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. 1987 Nov;84(21):7773–7777. doi: 10.1073/pnas.84.21.7773

Spatial segregation of mRNA encoding myelin-specific proteins.

B D Trapp 1, T Moench 1, M Pulley 1, E Barbosa 1, G Tennekoon 1, J Griffin 1
PMCID: PMC299383  PMID: 3478726

Abstract

The cellular and subcellular distributions of mRNAs encoding three myelin-specific proteins--myelin basic protein (MBP), proteolipid protein (PLP), and Po protein--were studied in tissue sections of developing rat nervous systems by in situ hybridization. The developmental appearance of these mRNAs closely paralleled the appearance of the proteins they encode as determined by immunocytochemistry. mRNA encoding the extrinsic membrane protein, MBP, was concentrated around oligodendrocyte and Schwann cell nuclei during initial stages of myelination; as myelination proceeded, MBP mRNA became distributed diffusely over myelinated fibers. In contrast, mRNAs encoding the intrinsic membrane proteins, PLP and Po, remained concentrated around oligodendrocyte (PLP) and Schwann cell (Po) nuclei at all stages of myelination. These results establish that myelinating cells spatially segregate certain myelin-specific mRNAs. The presence of MBP mRNA within the cytoplasmic domains of myelin internodes indicates that protein sorting during myelination involves transportation of mRNA to specific subcellular sites.

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Selected References

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

  1. Benjamins J. A., Iwata R., Hazlett J. Kinetics of entry of proteins into the myelin membrane. J Neurochem. 1978 Oct;31(4):1077–1085. doi: 10.1111/j.1471-4159.1978.tb00150.x. [DOI] [PubMed] [Google Scholar]
  2. Brahic M., Haase A. T. Detection of viral sequences of low reiteration frequency by in situ hybridization. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6125–6129. doi: 10.1073/pnas.75.12.6125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cohen S. R., Guarnieri M. Immunochemical measurement of myelin basic protein in developing rat brain: an index of myelin synthesis. Dev Biol. 1976 Mar;49(1):294–299. doi: 10.1016/0012-1606(76)90276-1. [DOI] [PubMed] [Google Scholar]
  4. Colman D. R., Kreibich G., Frey A. B., Sabatini D. D. Synthesis and incorporation of myelin polypeptides into CNS myelin. J Cell Biol. 1982 Nov;95(2 Pt 1):598–608. doi: 10.1083/jcb.95.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Kristensson K., Holmes K. V., Duchala C. S., Zeller N. K., Lazzarini R. A., Dubois-Dalcq M. Increased levels of myelin basic protein transcripts in virus-induced demyelination. Nature. 1986 Aug 7;322(6079):544–547. doi: 10.1038/322544a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kristensson K., Zeller N. K., Dubois-Dalcq M. E., Lazzarini R. A. Expression of myelin basic protein gene in the developing rat brain as revealed by in situ hybridization. J Histochem Cytochem. 1986 Apr;34(4):467–473. doi: 10.1177/34.4.2419396. [DOI] [PubMed] [Google Scholar]
  7. Lawrence J. B., Singer R. H. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell. 1986 May 9;45(3):407–415. doi: 10.1016/0092-8674(86)90326-0. [DOI] [PubMed] [Google Scholar]
  8. Lemke G., Axel R. Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell. 1985 Mar;40(3):501–508. doi: 10.1016/0092-8674(85)90198-9. [DOI] [PubMed] [Google Scholar]
  9. Lewis S. A., Cowan N. J. Temporal expression of mouse glial fibrillary acidic protein mRNA studied by a rapid in situ hybridization procedure. J Neurochem. 1985 Sep;45(3):913–919. doi: 10.1111/j.1471-4159.1985.tb04080.x. [DOI] [PubMed] [Google Scholar]
  10. Ludwin S. K. The function of perineuronal satellite oligodendrocytes: an immunohistochemical study. Neuropathol Appl Neurobiol. 1984 Mar-Apr;10(2):143–149. doi: 10.1111/j.1365-2990.1984.tb00345.x. [DOI] [PubMed] [Google Scholar]
  11. Ludwin S. K. The perineuronal satellite oligodendrocyte. A role in remyelination. Acta Neuropathol. 1979 Jun 15;47(1):49–53. doi: 10.1007/BF00698272. [DOI] [PubMed] [Google Scholar]
  12. Mentaberry A., Adesnik M., Atchison M., Norgård E. M., Alvarez F., Sabatini D. D., Colman D. R. Small basic proteins of myelin from central and peripheral nervous systems are encoded by the same gene. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1111–1114. doi: 10.1073/pnas.83.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Milner R. J., Lai C., Nave K. A., Lenoir D., Ogata J., Sutcliffe J. G. Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell. 1985 Oct;42(3):931–939. doi: 10.1016/0092-8674(85)90289-2. [DOI] [PubMed] [Google Scholar]
  14. Moench T. R., Gendelman H. E., Clements J. E., Narayan O., Griffin D. E. Efficiency of in situ hybridization as a function of probe size and fixation technique. J Virol Methods. 1985 Jun;11(2):119–130. doi: 10.1016/0166-0934(85)90035-7. [DOI] [PubMed] [Google Scholar]
  15. Naismith A. L., Hoffman-Chudzik E., Tsui L. C., Riordan J. R. Study of the expression of myelin proteolipid protein (lipophilin) using a cloned complementary DNA. Nucleic Acids Res. 1985 Oct 25;13(20):7413–7425. doi: 10.1093/nar/13.20.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rapaport R. N., Benjamins J. A. Kinetics of entry P0 protein into peripheral nerve myelin. J Neurochem. 1981 Jul;37(1):164–171. doi: 10.1111/j.1471-4159.1981.tb05304.x. [DOI] [PubMed] [Google Scholar]
  17. Roach A., Boylan K., Horvath S., Prusiner S. B., Hood L. E. Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell. 1983 Oct;34(3):799–806. doi: 10.1016/0092-8674(83)90536-6. [DOI] [PubMed] [Google Scholar]
  18. Sternberger N. H., Itoyama Y., Kies M. W., Webster H deF Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat C.N.S. J Neurocytol. 1978 Apr;7(2):251–263. doi: 10.1007/BF01217922. [DOI] [PubMed] [Google Scholar]
  19. Sternberger N. H., Itoyama Y., Kies M. W., Webster H. D. Myelin basic protein demonstrated immunocytochemically in oligodendroglia prior to myelin sheath formation. Proc Natl Acad Sci U S A. 1978 May;75(5):2521–2524. doi: 10.1073/pnas.75.5.2521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Trapp B. D., Itoyama Y., MacIntosh T. D., Quarles R. H. P2 protein in oligodendrocytes and myelin of the rabbit central nervous system. J Neurochem. 1983 Jan;40(1):47–54. doi: 10.1111/j.1471-4159.1983.tb12651.x. [DOI] [PubMed] [Google Scholar]
  21. Trapp B. D., McIntyre L. J., Quarles R. H., Sternberger N. H., Webster H. D. Immunocytochemical localization of rat peripheral nervous system myelin proteins: P2 protein is not a component of all peripheral nervous system myelin sheaths. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3552–3556. doi: 10.1073/pnas.76.7.3552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Zeller N. K., Hunkeler M. J., Campagnoni A. T., Sprague J., Lazzarini R. A. Characterization of mouse myelin basic protein messenger RNAs with a myelin basic protein cDNA clone. Proc Natl Acad Sci U S A. 1984 Jan;81(1):18–22. doi: 10.1073/pnas.81.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]

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