Role of nonmuscle myosin IIB and N-RAP in cell spreading and myofibril assembly in primary mouse cardiomyocytes

Cell Motility and the Cytoskeleton

Volumn 65, Issue 9, 2008, Pages 747-761

  Lu, Shajia ^a   Horowits, Robert ^a,b  

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

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Heart; Myofibrillogenesis; RNA interference; Sarcomere

Indexed keywords

ACTIN; ALPHA ACTININ; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; MYOSIN IIB; N RAP PROTEIN; PROTEASOME; PROTEIN DERIVATIVE; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL SPREADING; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO; ENZYME DEGRADATION; GENETIC TRANSFECTION; HEART MUSCLE CELL; MORPHOMETRICS; MOUSE; MUSCLE FIBRIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; RNA INTERFERENCE;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; GENE EXPRESSION REGULATION; MICE; MUSCLE PROTEINS; MYOCYTES, CARDIAC; MYOFIBRILS; NONMUSCLE MYOSIN TYPE IIB; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TIME FACTORS; UBIQUITIN;

EID: 50649110727     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20299     Document Type: Article

References (47)

1. Bao J, Jana SS, Adelstein RS. 2005. Vertebrate nonmuscle myosin II isoforms rescue small interfering RNA-induced defects in COS-7 cell cytokinesis. J Biol Chem 280(20):19594-19599.
2. Betapudi V, Licate LS, Egelhoff TT. 2006. Distinct roles of non-muscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration. Cancer Res 66(9):4725-4733.
3. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. 2001. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294(5547):1704-1708.
4. Cai Y, Biais N, Giannone G, Tanase M, Jiang G, Hofman JM, Wiggins CH, Silberzan P, Buguin A, Ladoux B, Sheetz MP. 2006. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 91(10):3907-3920.
5. Carroll SL, Horowits R. 2000. Myofibrillogenesis and formation of cell contacts mediate the localization of N-RAP in cultured chick cardiomyocytes. Cell Motil Cytoskeleton 47(1):63-76.
6. Carroll SL, Herrera AH, Horowits R. 2001. Targeting and functional role of N-RAP, a nebulin-related LIM protein, during myofibril assembly in cultured chick cardiomyocytes. J Cell Sci 114(Part 23):4229-4238.
7. Carroll S, Lu S, Herrera AH, Horowits R. 2004. N-RAP scaffolds IZ-I assembly during myofibrillogenesis in cultured chick cardiomyocytes. J Cell Sci 117(1):105-114
8. Conti MA, Adelstein RS, 2008. Nonmuscle myosin II moves in new directions. J Cell Sci 121 (Part 1):11-18.
9. Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS. 2004. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem 279(40):41263-41266.
10. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW. 1997. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci USA 94(17):9493-9498.
11. Dhume A, Lu S, Horowits R. 2006. Targeted disruption of N-RAP gene function by RNA interference: A role for N-RAP in myofibril organization. Cell Motil Cytoskeleton 63493-511.
12. 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(6):2268-2278.
13. Du A, Sanger JM, Linask KK, Sanger JW. 2003. Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesoderm. Dev Biol 257(2):382-394.
14. Ehler E, Rothen BM, Hämmerle SP, Komiyama M, Perriard J-C. 1999. Myofibrillogenesis in the developing chicken heart: Assembly of thez-disk, m-line and thick filaments. J Cell Sci 112:1529-1539.
15. Galdeen SA, Stephens S, Thomas DD, Titus MA. 2007. Talin influences the dynamics of the myosin VII-membrane interaction. Mol Biol Cell 18(10):4074-4084.
16. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. 2001. An overview of real-time quantitative PCR: Applications to quantify cytokine gene expression. Methods 25(4):386-401.
17. Golomb E, Ma X, Jana SS, Preston YA, Kawamoto S, Shoham NG, Goldin E, Conti MA, Sellers JR, Adelstein RS. 2004. Identification and characterization of nonmuscle myosin H-C, a new member of the myosin II family. J Biol Chem 279(4):2800-2808.
18. Greenberg CC, Connelly PS, Daniels MP, Horowits R. 2008. Krp1 (Sarcosin) promotes lateral fusion of myofibril assembly intermediates in cultured mouse cardiomyocytes, Exp Cell Res 314(5):1177-1191.
19. Gregorio CC, Antin PB. 2000. To the heart of myofibril assembly. Trends Cell Biol 10(9):355-362.
20. Handel SE, Greaser ML, Schultz E, Wang SM, Bulinski JC, Lin JJ, Lessard JL. 1991. Chicken cardiac myofibrillogenesis studied with antibodies specific for titin and the muscle and nonmuscle isoforms of actin and tropomyosin. Cell Tissue Res 263(3):419-430.
21. Hodge TP, Cross R, Kendrick-Jones J. 1992. Role of the COOH-terminal nonhelical tailpiece in the assembly of a vertebrate non-muscle myosin rod. J Cell Biol 118(5):1085-1095.
22. Imanaka-Yoshida K. 1997. Myofibrillogenesis in precardiac mesoderm explant culture. Cell Struct Funct 22(1):45-49.
23. Lee DH, Goldberg AL. 1998. Proteasome inhibitors: Valuable new tools for cell biologists. Trends Cell Biol 8(10):397-403.
24. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408.
25. LoRusso SM, Rhee D, Sanger JM, Sanger JW. 1997. Premyofibrils in spreading adult cardiomyocytes in tissue culture: Evidence for reexpression of the embryonic program for myofibrillogenesis in adult cells. Cell Motil Cytoskeleton 37(3):183-198; erratum 38(3):310.
26. Lu S, Borst DE, Horowits R. 2005. N-RAP expression during mouse heart development. Dev Dyn 233(1):201-212.
27. Luo G, Zhang JQ, Nguyen TP, Herrera AH, Paterson B, Horowits R. 1997. Complete cDNA sequence and tissue localization of N-RAP, a novel nebulin-related protein of striated muscle. Cell Motil Cytoskeleton 38(1):75-90.
28. Luo G, Herrera AH, Horowits R. 1999. Molecular interactions of N-RAP, a nebulin-related protein of striated muscle myotendon junctions and intercalated disks. Biochemistry 38(19):6135-6143.
29. Murakami N, Trenkner E, Elzinga M. 1993. Changes in expression of nonmuscle myosin heavy chain isoforms during muscle and nonmuscle tissue development. Dev Biol 157(1):19-27.
30. Rhee D, Sanger JM, Sanger JW. 1994. The premyofibril: Evidence for its role in myofibrillogenesis. Cell Motil Cytoskeleton 28(1):1-24.
31. Root DD, Wang K. 1994. Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry 33(42):12581-12591.
32. Rudy DE, Yatskievych TA, Antin PB, Gregorio CC. 2001. Assembly of thick, thin, and titin filaments in chick precardiac explants. Dev Dyn 221(1):61-71.
33. Sandquist JC, Swenson KI, Demali KA, Burridge K, Means AR. 2006. Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J Biol Chem 281(47):35873-35883.
34. 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(6-8):343-354.
35. 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(4):1159-1172.
36. Sellers JR. 2000. Myosins: A diverse superfamily. Biochim Biophys Acta 1496(1):3-22.
37. Straussman R, Squire JM, Ben-Ya'acov A, Ravid S. 2005. Skip residues and charge interactions in myosin II coiled-coils: Implications for molecular packing. J Mol Biol 353(3):613-628.
38. Straussman R, Ben-Ya'acov A, Woolfson DN, Ravid S. 2007. Kinking the coiled coil-negatively charged residues at the coiled-coil interface. J Mol Biol 366(4):1232-1242.
39. Takeda K, Yu ZX, Qian S, Chin TK, Adelstein RS, Ferrans VJ. 2000. Nonmuscle myosin II localizes to the Z-lines and intercalated discs of cardiac muscle and to the Z-lines of skeletal muscle. Cell Motil Cytoskeleton 46(1):59-68.
40. Takeda K, Kishi H, Ma X, Yu ZX, Adelstein RS. 2003. Ablation and mutation of nonmuscle myosin heavy chain II-B results in a defect in cardiac myocyte cytokinesis. Circ Res 93(4):330-337.
41. Tullio AN, Accili D, Ferrans VJ, Yu ZX, Takeda K, Grinberg A, Westphal H, Preston YA, Adelstein RS. 1997. Nonmuscle myosin H-B is required for normal development of the mouse heart. Proc Natl Acad Sci USA 94(23):12407-12412.
42. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF. 2007. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 176(5):573-580.
43. Wang SM, Greaser ML, Schultz E, Bulinski JC, Lin JJ, Lessard JL. 1988. Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin. J Cell Biol 107(3):1075-1083.
44. Willis MS, Ike C, Li L, Wang DZ, Glass DJ, Patterson C. 2007. Muscle ring finger 1, but not muscle ring finger 2, regulates cardiac hypertrophy in vivo. Circ Res 100(4):456-459.
45. Witt SH, Granzier H, Witt CC, Labeit S. 2005. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: Towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 350(4):713-722.
46. Zhang JQ, Weisberg A, Horowits R. 1998. Expression and purification of large nebulin fragments and their interaction with actin. Biophys J 74(1):349-359.
47. Zhang JQ, Elzey B, Williams G, Lu S, Law DJ, Horowits R. 2001. Ultrastructural and biochemical localization of N-RAP at the interface between myofibrils and intercalated disks in the mouse heart. Biochemistry 40(49):14898-14906.