Advertisement

Journal of Molecular Neuroscience

, Volume 4, Issue 4, pp 215–223 | Cite as

The structural complexities of the myelin basic protein gene from mouse are also present in shark

  • Raul A. Saavedra
  • Adam Lipson
  • K. Sean Kimbro
  • Cecilia Ljubetic
Article

Abstract

The Golli-mbp gene complex contains two overlapping transcription units with two distinct promoters, of which the downstream (myelin basic protein [mbp]) promoter is more frequently used. A previous comparison of the downstream promoter sequences from shark and mouse allowed the identification of two DNA sequences called the boxes I and II and the wobble zone. The boxes I and II sequence is a compositecis-acting motif that is thought to be involved in the regulation of the downstream promoter. It contains sequences similar to T-antigen, MyoD/E2A, and glucocorticoid receptor-binding sites. The wobble zone codes for an exon (5a in the nomenclature of Campagnoni et al., 1993) that is included in messenger RNAs transcribed from the upstream promoter. The polypeptides encoded by this exon from shark and mouse are 86 and 84 amino acids long, respectively. These polypeptides are overall 59% identical and include a region (residues 41–75 in shark and 39–73 in mouse) that is 89% identical between the two species. A primary sequence analysis showed that each of these polypeptides contains anN-glycosylation site, phosphorylation sites for Ca2+/calmodulin-dependent protein kinase, protein kinase C and casein kinase II, and partial ATP- and GTP-binding sites. The shark polypeptide also contains a phosphorylation site for proline-directed protein kinase. These observations are consistent with the notion that the intricate structure and regulation of the Golli-mbp gene complex arose during vertebrate evolution within a common ancestor to sharks and mammals.

Index Entries

Myelin basic protein promoter wobble zone overlapping transcription units gene expression evolution 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aruga J., Okano H., and Mikoshiba K. (1991) Identification of the new isoform of mouse myelin basic protein: the existence of exon 5a.J. Neurochem. 56, 1222–1226.PubMedCrossRefGoogle Scholar
  2. Blackwell T. K. and Weintraub H. (1990) Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection.Science 250, 1104–1110.PubMedCrossRefGoogle Scholar
  3. Boylan K. B., Ayres T. M., Popko B., Takahashi N., Hood L. E., and Prusiner S. B. (1990) Repetitive DNA (TGGA)n 5′ to the human myelin basic protein gene: a new form of oligonucleotide repetitive sequence showing length polymorphism.Genomics 6, 16–22.PubMedCrossRefGoogle Scholar
  4. Campagnoni A. T., Pribyl T. M., Campagnoni C. W., Kampf K., Amur-Umarjee S., Landry C. F., Handley V. W., Newman S. L., Garbay B., and Kitamura K. (1993) Structure and developmental regulation of Golli-mbp, a 105 Kb gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain.J. Biol. Chem. 268, 4930–4938.PubMedGoogle Scholar
  5. Cawthon R. M., Weiss R., Xu G., Viskochil D., Culver M., Stevens J., Robertson M., Dunn D., Gesteland R., O’Connell P., and White R. (1990) A major segment of the neurofibromatosis type 1 gene: cDNA sequence, genomic structure, and point mutations.Cell 62, 193–201.PubMedCrossRefGoogle Scholar
  6. Chan C. K., Ramwani J., and Moscarello M. A. (1988) Myelin basic protein binds GTP at a single site in the N-terminus.Biochem. Biophys. Res. Comm. 152, 1468–1473.PubMedCrossRefGoogle Scholar
  7. DeLucia A. L., Lewton B. A., Tjian R., and Tegtmeyer P. (1983) Topography of simian virus 40 A protein-DNA complexes: arrangement of pentanucleotide interaction sites at the origin of replication.J. Virol. 46, 143–150.PubMedGoogle Scholar
  8. DeVellis J. (1990) Developmental and hormonal regulation of gene expression in oligodendrocytes. Myelination and dysmyelination.Ann. NY Acad. Sci. 605, 81–89.CrossRefGoogle Scholar
  9. Devine-Beach K., Lashgari M. S., and Khalili K. (1990) Myelin basic protein gene transcription: identification of proximal and distal cis-acting regulatory elements.J. Biol. Chem. 265, 13,830–13,835.Google Scholar
  10. Dorai T. and Wang L. H. (1990) An alternative non-tyrosine protein kinase product of the c-sarc gene in chicken skeletal muscle.Mol. Cell. Biol. 12, 2359–2371.Google Scholar
  11. Dynan W. S. (1989) Modularity in promoters and enhancers.Cell 58, 1–4.PubMedCrossRefGoogle Scholar
  12. Fors L., Saavedra R. A., and Hood L. (1990) Cloning of the shark P0 promoter using a genomic walking technique based on the polymerase chain reaction.Nucleic Acids Res. 18, 2793–2799.PubMedCrossRefGoogle Scholar
  13. Fors L., Hood L., and Saavedra R. A. (1993) Sequence similarities of myelin basic protein promoters from mouse and shark: implications for the control of gene expression in myelinating cells.J. Neurochem. 60, 513–521.PubMedCrossRefGoogle Scholar
  14. Grima B., Zelenika D., and Pessac B. (1992) A novel transcript overlapping the myelin basic protein gene.J. Neurochem. 59, 2318–2323.PubMedCrossRefGoogle Scholar
  15. Inouye H. and Kirschner D. A. (1991) Folding and function of the myelin proteins from primary sequence data.J. Neurosci. Res. 28, 1–17.PubMedCrossRefGoogle Scholar
  16. Katsuki M., Sato M., Kimura M., Yokoyama M., Koloyoshi K., and Nomura T. (1988) Conversion of normal behaviour to shiverer by myelin basic protein antisense cDNA in transgenic mice.Science 241, 593–595.PubMedCrossRefGoogle Scholar
  17. Kitamura K., Newman S. L., Campagnoni C. W., Verdi J. M., Mohandas T., Handley V. W., and Campagnoni A. T. (1990) Expression of a novel transcript of the myelin basic protein gene.J. Neurochem. 54, 2032–2041.PubMedCrossRefGoogle Scholar
  18. Kumar S. and DeVellis J. (1989) Glucocorticoid mediated function in glial cells, inGlial Cell Receptors (Kimelberg, H. K., ed.), Raven, New York, pp. 243–263.Google Scholar
  19. Mathisen P. M., Pease S., Garvey J., Hood L., and Readhead C. (1993) Identification of a novel embryonic isoform of myelin basic protein that is expressed widely in the mouse embryo.Proc. Natl. Acad. Sci. USA 90, 10,125–10,129.CrossRefGoogle Scholar
  20. Milne T. J., Atkins A. R., Warren J. A., Auton W. P., and Smith R. (1990) Shark myelin basic protein: amino acid sequence secondary structure, and self-association.J. Neurochem. 55, 950–955.PubMedCrossRefGoogle Scholar
  21. Miura M., Tamura T., Aoyama A., and Mikoshiba K. (1989) The promoter elements of the mouse myelin basic protein gene function efficiently in NG108-15 neuronal/glial cells.Gene 75, 31–38.PubMedCrossRefGoogle Scholar
  22. Ohmstede C. A., Bland M. M., Merrill B. M., and Sahyoun N. (1991) Relationship of genes encoding Ca2+/calmodulin dependent protein kinase Gr and calspermin: a gene within a gene.Proc. Natl. Acad. Sci. USA 88, 5784–5788.PubMedCrossRefGoogle Scholar
  23. Popko B., Puckett C., and Hood L. (1988) A novel mutation in myelin-deficient mice results in unstable myelin basic protein gene transcripts.Neuron 1, 221–225.PubMedCrossRefGoogle Scholar
  24. Readhead C., Popko B., Takahashi N., Shine H. D., Saavedra R. A., Sidman R. L., and Hood L. (1987) Expression of myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype.Cell 48, 703–712.PubMedCrossRefGoogle Scholar
  25. Romer A. (1970)The Vertebrate Body. 4th Ed. Saunders, Philadelphia.Google Scholar
  26. Saavedra R. A., Fors L., Aebersold R. A., Arden B., Horvath S., Sanders J., and Hood L. (1989) The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system.J. Mol. Evol. 29, 149–156.PubMedCrossRefGoogle Scholar
  27. Spivack W. D., Zhong N., Salerno S., Saavedra R. A., and Gould R. M. (1993) Molecular cloning of the myelin basic proteins in the shark Squalus achanthias and the ray Raja erinacia.J. Neurosci. Res. 35, 577–584.PubMedCrossRefGoogle Scholar
  28. Takahashi N., Roach A., Teplow D. B., Prusiner S. B., and Hood L. (1985) Cloning and characterization of the myelin basic protein gene from mouse: one gene can encode both 14 kd and 18.5 kd MBPs by alternative usage of exons.Cell 42, 139–148.PubMedCrossRefGoogle Scholar
  29. Waehneldt T. V. (1990) Phylogeny of myelin proteins. Myelination and dysmyelination.Ann. NY Acad. Sci. 605, 15–28.PubMedCrossRefGoogle Scholar
  30. Waehneldt T. V., Matthieu J.-M., and Jeserich G. (1986) Appearance of myelin proteins during vertebrate evolution.Neurochem. Int. 9, 463–474.CrossRefPubMedGoogle Scholar
  31. Zelenika D., Grima B., and Pessac B. (1993) A new family of transcripts of the myelin basic protein gene: expression in brain and immune system.J. Neurochem. 60, 1574–1577.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc 1994

Authors and Affiliations

  • Raul A. Saavedra
    • 1
    • 2
  • Adam Lipson
    • 2
  • K. Sean Kimbro
    • 1
    • 2
  • Cecilia Ljubetic
    • 2
  1. 1.Department of Orthopedic SurgeryHarvard Medical SchoolBoston
  2. 2.Laboratory for the Study of Skeletal Disorders and RehabilitationThe Children’s Hospital, Enders Pediatric Research CenterBoston

Personalised recommendations