Alp/Enigma Family Proteins Cooperate in Z-Disc Formation and Myofibril Assembly

PLoS Genetics

Volumn 9, Issue 3, 2013, Pages

  Katzemich, Anja ^a   Liao, Kuo An ^a   Czerniecki, Stefan ^a   Schöck, Frieder ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; GREEN FLUORESCENT PROTEIN; INSECT PROTEIN; PROTEIN ZASP52; PROTEIN ZASP66; PROTEIN ZASP67; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; MOLECULAR IMAGING; MUSCLE FIBRIL; NONHUMAN; PDZ DOMAIN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STABILITY;

ACTININ; ANIMALS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; LIM DOMAIN PROTEINS; MUSCLE PROTEINS; MUSCLES; MYOFIBRILS; PDZ DOMAINS; PROTEIN BINDING; SARCOMERES;

VERTEBRATA;

EID: 84876000921     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003342     Document Type: Article

References (57)

1. Sheikh F, Bang ML, Lange S, Chen J, (2007) "Z"eroing in on the role of Cypher in striated muscle function, signaling, and human disease. Trends Cardiovasc Med 17: 258-262.
2. Jani K, Schöck F, (2007) Zasp is required for the assembly of functional integrin adhesion sites. J Cell Biol 179: 1583-1597.
3. Sparrow JC, Schöck F, (2009) The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10: 293-298.
4. Zheng M, Cheng H, Banerjee I, Chen J, (2010) ALP/Enigma PDZ-LIM domain proteins in the heart. J Mol Cell Biol 2: 96-102.
5. Hudson AM, Petrella LN, Tanaka AJ, Cooley L, (2008) Mononuclear muscle cells in Drosophila ovaries revealed by GFP protein traps. Dev Biol 314: 329-340.
6. Rohn JL, Sims D, Liu T, Fedorova M, Schöck F, et al. (2011) Comparative RNAi screening identifies a conserved core metazoan actinome by phenotype. J Cell Biol 194: 789-805.
7. Benna C, Peron S, Rizzo G, Faulkner G, Megighian A, et al. (2009) Post-transcriptional silencing of the Drosophila homolog of human ZASP: a molecular and functional analysis. Cell Tissue Res 337: 463-476.
8. Rui Y, Bai J, Perrimon N, (2010) Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLoS Genet 6: e1001208 doi:10.1371/journal.pgen.1001208.
9. Katzemich A, Long JY, Jani K, Lee BR, Schöck F, (2011) Muscle type-specific expression of Zasp52 isoforms in Drosophila. Gene Expr Patterns 11: 484-490.
10. van der Meer DL, Marques IJ, Leito JT, Besser J, Bakkers J, et al. (2006) Zebrafish cypher is important for somite formation and heart development. Dev Biol 299: 356-372.
11. Zhou Q, Chu PH, Huang C, Cheng CF, Martone ME, et al. (2001) Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J Cell Biol 155: 605-612.
12. Han HF, Beckerle MC, (2009) The ALP-Enigma protein ALP-1 functions in actin filament organization to promote muscle structural integrity in Caenorhabditis elegans. Mol Biol Cell 20: 2361-2370.
13. McKeown CR, Han HF, Beckerle MC, (2006) Molecular characterization of the Caenorhabditis elegans ALP/Enigma gene alp-1. Dev Dyn 235: 530-538.
14. Nahabedian JF, Qadota H, Stirman JN, Lu H, Benian GM, (2012) Bending amplitude- a new quantitative assay of C. elegans locomotion: identification of phenotypes for mutants in genes encoding muscle focal adhesion components. Methods 56: 95-102.
15. Reedy MC, Beall C, (1993) Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Dev Biol 160: 443-465.
16. Au Y, Atkinson RA, Guerrini R, Kelly G, Joseph C, et al. (2004) Solution structure of ZASP PDZ domain; implications for sarcomere ultrastructure and enigma family redundancy. Structure 12: 611-622.
17. Kim J, Kim I, Yang JS, Shin YE, Hwang J, et al. (2012) Rewiring of PDZ domain-ligand interaction network contributed to eukaryotic evolution. PLoS Genet 8: e1002510 doi:10.1371/journal.pgen.1002510.
18. Fukuzawa A, Lange S, Holt M, Vihola A, Carmignac V, et al. (2008) Interactions with titin and myomesin target obscurin and obscurin-like 1 to the M-band: implications for hereditary myopathies. J Cell Sci 121: 1841-1851.
19. Kontrogianni-Konstantopoulos A, Jones EM, Van Rossum DB, Bloch RJ, (2003) Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol Biol Cell 14: 1138-1148.
20. Reedy MC, Beall C, Fyrberg E, (1989) Formation of reverse rigor chevrons by myosin heads. Nature 339: 481-483.
21. Faulkner G, Pallavicini A, Formentin E, Comelli A, Ievolella C, et al. (1999) ZASP: a new Z-band alternatively spliced PDZ-motif protein. J Cell Biol 146: 465-475.
22. Zhou Q, Ruiz-Lozano P, Martone ME, Chen J, (1999) Cypher, a striated muscle-restricted PDZ and LIM domain-containing protein, binds to alpha-actinin-2 and protein kinase C. J Biol Chem 274: 19807-19813.
23. Bryantsev AL, Baker PW, Lovato TL, Jaramillo MS, Cripps RM, (2012) Differential requirements for Myocyte Enhancer Factor-2 during adult myogenesis in Drosophila. Dev Biol 361: 191-207.
24. Ehler E, Gautel M (2008) The sarcomere and sarcomerogenesis. In: Laing NG, editor. The sarcomere and skeletal muscle disease. New York: Springer. pp. 1-14.
25. Sanger JW, Wang J, Fan Y, White J, Sanger JM, (2010) Assembly and dynamics of myofibrils. J Biomed Biotechnol 2010: 858606.
26. Sanger JW, Wang J, Holloway B, Du A, Sanger JM, (2009) Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil Cytoskeleton 66: 556-566.
27. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW, (1997) Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci USA 94: 9493-9498.
28. Du A, Sanger JM, Sanger JW, (2008) Cardiac myofibrillogenesis inside intact embryonic hearts. Dev Biol 318: 236-246.
29. Friedrich BM, Fischer-Friedrich E, Gov NS, Safran SA, (2012) Sarcomeric pattern formation by actin cluster coalescence. PLoS Comput Biol 8: e1002544 doi:10.1371/journal.pcbi.1002544.
30. 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.
31. Fyrberg E, Kelly M, Ball E, Fyrberg C, Reedy MC, (1990) Molecular genetics of Drosophila alpha-actinin: mutant alleles disrupt Z disc integrity and muscle insertions. J Cell Biol 110: 1999-2011.
32. Selcen D, Engel AG, (2005) Mutations in ZASP define a novel form of muscular dystrophy in humans. Ann Neurol 57: 269-276.
33. Cheng H, Kimura K, Peter AK, Cui L, Ouyang K, et al. (2010) Loss of enigma homolog protein results in dilated cardiomyopathy. Circ Res 107: 348-356.
34. Huang C, Zhou Q, Liang P, Hollander MS, Sheikh F, et al. (2003) Characterization and in vivo functional analysis of splice variants of cypher. J Biol Chem 278: 7360-7365.
35. Arimura T, Hayashi T, Terada H, Lee SY, Zhou Q, et al. (2004) A Cypher/ZASP mutation associated with dilated cardiomyopathy alters the binding affinity to protein kinase C. J Biol Chem 279: 6746-6752.
36. Griggs R, Vihola A, Hackman P, Talvinen K, Haravuori H, et al. (2007) Zaspopathy in a large classic late-onset distal myopathy family. Brain 130: 1477-1484.
37. Xia H, Winokur ST, Kuo WL, Altherr MR, Bredt DS, (1997) Actinin-associated LIM protein: identification of a domain interaction between PDZ and spectrin-like repeat motifs. J Cell Biol 139: 507-515.
38. Torrado M, Senatorov VV, Trivedi R, Fariss RN, Tomarev SI, (2004) Pdlim2, a novel PDZ-LIM domain protein, interacts with alpha-actinins and filamin A. Invest Ophthalmol Vis Sci 45: 3955-3963.
39. Nakagawa N, Hoshijima M, Oyasu M, Saito N, Tanizawa K, et al. (2000) ENH, containing PDZ and LIM domains, heart/skeletal muscle-specific protein, associates with cytoskeletal proteins through the PDZ domain. Biochem Biophys Res Commun 272: 505-512.
40. Vallenius T, Scharm B, Vesikansa A, Luukko K, Schafer R, et al. (2004) The PDZ-LIM protein RIL modulates actin stress fiber turnover and enhances the association of alpha-actinin with F-actin. Exp Cell Res 293: 117-128.
41. Schulz TW, Nakagawa T, Licznerski P, Pawlak V, Kolleker A, et al. (2004) Actin/alpha-actinin-dependent transport of AMPA receptors in dendritic spines: role of the PDZ-LIM protein RIL. J Neurosci 24: 8584-8594.
42. Guy PM, Kenny DA, Gill GN, (1999) The PDZ domain of the LIM protein enigma binds to beta-tropomyosin. Mol Biol Cell 10: 1973-1984.
43. Klaavuniemi T, Kelloniemi A, Ylänne J, (2004) The ZASP-like motif in actinin-associated LIM protein is required for interaction with the alpha-actinin rod and for targeting to the muscle Z-line. J Biol Chem 279: 26402-26410.
44. Sharma P, Shathasivam T, Ignatchenko V, Kislinger T, Gramolini AO, (2011) Identification of an FHL1 protein complex containing ACTN1, ACTN4, and PDLIM1 using affinity purifications and MS-based protein-protein interaction analysis. Mol Bio Syst 7: 1185-1196.
45. Beqqali A, Monshouwer-Kloots J, Monteiro R, Welling M, Bakkers J, et al. (2010) CHAP is a newly identified Z-disc protein essential for heart and skeletal muscle function. J Cell Sci 123: 1141-1150.
46. Linnemann A, van der Ven PF, Vakeel P, Albinus B, Simonis D, et al. (2010) The sarcomeric Z-disc component myopodin is a multiadapter protein that interacts with filamin and alpha-actinin. Eur J Cell Biol 89: 681-692.
47. Weins A, Schwarz K, Faul C, Barisoni L, Linke WA, et al. (2001) Differentiation- and stress-dependent nuclear cytoplasmic redistribution of myopodin, a novel actin-bundling protein. J Cell Biol 155: 393-404.
48. Ooshio T, Irie K, Morimoto K, Fukuhara A, Imai T, et al. (2004) Involvement of LMO7 in the association of two cell-cell adhesion molecules, nectin and E-cadherin, through afadin and alpha-actinin in epithelial cells. J Biol Chem 279: 31365-31373.
49. Bauer K, Kratzer M, Otte M, de Quintana KL, Hagmann J, et al. (2000) Human CLP36, a PDZ-domain and LIM-domain protein, binds to alpha-actinin-1 and associates with actin filaments and stress fibers in activated platelets and endothelial cells. Blood 96: 4236-4245.
50. Klaavuniemi T, Alho N, Hotulainen P, Kelloniemi A, Havukainen H, et al. (2009) Characterization of the interaction between Actinin-Associated LIM Protein (ALP) and the rod domain of alpha-actinin. BMC Cell Biol 10: 22.
51. Klaavuniemi T, Ylänne J, (2006) Zasp/Cypher internal ZM-motif containing fragments are sufficient to co-localize with alpha-actinin-analysis of patient mutations. Exp Cell Res 312: 1299-1311.
52. Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, et al. (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487: 231-234.
53. Schöck F, Perrimon N, (2002) Cellular processes associated with germ band retraction in Drosophila. Dev Biol 248: 29-39.
54. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405-407.
55. Saide JD, Chin-Bow S, Hogan-Sheldon J, Busquets-Turner L, Vigoreaux JO, et al. (1989) Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster. J Cell Biol 109: 2157-2167.
56. Katzemich A, Kreisköther N, Alexandrovich A, Elliott C, Schöck F, et al. (2012) The function of the M-line protein, obscurin, in controlling the symmetry of the sarcomere in Drosophila flight muscle. J Cell Sci 125: 3367-3379.
57. Lakey A, Labeit S, Gautel M, Ferguson C, Barlow DP, et al. (1993) Kettin, a large modular protein in the Z-disc of insect muscles. EMBO J 12: 2863-2871.