Roles for αB-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 3 55-3, 2004, Pages

  Morrison, Lisa E ^a   Whittaker, Ross J ^a   Klepper, Robert E ^a   Wawrousek, Eric F ^b   Glembotski, Christopher C ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

Author keywords

Apoptosis; Glutathione; Knockout mouse; Necrosis; Small heat shock protein

Indexed keywords

ALPHA CRYSTALLIN; GLUTATHIONE; HEAT SHOCK PROTEIN; HSPB2 PROTEIN, MOUSE;

ALPHABC GENE; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ECHOCARDIOGRAPHY; ELECTRON MICROSCOPY; FEMALE; GENE; GENE DELETION; GENE OVEREXPRESSION; HEART FUNCTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HSPB2 GENE; KNOCKOUT MOUSE; MALE; MICROSCOPY; MOUSE; MOUSE STRAIN; NECROSIS; NONHUMAN; PRIORITY JOURNAL; SARCOMERE; ANIMAL; DISEASE MODEL; GENETICS; HEART CONTRACTION; HEART MUSCLE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; REPERFUSION INJURY;

ALPHA-CRYSTALLIN B CHAIN; ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; HEAT-SHOCK PROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NECROSIS; PHENOTYPE;

EID: 1342346688     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00715.2003     Document Type: Article

References (54)

1. Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113: 548-555, 1985.
2. Armstrong SC, Delacey M, and Ganote CE. Phosphorylation state of hsp27 and p38 MAPK during preconditioning and protein phosphatase inhibitor protection of rabbit cardiomyocytes. J Mol Cell Cardiol 31: 555-567, 1999.
3. Armstrong SC, Shivell CL, and Ganote CE. Differential translocation or phosphorylation of alpha B crystallin cannot be detected in ischemically preconditioned rabbit cardiomyocytes. J Mol Cell Cardiol 32: 1301-1314, 2000.
4. Barbato R, Menabo R, Dainese P, Carafoli E, Schiaffino S, and Di Lisa F. Binding of cytosolic proteins to myofibrils in ischemic rat hearts. Circ Res 78: 821-828, 1996.
5. Benjamin IJ, Shelton J, Garry DJ, and Richardson JA. Temporospatial expression of the small HSP/alpha B-crystallin in cardiac and skeletal muscle during mouse development. Dev Dyn 208: 75-84, 1997.
6. Bennardini F, Wrzosek A, and Chiesi M. Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ Res 71: 288-294, 1992.
7. Benndorf R, Sun X, Gilmont RR, Biederman KJ, Molloy MP, Goodmurphy CW, Cheng H, Andrews PC, and Welsh MJ. HSP22, a new member of the small heat shock protein superfamily, interacts with mimic of phosphorylated HSP27 [(3D)HSP27]. J Biol Chem 276: 26753-26761, 2001.
8. Bluhm WF, Martin JL, Mestril R, and Dillmann WH. Specific heat shock proteins protect microtubules during simulated ischemia in cardiac myocytes. Am J Physiol Heart Circ Physiol 275: H2243-H2249, 1998.
9. Brady JP, Garland D, Duglas-Tabor Y, Robison WG Jr, Groome A, and Wawrousek EF. Targeted disruption of the mouse alpha A-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein alpha B-crystallin. Proc Natl Acad Sci USA 94: 884-889, 1997.
10. Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, and Wawrousek EF. aB-Crystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci 42: 2924-2934, 2001.
11. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, and Hudson T. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member (Erratum). Cell 69: 385, 1992.
12. Concannon CG, Gorman AM, and Samali A. On the role of Hsp27 in regulating apoptosis. Apoptosis 8: 61-70, 2003.
13. Dillmann WH. Heat shock proteins and protection against ischemic injury. Infect Dis Obstet Gynecol 7: 55-57, 1999.
14. Dubin RA, Gopal-Srivastava R, Wawrousek EF, and Piatigorsky J. Expression of the murine alpha B-crystallin gene in lens and skeletal muscle: identification of a muscle-preferred enhancer. Mol Cell Biol 11: 4340-4349, 1991.
15. Epstein ND and Davis JS. Sensing stretch is fundamental. Cell 112: 147-150, 2003.
16. Golenhofen N, Arbeiter A, Koob R, and Drenckhahn D. Ischemia-induced association of the stress protein alpha B-crystallin with I-band portion of cardiac titin. J Mol Cell Cardiol 34: 309-319, 2002.
17. Golenhofen N, Htun P, Ness W, Koob R, Schaper W, and Drenckhahn D. Binding of the stress protein alpha B-crystallin to cardiac myofibrils correlates with the degree of myocardial damage during ischemia/reperfusion in vivo. J Mol Cell Cardiol 31: 569-580, 1999.
18. Golenhofen N, Ness W, Koob R, Htun P, Schaper W, and Drenckhahn D. Ischemia-induced phosphorylation and translocation of stress protein αB-crystallin to Z lines of myocardium. Am J Physiol Heart Circ Physiol 274: H1457-H1464, 1998.
19. Gopal-Srivastava R, Haynes JIn, and Piatigorsky J. Regulation of the murine aB-crystallin/small heat shock protein gene in cardiac muscle. Mol Cell Biol 15: 7081-7090, 1995.
20. Haynes JI II, Duncan MK, and Piatigorsky J. Spatial and temporal activity of the alpha B-crystallin/small heat shock protein gene promoter in transgenic mice. Dev Dyn 207: 75-88, 1996.
21. Ito H, Kamei K, Iwamoto I, Inaguma Y, Nohara D, and Kato K. Phosphorylation-induced change of the oligomerization state of alpha B-crystallin. J Biol Chem 276: 5346-5352, 2001.
22. Iwaki A, Nagano T, Nakagawa M, Iwaki T, and Fukumaki Y. Identification and characterization of the gene encoding a new member of the alpha-crystallin/small hsp family, closely linked to the alphaB-crystallin gene in a head-to-head manner. Genomics 45: 386-394, 1997.
23. Kajstura J, Cheng W, Reiss K, Clark WA, Sonnenblick EH, Krajewski S, Reed JC, Olivetti G, and Anversa P. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest 74: 86-107, 1996.
24. Kamradt MC, Chen F, and Cryns VL. The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 276: 16059-16063, 2001.
25. Kannan R, Ouyang B, Wawrousek E, Kaplowitz N, and Andley UP. Regulation of GSH in alphaA-expressing human lens epithelial cell lines and in alphaA knockout mouse lenses. Invest Ophthalmol Vis Sci 42: 409-416, 2001.
26. Kato K, Shinohara H, Kurobe N, Inaguma Y, Shimizu K, and Oshima K. Tissue distribution and developmental profiles of immunoreactive alpha B crystallin in the rat determined with a sensitive immunoassay system. Biochim Biophys Acta 1074: 201-208, 1991.
27. Kehrer JP and Lund LG. Cellular reducing equivalents and oxidative stress. Free Radic Biol Med 17: 65-75, 1994.
28. Knoll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, Bang ML, Hayashi T, Shiga N, Yasukawa H, Schaper W, McKenna W, Yokoyama M, Schork NJ, Omens JH, McCulloch AD, Kimura A, Gregorio CC, Poller W, Schaper J, Schultheiss HP, and Chien KR. The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell 111: 943-955, 2002.
29. Krief S, Faivre JF, Robert P, Le Douarin B, Brument-Larignon N, Lefrere I, Bouzyk MM, Anderson KM, Greller LD, Tobin FL, Souchet M, and Bril A. Identification and characterization of cvHsp. A novel human small stress protein selectively expressed in cardiovascular and insulin-sensitive tissues. J Biol Chem 274: 36592-36600, 1999.
30. Li J, Wang H, Stoner GD, and Bray TM. Dietary supplementation with cysteine prodrugs selectively restores tissue glutathione levels and redox status in protein-malnourished mice (1). J Nutr Biochem 13: 625-633, 2002.
31. Lutsch G, Vetter R, Offhauss U, Wieske M, Grone HJ, Klemenz R, and Benndorf R. Abundance and localization of the small heat shock proteins HSP25 and alpha B crystallin in rat and human heart. Circulation 96: 3466-3476, 1997.
32. Lutsch G, Vetter R, Offhauss U, Wieske M, Schimke I, Stahl J, and Benndorf R. Location of the small heat shock proteins HSP25 and alpha B crystallin in rat and human heart. Eur J Cell Biol 74: 43, 1997.
33. Mehlen P, Hickey E, Weber LA, and Arrigo AP. Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFalpha in NIH-3T3-ras cells. Biochem Biophys Res Commun 241: 187-192, 1997.
34. Mehlen P, Kretz-Remy C, Preville X, and Arrigo AP. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 15: 2695-2706, 1996.
35. Morrison LE, Hoover HE, Thuerauf DJ, and Glembotski CC. Mimicking phosphorylation of aB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ Res 92: 203-211, 2003.
36. Muntoni F, Catani G, Mateddu A, Rimoldi M, Congiu T, Faa G, Marrosu MG, Cianchetti C, and Porcu M. Familial cardiomyopathy, mental retardation and myopathy associated with desmin-type intermediate filaments. Neuromuscul Disord 4: 233-241, 1994.
37. Nakagawa M, Tsujimoto N, Nakagawa H, Iwaki T, Fukumaki Y, and Iwaki A. Association of HSPB2, a member of the small heat shock protein family, with mitochondria. Exp Cell Res 271: 161-168, 2001.
38. Piper H and Garcia-Dorado D. Prime causes of rapid cardiomyocyte death during reperfusion. Ann Thorac Surg 68: 1913-1919, 1999.
39. Porcu M, Muntoni F, Catani G, and Mereu D. Familial cardiac and skeletal myopathy associated with desmin accumulation. Clin Cardiol 17: 277-279, 1994.
40. Preville X, Schultz H, Knauf U, Gaestel M, and Arrigo AP. Analysis of the role of Hsp25 phosphorylation reveals the importance of the oligomerization state of this small heat shock protein in its protective function against TNFalpha- and hydrogen peroxide-induced cell death. J Cell Biochem 69: 436-452, 1998.
41. Ray PS, Martin JL, Swanson EA, Otani H, Dillmann WH, and Das DK. Transgene overexpression of αB crystallin confers simultaneous protection against cardiomyocyte apoptosis and necrosis during myocardial ischemia and reperfusion. FASEB J 15: 393-402, 2001.
42. Rebrin I, Kamzalov S, and Sohal RS. Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med 35: 626-635, 2003.
43. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, and Gaestel M. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274: 18947-18956, 1999.
44. Roth DM, Swaney JS, Dalton ND, Gilpin EA, and Ross J Jr. Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282: H2134-H2140, 2002.
45. Srinivasan AN, Nagineni CN, and Bhat SP. alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem 267: 23337-23341, 1992.
46. Sugiyama Y, Suzuki A, Kishikawa M, Akutsu R, Hirose T, Waye MM, Tsui SK, Yoshida S, and Ohno S. Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation. J Biol Chem 275: 1095-1104, 2000.
47. Suzuki A, Sugiyama Y, Hayashi Y, Nyu-i N, Yoshida M, Nonaka I, Ishiura S, Arahata K, and Ohno S. MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase. J Cell Biol 140: 1113-1124, 1998.
48. Tanaka N, Dalton N, Mao L, Rockman HA, Peterson KL, Gottshall KR, Hunter JJ, Chien KR, and Ross J Jr. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation 94: 1109-1117, 1996.
49. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, Chateau D, Chapon F, Tome F, Dupret JM, Paulin D, and Fardeau M. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20: 92-95, 1998.
50. Wang K and Spector A. α-Crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner. Eur J Biochem 242: 56-66, 1996.
51. White BC, Grossman LI, O'Neil BJ, DeGracia DJ, Neumar RW, Rafols JA, and Krause GS. Global brain ischemia and reperfusion. Ann Emerg Med 27: 588-594, 1996.
52. Wieske M, Benndorf R, Behlke J, Dolling R, Grelle G, Bielka H, and Lutsch G. Defined sequence segments of the small heat shock proteins HSP25 and aB-crystallin inhibit actin polymerization. Eur J Biochem 268: 2083-2090, 2001.
53. Yan LJ, Christians ES, Liu L, Xiao X, Sohal RS, and Benjamin IJ. Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J 21: 5164-5172, 2002.
54. Yoshida K, Aki T, Harada K, Shama KM, Kamoda Y, Suzuki A, and Ohno S. Translocation of HSP27 and MKBP in ischemic heart. Cell Struct Funct 24: 181-185, 1999.