Desmin-related cardiomyopathy: An unfolding story

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 4, 2011, Pages

  McLendon, Patrick M ^a   Robbins, Jeffrey ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Amyloid; B crystallin; Heart; Proteotoxicity

Indexed keywords

DESMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; CARDIOMYOPATHY; CELL METABOLISM; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DESMIN RELATED CARDIOMYOPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HEART MUSCLE CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; REVIEW;

ANIMALS; CARDIOMYOPATHIES; CELL DEATH; DESMIN; HUMANS; INCLUSION BODIES; MITOCHONDRIA, HEART; OXIDATIVE STRESS; PROTEIN UNFOLDING;

EID: 80053286909     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00601.2011     Document Type: Review

References (66)

1. Bär H, Strelkov SV, Sjöberg G, Aebi U, Herrmann H. The biology of desmin filaments: how do mutations affect their structure, assembly, and organisation? J Struct Biol 148: 137-152, 2004.
2. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292: 1552-1555, 2001.
3. Bova MP, Yaron O, Huang Q, Ding L, Haley DA, Stewart PL, Horwitz J. Mutation R120G in αB-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: 6137-6142, 1999.
4. Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, Wawrousek EF. αB-crystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci 42: 2924-2934, 2001.
5. Capetanaki Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med 12: 339-348, 2002.
6. Chávez Zobel AT, Loranger A, Marceau N, Thériault JR, Lambert H, Landry J. Distinct chaperone mechanisms can delay the formation of aggresomes by the myopathy-causing R120G αB-crystallin mutant. Hum Mol Genet 12: 1609-1620, 2003.
7. Chen Q, Liu JB, Horak KM, Zheng H, Kumarapeli AR, Li J, Li F, Gerdes AM, Wawrousek EF, Wang X. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ Res 97: 1018-1026, 2005.
8. Clark AR, Naylor CE, Bagnéris C, Keep NH, Slingsby C. Crystal structure of R120G disease mutant of human αB-crystallin domain dimer shows closure of a groove. J Mol Biol 408: 118-134, 2011.
9. Dalakas MC, Park KY, Semino-Mora C, Lee HS, Sivakumar K, Goldfarb LG. Desmin myopathy, a skeletal myopathy with cardiomyopathy caused by mutations in the desmin gene. N Engl J Med 342: 770-780, 2000.
10. Dong X, Liu J, Zheng H, Glasford JW, Huang W, Chen QH, Harden NR, Li F, Gerdes AM, Wang X. In situ dynamically monitoring the proteolytic function of the ubiquitin-proteasome system in cultured cardiac myocytes. Am J Physiol Heart Circ Physiol 287: H1417-H1425, 2004.
11. Edstrom L, Thornell LE, Eriksson A. A new type of hereditary distal myopathy with characteristic sarcoplasmic bodies and intermediate (skeletin) filaments. J Neurol Sci 47: 171-190, 1980.
12. Forloni G, Colombo L, Girola L, Tagliavini F, Salmona M. Antiamyloidogenic activity of tetracyclines: studies in vitro. FEBS J 487: 404-407, 2001.
13. Goebel HH. Desmin-related neuromuscular disorders. Muscle Nerve 18: 1306-1320, 1995.
14. Goebel HH, Voit T, Warlo I, Jacobs K, Johannsen U, Muller CR. Immunohistologic and electron microscopic abnormalities of desmin and dystrophin in familial cardiomyopathy and myopathy. Rev Neurol (Paris) 150: 452-459, 1994.
15. Goldfarb LG, Dalakas MC. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest 119: 1806-1813, 2009.
16. Goldfarb LG, Olive M, Vicart P, Goebel HH. Intermediate filament diseases: desminopathy. Adv Exp Med Biol 642: 131-164, 2008.
17. Goldfarb LG, Park KY, Cervenakova L, Gorokhova S, Lee HS, Vasconcelos O, Nagle JW, Semino-Mora C, Sivakumar K, Dalakas MC. Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat Genet 19: 402-403, 1998.
18. Goldfarb LG, Vicart P, Goebel HH, Dalakas MC. Desmin myopathy. Brain 127: 723-734, 2004.
19. Gottlieb RA, Finley KD, Mentzer RM Jr. Cardioprotection requires taking out the trash. Basic Res Cardiol 104: 169-180, 2009.
20. Gunawardena S, Goldstein LS. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch Neurol 62: 46-51, 2005.
21. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489, 2003.
22. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10: 524-530, 2000.
23. Kostareva A, Sjöberg G, Bruton J, Zhang SJ, Balogh J, Gudkova A, Hedberg B, Edström L, Westerblad H, Sejersen T. Mice expressing L345P mutant desmin exhibit morphological and functional changes of skeletal and cardiac mitochondria. J Muscle Res Cell Motil 29: 25-36, 2008.
24. Lazarov O, Robinson J, Tang YP, Hairston IS, Korade-Mirnics Z, Lee VM, Hersh LB, Sapolsky RM, Mirnics K, Sisodia SS. Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120: 701-713, 2005.
25. Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell LE, Babinet C, Paulin D. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol 139: 129-144, 1997.
26. Liu J, Chen Q, Huang W, Horak KM, Zheng H, Mestril R, Wang X. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J 20: 362-364, 2006.
27. Liu J, Tang M, Mestril R, Wang X. Aberrant protein aggregation is essential for a mutant desmin to impair the proteolytic function of the ubiquitin-proteasome system in cardiomyocytes. J Mol Cell Cardiol 40: 451-454, 2006.
28. Maloyan A, Gulick J, Glabe CG, Kayed R, Robbins J. Exercise reverses preamyloid oligomer and prolongs survival in αB-crystallinbased desmin-related cardiomyopathy. Proc Natl Acad Sci USA 104: 5995-6000, 2007.
29. Maloyan A, Osinska H, Lammerding J, Lee RT, Cingolani OH, Kass DA, Lorenz JN, Robbins J. Biochemical and mechanical dysfunction in a mouse model of desmin-related myopathy. Circ Res 104: 1021-1028, 2009.
30. Maloyan A, Sanbe A, Osinska H, Westfall M, Robinson D, Imahashi Ki Murphy E, Robbins J. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in αB-crystallin desmin-related cardiomyopathy. Circulation 112: 3451-3461, 2005.
31. Maloyan A, Sayegh J, Osinska H, Chua BH, Robbins J. Manipulation of death pathways in desmin-related cardiomyopathy. Circ Res 106: 1524-1532, 2010.
32. Meredith SC. Protein denaturation and aggregation. Ann NY Acad Sci 1066: 181-221, 2005.
33. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075, 2008.
34. Morrison LE, Whittaker RJ, Klepper RE, Wawrousek EF, Glembotski CC. Roles for αB-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model. Am J Physiol Heart Circ Physiol 286: H847-H855, 2004.
35. Munoz-Marmol AM, Strasser G, Isamat M, Coulombe PA, Yang Y, Roca X, Vela E, Mate JL, Coll J, Fernandez-Figueras MT, Navas- Palacios JJ, Ariza A, Fuchs E. A dysfunctional desmin mutation in a patient with severe generalized myopathy. Proc Natl Acad Sci USA 95: 11312-11317, 1998.
36. Olivé M, Goldfarb L, Moreno D, Laforet E, Dagvadorj A, Sambuughin N, Martínez-Matos JA, Martínez F, Alió J, Farrero E, Vicart P, Ferrer I. Desmin-related myopathy: clinical, electrophysiological, radiological, neuropathological and genetic studies. J Neurol Sci 219: 125-137, 2004.
37. Osborn M, Goebel HH. The cytoplasmic bodies in a congenital myopathy can be stained with antibodies to desmin, the muscle-specific intermediate filament protein. Acta Neuropathol 62: 149-152, 1983.
38. Pattison JS, Osinska H, Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res 109: 151-160, 2011.
39. Pattison JS, Sanbe A, Maloyan A, Osinska H, Klevitsky R, Robbins J. Cardiomyocyte expression of a polyglutamine preamyloid oligomer causes heart failure. Circulation 117: 2743-2751, 2008.
40. Perng MD, Muchowski PJ, van den IJssel P, Wu GJ, Hutcheson AM, Clark JI, Quinlan RA. The cardiomyopathy and lens cataract mutation in αB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro. J Biol Chem 274: 33235-33243, 1999.
41. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice. J Clin Invest 118: 2190-2199, 2008.
42. Rajasekaran NS, Connell P, Christians ES, Yan LJ, Taylor RP, Orosz A, Zhang XQ, Stevenson TJ, Peshock RM, Leopold JA, Barry WH, Loscalzo J, Odelberg SJ, Benjamin IJ. Human αB-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 130: 427-439, 2007.
43. Reimann J, Kunz WS, Vielhaber S, Kappes-Horn K, Schröder R. Mitochondrial dysfunction in myofibrillar myopathy. Neuropathol Appl Neurobiol 29: 45-51, 2003.
44. Rubinsztein DC. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443: 780-786, 2006.
45. Sanbe A, Gulick J, Hanks MC, Liang Q, Osinska H, Robbins J. Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ Res 92: 609-616, 2003.
46. Sanbe A, Osinska H, Saffitz JE, Glabe CG, Kayed R, Maloyan A, Robbins J. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci USA 101: 10132-10136, 2004.
47. Sanbe A, Osinska H, Villa C, Gulick J, Klevitsky R, Glabe CG, Kayed R, Robbins J. Reversal of amyloid-induced heart disease in desminrelated cardiomyopathy. Proc Natl Acad Sci USA 102: 13592-13597, 2005.
48. Schlossarek S, Carrier L. The ubiquitin-proteasome system in cardiomyopathies. Curr Opin Cardiol 26: 190-195, 2011.
49. Schlossarek S, Mearini G, Carrier L. Cardiac myosin-binding protein C in hypertrophic cardiomyopathy: mechanisms and therapeutic opportunities. J Mol Cell Cardiol 50: 613-620, 2011.
50. Schröder R, Goudeau B, Simon MC, Fischer D, Eggermann T, Clemen CS, Li Z, Reimann J, Xue Z, Rudnik-Schöneborn S, Zerres K, van der Ven PF, Fürst DO, Kunz WS, Vicart P. On noxious desmin: functional effects of a novel heterozygous desmin insertion mutation on the extrasarcomeric desmin cytoskeleton and mitochondria. Hum Mol Genet 12: 657-669, 2003.
51. Su H, Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 85: 253-262, 2010.
52. Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ, Nguyen L, Gerard RD, Levine B, Rothermel BA, Hill JA. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci USA 105: 9745-9750, 2008.
53. Thornell LE, Carlsson L, Li Z, Mericskay M, Paulin D. Null mutation in the desmin gene gives rise to a cardiomyopathy. J Mol Cell Cardiol 29: 2107-2124, 1997.
54. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, Chateau D, Chapon F, Tome F, Dupret JM, Paulin D, Fardeau M. A missense mutation in the αB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20: 92-95, 1998.
55. Vicart P, Dupret JM, Hazan J, Li Z, Gyapay G, Krishnamoorthy R, Weissenbach J, Fardeau M, Paulin D. Human desmin gene: cDNA sequence, regional localization and exclusion of the locus in a familial desmin-related myopathy. Hum Genet 98: 422-429, 1996.
56. Viswanathan J, Haapasalo A, Bottcher C, Miettinen R, Kurkinen KM, Lu A, Thomas A, Maynard CJ, Romano D, Hyman BT, Berezovska O, Bertram L, Soininen H, Dantuma NP, Tanzi RE, Hiltunen M. Alzheimer's disease-associated ubiquilin-1 regulates presenilin-1 accumulation and aggresome formation. Traffic 12: 330-348, 2011.
57. Wang X, Klevitsky R, Huang W, Glasford J, Li F, Robbins J. αB-crystallin modulates protein aggregation of abnormal desmin. Circ Res 93: 998-1005, 2003.
58. Wang X, Osinska H, Dorn GW 2nd, Nieman M, Lorenz JN, Gerdes AM, Witt S, Kimball T, Gulick J, Robbins J. Mouse model of desminrelated cardiomyopathy. Circulation 103: 2402-2407, 2001.
59. Wang X, Osinska H, Klevitsky R, Gerdes AM, Nieman M, Lorenz J, Hewett T, Robbins J. Expression of R120G-αB-crystallin causes aberrant desmin and αB-crystallin aggregation and cardiomyopathy in mice. Circ Res 89: 84-91, 2001.
60. Wang X, Osinska H, Gerdes AM, Robbins J. Desmin filaments and cardiac disease: establishing causality. J Card Fail 8: S287-S292, 2002.
61. Wang X, Robbins J. Heart failure and protein quality control. Circ Res 99: 1315-1328, 2006.
62. Willis MS, Patterson C. Into the heart: the emerging role of the ubiquitinproteasome system. J Mol Cell Cardiol 41: 567-579, 2006.
63. Willis MS, Schisler JC, Portbury AL, Patterson C. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 81: 439-448, 2009.
64. Willis MS, Townley-Tilson WH, Kang EY, Homeister JW, Patterson C. Sent to destroy: the ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res 106: 463-478, 2010.
65. Zheng H, Tang M, Zheng Q, Kumarapeli AR, Horak KM, Tian Z, Wang X. Doxycycline attenuates protein aggregation in cardiomyocytes and improves survival of a mouse model of cardiac proteinopathy. J Am Coll Cardiol 56: 1418-1426, 2010.
66. Zheng Q, Su H, Ranek MJ, Wang X. Autophagy and p62 in Cardiac Proteinopathy. Circ Res 109: 296-308, 2011.