Early incorporation of obscurin into nascent sarcomeres: Implication for myofibril assembly during cardiac myogenesis

Histochemistry and Cell Biology

Volumn 129, Issue 4, 2008, Pages 463-478

  Borisov, Andrei B ^a   Martynova, Marina G ^b   Russell, Mark W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

Cardiac myocytes; Myofibrillogenesis; Myosin; Obscurin; Sarcomere; Sarcoplasmic reticulum; Z disks

Indexed keywords

ACTIN; CONNECTIN; MYOSIN; OBSCURIN;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; HEART MUSCLE CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOLOCALIZATION; MUSCLE DEVELOPMENT; MYOFIBRILLOGENESIS; NONHUMAN; PRIORITY JOURNAL; RAT; SARCOMERE; SARCOPLASMIC RETICULUM;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEART; IMMUNOHISTOCHEMISTRY; MODELS, BIOLOGICAL; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MYOCYTES, CARDIAC; MYOFIBRILS; RATS; SARCOMERES;

RATTUS;

EID: 41049108809     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-008-0378-y     Document Type: Article

References (59)

1. Agarkova I, Perriard J-C (2005) The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15:477-485
2. Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard JC (2003) M-band: a safeguard for sarcomeric stability? J Muscle Res Cell Motil 24:191-203
3. Anversa P, Olivetti G, Bracchi PG, Loud AV (1981) Postnatal development of the M-band in rat cardiac myofibrils. Circ Res 48:561-568
4. Armani A, Galli S, Giacomello E, Bagnato P, Barone V, Rossi D, Sorrentino V (2006) Molecular interactions with obscurin are involved in the localization of muscle-specific small ankyrin 1 isoforms to subcompartments of the sarcoplasmic reticulum. Exp Cell Res 312:3456-3458
5. Arimura T, Matsumoto Y, Okazaki O, Hayashi T, Takahashi M, Inagaki N, Hinohara K, Ashizawa N, Yano K, Kimura A (2007) Structural analysis of obscurin gene in hypertrophic cardiomyopathy. Biochem Biophys Res Commun 362:281-287
6. Bader D, Masaki T, Fischman DA (1982) Immunocytochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763-770
7. Bagnato P, Barone V, Giacomello E, Rossi D, Sorrentino V (2003) Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils is striated muscles. J Cell Biol 160:245-253
8. Bang ML, Centner T, Fornoff F, Geach AJ, Gotthardt M, McNabb M, Witt CC, Labeit D, Gregorio CC, Granzier H, Labeit S (2001) 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
9. Borisov AB (1991) Myofibrillogenesis and reversible disassembly of myofibrils as adaptive reactions of cardiac muscle cells. Acta Physiol Scand 142(suppl 599):71-80
10. Borisov AB, Coro Antich RM, Rumyantsev PP (1985) DNA synthesis in cultures of atrial and ventricular rat cardiomyocytes. Tsitologia 27:990-994
11. Borisov AB, Goncharova EI, Pinaev GP, Rumyantsev PP (1989) Changes in α-actinin localization and myofibrillogenesis in rat cardiomyocytes in culture. Tsitologia 31:642-646
12. Borisov AB, Dedkov EI, Carlson BM (2001) Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat Rec 264:203-218
13. Borisov AB, Raeker MO, Kontrogianni-Konstantopoulos A, Yang K, Kurnit DM, Bloch RJ, Russell MW (2003) Rapid response of cardiac obscurin gene cluster to aortic stenosis: differential activation of Rho-GEF and MLCK and involvement in hypertrophic growth. Biochem Biophys Res Commun 310:910-918
14. Borisov AB, Kontrogianni-Konstantopoulos A, Bloch RJ, Westfall MV, Russell MW (2004) Dynamics of obscurin localization during differentiation and remodeling of cardiac myocaytes: obscurin as an integrator of myofibrillar structure. J Histochem Cytochem 52:1117-1127
15. Borisov AB, Sutter SB, Kontrogianni-Konstantopoulos A, Bloch RJ, Westfall MV, Russell MW (2006) Essential role of obscurin in cardiac myofibrillogenesis and hypertrophic response: evidence from small interfering RNA-mediated gene silencing. Histochem Cell Biol 125:227-238
16. Burridge K, Wennerberg K (2004) Rho and Rac take center stage. Cell 116:167-179
17. Carlsson E, Kjörell U, Thornell L-E, Lambertsson A, Strehler E (1982) Differentiation of the myofibrils and the intermediate filament system during postnatal development of the rat heart. Eur J Cell Biol 27:62-73
18. Dlugosz AA, Antin PB, Nachmias VT, Holtzer H (1984) The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J Cell Biol 99:2268-2278
19. Du A, Sanger JM, Linask KK, Sanger JW (2003) Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm. Dev Biol 257:382-394
20. Ehler E, Rothen BM, Haemmerle SP, Komiyama M, Perriard JC (1999) Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filaments. J Cell Sci 112:1529-1539
21. Ehler E, Fowler VM, Perriard J-C (2004) Myofibrillogenesis in the developing chicken heart: role of actin isoforms and the pointed end actin capping protein tropomodulin during thin filament assembly. Dev Dyn 229:745-755
22. Epstein ND, Davis JS (2003) Sensing stretch is fundamental. Cell 112:147-150
23. Fridlianskaia II, Goncharova EI, Borisov AB, Krylova TA, Pinaev GP (1989) Monoclonal antibody to the muscle isoform of α-actinin-a marker for studies of differentiation of skeletal and cardiac muscle. Tsitologiia 31:1234-1237
24. Fukuzawa A, Idowu S, Gautel M (2005) Complete human gene structure of obscurin: implications for isoform generation by differential splicing. J Muscle Res Cell Motil 26:427-434
25. Granzier HL, Labeit S (2005) Titin and its associated proteins: the third myofilament system of the sarcomere. Adv Protein Chem 71:89-119
26. Granzier HL, Labeit S (2006) The giant muscle protein titin is an adjustable molecular spring. Exerc Sport Sci Rev 34:50-53
27. Holtzer H, Hijikata T, Lin ZX, Zhang ZQ, Holzer S, Protasi F, Franzini-Armstrong C, Sweeney HL (1997) Independent assembly of 1.6 micron long bipolar MHC filaments and I-Z-I bodies. Cell Struct Funct 22:83-93
28. Huxley AF (2000) Cross-bridge action: present views, prospects, and unknowns. J Biomech 33:1189-1195
29. Kaarbo M, Crane DI, Murrell WG (2003) RhoA is highly up-regulated in the process of early heart development of the chick and important for normal embryogenesis. Dev Dyn 227:35-47
30. 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
31. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Bloch RJ (2005) De novo myofibrillogenesis in C2C12 cells: evidence for the independent assembly of M-bands and Z-disks. Am J Physiol 290:C626-C637
32. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Sutter S, Borisov AB, Pumplin DW, Russell MW, Bloch RJ (2006) Obscurin modulates the assembly and organization of sarcomeres and the sarcoplasmic reticulum. FASEB J 20:2102-2111
33. Lange S, Agarkova I, Perriard J-C, Ehler E (2005) The sarcomeric M-band during development and in disease. J Muscle Res Cell Motil 26:375-379
34. Lange S, Ehler E, Gautel M (2006) From A to Z and back? Multicompartment protein in the sarcomere. Trends Cell Biol 16:11-18
35. LeWinter MM, Wu Y, Labeit S, Granzier H (2007) Cardiac titin: structure, functions and role in disease. Clin Chim Acta 375:1-9
36. Miller G, Musa H, Gautel M, Peckham M (2003) A targeted deletion of the C-terminal end of titin, including the titin kinase domain, impairs myofibrillogenesis. J Cell Sci 116:4811-4819
37. Musa H, Meek S, Gautel M, Peddie D, Smith AJH, Peckham M (2006) Targeted homozygous deletion of M-band titin in cardiomyocytes prevents sarcomere formation. J Cell Sci 119:4322-4331
38. Ojima K, Lin ZX, Zhang ZQ, Hijikata T, Holtzer S, Labeit S, Sweeney HL, Holtzer H (1999) Initiation and maturation of I-Z-I bodies in the growth tips of transfected myotubes. J Cell Sci 112:4101-4112
39. Peng J, Raddatz K, Labeit S, Granzier H, Gotthardt M (2005) Muscle atrophy in titin M-line deficient mice. J Muscle Res Cell Motil 26:381-388
40. Person V, Kostin S, Suzuki K, Labeit S, Schaper J (2000) Antisense oligonucleotide experiments elucidate the essential role of titin in sarcomerogenesis in adult cardiomyocytes in long-term culture. J Cell Sci 113:3851-3859
41. Porter NC, Resneck WG, O'Neill A, Van Rossum DB, Stone MR, Bloch RJ (2005) Association of small ankyrin 1 with the sarcoplasmic reticulum. Mol Membr Biol 22:421-432
42. Raeker MO, Su F, Geisler SB, Borisov AB, Kontrogianni-Konstantopoulos A, Lyons SE, Russell MW (2006) Obscurin is required for the lateral alignment of striated myofibrils in zebrafish. Dev Dyn 235:2018-1029
43. Rhee D, Sanger JM, Sanger JW (1994) The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil Cytoskeleton 28:1-24
44. Rumyantsev PP (1976) Myofibrillogenesis and its relationships with cell proliferation during development and regeneration of skeletal, cardiac and smooth muscles. Acta Histochem 17(suppl):215-218
45. Rumyantsev PP (1977) Interrelations of the proliferation and differentiation processes during cardiac myogenesis and regeneration. Int Rev Cytol 51:187-273
46. Rumyantsev PP (1991) Growth and hyperplasia of cardiac muscle cells. Harwood Academic Publishers, New York
47. Russell MW, Raeker MO, Korytkowski KA, Sonneman KJ (2002) 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
48. Sanger JW, Kang S, Siebrands CC, Freeman N, Du A, Wang J, Stout AL, Sanger JM (2005) How to build a myofibril. J Muscle Res Cell Motil 26:343-354
49. Schoenauer R, Bertoncini P, Machaidze G, Aebi U, Perriard JC, Hegner M, Agarkova I (2005) Myomesin as a molecular spring with adaptable elasticity. J Mol Biol 349:367-379
50. Schultheiss T, Lin ZX, Lu MH, Murray J, Fischman DA, Weber K, Masaki T, Imamura M, Holtzer H (1990) Differential distribution of subsets of myofibrillar proteins in cardiac nonstriated and striated myofibrils. J Cell Biol 110:1159-1172
51. Seeley M, Huang W, Chen Z, Wolff WO, Lin X, Xu X (2007) Depletion of zebrafish titin reduces cardiac contractility by disrupting the assembly of Z-discs and A-bands. Circ Res 100:238-245
52. Tokuyasu KT, Maher PA (1987) Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryo. II. Generation of alpha-actinin dots within titin spots at the time of the first myofibril formation. J Cell Biol 105:2795-2801
53. Trinick J, Tskhovrebova L (1999) Titin: a molecular control freak. Trends Cell Biol 9:377-380
54. Trombitás K, Greaser M, French G, Granzier H (1998) PEVK extension of human soleus muscle titin revealed by immunolabeling with the anti-titin antibody 9D10. J Struct Biol 4:679-689
55. Tskhovrebova L, Trinick J (2003) Titin: properties and family relationship. Nat Rev Mol Cell Biol 4:679-689
56. Wei L, Imanaka-Yoshida K, Wang L, Zhan S, Schneider MD (2002) Inhibition of Rho family GTPases by Rho GDP dissociation inhibitor disrupts cardiac morphogenesis and inhibits cardiomyocyte proliferation. Development 129:1705-1714
57. Weinert S, Bergmann N, Luo X, Erdmann B, Gotthargt M (2006) M line-deficient titin causes cardiac lethality through impaired maturation of the sarcomere. J Cell Biol 173:559-570
58. Witt CC, Burkart C, Labeit D, McNabb M, Wu Y, Granzier H, Labeit S (2006) Nebulin regulates thin filament length, contractility, and Z-disk structure in vivo. EMBO J 25:3843-3855
59. Young P, Ehler E, Gautel M (2001) Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly. J Cell Biol 154:123-136