Human αB-Crystallin Mutation Causes Oxido-Reductive Stress and Protein Aggregation Cardiomyopathy in Mice

Cell

Volumn 130, Issue 3, 2007, Pages 427-439

  Rajasekaran, Namakkal S ^a   Connell, Patrice ^b   Christians, Elisabeth S ^b,c   Yan, Liang Jun ^b   Taylor, Ryan P ^a   Orosz, András ^a   Zhang, Xiu Q ^a   Stevenson, Tamara J ^a   Peshock, Ronald M ^b   Leopold, Jane A ^d   Barry, William H ^a   Loscalzo, Joseph ^d   Odelberg, Shannon J ^a   Benjamin, Ivor J ^a,b  

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

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c Centre de Biologie du Developpement Toulouse   (France)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

HUMDISEASE; SIGNALING

Indexed keywords

ALPHA CRYSTALLIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; GENE MUTATION; GENE OVEREXPRESSION; HEART VENTRICLE HYPERTROPHY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN AGGREGATION; REDUCTION KINETICS; TRANSGENIC MOUSE;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 34547681313     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.06.044     Document Type: Article

References (46)

1. Baek S.H., Min J.N., Park E.M., Han M.Y., Lee Y.S., Lee Y.J., and Park Y.M. Role of small heat shock protein HSP25 in radioresistance and glutathione-redox cycle. J. Cell. Physiol. 183 (2000) 100-107
2. Benjamin I.J., and Schneider M.D. Learning from failure: congestive heart failure in the postgenomic age. J. Clin. Invest. 115 (2005) 495-499
3. Bova M.P., Yaron O., Huang Q., Ding L., Haley D.A., Stewart P.L., and Horwitz J. Mutation R120G in alphaB-crystallin, which is linked to a desmin- related myopathy, results in an irregular structure and defective chaperone-like function. Proc. Natl. Acad. Sci. USA 96 (1999) 6137-6142
4. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
5. Chance B., Sies H., and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59 (1979) 527-605
6. Christians E.S., Yan L.J., and Benjamin I.J. Heat shock factor 1 and heat shock proteins: Critical partners in protection against acute cell injury. Crit. Care Med. 30 (2002) S43-S50
7. Clemen C.S., Fischer D., Roth U., Simon S., Vicart P., Kato K., Kaminska A.M., Vorgerd M., Goldfarb L.G., Eymard B., et al. Hsp27-2D-gel electrophoresis is a diagnostic tool to differentiate primary desminopathies from myofibrillar myopathies. FEBS Lett. 579 (2005) 3777-3782
8. Dalakas M.C., Park K.Y., Semino-Mora C., Lee H.S., Sivakumar K., and Goldfarb L.G. Desmin myopathy, a skeletal myopathy with cardiomyopathy caused by mutations in the desmin gene. N. Engl. J. Med. 342 (2000) 770-780
9. Fardeau M., Godet-Guillain J., Tome F.M., Collin H., Gaudeau S., Boffety C., and Vernant P. Rev. Neurol. (Paris) 134 (1978) 411-425
10. Finner H. On a monotonicity problem with in step-down multiple test procedures. J. Am. Stat. Assoc. 88 (1993) 920-923
11. Gething M.J., and Sambrook J. Protein folding in the cell. Nature 355 (1992) 33-45
12. Goldfarb L.G., Park K.Y., Cervenakova L., Gorokhova S., Lee H.S., Vasconcelos O., Nagle J.W., Semino-Mora C., Sivakumar K., and Dalakas M.C. Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat. Genet. 19 (1998) 402-403
13. Goldfarb L.G., Vicart P., Goebel H.H., and Dalakas M.C. Desmin myopathy. Brain 127 (2004) 723-734
14. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106 (1980) 207-212
15. Gupte S.A., Levine R.J., Gupte R.S., Young M.E., Lionetti V., Labinskyy V., Floyd B.C., Ojaimi C., Bellomo M., Wolin M.S., et al. Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J. Mol. Cell. Cardiol. 41 (2006) 340-349
16. Handy D.E., Hang G., Scolaro J., Metes N., Razaq N., Yang Y., and Loscalzo J. Aminoglycosides decrease glutathione peroxidase-1 activity by interfering with selenocysteine incorporation. J. Biol. Chem. 281 (2006) 3382-3388
17. Hansen J.M., Go Y.M., and Jones D.P. Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 215-234
18. Hochman J.H., Schindler M., Lee J.G., and Ferguson-Miller S. Lateral mobility of cytochrome c on intact mitochondrial membranes as determined by fluorescence redistribution after photobleaching. Proc. Natl. Acad. Sci. USA 79 (1982) 6866-6870
19. Johnston J.A., Ward C.L., and Kopito R.R. Aggresomes: A cellular response to misfolded proteins. J. Cell Biol. 143 (1998) 1883-1898
20. Kappe G., Franck E., Verschuure P., Boelens W.C., Leunissen J.A., and de Jong W.W. The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones 8 (2003) 53-61
21. Klemenz R., Frohli E., Steiger R.H., Schafer R., and Aoyama A. Alpha B-crystallin is a small heat shock protein. Proc. Natl. Acad. Sci. USA 88 (1991) 3652-3656
22. Kletzien R.F., Harris P.K., and Foellmi L.A. Glucose-6-phosphate dehydrogenase: a "housekeeping" enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J. 8 (1994) 174-181
23. Knowlton A.A., Kapadia S., Torre-Amione G., Durand J.B., Bies R., Young J., and Mann D.L. Differential expression of heat shock proteins in normal and failing human hearts. J. Mol. Cell. Cardiol. 30 (1998) 811-818
24. Kumar L.V., Ramakrishna T., and Rao C.M. Structural and functional consequences of the mutation of a conserved arginine residue in alphaA and alphaB crystallins. J. Biol. Chem. 274 (1999) 24137-24141
25. Kumar M.S., Reddy P.Y., Sreedhar B., and Reddy G.B. Alphab-crystallin-assisted reactivation of glucose-6-phosphate dehydrogenase upon refolding. Biochem. J. 391 (2005) 335-341
26. Leopold J.A., Cap A., Scribner A.W., Stanton R.C., and Loscalzo J. Glucose-6-phosphate dehydrogenase deficiency promotes endothelial oxidant stress and decreases endothelial nitric oxide bioavailability. FASEB J. 15 (2001) 1771-1773
27. Leopold J.A., Dam A., Maron B.A., Scribner A.W., Liao R., Handy D.E., Stanton R.C., Pitt B., and Loscalzo J. Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat. Med. 13 (2007) 189-197
28. Leopold J.A., Walker J., Scribner A.W., Voetsch B., Zhang Y.Y., Loscalzo A.J., Stanton R.C., and Loscalzo J. Glucose-6-phosphate dehydrogenase modulates vascular endothelial growth factor-mediated angiogenesis. J. Biol. Chem. 278 (2003) 32100-32106
29. Liu M., Ke T., Wang Z., Yang Q., Chang W., Jiang F., Tang Z., Li H., Ren X., Wang X., et al. Identification of a CRYAB mutation associated with autosomal dominant posterior polar cataract in a Chinese family. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3461-3466
30. Maloyan A., Sanbe A., Osinska H., Westfall M., Robinson D., Imahashi K., Murphy E., and Robbins J. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in alpha-B-crystallin desmin-related cardiomyopathy. Circulation 112 (2005) 3451-3461
31. Mehlen P., Schulze-Osthoff K., and 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. 271 (1996) 16510-16514
32. Morimoto R.I. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12 (1998) 3788-3796
33. Perng M.D., Muchowski P.J., van Den I.P., Wu G.J., Hutcheson A.M., Clark J.I., and Quinlan R.A. The cardiomyopathy and lens cataract mutation in alphaB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro. J. Biol. Chem. 274 (1999) 33235-33243
34. Pilotto A., Marziliano N., Pasotti M., Grasso M., Costante A.M., and Arbustini E. alphaB-crystallin mutation in dilated cardiomyopathies: low prevalence in a consecutive series of 200 unrelated probands. Biochem. Biophys. Res. Commun. 346 (2006) 1115-1117
35. Preville X., Salvemini F., Giraud S., Chaufour S., Paul C., Stepien G., Ursini M.V., and Arrigo A.P. Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp. Cell Res. 247 (1999) 61-78
36. Russell R.L., Siedlak S.L., Raina A.K., Bautista J.M., Smith M.A., and Perry G. Increased neuronal glucose-6-phosphate dehydrogenase and sulfhydryl levels indicate reductive compensation to oxidative stress in Alzheimer disease. Arch. Biochem. Biophys. 370 (1999) 236-239
37. Sam F., Kerstetter D.L., Pimental D.R., Mulukutla S., Tabaee A., Bristow M.R., Colucci W.S., and Sawyer D.B. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J. Card. Fail. 11 (2005) 473-480
38. Sanbe A., Osinska H., Saffitz J.E., Glabe C.G., Kayed R., Maloyan A., and Robbins J. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc. Natl. Acad. Sci. USA 101 (2004) 10132-10136
39. Selcen D., Ohno K., and Engel A.G. Myofibrillar myopathy: clinical, morphological and genetic studies in 63 patients. Brain 127 (2004) 439-451
40. Simons J.F., Ferro-Novick S., Rose M.D., and Helenius A. BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J. Cell Biol. 130 (1995) 41-49
41. Tome M.E., Johnson D.B., Samulitis B.K., Dorr R.T., and Briehl M.M. Glucose 6-phosphate dehydrogenase overexpression models glucose deprivation and sensitizes lymphoma cells to apoptosis. Antioxid. Redox Signal. 8 (2006) 1315-1327
42. Trotter E.W., and Grant C.M. Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 46 (2002) 869-878
43. Vicart P., Caron A., Guicheney P., Li Z., Prevost M.C., Faure A., Chateau D., Chapon F., Tome F., Dupret J.M., et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20 (1998) 92-95
44. Wang X., Osinska H., Klevitsky R., Gerdes A.M., Nieman M., Lorenz J., Hewett T., and Robbins J. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ. Res. 89 (2001) 84-91
45. Xiao X., and Benjamin I.J. Stress-response proteins in cardiovascular disease. Am. J. Hum. Genet. 64 (1999) 685-690
46. Yan L.J., Christians E.S., Liu L., Xiao X., Sohal R.S., and Benjamin I.J. Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J. 21 (2002) 5164-5172