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. 2003 Mar;163(3):905–915. doi: 10.1093/genetics/163.3.905

DIM-1, a novel immunoglobulin superfamily protein in Caenorhabditis elegans, is necessary for maintaining bodywall muscle integrity.

Teresa M Rogalski 1, Mary M Gilbert 1, Danelle Devenport 1, Kenneth R Norman 1, Donald G Moerman 1
PMCID: PMC1462474  PMID: 12663531

Abstract

The UNC-112 protein is required during initial muscle assembly in C. elegans to form dense bodies and M-lines. Loss of this protein results in arrest at the twofold stage of embryogenesis. In contrast, a missense mutation in unc-112 results in viable animals that have disorganized bodywall muscle and are paralyzed as adults. Loss or reduction of dim-1 gene function can suppress the severe muscle disruption and paralysis exhibited by these mutant hermaphrodites. The overall muscle structure in hermaphrodites lacking a functional dim-1 gene is slightly disorganized, and the myofilament lattice is not as strongly anchored to the muscle cell membrane as it is in wild-type muscle. The dim-1 gene encodes two polypeptides that contain three Ig-like repeats. The short DIM-1 protein isoform consists entirely of three Ig repeats and is sufficient for wild-type bodywall muscle structure and stability. DIM-1(S) localizes to the region of the muscle cell membrane around and between the dense bodies, which are the structures that anchor the actin filaments and may play a role in stabilizing the thin rather than the thick filament components of the sarcomere.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Ayme-Southgate A., Southgate R., Saide J., Benian G. M., Pardue M. L. Both synchronous and asynchronous muscle isoforms of projectin (the Drosophila bent locus product) contain functional kinase domains. J Cell Biol. 1995 Feb;128(3):393–403. doi: 10.1083/jcb.128.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bang M. L., Mudry R. E., McElhinny A. S., Trombitás K., Geach A. J., Yamasaki R., Sorimachi H., Granzier H., Gregorio C. C., Labeit S. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J Cell Biol. 2001 Apr 16;153(2):413–427. doi: 10.1083/jcb.153.2.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benian G. M., Kiff J. E., Neckelmann N., Moerman D. G., Waterston R. H. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature. 1989 Nov 2;342(6245):45–50. doi: 10.1038/342045a0. [DOI] [PubMed] [Google Scholar]
  5. Benian G. M., L'Hernault S. W., Morris M. E. Additional sequence complexity in the muscle gene, unc-22, and its encoded protein, twitchin, of Caenorhabditis elegans. Genetics. 1993 Aug;134(4):1097–1104. doi: 10.1093/genetics/134.4.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benian G. M., Tinley T. L., Tang X., Borodovsky M. The Caenorhabditis elegans gene unc-89, required fpr muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J Cell Biol. 1996 Mar;132(5):835–848. doi: 10.1083/jcb.132.5.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bini L., Heid H., Liberatori S., Geier G., Pallini V., Zwilling R. Two-dimensional gel electrophoresis of Caenorhabditis elegans homogenates and identification of protein spots by microsequencing. Electrophoresis. 1997 Mar-Apr;18(3-4):557–562. doi: 10.1002/elps.1150180337. [DOI] [PubMed] [Google Scholar]
  8. Burridge K., Chrzanowska-Wodnicka M. Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol. 1996;12:463–518. doi: 10.1146/annurev.cellbio.12.1.463. [DOI] [PubMed] [Google Scholar]
  9. C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998 Dec 11;282(5396):2012–2018. doi: 10.1126/science.282.5396.2012. [DOI] [PubMed] [Google Scholar]
  10. Cassata G., Kagoshima H., Prétôt R. F., Aspöck G., Niklaus G., Bürglin T. R. Rapid expression screening of Caenorhabditis elegans homeobox open reading frames using a two-step polymerase chain reaction promoter-gfp reporter construction technique. Gene. 1998 May 28;212(1):127–135. doi: 10.1016/s0378-1119(98)00137-1. [DOI] [PubMed] [Google Scholar]
  11. Chishti A. H., Kim A. C., Marfatia S. M., Lutchman M., Hanspal M., Jindal H., Liu S. C., Low P. S., Rouleau G. A., Mohandas N. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci. 1998 Aug;23(8):281–282. doi: 10.1016/s0968-0004(98)01237-7. [DOI] [PubMed] [Google Scholar]
  12. Einheber S., Fischman D. A. Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2157–2161. doi: 10.1073/pnas.87.6.2157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Francis G. R., Waterston R. H. Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol. 1985 Oct;101(4):1532–1549. doi: 10.1083/jcb.101.4.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Francis R., Waterston R. H. Muscle cell attachment in Caenorhabditis elegans. J Cell Biol. 1991 Aug;114(3):465–479. doi: 10.1083/jcb.114.3.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fürst D. O., Gautel M. The anatomy of a molecular giant: how the sarcomere cytoskeleton is assembled from immunoglobulin superfamily molecules. J Mol Cell Cardiol. 1995 Apr;27(4):951–959. doi: 10.1016/0022-2828(95)90064-0. [DOI] [PubMed] [Google Scholar]
  16. Gallagher P. J., Herring B. P. The carboxyl terminus of the smooth muscle myosin light chain kinase is expressed as an independent protein, telokin. J Biol Chem. 1991 Dec 15;266(35):23945–23952. [PMC free article] [PubMed] [Google Scholar]
  17. Gettner S. N., Kenyon C., Reichardt L. F. Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol. 1995 May;129(4):1127–1141. doi: 10.1083/jcb.129.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Harpaz Y., Chothia C. Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J Mol Biol. 1994 May 13;238(4):528–539. doi: 10.1006/jmbi.1994.1312. [DOI] [PubMed] [Google Scholar]
  19. Hedgecock E. M., Culotti J. G., Hall D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron. 1990 Jan;4(1):61–85. doi: 10.1016/0896-6273(90)90444-k. [DOI] [PubMed] [Google Scholar]
  20. Hresko M. C., Schriefer L. A., Shrimankar P., Waterston R. H. Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in Caenorhabditis elegans. J Cell Biol. 1999 Aug 9;146(3):659–672. doi: 10.1083/jcb.146.3.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Labeit S., Gautel M., Lakey A., Trinick J. Towards a molecular understanding of titin. EMBO J. 1992 May;11(5):1711–1716. doi: 10.1002/j.1460-2075.1992.tb05222.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Labeit S., Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 1995 Oct 13;270(5234):293–296. doi: 10.1126/science.270.5234.293. [DOI] [PubMed] [Google Scholar]
  23. Lakey A., Labeit S., Gautel M., Ferguson C., Barlow D. P., Leonard K., Bullard B. Kettin, a large modular protein in the Z-disc of insect muscles. EMBO J. 1993 Jul;12(7):2863–2871. doi: 10.1002/j.1460-2075.1993.tb05948.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Letunic Ivica, Goodstadt Leo, Dickens Nicholas J., Doerks Tobias, Schultz Joerg, Mott Richard, Ciccarelli Francesca, Copley Richard R., Ponting Chris P., Bork Peer. Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res. 2002 Jan 1;30(1):242–244. doi: 10.1093/nar/30.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moerman D. G., Baillie D. L. Formaldehyde mutagenesis in the nematode Caenorhabditis elegans. Mutat Res. 1981 Feb;80(2):273–279. doi: 10.1016/0027-5107(81)90100-7. [DOI] [PubMed] [Google Scholar]
  26. Moerman D. G., Benian G. M., Barstead R. J., Schriefer L. A., Waterston R. H. Identification and intracellular localization of the unc-22 gene product of Caenorhabditis elegans. Genes Dev. 1988 Jan;2(1):93–105. doi: 10.1101/gad.2.1.93. [DOI] [PubMed] [Google Scholar]
  27. Moerman D. G., Plurad S., Waterston R. H., Baillie D. L. Mutations in the unc-54 myosin heavy chain gene of Caenorhabditis elegans that alter contractility but not muscle structure. Cell. 1982 Jul;29(3):773–781. doi: 10.1016/0092-8674(82)90439-1. [DOI] [PubMed] [Google Scholar]
  28. Mullen G. P., Rogalski T. M., Bush J. A., Gorji P. R., Moerman D. G. Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol Biol Cell. 1999 Oct;10(10):3205–3221. doi: 10.1091/mbc.10.10.3205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Obermann W. M., Gautel M., Weber K., Fürst D. O. 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. 1997 Jan 15;16(2):211–220. doi: 10.1093/emboj/16.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Okagaki T., Weber F. E., Fischman D. A., Vaughan K. T., Mikawa T., Reinach F. C. The major myosin-binding domain of skeletal muscle MyBP-C (C protein) resides in the COOH-terminal, immunoglobulin C2 motif. J Cell Biol. 1993 Nov;123(3):619–626. doi: 10.1083/jcb.123.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Parast M. M., Otey C. A. Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J Cell Biol. 2000 Aug 7;150(3):643–656. doi: 10.1083/jcb.150.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Price M. G., Gomer R. H. Skelemin, a cytoskeletal M-disc periphery protein, contains motifs of adhesion/recognition and intermediate filament proteins. J Biol Chem. 1993 Oct 15;268(29):21800–21810. [PubMed] [Google Scholar]
  33. Reddy K. B., Gascard P., Price M. G., Negrescu E. V., Fox J. E. Identification of an interaction between the m-band protein skelemin and beta-integrin subunits. Colocalization of a skelemin-like protein with beta1- and beta3-integrins in non-muscle cells. J Biol Chem. 1998 Dec 25;273(52):35039–35047. doi: 10.1074/jbc.273.52.35039. [DOI] [PubMed] [Google Scholar]
  34. Rhind N. R., Miller L. M., Kopczynski J. B., Meyer B. J. xol-1 acts as an early switch in the C. elegans male/hermaphrodite decision. Cell. 1995 Jan 13;80(1):71–82. doi: 10.1016/0092-8674(95)90452-2. [DOI] [PubMed] [Google Scholar]
  35. Rogalski T. M., Mullen G. P., Gilbert M. M., Williams B. D., Moerman D. G. The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol. 2000 Jul 10;150(1):253–264. doi: 10.1083/jcb.150.1.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rogalski T. M., Williams B. D., Mullen G. P., Moerman D. G. Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev. 1993 Aug;7(8):1471–1484. doi: 10.1101/gad.7.8.1471. [DOI] [PubMed] [Google Scholar]
  37. Salmikangas P., Mykkänen O. M., Grönholm M., Heiska L., Kere J., Carpén O. Myotilin, a novel sarcomeric protein with two Ig-like domains, is encoded by a candidate gene for limb-girdle muscular dystrophy. Hum Mol Genet. 1999 Jul;8(7):1329–1336. doi: 10.1093/hmg/8.7.1329. [DOI] [PubMed] [Google Scholar]
  38. Shirinsky V. P., Vorotnikov A. V., Birukov K. G., Nanaev A. K., Collinge M., Lukas T. J., Sellers J. R., Watterson D. M. A kinase-related protein stabilizes unphosphorylated smooth muscle myosin minifilaments in the presence of ATP. J Biol Chem. 1993 Aug 5;268(22):16578–16583. [PubMed] [Google Scholar]
  39. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  40. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wick M., Bürger C., Brüsselbach S., Lucibello F. C., Müller R. Identification of serum-inducible genes: different patterns of gene regulation during G0-->S and G1-->S progression. J Cell Sci. 1994 Jan;107(Pt 1):227–239. doi: 10.1242/jcs.107.1.227. [DOI] [PubMed] [Google Scholar]
  42. Williams B. D., Waterston R. H. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol. 1994 Feb;124(4):475–490. doi: 10.1083/jcb.124.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yandell M. D., Edgar L. G., Wood W. B. Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1381–1385. doi: 10.1073/pnas.91.4.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]

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