Myelin in cartilaginous fish

Abstract

Myelin is probably one of the most fascinating and innovative biological acquisition: a glia plasma membrane tightly wrapped around an axon and insulating it. Chondrichthyans (cartilaginous fishes) form a large group of vertebrates, and they are among oldest extant jawed vertebrate lineage. It has been known from studies 150 years ago, that they are positioned at the root of the successful appearance of compact myelin and main adhesive proteins in vertebrates. More importantly, the ultrastructure of their compact myelin is indistinguishable from the one observed in tetrapods and the first true myelin basic protein (MBP) and myelin protein zero (MPZ) seem to have originated on cartilaginous fish or their ancestors, the placoderms. Thus, the study of their myelin formation would bring new insights in vertebrate׳s myelin evolution. Chondrichthyans central nervous system (CNS) myelin composition is also very similar to peripheral nervous system (PNS) myelin composition. And while they lack true proteolipid protein (PLP) like tetrapods, they express a DM-like protein in their myelin. This article is part of a Special Issue entitled SI: Myelin Evolution.

Keywords: Chondrichthyans; DM20; Elasmobranchs; Myelin; Myelin protein zero; PLP; mbp.

Figure 1. Phylogeny of Myelin from Chondrichthyes perspective

Sequence EST alignment for known MPZ from elasmobranchs (50% homology to mammalian MPZ) with coelacanths, zebrafish, chicken and mouse as outgroups. The results confirm what has been proposed for the phylogenetic origin of MPZ: sequences from chondrichthyans and actinopterygians aligned closer than tetrapod MPZ. The Holocephali MPZ had diverged far apart from the known Heterodontus sequence. The bar at the bottom provides a scale for the length of the tree arms (these indicate the amount of genetic change and represent evolutionary lineages changing over time). The vertical lines value corresponds to the confidence of that the sequences to the right of the node cluster together to the exclusion of any other.

Figure 2. Phylogeny of Myelin Basic Protein

Sequence EST alignment for known MBPs from elasmobranchs with chicken and mouse as outgroups. The results confirm what has been proposed for the phylogenetic origin of chondrichthyans: sequences from Squalus and Leucoraja were closer to one another than either is to the Galeomorph sharks, while Holocephali placed separate from the rest. The bar at the bottom provides a scale for the length of the tree arms (these indicate the amount of genetic change and represent evolutionary lineages changing over time). The vertical lines value corresponds to the confidence of that the sequences to the right of the node cluster together to the exclusion of any other.

Figure 3. Comparison of Myelin morphology and composition across evolution

The cartoon shows the main differences between agnathans pseudo-myelin and gnathostomes true myelin. Although both have distinct PNS and CNS, agnathans axons are loosely wrapped by glial cells. Compact myelin appeared in chondrichthyans coinciding also with the appearance of MPZ and MBP. Later, tetrapods diverged their CNS myelin components from the original MPZ to PLP as main adhesive molecule.

Figure 4. Phylogeny of Myelin from Chondrichthyes perspective

The phylogenetic tree summarizes the review on the evolution of main myelin proteins. Although compact myelin has been observed in non-chordates, upon the appearance of compact myelin in chondrichthyans, little has changed except for the transition of CNS myelin from MPZ to PLP/DM20 in tetrapods. The earliest MBP-like appeared in the ancestor to agnathans.