Understanding Myelination Through Studying Its Evolution

Schweigreiter, Rüdiger; Roots, Betty I.; Bandtlow, Christine E.; Gould, Robert M.

doi:10.1016/s0074-7742(06)73007-0

Cited by 43 publications

(52 citation statements)

References 318 publications

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“…5a) as well as in COS-7 cells (data not shown). It has been reported that PI3K activity regulates the activity of the HMGR promoter by modulating the SREBP-2 biosynthesis in cancer cells (29). Although our deletion studies suggest that SRE does not mediate the transcriptional effects of neuregulins (Fig.…”

Section: Discussionmentioning

confidence: 56%

“…Myelination allowed vertebrates to develop complex brains in relatively small volumes (29). Although glial cells from invertebrates like Drosophila do establish close contacts with neuronal axons, they do not form myelin sheaths (44).…”

Section: Discussionmentioning

confidence: 99%

“…However, not all vertebrates myelinate; agnathes like hagfishes and lampreys lack myelinated axons. Although some invertebrates show axons covered by multilayered glial cell membranes, resembling myelin membranes, a "true" myelin sheet is not found in invertebrates (29).…”

Section: Intracellular Pathways Involved In Neuregulin 1 Signaling-mentioning

confidence: 97%

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Transcriptional Control of Cholesterol Biosynthesis in Schwann Cells by Axonal Neuregulin 1

Pertusa

Morenilla‐Palao

Carteron

et al. 2007

Journal of Biological Chemistry

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A characteristic feature of many vertebrate axons is their wrapping by a lamellar stack of glially derived membranes known as the myelin sheath. Myelin is a cholesterol-rich membrane that allows for rapid saltatory nerve impulse conduction. Axonal neuregulins instruct glial cells on when and how much myelin they should produce. However, how neuregulin regulates myelin sheath development and thickness is unknown. Here we show that neuregulin receptors are activated by drops in plasma membrane cholesterol, suggesting that they can sense sterol levels. In Schwann cells neuregulin-1 increases the transcription of the 3-hydroxy-3-methylglutarylcoenzyme A reductase, the rate-limiting enzyme for cholesterol biosynthesis. Neuregulin activity is mediated by the phosphatidylinositol 3-kinase pathway and a cAMP-response element located on the reductase promoter. We propose that by activating neuregulin receptors, neurons exploit a cholesterol homeostatic mechanism forcing Schwann cells to produce new membranes for the myelin sheath. We also show that a strong phylogenetic correlation exists between myelination and cholesterol biosynthesis, and we propose that the absence of the sterol branch of the mevalonate pathway in invertebrates precluded the myelination of their nervous system.

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Section: Discussionmentioning

confidence: 56%

Section: Discussionmentioning

confidence: 99%

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Transcriptional Control of Cholesterol Biosynthesis in Schwann Cells by Axonal Neuregulin 1

Pertusa

Morenilla‐Palao

Carteron

et al. 2007

Journal of Biological Chemistry

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“…Once KCNQ channels appeared, all of the molecular components for construction of the nodes of Ranvier were in place. By this time the key genes for myelin components had also evolved (32,33).…”

Section: Evolution Of Namentioning

confidence: 99%

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

Zakon

2012

Proc. Natl. Acad. Sci. U.S.A.

141

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Voltage-gated Na + -permeable (Nav) channels form the basis for electrical excitability in animals. Nav channels evolved from Ca 2+ channels and were present in the common ancestor of choanoflagellates and animals, although this channel was likely permeable to both Na + and Ca 2+. Thus, like many other neuronal channels and receptors, Nav channels predated neurons. Invertebrates possess two Nav channels (Nav1 and Nav2), whereas vertebrate Nav channels are of the Nav1 family. Approximately 500 Mya in early chordates Nav channels evolved a motif that allowed them to cluster at axon initial segments, 50 million years later with the evolution of myelin, Nav channels "capitalized" on this property and clustered at nodes of Ranvier. The enhancement of conduction velocity along with the evolution of jaws likely made early gnathostomes fierce predators and the dominant vertebrates in the ocean. Later in vertebrate evolution, the Nav channel gene family expanded in parallel in tetrapods and teleosts (∼9 to 10 genes in amniotes, 8 in teleosts). This expansion occurred during or after the late Devonian extinction, when teleosts and tetrapods each diversified in their respective habitats, and coincided with an increase in the number of telencephalic nuclei in both groups. The expansion of Nav channels may have allowed for more sophisticated neural computation and tailoring of Nav channel kinetics with potassium channel kinetics to enhance energy savings. Nav channels show adaptive sequence evolution for increasing diversity in communication signals (electric fish), in protection against lethal Nav channel toxins (snakes, newts, pufferfish, insects), and in specialized habitats (naked mole rats).gene duplication | nervous system M ulticellular animals evolved >650 million years ago (1). The nervous system and muscles evolved shortly thereafter. The phylogeny of basal metazoans is poorly resolved, likely because of the rapid radiation of these then-new life forms (2), so depending on the phylogeny one embraces, the nervous system evolved once, once with a loss in sponges, or twice independently in ctenophora and bilateria + cnidaria or bilateria and cnidaria + ctenophora (3, 4). However, in all animals with nervous systems, neurons generate action potentials (APs), release excitatory and inhibitory neurotransmitters, form circuits, receive sensory input, innervate muscle, and direct behavior.The history of brain evolution and its key neural genes would fill volumes. I will use voltage-dependent Na + (Nav, Na-permeable voltage-dependent = protein; scn, sodium channel = gene) channels as an exemplar to tell this story because all neuronal excitability depends on Nav channels, there is a good understanding of their function and regulation from biophysical, biochemical, and modeling studies, and there are fascinating examples of ecologically relevant adaptations. An additional rationale is that although many proteins, such as immunoglobins, sperm and egg receptors, olfactory receptors, opsins, and surface proteins of pathogens, a...

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“…By going beyond a single instance of this innovation, analyzing the similarities and differences among independently evolved cases, we can better understand the key principles governing its contributions to nervous system organization and function. Although myelin is widely considered to be a strictly vertebrate innovation, structurally similar and functionally almost identical innovations have arisen apparently independently in three other taxa: oligochaetes, decapod shrimp, and copepods (for reviews see Schweigreiter et al, 2006;Hartline and Colman, 2007;Roots, 2008). Invertebrate myelins share many (but not all) of the characteristics of vertebrate myelin, including multilamellar lipid-rich membranous sheaths and periodic interruptions in the sheath termed ''nodes.''…”

mentioning

confidence: 99%

Novel organization and development of copepod myelin. i. ontogeny

Wilson

Hartline

2011

J of Comparative Neurology

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Nerve impulse conduction is greatly increased by myelin, a multilayered membranous sheath surrounding axons. Best known from and most extensively investigated among vertebrates, a few invertebrates, including some superfamilies of copepod, have functionally and structurally similar myelin-like sheaths surrounding their axons. We examined the development of myelin ultrastructure in Bestiolina similis, a paracalanoid copepod. Development occurred in a novel way: initial myelination always appeared first as a partial layer, which in later stages came to encircle an axon completely. This partial myelin first appeared in a single pair of reidentifiable fibers, at the second naupliar stage. Two additional pairs of reidentifiable fibers also became partially myelinated by the third naupliar stage. The number of myelin layers in this trio of axon pairs increased with development, but, at any one stage, each axon had the same number of layers along its entire length. These axons disappeared after the copepodite metamorphosis. After metamorphosis, the fiber that took over as largest in the nerve cord became the most heavily myelinated and was identified as the lateral dorsal giant fiber. The rate of myelination was also characterized in the antennular nerve as a representative of the peripheral nervous system. As axons became larger, they were more likely to be partially, and then completely, myelinated, the latter having a lower ratio of axon core to fiber diameter than the former. Copepod myelin is an instructive example of convergent evolution, with far-reaching consequences for nervous system functioning and the behavior that nervous systems subserve.

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Understanding Myelination Through Studying Its Evolution

Cited by 43 publications

References 318 publications

Transcriptional Control of Cholesterol Biosynthesis in Schwann Cells by Axonal Neuregulin 1

Transcriptional Control of Cholesterol Biosynthesis in Schwann Cells by Axonal Neuregulin 1

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

Novel organization and development of copepod myelin. i. ontogeny

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