The UNC-45 chaperone is critical for establishing Myosin-Based myofibrillar organization and cardiac contractility in the Drosophila heart model

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Melkani, Girish C ^a,b   Bodmer, Rolf ^b   Ocorr, Karen ^b   Bernstein, Sanford I ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MYOSIN; PROTEIN UNC 45; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MYOSIN HEAVY CHAIN; UNC 45 PROTEIN, DROSOPHILA; UNC-45 PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHROPOD LARVA; ARTICLE; CONGENITAL HEART MALFORMATION; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DIASTOLE; DISEASE SEVERITY; DROSOPHILA; FEMALE; GENE SILENCING; HEART ARRHYTHMIA; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HISTOPATHOLOGY; IN VIVO STUDY; LIFESPAN; MALE; METAMORPHOSIS; NONHUMAN; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PUPA (LIFE CYCLE STAGE); RNA INTERFERENCE; SYSTOLE; VIDEORECORDING; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; HEART; HEART MUSCLE; LARVA; METABOLISM; MUSCLE CONTRACTION; MUSCLE FIBRIL; PHYSIOLOGY; SARCOMERE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HEART; LARVA; MALE; MODELS, ANIMAL; MOLECULAR CHAPERONES; MUSCLE CONTRACTION; MYOCARDIUM; MYOFIBRILS; MYOSIN HEAVY CHAINS; MYOSINS; SARCOMERES;

EID: 79960707770     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022579     Document Type: Article

References (57)

1. Odronitz F, Kollmar M, (2007) Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol 8: R196.
2. Epstein HF, Bernstein SI, (1992) Genetic approaches to understanding muscle development. Dev Biol 154: 231-244.
3. Seidman JG, Seidman C, (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104: 557-567.
4. Morita H, Nagai R, Seidman JG, Seidman CE, (2010) Sarcomere gene mutations in hypertrophy and heart failure. J Cardiovasc Transl Res 3: 297-303.
5. Tsoutsman T, Bagnall RD, Semsarian C, (2008) Impact of multiple gene mutations in determining the severity of cardiomyopathy and heart failure. Clin Exp Pharmacol Physiol 35: 1349-1357.
6. Wiegand V, Ebecke M, Figulla H, Schuler S, Kreuzer H, (1989) Structure and function of contractile proteins in human dilated cardiomyopathy. Clin Cardiol 12: 656-660.
7. Lowes BD, Minobe W, Abraham WT, Rizeq MN, Bohlmeyer TJ, et al. (1997) Changes in gene expression in the intact human heart. Downregulation of alpha-myosin heavy chain in hypertrophied, failing ventricular myocardium. J Clin Invest 100: 2315-2324.
8. Cammarato A, Dambacher CM, Knowles AF, Kronert WA, Bodmer R, et al. (2008) Myosin transducer mutations differentially affect motor function, myofibril structure, and the performance of skeletal and cardiac muscles. Mol Biol Cell 19: 553-562.
9. Mogami K, O'Donnell PT, Bernstein SI, Wright TR, Emerson CP Jr, (1986) Mutations of the Drosophila myosin heavy-chain gene: effects on transcription, myosin accumulation, and muscle function. Proc Natl Acad Sci U S A 83: 1393-1397.
10. Oldfors A, (2007) Hereditary myosin myopathies. Neuromuscul Disord 17: 355-67.
11. Srikakulam R, Winkelmann DA, (1999) Myosin II folding is mediated by a molecular chaperonin. J Biol Chem 274: 27265-27273.
12. Knowlton AA, Kapadia S, Torre-Amione G, Durand JB, Bies R, et al. (1998) Differential expression of heat shock proteins in normal and failing human hearts. J Mol Cell Cardiol 30: 811-818.
13. Willis MS, Schisler JC, Portbury AL, Patterson C, (2009) Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 81: 439-448.
14. Willis MS, Patterson C, (2010) Hold me tight: Role of the heat shock protein family of chaperones in cardiac disease. Circulation 122: 1740-1751.
15. Epstein HF, Thomson JN, (1974) Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature 250: 579-580.
16. Barral JM, Bauer CC, Ortiz I, Epstein HF, (1998) unc-45 mutations in Caenorhabditis elegans implicate a CRO1/She4p-like domain in myosin assembly. J Cell Biol 143: 1215-1225.
17. Lee CF, Melkani GC, Yu Q, Suggs JA, Kronert WA, et al. (2011) Drosophila UNC-45 accumulates in embryonic blastoderm and in muscles and is essential for muscle myosin stability. J Cell Sci 124: 699-705.
18. Yu Q, Bernstein SI, (2003) UCS proteins: managing the myosin motor. Curr Biol 13: R525-527.
19. Landsverk ML, Li S, Hutagalung AH, Najafov A, Hoppe T, et al. (2007) The UNC-45 chaperone mediates sarcomere assembly through myosin degradation in Caenorhabditis elegans. J Cell Biol 177: 205-210.
20. Barral JM, Hutagalung AH, Brinker A, Hartl FU, Epstein HF, (2002) Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295: 669-671.
21. Melkani GC, Lee CF, Cammarato A, Bernstein SI, (2010) Drosophila UNC-45 prevents heat-induced aggregation of skeletal muscle myosin and facilitates refolding of citrate synthase. Biochem Biophys Res Commun 396: 317-322.
22. Bernick EP, Zhang PJ, Du S, (2010) Knockdown and overexpression of Unc-45b result in defective myofibril organization in skeletal muscles of zebrafish embryos. BMC Cell Biol 11: 70.
23. Srikakulam R, Liu L, Winkelmann DA, (2008) Unc45b forms a cytosolic complex with Hsp90 and targets the unfolded myosin motor domain. PLoS One 3: e2137.
24. Price MG, Landsverk ML, Barral JM, Epstein HF, (2002) Two mammalian UNC-45 isoforms are related to distinct cytoskeletal and muscle-specific functions. J Cell Sci 115: 4013-4023.
25. Kachur TM, Pilgrim DB, (2008) Myosin assembly, maintenance and degradation in muscle: Role of the chaperone UNC-45 in myosin thick filament dynamics. Int J Mol Sci, 9: 1863-1875.
26. Etard C, Behra M, Fischer N, Hutcheson D, Geisler R, et al. (2007) The UCS factor Steif/Unc-45b interacts with the heat shock protein Hsp90a during myofibrillogenesis. Dev Biol 308: 133-143.
27. Lee CF, Hauenstein AV, Fleming JK, Gasper WC, Engelke V, et al. (2011) X-ray crystal structure of the UCS domain-containing UNC-45 myosin chaperone from Drosophila melanogaster. Structure 19: 397-408.
28. Wong KC, Naqvi NI, Iino Y, Yamamoto M, Balasubramanian MK, (2000) Fission yeast Rng3p: an UCS-domain protein that mediates myosin II assembly during cytokinesis. J Cell Sci 113: 2421-2432.
29. Lord M, Pollard TD, (2004) UCS protein Rng3p activates actin filament gliding by fission yeast myosin-II. J Cell Biol 167: 315-325.
30. Amorim MJ, Mata J, (2009) Rng3, a member of the UCS family of myosin co-chaperones, associates with myosin heavy chains cotranslationally. EMBO Rep 10: 186-191.
31. Shi H, Blobel G, (2010) UNC-45/CRO1/She4p (UCS) protein forms elongated dimer and joins two myosin heads near their actin binding region. Proc Natl Acad Sci U S A 107: 21382-21387.
32. Wohlgemuth SL, Crawford BD, Pilgrim DB, (2007) The myosin co-chaperone UNC-45 is required for skeletal and cardiac muscle function in zebrafish. Dev Biol 303: 483-492.
33. Geach TJ, Zimmerman LB, (2010) Paralysis and delayed Z-disc formation in the Xenopus tropicalis unc45b mutant dicky ticker. BMC Dev Biol 10: 75.
34. Kachur TM, Audhya A, Pilgrim DB, (2008) UNC-45 is required for NMY-2 contractile function in early embryonic polarity establishment and germline cellularization in C. elegans. Dev Biol 314: 287-299.
35. Anderson MJ, Pham VN, Vogel AM, Weinstein BM, Roman BL, (2008) Loss of unc45a precipitates arteriovenous shunting in the aortic arches. Dev Biol 318: 258-267.
36. Janiesch PC, Kim J, Mouysset J, Barikbin R, Lochmuller H, et al. (2007) The ubiquitin-selective chaperone CDC-48/p97 links myosin assembly to human myopathy. Nat Cell Biol 9: 379-390.
37. Ocorr K, Perrin L, Lim HY, Qian L, Wu X, et al. (2007) Genetic control of heart function and aging in Drosophila. Trends Cardiovasc Med 17: 177-182.
38. Ocorr K, Reeves NL, Wessells RJ, Fink M, Chen HS, et al. (2007) KCNQ potassium channel mutations cause cardiac arrhythmias in Drosophila that mimic the effects of aging. Proc Natl Acad Sci U S A 104: 3943-3948.
39. Wolf MJ, Amrein H, Izatt JA, Choma MA, Reedy MC, et al. (2006) Drosophila as a model for the identification of genes causing adult human heart disease. Proc Natl Acad Sci U S A 103: 1394-1399.
40. Neely GG, Kuba K, Cammarato A, Isobe K, Amann S, et al. (2010) A global in vivo Drosophila RNAi screen identifies NOT3 as a conserved regulator of heart function. Cell 141: 142-153.
41. Cripps RM, Olson EN, (2002) Control of cardiac development by an evolutionarily conserved transcriptional network. Dev Biol 246: 14-28.
42. Molina MR, Cripps RM, (2001) Ostia, the inflow tracts of the Drosophila heart, develop from a genetically distinct subset of cardial cells. Mech Dev 109: 51-59.
43. Curtis NJ, Ringo JM Dowse HB, (1999) Morphology of the pupal heart, adult heart, and associated tissues in the fruit fly, Drosophila melanogaster. J Morphol 240: 225-235.
44. Zeitouni B, Senatore S, Severac D, Aknin C, Semeriva M, et al. (2007) Signalling pathways involved in adult heart formation revealed by gene expression profiling in Drosophila. PLoS Genet 3: 1907-1921.
45. Monier B, Astier M, Semeriva M, Perrin L, (2005) Steroid-dependent modification of Hox function drives myocyte reprogramming in the Drosophila heart. Development 132: 5283-5293.
46. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
47. Han Z, Olson EN, (2005) Hand is a direct target of Tinman and GATA factors during Drosophila cardiogenesis and hematopoiesis. Development 132: 3525-3536.
48. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
49. McGuire SE, Mao Z, Davis RL, (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004: pl6.
50. Hayashi M, Imanaka-Yoshida K, Yoshida T, Wood M, Fearns C, et al. (2006) A crucial role of mitochondrial Hsp40 in preventing dilated cardiomyopathy. Nat Med 12: 128-132.
51. Inagaki N, Hayashi T, Arimura T, Koga Y, Takahashi M, et al. (2006) Alpha B-crystallin mutation in dilated cardiomyopathy. Biochem Biophys Res Commun 342: 379-386.
52. Stanley BA, Liu P, Kirshenbaum LA, Van Eyk JE, (2005) Proteomic analysis of ischemic heart failure patients reveals increases in a myosin assembly protein (UNC-45). Circ Res 97 10 (abstract).
53. Lo PC, Frasch M, (2001) A role for the COUP-TF-related gene seven-up in the diversification of cardioblast identities in the dorsal vessel of Drosophila. Mech Dev 104: 49-60.
54. Ocorr K, Fink M, Cammarato A, Bernstein S, Bodmer R, (2009) Semi-automated Optical Heartbeat Analysis of small hearts. J Vis Exp 10: 3791/1425.
55. Fink M, Callol-Massot C, Chu A, Ruiz-Lozano P, Izpisua Belmonte JC, (2009) A new method for detection and quantification of heartbeat parameters in Drosophila, zebrafish, and embryonic mouse hearts. Biotechniques 46: 101-113.
56. Alayari NN, Vogler G, Taghli-Lamallem O, Ocorr K, Bodmer R, et al. (2009) Fluorescent labeling of Drosophila heart structures. J Vis Exp 10-3791/1423.
57. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.