Journal of Cell Science, Vol 107, Issue 3 377-386, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Rearrangement of mRNAs for costamere proteins during costamere development in cultured skeletal muscle from chicken

EJ Morris and AB Fulton
Department of Biochemistry, University of Iowa, Iowa City 52242.

Mature skeletal myofibrils are surrounded by costameres, ribs of metavinculin, vinculin, intermediate filaments, and other proteins that connect the myofibril to the extracellular matrix. Costameres have recently been shown to be the sites at which the forces generated by the myofibril are transduced laterally into the extracellular matrix. We observed costameres developing in cultured skeletal muscles, grown in micromass culture from cells taken from embryonic chicken leg. We detected proteins by immunofluorescence and mRNA by in situ hybridization. Antibody and probe signals were imaged by laser scanning confocal microscopy. Antibody to vimentin protein is first detected in stripes in register with the Z line of the myofibril, at approximately day 12 after fusion; soon thereafter probe to vimentin mRNA is also detected in the same stripes. Optical sections indicate that vimentin mRNA and protein are very close, no more than 0.1 mm apart and possibly in immediate contact. Antibody to vimentin is detected in stripes only in cells that twitch spontaneously. Antibodies and probes to desmin and vinculin protein and mRNA are next detected in stripes of the same periodicity, at approximately day 17 after fusion. Vinculin protein (but not mRNA) is detected at focal contacts much earlier in development. Controls for bleed through of fluorescence, RNase H sensitivity, hybridization without probe, and binding to the myofibril all gave appropriate results. Probes to glyceraldehyde-3-phosphate dehydrogenase, a glycolytic enzyme, stained diffusely and did not associate with the myofibril. These results show that components of the costamere arrive at the structure in a defined sequence, and that mRNA organization is a conspicuous, precise and temporally controlled aspect of costamere development. These results may have wider implications. In these cells, some mRNAs are positioned with submicrometer precision in space and differentially over time. Particular mRNAs differ in the time and place of such positioning. This implies both that cellular structures provide physical cues for such positioning and that mRNA contains information that interacts with such cues in a message-specific manner. If such precision in mRNA location is found in other somatic cells, it could have significant implications for the ways in which cells generate and maintain cellular structures.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				M. P. Walker, T.K. Rajendra, L. Saieva, J. L. Fuentes, L. Pellizzoni, and A. G. Matera SMN complex localizes to the sarcomeric Z-disc and is a proteolytic target of calpain Hum. Mol. Genet., November 1, 2008; 17(21): 3399 - 3410. [Abstract] [Full Text] [PDF]

				M.-E. Huot, N. Bisson, L. Davidovic, R. Mazroui, Y. Labelle, T. Moss, and E. W. Khandjian The RNA-binding Protein Fragile X-related 1 Regulates Somite Formation in Xenopus laevis Mol. Biol. Cell, September 1, 2005; 16(9): 4350 - 4361. [Abstract] [Full Text] [PDF]

				M. Nissinen, T. Kaisto, P. Salmela, J. Peltonen, and K. Metsikko Restricted Distribution of mRNAs Encoding a Sarcoplasmic Reticulum or Transverse Tubule Protein in Skeletal Myofibers J. Histochem. Cytochem., February 1, 2005; 53(2): 217 - 227. [Abstract] [Full Text] [PDF]

				D. Willis, K. W. Li, J.-Q. Zheng, J. H. Chang, A. Smit, T. Kelly, T. T. Merianda, J. Sylvester, J. van Minnen, and J. L. Twiss Differential Transport and Local Translation of Cytoskeletal, Injury-Response, and Neurodegeneration Protein mRNAs in Axons J. Neurosci., January 26, 2005; 25(4): 778 - 791. [Abstract] [Full Text] [PDF]

				T. Abe, K. Takano, A. Suzuki, Y. Shimada, M. Inagaki, N. Sato, T. Obinata, and T. Endo Myocyte differentiation generates nuclear invaginations traversed by myofibrils associating with sarcomeric protein mRNAs J. Cell Sci., December 15, 2004; 117(26): 6523 - 6534. [Abstract] [Full Text] [PDF]

				B. Engels, S. van 't Padje, L. Blonden, L.-a. Severijnen, B. A. Oostra, and R. Willemsen Characterization of Fxr1 in Danio rerio; a simple vertebrate model to study costamere development J. Exp. Biol., September 1, 2004; 207(19): 3329 - 3338. [Abstract] [Full Text] [PDF]

				E. J. Mientjes, R. Willemsen, L. L. Kirkpatrick, I. M. Nieuwenhuizen, M. Hoogeveen-Westerveld, M. Verweij, S. Reis, B. Bardoni, A. T. Hoogeveen, B. A. Oostra, et al. Fxr1 knockout mice show a striated muscle phenotype: implications for Fxr1p function in vivo Hum. Mol. Genet., July 1, 2004; 13(13): 1291 - 1302. [Abstract] [Full Text] [PDF]

				B. M. Jockusch, S. Huttelmaier, and S. Illenberger From the Nucleus Toward the Cell Periphery: a Guided Tour for mRNAs Physiology, February 1, 2003; 18(1): 7 - 11. [Abstract] [Full Text] [PDF]

				M. Al-Maghrebi, H. Brule, M. Padkina, C. Allen, W. M. Holmes, and Z. E. Zehner The 3' untranslated region of human vimentin mRNA interacts with protein complexes containing eEF-1{gamma} and HAX-1 Nucleic Acids Res., December 1, 2002; 30(23): 5017 - 5028. [Abstract] [Full Text] [PDF]

				M. Fluck, A. Ziemiecki, R. Billeter, and M. Muntener Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration J. Exp. Biol., August 15, 2002; 205(16): 2337 - 2348. [Abstract] [Full Text] [PDF]

				D. Davy, H. Campbell, S Fountain, D de Jong, and M. Crouch The flightless I protein colocalizes with actin- and microtubule-based structures in motile Swiss 3T3 fibroblasts: evidence for the involvement of PI 3-kinase and Ras-related small GTPases J. Cell Sci., January 2, 2001; 114(3): 549 - 562. [Abstract] [PDF]

				E. Morris, K Evason, C Wiand, T. L'Ecuyer, and A. Fulton Misdirected vimentin messenger RNA alters cell morphology and motility J. Cell Sci., January 7, 2000; 113(13): 2433 - 2443. [Abstract] [PDF]

				J Foucrier, M. Grand, F De Conto, Y Bassaglia, G Geraud, K Scherrer, and I Martelly Dynamic distribution and formation of a para-sarcomeric banding pattern of prosomes during myogenic differentiation of satellite cells in vitro J. Cell Sci., January 4, 1999; 112(7): 989 - 1001. [Abstract] [PDF]

				J. Frenette and J. G. Tidball Mechanical loading regulates expression of talin and its mRNA, which are concentrated at myotendinous junctions Am J Physiol Cell Physiol, September 1, 1998; 275(3): C818 - C825. [Abstract] [Full Text] [PDF]

				P Goldspink, W Sharp, and B Russell Localization of cardiac (alpha)-myosin heavy chain mRNA is regulated by its 3' untranslated region via mechanical activity and translational block J. Cell Sci., January 12, 1997; 110(23): 2969 - 2978. [Abstract] [PDF]

				J. Veyrune, G. Campbell, J Wiseman, J. Blanchard, and J. Hesketh A localisation signal in the 3' untranslated region of c-myc mRNA targets c-myc mRNA and beta-globin reporter sequences to the perinuclear cytoplasm and cytoskeletal-bound polysomes J. Cell Sci., January 6, 1996; 109(6): 1185 - 1194. [Abstract] [PDF]

				S. Huttelmaier, S. Illenberger, I. Grosheva, M. Rudiger, R. H. Singer, and B. M. Jockusch Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins J. Cell Biol., November 26, 2001; 155(5): 775 - 786. [Abstract] [Full Text] [PDF]