Myofibril assembly visualized by imaging N-RAP, alpha-actinin, and actin in living cardiomyocytes

Experimental Cell Research

Volumn 315, Issue 12, 2009, Pages 2126-2139

  Manisastry, Shyam M ^a   Zaal, Kristien J M ^a   Horowits, Robert ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Heart; Myofibrillogenesis; Sarcomere

Indexed keywords

ACTIN; ALPHA ACTININ; CELL PROTEIN; PROTEIN N RAP; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BLEACHING; CHICK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO CELL; FLUORESCENCE; GENETIC TRANSFECTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOBLOTTING; MUSCLE FIBRIL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN STRUCTURE;

EID: 66149149492     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.02.006     Document Type: Article

References (47)

1. Gregorio C.C., and Antin P.B. To the heart of myofibril assembly. Trends Cell Biol. 10 (2000) 355-362
2. Sanger J.W., Kang S., Siebrands C.C., Freeman N., Du A., Wang J., Stout A.L., and Sanger J.M. How to build a myofibril. J. Muscle Res. Cell. Motil. 26 (2005) 343-354
3. Rhee D., Sanger J.M., and Sanger J.W. The premyofibril: evidence for its role in myofibrillogenesis. Cell. Motil. Cytoskeleton. 28 (1994) 1-24
4. Dabiri G.A., Turnacioglu K.K., Sanger J.M., and Sanger J.W. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9493-9498
5. Imanaka-Yoshida K. Myofibrillogenesis in precardiac mesoderm explant culture. Cell Struct. Funct. 22 (1997) 45-49
6. Ehler E., Rothen B.M., Hämmerle S.P., Komiyama M., and Perriard J.-C. Myofibrillogenesis in the developing chicken heart: assembly of the z-disk, m-line and thick filaments. J. Cell Sci. 112 (1999) 1529-1539
7. Rudy D.E., Yatskievych T.A., Antin P.B., and Gregorio C.C. Assembly of thick, thin, and titin filaments in chick precardiac explants. Dev. Dyn. 221 (2001) 61-71
8. Lu S., Borst D.E., and Horowits R. N-RAP expression during mouse heart development. Dev. Dyn. 233 (2005) 201-212
9. Dlugosz A.A., Antin P.B., Nachmias V.T., and Holtzer H. The relationship between stress fiber-like structures and nascent myofibrils in cultured cardiac myocytes. J. Cell Biol. 99 (1984) 2268-2278
10. Handel S.E., Greaser M.L., Schultz E., Wang S.M., Bulinski J.C., Lin J.J., and Lessard J.L. Chicken cardiac myofibrillogenesis studied with antibodies specific for titin and the muscle and nonmuscle isoforms of actin and tropomyosin. Cell Tissue Res. 263 (1991) 419-430
11. Schultheiss T., Lin Z.X., Lu M.H., Murray J., Fischman D.A., 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 (1990) 1159-1172
12. Wang S.M., Greaser M.L., Schultz E., Bulinski J.C., Lin J.J., and Lessard J.L. Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin. J. Cell Biol. 107 (1988) 1075-1083
13. Holtzer H., Hijikata T., Lin Z.X., Zhang Z.Q., Holtzer S., Protasi F., Franzini-Armstrong C., and Sweeney H.L. Independent assembly of 1.6 microns long bipolar MHC filaments and I-Z-I bodies. Cell Struct. Funct. 22 (1997) 83-93
14. Srikakulam R., and Winkelmann D.A. Chaperone-mediated folding and assembly of myosin in striated muscle. J. Cell Sci. 117 (2004) 641-652
15. Imanaka-Yoshida K., Knudsen K.A., and Linask K.K. N-cadherin is required for the differentiation and initial myofibrillogenesis of chick cardiomyocytes. Cell Motil. Cytoskeleton 39 (1998) 52-62
16. Du A., Sanger J.M., Linask K.K., and Sanger J.W. Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm. Dev. Biol. 257 (2003) 382-394
17. Du A., Sanger J.M., and Sanger J.W. Cardiac myofibrillogenesis inside intact embryonic hearts. Dev. Biol. 318 (2008) 236-246
18. Tullio A.N., Accili D., Ferrans V.J., Yu Z.X., Takeda K., Grinberg A., Westphal H., Preston Y.A., and Adelstein R.S. Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 12407-12412
19. Lu S., and Horowits R. Role of nonmuscle myosin IIB and N-RAP in cell spreading and myofibril assembly in primary mouse cardiomyocytes. Cell Motil. Cytoskeleton 65 (2008) 747-761
20. Greenberg C.C., Connelly P.S., Daniels M.P., and Horowits R. Krp1 (Sarcosin) promotes lateral fusion of myofibril assembly intermediates in cultured mouse cardiomyocytes. Exp. Cell Res. 314 (2008) 1177-1191
21. Carroll S.L., and Horowits R. Myofibrillogenesis and formation of cell contacts mediate the localization of N-RAP in cultured chick cardiomyocytes. Cell Motil. Cytoskeleton 47 (2000) 63-76
22. Lu S., Carroll S.L., Herrera A.H., Ozanne B., and Horowits R. New N-RAP-binding partners α-actinin, filamin and Krp1 detected by yeast two-hybrid screening: implications for myofibril assembly. J. Cell Sci. 116 (2003) 2169-2178
23. Luo G., Herrera A.H., and Horowits R. Molecular interactions of N-RAP, a nebulin-related protein of striated muscle myotendon junctions and intercalated disks. Biochemistry 38 (1999) 6135-6143
24. Lu S., Borst D.E., and Horowits R. Expression and alternative splicing of N-RAP during mouse skeletal muscle development. Cell Motil. Cytoskeleton 65 (2008) 945-954
25. Carroll S., Lu S., Herrera A.H., and Horowits R. N-RAP scaffolds I-Z-I assembly during myofibrillogenesis in cultured chick cardiomyocytes. J. Cell Sci. 117 (2004) 105-114
26. Carroll S.L., Herrera A.H., and Horowits R. Targeting and functional role of N-RAP, a nebulin-related LIM protein, during myofibril assembly in cultured chick cardiomyocytes. J. Cell Sci. 114 (2001) 4229-4238
27. Dhume A., Lu S., and Horowits R. Targeted disruption of N-RAP gene function by RNA interference: a role for N-RAP in myofibril organization. Cell Motil. Cytoskeleton 63 (2006) 493-511
28. Mohiddin S.A., Lu S., Cardoso J.-P., Carroll S.L., Jha S., Horowits R., and Fananapazir L. Genomic organization, alternative splicing, and expression of human and mouse N-RAP, a nebulin-related LIM protein of striated muscle. Cell Motil. Cytoskeleton 55 (2003) 200-212
29. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., and Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22 (2004) 1567-1572
30. Wang J., Shaner N., Mittal B., Zhou Q., Chen J., Sanger J.M., and Sanger J.W. Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil. Cytoskeleton 61 (2005) 34-48
31. Luo G., Zhang J.Q., Nguyen T.P., Herrera A.H., Paterson B., and Horowits R. Complete cDNA sequence and tissue localization of N-RAP, a novel nebulin-related protein of striated muscle. Cell Motil. Cytoskeleton 38 (1997) 75-90
32. Waterman-Storer C.M., Sanger J.W., and Sanger J.M. Dynamics of organelles in the mitotic spindles of living cells: membrane and microtubule interactions. Cell Motil. Cytoskeleton 26 (1993) 19-39
33. Motulsky H., and Christopoulos A. Fitting Models to Biological Data Using Linear and Nonlinear Regression: A Practical Guide to Curve Fitting (2004), Oxford University Press, Oxford ; New York
34. Nwe T.M., Maruyama K., and Shimada Y. Relation of nebulin and connectin (titin) to dynamics of actin in nascent myofibrils of cultured skeletal muscle cells. Exp. Cell. Res. 252 (1999) 33-40
35. Dome J.S., Mittal B., Pochapin M.B., Sanger J.M., and Sanger J.W. Incorporation of fluorescently labeled actin and tropomyosin into muscle cells. Cell. Differ. 23 (1988) 37-52
36. Shimada Y., Suzuki H., and Konno A. Dynamics of actin in cardiac myofibrils and fibroblast stress fibers. Cell Struct. Funct. 22 (1997) 59-64
37. Suzuki H., Komiyama M., Konno A., and Shimada Y. Exchangeability of actin in cardiac myocytes and fibroblasts as determined by fluorescence photobleaching recovery. Tissue Cell. 30 (1998) 274-280
38. Littlefield R., Almenar-Queralt A., and Fowler V.M. Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat. Cell. Biol. 3 (2001) 544-551
39. Papponen H., Kaisto T., Leinonen S., Kaakinen M., and Metsikko K. Evidence for gamma-actin as a Z disc component in skeletal myofibers. Exp. Cell. Res. (2008)
40. Moncman C.L., and Wang K. Nebulette: a 107 kD nebulin-like protein in cardiac muscle. Cell Motil. Cytoskeleton 32 (1995) 205-225
41. Wang K., Knipfer M., Huang Q.Q., van Heerden A., Hsu L.C., Gutierrez G., Quian X.L., and Stedman H. Human skeletal muscle nebulin sequence encodes a blueprint for thin filament architecture: sequence motifs and affinity profiles of tandem repeats and terminal SH3. J. Biol. Chem. 271 (1996) 4304-4314
42. Wright J., Huang Q.Q., and Wang K. Nebulin is a full-length template of actin filaments in the skeletal muscle sarcomere: an immunoelectron microscopic study of its orientation and span with site-specific monoclonal antibodies. J. Muscle Res. Cell. Motil. 14 (1993) 476-483
43. Labeit S., and Kolmerer B. The complete primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248 (1995) 308-315
44. Feuerstein R., Wang X., Song D., Cooke N.E., and Liebhaber S.A. The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10655-10659
45. Sanchez-Garcia I., Axelson H., and Rabbitts T.H. Functional diversity of LIM proteins: amino-terminal activation domains in the oncogenic proteins RBTN1 and RBTN2. Oncogene 10 (1995) 1301-1306
46. Gehmlich K., Geier C., Osterziel K.J., Van Der Ven P.F., and Furst D.O. Decreased interactions of mutant muscle LIM protein (MLP) with N-RAP and alpha-actinin and their implication for hypertrophic cardiomyopathy. Cell Tissue Res. 317 (2004) 129-136
47. Gregorio C.C., Granzier H., Sorimachi H., and Labeit S. Muscle assembly: a titanic achievement?. Curr. Opin. Cell Biol. 11 (1999) 18-25