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      The Melanin-Concentrating Hormone (MCH) System: A Tale of Two Peptides

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          Abstract

          The melanin-concentrating hormone (MCH) system is a robust integrator of exogenous and endogenous information, modulating arousal and energy balance in mammals. Its predominant function in teleosts, however, is to concentrate melanin in the scales, contributing to the adaptive color change observed in several teleost species. These contrasting functions resulted from a gene duplication that occurred after the teleost divergence, which resulted in the generation of two MCH-coding genes in this clade, which acquired distinctive sequences, distribution, and functions, examined in detail here. We also describe the distribution of MCH immunoreactivity and gene expression in a large number of species, in an attempt to identify its core elements. While initially originated as a periventricular peptide, with an intimate relationship with the third ventricle, multiple events of lateral migration occurred during evolution, making the ventrolateral and dorsolateral hypothalamus the predominant sites of MCH in teleosts and mammals, respectively. Substantial differences between species can be identified, likely reflecting differences in habitat and behavior. This observation aligns well with the idea that MCH is a major integrator of internal and external information, ensuring an appropriate response to ensure the organism’s homeostasis. New studies on the MCH system in species that have not yet been investigated will help us understand more precisely how these habitat changes are connected to the hypothalamic neurochemical circuits, paving the way to new intervention strategies that may be used with pharmacological purposes.

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          Most cited references134

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          From 2R to 3R: evidence for a fish-specific genome duplication (FSGD).

          An important mechanism for the evolution of phenotypic complexity, diversity and innovation, and the origin of novel gene functions is the duplication of genes and entire genomes. Recent phylogenomic studies suggest that, during the evolution of vertebrates, the entire genome was duplicated in two rounds (2R) of duplication. Later, approximately 350 mya, in the stem lineage of ray-finned (actinopterygian) fishes, but not in that of the land vertebrates, a third genome duplication occurred-the fish-specific genome duplication (FSGD or 3R), leading, at least initially, to up to eight copies of the ancestral deuterostome genome. Therefore, the sarcopterygian (lobe-finned fishes and tetrapods) genome possessed originally only half as many genes compared to the derived fishes, just like the most-basal and species-poor lineages of extant fishes that diverged from the fish stem lineage before the 3R duplication. Most duplicated genes were secondarily lost, yet some evolved new functions. The genomic complexity of the teleosts might be the reason for their evolutionary success and astounding biological diversity.
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            Elephant shark genome provides unique insights into gnathostome evolution

            The emergence of jawed vertebrates (gnathostomes) from jawless vertebrates was accompanied by major morphological and physiological innovations, such as hinged jaws, paired fins and immunoglobulin-based adaptive immunity. Gnathostomes subsequently diverged into two groups, the cartilaginous fishes and the bony vertebrates. Here we report the whole-genome analysis of a cartilaginous fish, the elephant shark (Callorhinchus milii). We find that the C. milii genome is the slowest evolving of all known vertebrates, including the ‘living fossil’ coelacanth, and features extensive synteny conservation with tetrapod genomes, making it a good model for comparative analyses of gnathostome genomes. Our functional studies suggest that the lack of genes encoding secreted calcium-binding phosphoproteins in cartilaginous fishes explains the absence of bone in their endoskeleton. Furthermore, the adaptive immune system of cartilaginous fishes is unusual: it lacks the canonical CD4 co-receptor and most transcription factors, cytokines and cytokine receptors related to the CD4 lineage, despite the presence of polymorphic major histocompatibility complex class II molecules. It thus presents a new model for understanding the origin of adaptive immunity. Supplementary information The online version of this article (doi:10.1038/nature12826) contains supplementary material, which is available to authorized users.
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              Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution.

              Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                26 November 2019
                2019
                : 13
                : 1280
                Affiliations
                [1] 1Departamento de Anatomia, Instituto de Ciências Biomedicas, Universidade de São Paulo , São Paulo, Brazil
                [2] 2Department of Neurosurgery, Yale School of Medicine , New Haven, CT, United States
                [3] 3Nucleo de Neurociencias e Comportamento, Instituto de Psicologia, Universidade de São Paulo , São Paulo, Brazil
                Author notes

                Edited by: Dan Larhammar, Uppsala University, Sweden

                Reviewed by: Hervé Tostivint, Muséum National d’Histoire Naturelle, France; Gina Leinninger, Michigan State University, United States

                *Correspondence: Jackson C. Bittencourt, jcbitten@ 123456icb.usp.br

                This article was submitted to Neuroendocrine Science, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2019.01280
                6901935
                31849590
                747d49c5-2bb4-4603-99c9-99cfac99c00e
                Copyright © 2019 Diniz and Bittencourt.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 August 2019
                : 11 November 2019
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 145, Pages: 23, Words: 0
                Funding
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo 10.13039/501100001807
                Award ID: 2010/52068-0
                Award ID: 2016/02224-1
                Award ID: 2016/02748-0
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior 10.13039/501100002322
                Award ID: 848/15
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico 10.13039/501100003593
                Award ID: 426378/2016-4
                Categories
                Neuroscience
                Review

                Neurosciences
                nei,mchr1,mchr2,lateral hypothalamus,neuropeptides,vertebrates
                Neurosciences
                nei, mchr1, mchr2, lateral hypothalamus, neuropeptides, vertebrates

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