu Q., Lee C.F., Wang W., Karamanlidis G., Kuroda J., Matsushima S., Sadoshima J., Tian R. Elimination of NADPH oxidase activity promotes reductive stress and sensitizes the heart to ischemic injury. J.Am. Heart Assoc. 2014, 3:e000555.
23. Badia M.C., Giraldo E., Dasi F., Alonso D., Lainez J.M., Lloret A., Vina J. Reductive stress in young healthy individuals at risk of Alzheimer disease. Free Radic. Biol. Med. 2013, 63:274-279.
24. Liu H., Colavitti R., Rovira T. Finkel, redox-dependent transcriptional regulation. Circ. Res. 2005, 97:967-974.
25. Ishikawa M., Numazawa S., Yoshida T. Redox regulation of the transcriptional repressor Bach1. Free Radic. Biol. Med. 2005, 38:1344-1352.
26. Shaikhali J., Noren L., de Dios Barajas-Lopez J., Srivastava V., Konig J., Sauer U.H., Wingsle G., Dietz K.J., Strand A. Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J. Biol. Chem. 2012, 287:27510-27525.
27. Rajasekaran N.S., Firpo M.A., Milash B.A., Weiss R.B., Benjamin I.J. Global expression profiling identifies a novel biosignature for protein aggregation R120GCryAB cardiomyopathy in mice. Physiol. Genomics 2008, 35:165-172.
28. Dimmeler S., Zeiher A.M. A "reductionist" view of cardiomyopathy. Cell 2007, 130:401-402.
29. Krishnan N., Fu C., Pappin D.J., Tonks N.K. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci. Signal. 2011, 4:ra86.
30. Mustafa A.K., Gadalla M.M., Sen N., Kim S., Mu W., Gazi S.K., Barrow R.K., Yang G., Wang R., Snyder S.H. H2S signals through protein S-sulfhydration. Sci. Signal. 2009, 2:ra72.
31. Ogawa H., Takahashi K., Miura S., Imagawa T., Saito S., Tominaga M., Ohta T. H(2)S functions as a nociceptive messenger through transient receptor potential ankyrin 1 (TRPA1) activation. Neuroscience 2012, 218:335-343.
32. Sen N., Paul B.D., Gadalla M.M., Mustafa A.K., Sen T., Xu R., Kim S., Snyder S.H. Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol. Cell 2012, 45:13-24.
33. Oguri G., Nakajima T., Yamamoto Y., Takano N., Tanaka T., Kikuchi H., Morita T., Nakamura F., Yamasoba T., Komuro I. Effects of methylglyoxal on human cardiac fibroblast: roles of transient receptor potential ankyrin 1 (TRPA1)channels. Am. J. Physiol. Heart Circ. Physiol. 2014, 307:H1339-H1352.
34. Ida T., Sawa T., Ihara H., Tsuchiya Y., Watanabe Y., Kumagai Y., Suematsu M., Motohashi H., Fujii S., Matsunaga T., Yamamoto M., Ono K., Devarie-Baez N.O., Xian M., Fukuto J.M., Akaike T. Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7606-7611.
35. Nishida M., Sawa T., Kitajima N., Ono K., Inoue H., Ihara H., Motohashi H., Yamamoto M., Suematsu M., Kurose H., van der Vliet A., Freeman B.A., Shibata T., Uchida K., Kumagai Y., Akaike T. Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 2012, 8:714-724.
36. Enyedi B., Varnai P., Geiszt M. Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid. Redox Signal. 2010, 13:721-729.
37. Hwang C., Sinskey A.J., Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 1992, 257:1496-1502.
38. Laurindo F.R., Pescatore L.A., Fernandes Dde C. Protein disulfide isomerase in redox cell signaling and homeostasis. Free Radic. Biol. Med. 2012, 52:1954-1969.
39. Wassler M., Fries E. Proteolytic cleavage of haptoglobin occurs in a subcompartment of the endoplasmic reticulum: evidence from membrane fusion in vitro. J. Cell Biol. 1993, 123:285-291.
40. Lemberg M.K., Martoglio B. Requirements for signal peptide peptidase-catalyzed intramembrane proteolysis. Mol. Cell 2002, 10:735-744.
41. Kowarik M., Kung S., Martoglio B., Helenius A. Protein folding during cotranslational translocation in the endoplasmic reticulum. Mol. Cell 2002, 10:769-778.
42. Rajasekaran N.S., Varadharaj S., Khanderao G.D., Davidson C.J., Kannan S., Firpo M.A., Zweier J.L., Benjamin I.J. Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid. Redox Signal. 2011, 14:957-971.
43. Kobayashi M., Li L., Iwamoto N., Nakajima-Takagi Y., Kaneko H., Nakayama Y., Eguchi M., Wada Y., Kumagai Y., Yamamoto M. The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol. Cell. Biol. 2009, 29:493-502.
44. Kwak M.K., Wakabayashi N., Greenlaw J.L., Yamamoto M., Kensler T.W. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 2003, 23:8786-8794.
45. McMahon M., Itoh K., Yamamoto M., Hayes J.D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 2003, 278:21592-21600.
46. Kobayashi M., Yamamoto M. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv. Enzym. Regul. 2006, 46:113-140.
47. Shibata T., Ohta T., Tong K.I., Kokubu A., Odogawa R., Tsuta K., Asamura H., Yamamoto M., Hirohashi S. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13568-13573.
48. Hosoya T., Maruyama A., Kang M.I., Kawatani Y., Shibata T., Uchida K., Warabi E., Noguchi N., Itoh K., Yamamoto M. Differential responses of the Nrf2-Keap1 system to laminar and oscillatory shear stresses in endothelial cells. J. Biol. Chem. 2005, 280:27244-27250.
49. Taguchi K., Fujikawa N., Komatsu M., Ishii T., Unno M., Akaike T., Motohashi H., Yamamoto M. Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13561-13566.
50. Ke B., Shen X.D., Zhang Y., Ji H., Gao F., Yue S., Kamo N., Zhai Y., Yamamoto M., Busuttil R.W., Kupiec-Weglinski J.W. KEAP1-NRF2 complex in ischemia-induced hepatocellular damage of mouse liver transplants. J. Hepatol. 2013, 59:1200-1207.
51. Taguchi K., Motohashi H., Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011, 16:123-140.
52. Li J., Ichikawa T., Villacorta L., Janicki J.S., Brower G.L., Yamamoto M., Cui T. Nrf2 protects against maladaptive cardiac responses to hemodynamic stress. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1843-1850.
53. Brewer A.C., Mustafi S.B., Murray T.V., Rajasekaran N.S., Benjamin I.J. Reductive stress linked to small HSPs, G6PD, and Nrf2 pathways in heart disease. Antioxid. Redox Signal. 2013, 18:1114-1127.
54. Kwak M.K., Itoh K., Yamamoto M., Kensler T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 2002, 22:2883-2892.
55. Cullinan S.B., Zhang D., Hannink M., Arvisais E., Kaufman R.J., Diehl J.A. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 2003, 23:7198-7209.
56. Huang H.C., Nguyen T., Pickett C.B. Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J. Biol. Chem. 2002, 277:42769-42774.
57. Nguyen T., Sherratt P.J., Huang H.C., Yang C.S., Pickett C.B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26S proteasome. J. Biol. Chem. 2003, 278:4536-4541.
58. Stewart D., Killeen E., Naquin R., Alam S., Alam J. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 2003, 278:2396-2402.
59. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.S., Ueno I., Sakamoto A., Tong K.I., Kim M., Nishito Y., Iemura S., Natsume T., Ueno T., Kominami E., Motohashi H., Tanaka K., Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 2010, 12:213-223.
60. Narasimhan M., Patel D., Vedpathak D., Rathinam M., Henderson G., Mahimainathan L. Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells. PLoS One 2012, 7:e51111.
61. Narasimhan M., Riar A.K., Rathinam M.L., Vedpathak D., Henderson G., Mahimainathan L. Hydrogen peroxide responsive miR153 targets Nrf2/ARE cytoprotection in paraquat induced dopaminergic neurotoxicity. Toxicol. Lett. 2014, 228:179-191.
62. Newman J.R., Keating A.E. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 2003, 300:2097-2101.
63. Blank V. Small Maf proteins in mammalian gene control: mere dimerization partners or dynamic transcriptional regulators?. J. Mol. Biol. 2008, 376:913-925.
64. Eggler A.L., Liu G., Pezzuto J.M., van Breemen R.B., Mesecar A.D. Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10070-10075.
65. Oyake T., Itoh K., Motohashi H., Hayashi N., Hoshino H., Nishizawa M., Yamamoto M., Igarashi K. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 1996, 16:6083-6095.
66. Blank V., Andrews N.C. The Maf transcription factors: regulators of differentiation. Trends Biochem. Sci. 1997, 22:437-441.
67. Igarashi K., Sun J. The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid. Redox Signal. 2006, 8:107-118.
68. Liu G.H., Qu J., Shen X. NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim. Biophys. Acta 2008, 1783:713-727.
69. Aro A. Antioxidant supplementation and risk of chronic disease. Forum Nutr. 2003, 56:361-363.
70. Green A.C., Hughes M.C., Ibiebele T.I., Williams G.M., van der Pols J.C., Ortonne J.P. Antioxidant supplementation and risk of skin cancers. J. Nutr. 2008, 138:978. (author reply 979).
71. Plummer M., Vivas J., Lopez G., Bravo J.C., Peraza S., Carillo E., Cano E., Castro D., Andrade O., Sanchez V., Garcia R., Buiatti E., Aebischer C., Franceschi S., Oliver W., Munoz N. Chemoprevention of precancerous gastric lesions with antioxidant vitamin supplementation: a randomized trial in a high-risk population. J. Natl. Cancer Inst. 2007, 99:137-146.
72. Miller E.R., Appel L.J., Levander O.A., Levine D.M. The effect of antioxidant vitamin supplementation on traditional cardiovascular risk factors. J. Cardiovasc. Risk 1997, 4:19-24.
73. Czernichow S., Vergnaud A.C., Galan P., Arnaud J., Favier A., Faure H., Huxley R., Hercberg S., Ahluwalia N. Effects of long-term antioxidant supplementation and association of serum antioxidant concentrations with risk of metabolic syndrome in adults. Am. J. Clin. Nutr. 2009, 90:329-335.
74. Mennen L.I., de Courcy G.P., Guilland J.C., Ducros V., Bertrais S., Nicolas J.P., Maurel M., Zarebska M., Favier A., Franchisseur C., Hercberg S., Galan P. Homocysteine, cardiovascular disease risk factors, and habitual diet in the French Supplementation with Antioxidant Vitamins and Minerals Study. Am. J. Clin. Nutr. 2002, 76:1279-1289.
75. Goudev A., Kyurkchiev S., Gergova V., Karshelova E., Georgiev D., Atar D., Kehayov I., Nachev C. Reduced concentrations of soluble adhesion molecules after antioxidant supplementation in postmenopausal women with high cardiovascular risk profiles-a randomized double-blind study. Cardiology 2000, 94:227-232.
76. Kannan S., Muthusamy V.R., Whitehead K.J., Wang L., Gomes A.V., Litwin S.E., Kensler T.W., Abel E.D., Hoidal J.R., Rajasekaran N.S. Nrf2 deficiency prevents reductive stress-induced hypertrophic cardiomyopathy. Cardiovasc. Res. 2013, 100:63-73.
77. Cox J.S., Shamu C.E., Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 1993, 73:1197-1206.
78. Schulz T.J., Zarse K., Voigt A., Urban N., Birringer M., Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 2007, 6:280-293.
79. Zhang X., Min X., Li C., Benjamin I.J., Qian B., Zhang X., Ding Z., Gao X., Yao Y., Ma Y., Cheng Y., Liu L. Involvement of reductive stress in the cardiomyopathy in transgenic mice with cardiac-specific overexpression of heat shock protein 27. Hypertension 2010, 55:1412-1417.
80. Margaritelis N.V., Kyparos A., Paschalis V., Theodorou A.A., Panayiotou G., Zafeiridis A., Dipla K., Nikolaidis M.G., Vrabas I.S. Reductive stress after exercise: the issue of redox individuality. Redox Biol. 2014, 2:520-528.