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. 1985 Aug 1;101(2):630–638. doi: 10.1083/jcb.101.2.630

The Golgi apparatus remains associated with microtubule organizing centers during myogenesis

PMCID: PMC2113672  PMID: 3894380

Abstract

In vitro myogenesis involves a dramatic reorganization of the microtubular network, characterized principally by the relocalization of microtubule nucleating sites at the surface of the nuclei in myotubes, in marked contrast with the classical pericentriolar localization observed in myoblasts (Tassin, A. M., B. Maro, and M. Bornens, 1985, J. Cell Biol., 100:35-46). Since a spatial relationship between the Golgi apparatus and the centrosome is observed in most animal cells, we have decided to follow the fate of the Golgi apparatus during myogenesis by an immunocytochemical approach, using wheat germ agglutinin and an affinity-purified anti-galactosyltransferase. We show that Golgi apparatus in myotubes displays a perinuclear distribution which is strikingly different from the polarized juxtanuclear organization observed in myoblasts. As a result, the Golgi apparatus in myotubes is situated close to the microtubule organizing center (MTOC), the cis-side being situated at a fixed distance from the nuclear envelope, a situation which suggests the existence of a structural association between the Golgi apparatus and the nuclear periphery. This is supported by experiments of microtubule depolymerization by nocodazole, in which a minimal effect was observed on Golgi apparatus localization in myotubes in contrast with the dramatic scattering observed in myoblasts. In both cell types, electron microscopy reveals that microtubule disruption generates individual dictyosomes; this suggests that the connecting structures between dictyosomes are principally affected. This structural dependency of the Golgi apparatus upon microtubules is not apparently accompanied by a reverse dependency of MTOC structure or function upon Golgi apparatus activity. Golgi apparatus modification by monensin, as effective in myotubes as in myoblasts, is without apparent effect on MTOC localization or activity and on microtubule stability. The main result of our study is to show that in a cell type where the MTOC is dissociated from centrioles and where antero-posterior polarity has disappeared, the association between the Golgi apparatus and the MTOC is maintained. The significance of such a tight association is discussed.

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Selected References

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  1. Berger E. G., Mandel T., Schilt U. Immunohistochemical localization of galactosyltransferase in human fibroblasts and HeLa cells. J Histochem Cytochem. 1981 Mar;29(3):364–370. doi: 10.1177/29.3.6787115. [DOI] [PubMed] [Google Scholar]
  2. Busson-Mabillot S., Chambaut-Guérin A. M., Ovtracht L., Muller P., Rossignol B. Microtubules and protein secretion in rat lacrimal glands: localization of short-term effects of colchicine on the secretory process. J Cell Biol. 1982 Oct;95(1):105–117. doi: 10.1083/jcb.95.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Collot M., Louvard D., Singer S. J. Lysosomes are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci U S A. 1984 Feb;81(3):788–792. doi: 10.1073/pnas.81.3.788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Couchman J. R., Rees D. A. Organelle-cytoskeleton relationships in fibroblasts: mitochondria, Golgi apparatus, and endoplasmic reticulum in phases of movement and growth. Eur J Cell Biol. 1982 Apr;27(1):47–54. [PubMed] [Google Scholar]
  5. De Brabander M. J., Van de Veire R. M., Aerts F. E., Borgers M., Janssen P. A. The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro. Cancer Res. 1976 Mar;36(3):905–916. [PubMed] [Google Scholar]
  6. Geiger B., Rosen D., Berke G. Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J Cell Biol. 1982 Oct;95(1):137–143. doi: 10.1083/jcb.95.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  8. Kupfer A., Dennert G., Singer S. J. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7224–7228. doi: 10.1073/pnas.80.23.7224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kupfer A., Louvard D., Singer S. J. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2603–2607. doi: 10.1073/pnas.79.8.2603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Käriäinen L., Hashimoto K., Saraste J., Virtanen I., Penttinen K. Monensin and FCCP inhibit the intracellular transport of alphavirus membrane glycoproteins. J Cell Biol. 1980 Dec;87(3 Pt 1):783–791. doi: 10.1083/jcb.87.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Maro B., Bornens M. Reorganization of HeLa cell cytoskeleton induced by an uncoupler of oxidative phosphorylation. Nature. 1982 Jan 28;295(5847):334–336. doi: 10.1038/295334a0. [DOI] [PubMed] [Google Scholar]
  12. Maro B., Marty M. C., Bornens M. In vivo and in vitro effects of the mitochondrial uncoupler FCCP on microtubules. EMBO J. 1982;1(11):1347–1352. doi: 10.1002/j.1460-2075.1982.tb01321.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Maunoury M. R. Localisation immunocytochimique de la centrosphère de cellules tumorales humaines par utilisation d'anticorps naturels de lapin. C R Acad Sci Hebd Seances Acad Sci D. 1978 Feb 13;286(6):503–506. [PubMed] [Google Scholar]
  14. Pastan I. H., Willingham M. C. Journey to the center of the cell: role of the receptosome. Science. 1981 Oct 30;214(4520):504–509. doi: 10.1126/science.6170111. [DOI] [PubMed] [Google Scholar]
  15. Pfeffer S. R., Drubin D. G., Kelly R. B. Identification of three coated vesicle components as alpha- and beta-tubulin linked to a phosphorylated 50,000-dalton polypeptide. J Cell Biol. 1983 Jul;97(1):40–47. doi: 10.1083/jcb.97.1.40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. ROBBINS E., GONATAS N. K. HISTOCHEMICAL AND ULTRASTRUCTURAL STUDIES ON HELA CELL CULTURES EXPOSED TO SPINDLE INHIBITORS WITH SPECIAL REFERENCE TO THE INTERPHASE CELL. J Histochem Cytochem. 1964 Sep;12:704–711. doi: 10.1177/12.9.704. [DOI] [PubMed] [Google Scholar]
  17. Rogalski A. A., Singer S. J. Associations of elements of the Golgi apparatus with microtubules. J Cell Biol. 1984 Sep;99(3):1092–1100. doi: 10.1083/jcb.99.3.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Roth J., Berger E. G. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae. J Cell Biol. 1982 Apr;93(1):223–229. doi: 10.1083/jcb.93.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rothman J. E., Miller R. L., Urbani L. J. Intercompartmental transport in the Golgi complex is a dissociative process: facile transfer of membrane protein between two Golgi populations. J Cell Biol. 1984 Jul;99(1 Pt 1):260–271. doi: 10.1083/jcb.99.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rothman J. E., Urbani L. J., Brands R. Transport of protein between cytoplasmic membranes of fused cells: correspondence to processes reconstituted in a cell-free system. J Cell Biol. 1984 Jul;99(1 Pt 1):248–259. doi: 10.1083/jcb.99.1.248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tartakoff A. M., Vassalli P. Lectin-binding sites as markers of Golgi subcompartments: proximal-to-distal maturation of oligosaccharides. J Cell Biol. 1983 Oct;97(4):1243–1248. doi: 10.1083/jcb.97.4.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tartakoff A. M., Vassalli P. Plasma cell immunoglobulin secretion: arrest is accompanied by alterations of the golgi complex. J Exp Med. 1977 Nov 1;146(5):1332–1345. doi: 10.1084/jem.146.5.1332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wehland J., Henkart M., Klausner R., Sandoval I. V. Role of microtubules in the distribution of the Golgi apparatus: effect of taxol and microinjected anti-alpha-tubulin antibodies. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4286–4290. doi: 10.1073/pnas.80.14.4286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wehland J., Sandoval I. V. Cells injected with guanosine 5'-[alpha, beta-methylene]triphosphate, an alpha, beta-nonhydrolyzable analog of GTP, show anomalous patterns of tubulin polymerization affecting cell translocation, intracellular movement, and the organization of Golgi elements. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1938–1941. doi: 10.1073/pnas.80.7.1938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wehland J., Willingham M. C. A rat monoclonal antibody reacting specifically with the tyrosylated form of alpha-tubulin. II. Effects on cell movement, organization of microtubules, and intermediate filaments, and arrangement of Golgi elements. J Cell Biol. 1983 Nov;97(5 Pt 1):1476–1490. doi: 10.1083/jcb.97.5.1476. [DOI] [PMC free article] [PubMed] [Google Scholar]

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