Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T19:41:45.593Z Has data issue: false hasContentIssue false
  • English
  • Français

The myelin proteolipid DMalpha in fishes

Published online by Cambridge University Press:  10 June 2009

Christian Brösamle
Christian Brösamle*
Affiliation:
Institute of Biochemistry, Ludwig-Maximilians Universität München, Germany
*
Correspondence should be addressed to: Christian Brösamle, Institute of Biochemistry, Ludwig-Maximilians, Universität München Schillerstr, 44 80336 München Germany phone: +49 89 2180 75451 fax: +49 89 2180 75415 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Vertebrate myelin membranes are compacted and held in close apposition by three structural proteins of myelin, myelin basic protein, myelin protein zero (MPZ) and myelin proteolipid protein (PLP1/DMalpha). PLP1/DMalpha is considered to function as a scaffolding protein and play a role in intracellular trafficking in oligodendrocytes. In humans, point mutations, duplications or deletions of PLP1 are associated with Pelizaeus–Merzbacher disease and spastic paraplegia Type 2. PLP1 is highly conserved between mammals, but less so in lower vertebrates. This has led some researchers to question whether certain fish species express PLP1 orthologues at all, and to suggest that the function of PLP1/DMalpha in the central nervous system (CNS) may have been taken over by MPZ. Here, we review the evidence for the conservation of orthologues of PLP1/DMalpha in actinopterygian fishes and provide a comparison of currently available sequence data across 17 fish species. Our analysis demonstrates that orthologues of PLP1/DMalpha have been retained and are functionally expressed in many, if not all, extant species of bony fish. Many of the amino acids that, when mutated, are associated with severe CNS pathology are conserved in teleosts, demonstrating conservation of essential functions and justifying the development of novel disease models in species such as the zebrafish.

Keywords

DM20/PLP1evolutionPelizaeus–Merzbacher diseasezebrafishanimal model
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 2 , May 2010 , pp. 109 - 112
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Brösamle, C. and Halpern, M.E. (2002) Characterization of myelination in the developing zebrafish. Glia 39, 47–57.CrossRefGoogle ScholarPubMed
Garbern, J.Y. (2007) Pelizaeus–Merzbacher disease: genetic and cellular pathogenesis. Cellular and Molecular Life Sciences 64, 50–65.CrossRefGoogle ScholarPubMed
Geltner, D., Kitagawa, K. and Yoshida, M. (1998) Remarkable diversity of proteolipid proteins in fish. Journal of Neuroscience Research 54, 289–295.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Gow, A. and Lazzarini, R.A. (1996) A cellular mechanism governing the severity of Pelizaeus–Merzbacher disease. Nature Genetics 13, 422–428.CrossRefGoogle ScholarPubMed
Gow, A., Southwood, C.M. and Lazzarini, R.A. (1998) Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus–Merzbacher disease. Journal of Cell Biology 140, 925–934.CrossRefGoogle Scholar
Griffiths, I., Klugmann, M., Anderson, T., Yool, D., Thomson, C., Schwab, M.H. et al. (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610–1613.CrossRefGoogle ScholarPubMed
Inoue, K. (2005) PLP1-related inherited dysmyelinating disorders: Pelizaeus–Merzbacher disease and spastic paraplegia type 2. Neurogenetics 6, 1–16.CrossRefGoogle ScholarPubMed
Jeserich, G., Klempahn, K. and Pfeiffer, M. (2008) Features and functions of oligodendrocytes and myelin proteins of lower vertebrate species. Journal of Molecular Neuroscience 35, 117–126.CrossRefGoogle ScholarPubMed
Kitagawa, K., Sinoway, M.P., Yang, C., Gould, R.M. and Colman, D.R. (1993) A proteolipid protein gene family: expression in sharks and rays and possible evolution from an ancestral gene encoding a pore-forming polypeptide. Neuron 11, 433–448.CrossRefGoogle ScholarPubMed
Klugmann, M., Schwab, M.H., Puhlhofer, A., Schneider, A., Zimmermann, F., Griffiths, I.R. et al. (1997) Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18, 59–70.CrossRefGoogle ScholarPubMed
Kurihara, T., Sakuma, M. and Gojobori, T. (1997) Molecular evolution of myelin proteolipid protein. Biochemical and Biophysical Research Communications 237, 559–561.CrossRefGoogle ScholarPubMed
Lieschke, G.J. and Currie, P.D. (2007) Animal models of human disease: zebrafish swim into view. Nature Reviews Genetics 8, 353–367.CrossRefGoogle ScholarPubMed
Lin, W. and Popko, B. (2009) Endoplasmic reticulum stress in disorders of myelinating cells. Nature Neuroscience 12, 379–385.CrossRefGoogle ScholarPubMed
Möbius, W., Patzig, J., Nave, K.-A. and Werner, H. (2009) Phylogeny of proteolipid proteins: divergence constraints and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biology. doi:10.1017/S1740925X0900009XGoogle Scholar
Morris, J.K., Willard, B.B., Yin, X., Jeserich, G., Kinter, M. and Trapp, B.D. (2004) The 36K protein of zebrafish CNS myelin is a short-chain dehydrogenase. Glia 45, 378–391.CrossRefGoogle ScholarPubMed
Nave, K.A., Lai, C., Bloom, F.E. and Milner, R.J. (1987) Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proceedings of the National Academy of Sciences of the U.S.A. 84, 5665–5669.CrossRefGoogle ScholarPubMed
Nave, K.A. and Trapp, B.D. (2008) Axon-glial signaling and the glial support of axon function. Annual Review of Neuroscience 31, 535–561.CrossRefGoogle ScholarPubMed
Postlethwait, J., Amores, A., Force, A. and Yan, Y.L. (1999) The zebrafish genome. Methods in Cell Biology 60, 149–163.CrossRefGoogle ScholarPubMed
Schweitzer, J., Becker, T., Schachner, M., Nave, K.A. and Werner, H. (2006) Evolution of myelin proteolipid proteins: gene duplication in teleosts and expression pattern divergence. Molecular and Cellular Neuroscience 31, 161–177.CrossRefGoogle ScholarPubMed
Shy, M.E., Hobson, G., Jain, M., Boespflug-Tanguy, O., Garbern, J., Sperle, K. et al. (2003) Schwann cell expression of PLP1 but not DM20 is necessary to prevent neuropathy. Annals of Neurology 53, 354–365.CrossRefGoogle Scholar
Stecca, B., Southwood, C.M., Gragerov, A., Kelley, K.A., Friedrich, V.L. Jr. and Gow, A. (2000) The evolution of lipophilin genes from invertebrates to tetrapods: DM-20 cannot replace proteolipid protein in CNS myelin. Journal of Neuroscience 20, 4002–4010.CrossRefGoogle ScholarPubMed
Stratmann, A. and Jeserich, G. (1995) Molecular cloning and tissue expression of a cDNA encoding IP1 – a P0-like glycoprotein of trout CNS myelin. Journal of Neurochemistry 64, 2427–2436.CrossRefGoogle ScholarPubMed
Tohyama, Y., Ichimiya, T., Kasama-Yoshida, H., Cao, Y., Hasegawa, M., Kojima, H. et al. (2000) Phylogenetic relation of lungfish indicated by the amino acid sequence of myelin DM20. Brain Research Molecular Brain Research 80, 256–259.CrossRefGoogle ScholarPubMed
Tohyama, Y., Kasama-Yoshida, H., Sakuma, M., Kobayashi, Y., Cao, Y., Hasegawa, M. et al. (1999) Gene structure and amino acid sequence of Latimeria chalumnae (coelacanth) myelin DM20: phylogenetic relation of the fish. Neurochemical Research 24, 867–873.CrossRefGoogle ScholarPubMed
Venkatesh, B., Erdmann, M.V. and Brenner, S. (2001) Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proceedings of the National Academy of Sciences of the U.S.A. 98, 11382–11387.CrossRefGoogle ScholarPubMed
Yoshida, M., Shan, W.S. and Colman, D.R. (1999) Conserved and divergent expression patterns of the proteolipid protein gene family in the amphibian central nervous system. Journal of Neuroscience Research 57, 13–22.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Zalc, B. and Colman, D.R. (2000) Origins of vertebrate success. Science 288, 271–272.CrossRefGoogle ScholarPubMed