Abstract
During evolution, both the architecture and the cellular physiology of muscles have been remarkably maintained. Striated muscles of invertebrates, although less complex, strongly resemble vertebrate skeletal muscles. In particular, the basic contractile unit called the sarcomere is almost identical between vertebrates and invertebrates. In vertebrate muscles, sarcomeric actin filaments are anchored to attachment points called Z-disks, which are linked to the extra-cellular matrix (ECM) by a muscle specific focal adhesion site called the costamere. In this review, we focus on the dense body of the animal model Caenorhabditis elegans. The C. elegans dense body is a structure that performs two in one roles at the same time, that of the Z-disk and of the costamere. The dense body is anchored in the muscle membrane and provides rigidity to the muscle by mechanically linking actin filaments to the ECM. In the last few years, it has become increasingly evident that, in addition to its structural role, the dense body also performs a signaling function in muscle cells. In this paper, we review recent advances in the understanding of the C. elegans dense body composition and function.
Similar content being viewed by others
References
Barstead RJ, Kleiman L, Waterston RH (1991) Cloning, sequencing, and mapping of an alpha-actinin gene from the nematode Caenorhabditis elegans. Cell Motil Cytoskeleton 20:69–78
Barstead RJ, Waterston RH (1989) The basal component of the nematode dense-body is vinculin. J Biol Chem 264:10177–10185
Barstead RJ, Waterston RH (1991) Vinculin is essential for muscle function in the nematode. J Cell Biol 114:715–724
Barsukov IL, Prescot A, Bate N, Patel B, Floyd DN, Bhanji N, Bagshaw CR, Letinic K, Di Paolo G, De Camilli P, Roberts GC, Critchley DR (2003) Phosphatidylinositol phosphate kinase type 1gamma and beta1-integrin cytoplasmic domain bind to the same region in the talin FERM domain. J Biol Chem 278:31202–31209
Broday L, Kolotuev I, Didier C, Bhoumik A, Podbilewicz B, Ronai Z (2004) The LIM domain protein UNC-95 is required for the assembly of muscle attachment structures and is regulated by the RING finger protein RNF-5 in C. elegans. J Cell Biol 165:857–867
C . elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology (1998) Science 282:2012–2018
Calderwood DA, Yan B, de Pereda JM, Alvarez BG, Fujioka Y, Liddington RC, Ginsberg MH (2002) The phosphotyrosine binding-like domain of talin activates integrins. J Biol Chem 277:21749–21758
Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH (1999) The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274:28071–28074
Chen HC, Appeddu PA, Parsons JT, Hildebrand JD, Schaller MD, Guan JL. (1995) Interaction of focal adhesion kinase with cytoskeletal protein talin. J Biol Chem 270:16995–16999
Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M, Jindal H, Liu SC, Low PS, Rouleau GA, Mohandas N, Chasis JA, Conboy JG, Gascard P, Takakuwa Y, Huang SC, Benz EJ Jr, Bretscher A, Fehon RG, Gusella JF, Ramesh V, Solomon F, Marchesi VT, Tsukita S, Tsukita S, Hoover KB, et al (1998) The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23:281–282
Cox EA, Hardin J (2004) Sticky worms: adhesion complexes in C. elegans. J Cell Sci 117:1885–1897
Cram EJ, Clark SG, Schwarzbauer JE. (2003) Talin loss-of-function uncovers roles in cell contractility and migration in C elegans. J Cell Sci 116:3871–3878
Crawford AW, Beckerle MC (1991) Purification and characterization of zyxin, an 82,000-dalton component of adherens junctions. J Biol Chem 266:5847–5853
Crawford AW, Michelsen JW, Beckerle MC (1992) An interaction between zyxin and alpha-actinin. J Cell Biol 116:1381–1393
Delcommenne M, Tan C, Gray V, Rue L, Woodgett J, Dedhar S (1998) Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc Natl Acad Sci USA 95:11211–11216
Didier C, Broday L, Bhoumik A, Israeli S, Takahashi S, Nakayama K, Thomas SM, Turner CE, Henderson S, Sabe H, Ronai Z (2003) RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol Cell Biol 23:5331–5345
Ervasti JM (2003) Costameres: the Achilles’ heel of Herculean muscle. J Biol Chem 278:13591–13594
Flaherty DB, Gernert KM, Shmeleva N, Tang X, Mercer KB, Borodovsky M, Benian GM (2002) Titins in C.elegans with unusual features: coiled-coil domains, novel regulation of kinase activity and two new possible elastic regions. J Mol Biol 323:533–549
Francis GR, Waterston RH (1985) Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol 101:1532–1549
Gettner SN, Kenyon C, Reichardt LF (1995) Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol 129:1127–1141
Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, G. Radeva J. Filmus, Bell JC, Dedhar S (1996) Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379:91–96
Hikita T, Qadota H, Tsuboi D, Taya S, Moerman DG, Kaibuchi K. (2005) Identification of a novel Cdc42 GEF that is localized to the PAT-3-mediated adhesive structure. Biochem Biophys Res Commun 335:139–145
Hobert O, Moerman DG, Clark KA, Beckerle MC, Ruvkun G (1999) A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in Caenorhabditis elegans. J Cell Biol 144:45–57
Hobert O, Schilling JW, Beckerle MC, Ullrich A, Jallal B (1996) SH3 domain-dependent interaction of the proto-oncogene product Vav with the focal contact protein zyxin. Oncogene 12:1577–1581
Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K (1986) Interaction of plasma membrane fibronectin receptor with talin-a transmembrane linkage. Nature 320:531–533
Hresko MC, Williams BD, Waterston RH (1994) Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 124:491–506
Hynes R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687
Kadrmas JL, Beckerle MC (2004) The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5:920–931
Krause M (1995) MyoD and myogenesis in C. elegans. Bioessays 17:219–228
Labouesse M, Georges-Labouesse E (2003) Cell adhesion: parallels between vertebrate and invertebrate focal adhesions. Curr Biol 13:R528–R530
Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E, Kristensen J, Brandmeier B, Franzen G, Hedberg B, Gunnarsson LG, Hughes SM, Marchand S, Sejersen T, Richard I, Edstrom L, Ehler E, Udd B, Gautel M (2005) The kinase domain of titin controls muscle gene expression and protein turnover. Science 308:1599–1603
Lee M, Cram EJ, Shen B, Schwarzbauer JE (2001) Roles for beta(pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads. J Biol Chem 276:36404–36410
Lin X, Qadota H, Moerman DG, Williams BD (2003) C elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr Biol 13:922–932
Mackenzie JM Jr, Epstein HF (1980) Paramyosin is necessary for determination of nematode thick filament length in vivo. Cell 22:747–755
Mackenzie JM Jr, Garcea RL, Zengel JM, Epstein HF (1978) Muscle development in Caenorhabditis elegans: mutants exhibiting retarded sarcomere construction. Cell 15:751–762
Mackinnon AC, Qadota H, Norman KR, Moerman DG, Williams BD (2002) C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 12:787–797
McKeown CR, Han HF, Beckerle MC 2006. Molecular characterization of the Caenorhabditis elegans ALP/Enigma gene alp-1. Dev Dyn 235:530–538
Mercer KB, Flaherty DB, Miller RK, Qadota H, Tinley TL, Moerman DG, Benian GM (2003) Caenorhabditis elegans UNC-98, a C2H2 Zn finger protein, is a novel partner of UNC-97/PINCH in muscle adhesion complexes. Mol Biol Cell 14:2492–2507
Moerman DG, Fire A (1997) C. elegans II. Cold Spring Harbor Press, Cold Spring Harbor pp 417–470
Moerman DG, Williams BD (2006) Sarcomere assembly in C. elegans muscle (January 16, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.81.1, http://www.wormbook.org
Moulder GL, Huang MM, Waterston RH, Barstead RJ (1996) Talin requires beta-integrin, but not vinculin, for its assembly into focal adhesion-like structures in the nematode Caenorhabditis elegans. Mol Biol Cell 7:1181–1193
Nix DA, Beckerle MC (1997) Nuclear-cytoplasmic shuttling of the focal contact protein, zyxin: a potential mechanism for communication between sites of cell adhesion and the nucleus. J Cell Biol 138:1139–1147
Pashmforoush M, Pomies P, Peterson KL, Kubalak S, Ross J Jr, Hefti A, Aebi U, Beckerle MC, Chien KR (2001) Adult mice deficient in actinin-associated LIM-domain protein reveal a developmental pathway for right ventricular cardiomyopathy. Nat Med 7:591–597
Price LS, Leng J, Schwartz MA, Bokoch GM (1998) Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell 9:1863–1871
Pyle WG, Solaro RJ (2004) At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res 94:296–305
Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. Embo J 18:578–585
Rogalski TM, Mullen GP, Gilbert MM, Williams BD, Moerman DG (2000). 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 150:253–264
Samarel AM (2005) Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 289:H2291–H2301
Schmeichel KL, Beckerle MC (1994) The LIM domain is a modular protein-binding interface. Cell 79:211–219
Schmeichel KL, Beckerle MC (1997) Molecular dissection of a LIM domain. Mol Biol Cell 8:219–230
Smith P, Leung-Chiu WM, Montgomery R, Orsborn A, Kuznicki K, Gressman-Coberly E, Mutapcic L, Bennett K (2002) The GLH proteins, Caenorhabditis elegans P granule components, associate with CSN-5 and KGB-1, proteins necessary for fertility, and with ZYX-1, a predicted cytoskeletal protein. Dev Biol 251:333–347
Vatta M, Mohapatra B, Jimenez S, Sanchez X, Faulkner G, Perles Z, Sinagra G, Lin JH, Vu TM, Zhou Q, Bowles KR, Di Lenarda A, Schimmenti L, Fox M, Chrisco MA, Murphy RT, McKenna W, Elliott P, Bowles NE, Chen J, Valle G, Towbin JA (2003) Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 42:2014–2027
Wang Y, Gilmore TD (2003) Zyxin and paxillin proteins: focal adhesion plaque LIM domain proteins go nuclear. Biochim Biophys Acta 1593:115–120
Wick M, Burger C, Brusselbach S, Lucibello FC, Muller R (1994) A novel member of human tissue inhibitor of metalloproteinases (TIMP) gene family is regulated during G1 progression, mitogenic stimulation, differentiation, and senescence. J Biol Chem 269:18953–18960
Williams BD, Waterston RH (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475–490
Woods AJ, Roberts MS, Choudhary J, Barry ST, Mazaki Y, Sabe H, Morley SJ, Critchley DR, Norman JC (2002) Paxillin associates with poly(A)-binding protein 1 at the dense endoplasmic reticulum and the leading edge of migrating cells. J Biol Chem 277:6428–6437
Wu C, Dedhar S (2001) Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 155:505–510
Zengel JM, Epstein HF (1980) Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans. Cell Motil 1:73–97
Zhang Y, Chen K, Guo L, Wu C (2002) Characterization of PINCH-2, a new focal adhesion protein that regulates the PINCH-1-ILK interaction, cell spreading, and migration. J Biol Chem 277:38328–38338
Zhou Q, Chu PH, Huang C, Cheng CF, Martone ME, Knoll G, Shelton GD, Evans S, Chen J (2001) Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J Cell Biol 155:605–612
Acknowledgments
The authors thank John C. Sparrow, Renaud Legouis and Joëlle Thomas for critical reading this manuscript and Yannick Schwab for technical assistance concerning electron microscopy.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lecroisey, C., Ségalat, L. & Gieseler, K. The C. elegans dense body: anchoring and signaling structure of the muscle. J Muscle Res Cell Motil 28, 79–87 (2007). https://doi.org/10.1007/s10974-007-9104-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10974-007-9104-y