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Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection

Published online by Cambridge University Press:  05 June 2009

Wiebke Möbius ,
Julia Patzig ,
Klaus-Armin Nave  and
Hauke B. Werner
Wiebke Möbius
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Julia Patzig
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Klaus-Armin Nave
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
Hauke B. Werner*
Affiliation:
Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Göttingen, Germany
*
Correspondence should be addressed to: Hauke B. Werner, Department of Neurogenetics, Max-Planck Institute of Experimental Medicine, Hermann-Rein-Str. 3, D-37075 Goettingen, Germany phone: ++49551 389-9759 fax: ++49 551 389-9758 email: hauke@em.mpg.de
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Abstract

The protein composition of myelin in the central nervous system (CNS) has changed at the evolutionary transition from fish to tetrapods, when a lipid-associated transmembrane-tetraspan (proteolipid protein, PLP) replaced an adhesion protein of the immunoglobulin superfamily (P0) as the most abundant constituent. Here, we review major steps of proteolipid evolution. Three paralog proteolipids (PLP/DM20/DMα, M6B/DMγ and the neuronal glycoprotein M6A/DMβ) exist in vertebrates from cartilaginous fish to mammals, and one (M6/CG7540) can be traced in invertebrate bilaterians including the planktonic copepod Calanus finmarchicus that possess a functional myelin equivalent. In fish, DMα and DMγ are coexpressed in oligodendrocytes but are not major myelin components. PLP emerged at the root of tetrapods by the acquisition of an enlarged cytoplasmic loop in the evolutionary older DMα/DM20. Transgenic experiments in mice suggest that this loop enhances the incorporation of PLP into myelin. The evolutionary recruitment of PLP as the major myelin protein provided oligodendrocytes with the competence to support long-term axonal integrity. We suggest that the molecular shift from P0 to PLP also correlates with the concentration of adhesive forces at the radial component, and that the new balance between membrane adhesion and dynamics was favorable for CNS myelination.

Keywords

MyelinoligodendrocyteSchmidt–Lanterman incisurePelizaeus-Merzbacher diseasespastic paraplegianeurite outgrowthPLP/DM20M6OSP/claudin-11P0/MPZ
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 2 , May 2008 , pp. 111 - 127
Copyright
Copyright © Cambridge University Press 2009

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