De novo myofibrillogenesis in C2C12 cells: Evidence for the independent assembly of M bands and Z disks

American Journal of Physiology - Cell Physiology

Volumn 290, Issue 2, 2006, Pages

  Kontrogianni Konstantopoulos, Aikaterini ^a   Catino, Dawn H ^a   Strong, John C ^a   Bloch, Robert J ^a  

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

Author keywords

actinin; A band; Myomesin; Myosin; Obscurin; Titin

Indexed keywords

ALPHA ACTININ; CONNECTIN; EPITOPE; MUSCLE PROTEIN; MYOMESIN; MYOSIN; OBSCURIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; ACTIN; ACTININ; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FAST MUSCLE; HEAVY CHAIN; MOUSE; MUSCLE CELL; MUSCLE FIBRIL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SARCOMERE; ANIMAL; CELL LINE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; ULTRASTRUCTURE;

ANIMALIA;

ACTININ; ACTINS; ANIMALS; CELL LINE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MICE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOFIBRILS; MYOSINS; PROTEIN KINASES;

EID: 33644864092     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00442.2005     Document Type: Article

References (49)

1. Agarkova I, Ehler E, Lange S, Schoenauer R, and Perriard JC. M-band: a safeguard for sarcomere stability? J Muscle Res Cell Motil 24: 191-203, 2003.
2. Ahuja P, Perriard E, Perriard JC, and Ehler E. Sequential myofibrillar breakdown accompanies mitotic division of mammalian cardiomyocytes. J Cell Sci 117: 3295-3306, 2004.
3. Auerbach D, Rothen-Ruthishauser B, Bantle S, Leu M, Ehler E, Helfman D, and Perriard JC. Molecular mechanisms of myofibril assembly in heart. Cell Struct Funct 22: 139-146, 1997.
4. Bagnato P, Barone V, Giacomello E, Rossi D, and Sorrentino V. Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles. J Cell Biol 160: 245-253, 2003.
5. Bang ML, Centner T, Fornoff F, Geach AJ, Gotthardt M, McNabb M, Witt CC, Labeit D, Gregorio CC, Granzier H, and Labeit S. The complete gene sequence of titin, expression of an unusual ∼700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ Res 89: 1065-1072, 2001.
6. Beall CJ, Sepanski MA, and Fyrberg EA. Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Genes Dev 3: 131-140, 1989.
7. Benian GM, Tinley TL, Tang X, and Borodovsky M. The Caenorhabditis elegans gene unc-89, required for muscle M-band assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J Cell Biol 132: 835-848, 1996.
8. Borisov AB, Kontrogianni-Konstantopoulos A, Bloch RJ, Westfall MV, and Russell MW. Dynamics of obscurin localization during differentiation and remodeling of cardiac myocytes: obscurin as an integrator of myofibrillar structure. J Histochem Cytochem 52: 1117-1127, 2004.
9. Centner T, Fougerousse F, Freiburg A, Witt C, Beckmann JS, Granzier H, Trombitás K, Gregorio CC, and Labeit S. Molecular tools for the study of titin's differential expression. Adv Exp Med Biol 481: 35-52, 2000.
10. Centner T, Yano J, Kimura E, McElhinny AS, Pelin K, Witt CC, Bang ML, Trombitás K, Granzier H, Gregorio CC, Sorimachi H, and Labeit S. Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. J Mol Biol 306: 717-726, 2001.
11. 12 co-culture on a fibroblast substratum enables sustained survival of contractile, highly differentiated myotubes with peripheral nuclei and adult fast myosin expression. Cell Motil Cytoskeleton 58: 200-211, 2004.
12. Dabiri GA, Turnacioglu KK, Sanger JM, and Sanger JW. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci USA 94: 9493-9498, 1997.
13. Du A, Sanger JM, Linask KK, and Sanger JW. Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm. Dev Biol 257: 382-394, 2003.
14. Ehler E, Rothen BM, Hämmerle SP, Komiyama M, and Perriard JC. Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-band and the thick filaments. J Cell Sci 112: 1529-1539, 1999.
15. Fürst DO, Obermann WM, and van der Ven PF. Structure and assembly of the sarcomeric M band. Rev Physiol Biochem Pharmacol 138: 163-202, 1999.
16. Fürst DO, Osborn M, and Weber K. Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol 109: 517-527, 1989.
17. Gautel M, Mues A, and Young P. Control of sarcomeric assembly: the flow of information on titin. Rev Physiol Biochem Pharmacol 138: 97-137, 1999.
18. Gotthardt M, Hammer RE, Hübner N, Monti J, Witt CC, McNabb M, Richardson JA, Granzier H, Labeit S, and Herz J. Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structure. J Biol Chem 278: 6059-6065, 2003.
19. Gregorio CC and Antin PB. To the heart of myofibril assembly. Trends Cell Biol 10: 355-362, 2000.
20. 2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J Cell Biol 143: 1013-1027, 1998.
21. Grove BK, Kurer V, Lehner C, Doetschman TC, Perriard JC, and Eppenberger HM. A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98: 518-524, 1984.
22. Hill CS, Duran S, Lin ZX, Weber K, and Holtzer H. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J Cell Biol 103: 2185-2196, 1986.
23. Holtzer H, Hijikata T, Lin ZX, Zhang ZQ, Holtzer S, Protasi F, Franzini-Armstrong C, and Sweeney HL. Independent assembly of 1.6 microns long bipolar MHC filaments and I-Z-I bodies. Cell Struct Funct 22: 83-93, 1997.
24. Kontrogianni-Konstantopoulos A and Bloch RJ. The hydrophilic domain of small ankyrin-1 interacts with the two N-terminal immunoglobulin domains of titin. J Biol Chem 278: 3985-3991, 2003.
25. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Randall WR, and Bloch RJ. Obscurin regulates the organization of myosin into A bands. Am J Physiol Cell Physiol 287: C209-C217, 2004.
26. Kontrogianni-Konstantopoulos A, Jones EM, Van Rossum DB, and Bloch RJ. Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol Biol Cell 14: 1138-1148, 2003.
27. Labeit S, Kolmerer B, and Linke WA. The giant protein titin: emerging roles in physiology and pathophysiology. Circ Res 80: 290-294, 1997.
28. Lin Z, Lu MH, Schultheiss T, Choi J, Holtzer S, DiLullo C, Fischman DA, and Holtzer H. Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil Cytoskeleton 29: 1-19, 1994.
29. McElhinny AS, Kazmierski ST, Labeit S, and Gregorio CC. Nebulin: the nebulous, multifunctional giant of striated muscle. Trends Cardiovasc Med 13: 195-201, 2003.
30. Miller G, Musa H, Gautel M, and Peckham M. A targeted deletion of the C-terminal end of titin, including the titin kinase domain, impairs myofibrillogenesis. J Cell Sci 116: 4811-4819, 2003.
31. Millevoi S, Trombitás K, Kolmerer B, Kostin S, Schaper J, Pelin K, Granzier H, and Labeit S. Characterization of nebulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J Mol Biol 282: 111-123, 1998.
32. Obermann WM, Gautel M, Weber K, and Fürst DO. Molecular structure of the sarcomeric M band: mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J 16: 211-220, 1997.
33. Ojima K, Lin ZX, Zhang ZQ, Hijikata T, Holtzer S, Labeit S, Sweeney HL, and Holtzer H. Initiation and maturation of I-Z-I bodies in the growth tips of transfected myotubes. J Cell Sci 112: 4101-4112, 1999.
34. Rhee D, Sanger JM, and Sanger JW. The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil Cytoskeleton 28: 1-24, 1994.
35. Rudy DE, Yatskievych TA, Antin PB, and Gregorio CC. Assembly of thick, thin, and titin filaments in chick precardiac explants. Dev Dyn 221: 61-71, 2001.
36. Russell MW, Raeker MO, Korytkowski KA, and Sonneman KJ. Identification, tissue expression and chromosomal localization of human Obscurin-MLCK, a member of the titin and Dbl families of myosin light chain kinases. Gene 282: 237-246, 2002.
37. Sanger JW, Chowrashi P, Shaner NC, Spalthoff S, Wang J, Freeman NL, and Sanger JM. Myofibrillogenesis in skeletal muscle cells. Clin Orthop Relat Res 403, Suppl: S153-S162, 2002.
38. Schultheiss T, Lin ZX, Lu MH, Murray J, Fischman DA, Weber K, Masaki T, Imamura M, and Holtzer H. Differential distribution of subsets of myofibrillar proteins in cardiac nonstriated and striated myofibrils. J Cell Biol 110: 1159-1172, 1990.
39. Silberstein L, Webster SG, Travis M, and Blau HM. Developmental progression of myosin gene expression in cultured muscle cells. Cell 46: 1075-1081, 1986.
40. Toyama Y, Forry-Schaudies S, Hoffman B, and Holtzer H. Effects of taxol and Colcemid on myofibrillogenesis. Proc Natl Acad Sci USA 79: 6556-6560, 1982.
41. Van der Loop FT, van der Ven PF, Fürst DO, Gautel M, van Eys GJ, and Ramaekers FC. Integration of titin into the sarcomeres of cultured differentiating human skeletal muscle cells. Eur J Cell Biol 69: 301-307, 1996.
42. Van der Ven PF, Bartsch JW, Gautel M, Jockusch H, and Fürst DO. A functional knock-out of titin results in defective myofibril assembly. J Cell Sci 113: 1405-1414, 2000.
43. Van der Ven PF, Ehler E, Perriard JC, and Fürst DO. Thick filament assembly occurs after the formation of a cytoskeletal scaffold. J Muscle Res Cell Motil 20: 569-579, 1999.
44. Van der Ven PF and Fürst DO. Assembly of titin, myomesin and M-protein into the sarcomeric M band in differentiating human skeletal muscle cells in vitro. Cell Struct Funct 22: 163-171, 1997.
45. Van der Ven PF and Fürst DO. Expression of sarcomeric proteins and assembly of myofibrils in the putative myofibroblast cell line BHK-21/C13. J Muscle Res Cell Motil 19: 767-775, 1998.
46. Wang SM, Lo MC, Shang C, Kao SC, and Tseng YZ. Role of M-band proteins in sarcomeric titin assembly during cardiac myofibrillogenesis. J Cell Biochem 71: 82-95, 1998.
47. Williams BD and Waterston RH. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124: 475-490, 1994.
48. Yang YG, Obinata T, and Shimada Y. Developmental relationship of myosin binding proteins (myomesin, connectin and C-protein) to myosin in chicken somites as studied by immunofluorescence microscopy. Cell Struct Funct 25: 177-185, 2000.
49. Young P, Ehler E, and Gautel M. Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly. J Cell Biol 154: 123-136, 2001.