The complete mouse nebulin gene sequence and the identification of cardiac nebulin

Journal of Molecular Biology

Volumn 328, Issue 4, 2003, Pages 835-846

  Kazmierski, Steven T ^a   Antin, Parker B ^a   Witt, Christian C ^b   Huebner, Norbert ^c   McElhinny, Abigail S ^a   Labeit, Siegfried ^b   Gregorio, Carol C ^a,d  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d The University of Arizona   (United States)

Author keywords

Heart muscle; Myofibril; Nebulin; Sarcomere; Thin filament

Indexed keywords

ANTIBODY; COMPLEMENTARY DNA; MESSENGER RNA; NEBULIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; EMBRYO; EXON; FETUS; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC CODE; GENETIC TRANSCRIPTION; HEART MUSCLE CELL; HUMAN; IN SITU HYBRIDIZATION; INTRON; MOLECULAR DYNAMICS; MOUSE; MUSCLE FIBRIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SKELETAL MUSCLE; THIN FILAMENT; XENOPUS LAEVIS;

ANURA; VERTEBRATA; XENOPUS LAEVIS;

EID: 0037427450     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00348-6     Document Type: Article

References (60)

1. Pelin K., Ridanpaa M., Donner K., Wilton S., Krishnarajah J., Laing N., et al. Refined localization of the genes for nebulin and titin on chromosome 2q allows the assignment of nebulin as a candidate gene for autosomal recessive nemaline myopathy. Eur. J. Hum. Genet. 5:1997;229-234.
2. Schurr E., Skamene E., Gros P. Mapping of the gene coding for the muscle protein nebulin (Neb) to the proximal region of mouse chromosome 2. Cytogenet. Cell Genet. 57:1991;214-216.
3. Pelin K., Hilpela P., Donner K., Sewry C., Akkari P.A., Wilton S.D., et al. Mutations in the nebulin gene associated with autosomal recessive nemaline myopathy. Proc. Natl Acad. Sci. USA. 96:1999;2305-2310.
4. Wang K., Wright J. Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line. J. Cell. Biol. 107:1988;2199-2212.
5. Wright J., Huang Q.-Q., 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.
6. Millevoi S., Trombitas K., Kolmerer B., Kostin S., Schaper J., Pelin K., et al. Characterization of nebulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J. Mol. Biol. 282:1998;111-123.
7. Herrera A.H., Elzey B., Law D.J., Horowits R. Terminal regions of mouse nebulin: sequence analysis and complementary localization with N-RAP. Cell Motil. Cytoskeleton. 45:2000;211-222.
8. McElhinny A.S., Kolmerer B., Fowler V.M., Labeit S., Gregorio C.C. The N-terminal end of nebulin interacts with tropomodulin at the pointed ends of the thin filaments. J. Biol. Chem. 276:2001;583-592.
9. Hu D.H., Kimura S., Maruyama K. Sodium dodecyl sulfate gel electrophoretic studies of connectin-like high molecular weight proteins of various types of vertebrate and invertebrate muscle. J. Biochem. (Tokyo). 99:1986;1485-1492.
10. Locker R.H., Wild D.J.C. A comparative study of high molecular weight proteins in various types of muscle across the animal kingdom. J. Biochem. (Tokyo). 99:1986;1473-1484.
11. Labeit S., Kolmerer B. The complete primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248:1995;308-315.
12. Kruger M., Wright J., Wang K. Nebulin as a length regulator of thin filaments of vertebrate skeletal muscles: correlation of thin filament length, nebulin size, and epitope profile. J. Cell Biol. 115:1991;97-107.
13. Labeit S., Gibson T., Lakey A., Leonard K., Zeviani M., Knight P., et al. Evidence that nebulin is a protein-ruler in muscle thin filaments. FEBS Letters. 282:1991;313-316.
14. Trinick J. Titin and nebulin: protein rulers in muscle? Trends Biochem. Sci. 19:1994;405-409.
15. Wang K., Knipfer M., Huang Q.-Q., van Heerden A., Hsu L.C.-L., Gutierrez G., et al. Human skeletal muscle nebulin sequence encodes a blueprint for thin filament architecture. J. Biol. Chem. 271:1996;4304-4314.
16. Holmes K.C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature (London). 347:1990;44-49.
17. Jin J.-P., Wang K. Cloning, expression and protein interaction of human nebulin fragments composed of varying numbers of sequence modules. J. Biol. Chem. 266:1991;21215-21223.
18. Chen M.-J.G., Shih C.-L., Wang K. Nebulin is an actin-binding, length regulating template protein of the thin filaments of skeletal muscle: actin-interaction and confirmation of a two module human nebulin fragment. Biophys. J. 64:1993;147-159.
19. Pfuhl M., Winder S.J., Castiglione-Morelli M.A., Labeit S., Pastore A. Correlation between conformational and binding properties of nebulin repeats. J. Mol. Biol. 257:1996;367-384.
20. Bang M.-L., Gregorio C.C., Labeit S. Molecular dissection of the interaction of desmin with the C-terminal region of nebulin. J. Struct. Biol. 137:2002;119-127.
21. Bang M.-L., Mudry R.E., McElhinny A.S., Trombitas K., Geach A.J., Yamasaki R., et al. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J. Cell Biol. 153:2001;413-427.
22. Clark K.A., McElhinny A.S., Beckerle M.C., Gregorio C.C. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18:2002;637-706.
23. Root D.D., Wang K. Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry. 33:1994;12581-12591.
24. Root D.D., Wang K. High-affinity actin-binding nebulin fragments influence the ActoS1 complex. Biochemistry. 40:2001;1171-1186.
25. Zhang J.Q., Luo G., Herrera A.H., Paterson B., Horowits R. cDNA cloning of mouse nebulin: evidence that the nebulin-coding sequence is highly conserved among vertebrates. Eur. J. Biochem. 239:1996;835-841.
26. Burge C., Karlin S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268:1997;78-94.
27. Xu Y., Uberbacher E.C. Automated gene identification in large-scale genomic sequences. J. Comput. Biol. 4:1997;325-338.
28. Hyatt, D., Snoddy, J., Schmoyer, D., Chen, G., Fischer, K., Parang, M., et al. (2000). Improved analysis and annotation tools for whole-genome computational annotation and analysis: GRAIL-EXP genome analysis toolkit and related analysis tools. Genome Sequencing and Biology Meeting, May.
29. Stevensen B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell. Biol. 103:1986;755-766.
30. Willott E., Balda M.S., Fanning A.S., Jameson B., Van Itallie C., Anderson J.M. The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc. Natl Acad. Sci. USA. 90:1993;7834-7838.
31. Stedman H., Browning K., Oliver N., Oronzi-Scott M., Fischbeck K., Sarkar S., et al. Nebulin cDNAs detect a 25-kilobase transcript in skeletal muscle and localize to human chromosome 2. Genomics. 2:1988;1-7.
32. Fulton A.B., Alftine C. Organization of protein and mRNA for titin and other myofibril components during myofibrillogenesis in cultured chicken skeletal muscle. Cell Struct. Funct. 22:1997;51-58.
33. Singer R.H. The cytoskeleton and mRNA localization. Curr. Opin. Cell. Biol. 4:1992;15-19.
34. Fulton A.B. Spatial organization of the synthesis of cytoskeletal proteins. J. Cell. Biochem. 52:1993;148-152.
35. Bang M.-L., Centner T., Fornoff F., Geach A.J., Gotthardt M., McNabb M., et al. 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. 89:2001;1065-1072.
36. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., et al. Initial sequencing and analysis of the human genome. Nature. 409:2001;860-921.
37. Venter J.C. The sequence of the human genome. Science. 291:2001;1304-1351.
38. Furano A.V., Usdin K. DNA "fossils" and phylogenetic analysis: using L1 (LINE-1, long interspersed repeated) DNA to determine the evolutionary history of mammals. J. Biol. Chem. 270:1995;25301-25304.
39. Moncman C.L., Wang K. Nebulette: a 107 kDa nebulin-like protein in cardiac muscle. Cell Motil. Cytoskeleton. 32:1995;205-225.
40. Luo G., Zhang J.Q., Nguyen T.P., Herrera A.H., Paterson B., 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.
41. Carroll S.L., 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.
42. Furst D.O., Osborn M., Nave R., Weber K. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J. Cell. Biol. 106:1988;1563-1572.
43. Fock U., Hinssen H. Nebulin is a thin filament protein of the cardiac muscle of the agnathans. J. Muscle Res. Cell Motil. 23:2002;205-213.
44. Shimada Y., Komiyama M., Begum S., Maruyama K. Development of connectin/titin and nebulin in striated muscles of chicken. Advan. Biophys. 33:1996;223-234.
45. Robinson T.F., Winegrad S. The measurement and dynamic implications of thin filament lengths in heart muscle. J. Physiol. (London). 286:1979;607-619.
46. Littlefield R., Fowler V.M. Defining actin filament length in striated muscle: rulers and caps or dynamic stability. Annu. Rev.Cell Dev. Biol. 14:1998;487-525.
47. Freiberg A., Trombitas K., Hell W., Cazorla O., Fougerousse F., Centner T., et al. Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ. Res. 86:2000;1114-1121.
48. Trombitas K., Wu Y., Labeit D., Labeit S., Granzier H. Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently. Am. J. Physiol. Heart Circ. Physiol. 281:2001;H1793-H1799.
49. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215:1990;403-410.
50. Schwartz S., Zhang Z., Frazer K.A., Smit A., Riemer C., Bouck J., et al. PipMaker - a web server for aligning two genomic DNA sequences. Genome Res. 10:2000;577-586.
51. Gustafson T.A., Bahl J.J., Markham B.E., Roeske W.R., Morkin E. Hormonal regulation of myosin heavy chain and α-actin gene expression in cultured fetal rat heart myocytes. J. Biol. Chem. 262:1987;13316-13322.
52. Grapin-Botton A., Majithia A.R., Melton D.A. Key events of pancreas formation are triggered in gut endoderm by ectopic expression of pancreatic regulatory genes. Genes Dev. 15:2001;444-454.
53. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36:1991;685-695.
54. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
55. Eilertsen K.J., Keller T.C.S. Identification and characterization of two huge protein components of the brush border cytoskeleton: evidence for a cellular isoform of titin. J. Cell. Biol. 119:1992;549-557.
56. Granzier H.L.M., Wang K. Gel electrophoresis of giant proteins: solubilization and silver-staining of titin and nebulin from single muscle fiber segments. Electrophoresis. 14:1993;56-64.
57. Gregorio C.C., Weber A., Bondad M., Pennise C.R., Fowler V.M. Requirement of pointed end capping by tropomodulin to maintain actin filament length in embryonic chick cardiac myocytes. Nature. 377:1995;83-86.
58. Knight P.J., Trinick J.A. Preparation of myofibrils. Methods Enzymol. 85:1982;9-12.
59. Fowler V.M., Sussmann M.A., Miller P.G., Flucher B.E., Daniels M.P. Tropomodulin is associated with the free (pointed) ends of the thin filaments in rat skeletal muscle. J. Cell. Biol. 120:1993;411-420.
60. Grove B.K., Cerny L., Perriard J.C., Eppenberger H.M. Myomesin and M protein: expression of two M-band proteins in pectoral muscle and heart during development. J. Cell. Biol. 101:1985;1413-1421.