Abstract
During the process of vertebrate evolution, many thermogenic organs and mechanisms have appeared. Mammalian brown adipose tissue (BAT) generates heat through the uncoupling oxidative phosphorylation of mitochondria, acts as a natural defense against hypothermia and inhibits the development of obesity. Although the existence, cellular origin and molecular identity of BAT in humans have been well studied, the genetic and functional characteristics of BAT from lampreys remain unknown. Here, we identified and characterized a novel, naturally existing brown-like adipocytes at the lamprey brain periphery. Similar to human BAT, the lamprey brain periphery contains brown-like adipocytes that maintain the same morphology as human brown adipocytes, containing multilocular lipid droplets and high mitochondrion numbers. Furthermore, we found that brown-like adipocytes in the periphery of lamprey brains responded to thermogenic reagent treatment and cold exposure and that lamprey UCP2 promoted precursor adipocyte differentiation. Molecular mapping by RNA-sequencing showed that inflammation in brown-like adipocytes treated with LPS and 25HC was enhanced compared to controls. The results of this study provide new evidence for human BAT research and demonstrate the multilocular adipose cell functions of lampreys, including: (1) providing material energy and protecting structure, (2) generating additional heat and contributing to adaptation to low-temperature environments, and (3) resisting external pathogens.
Highlights
There are large number of obesity-related diseases, including type 2 diabetes, insulin resistance, heart disease, dyslipidemia, hypertension and various cancers (Bornfeldt and Tabas, 2011; Harms and Seale, 2013)
Lamprey brain tissues are surrounded by a group of large cells distributed from the olfactory bulb to the cerebellum, especially in the diencephalon, mesencephalon, and cerebellum (Figures 1A,B)
There were white adipocytes, blood vessels surrounded by multiple large cells, and pigment cells that could be clearly seen in the peripheral brain tissue
Summary
There are large number of obesity-related diseases, including type 2 diabetes, insulin resistance, heart disease, dyslipidemia, hypertension and various cancers (Bornfeldt and Tabas, 2011; Harms and Seale, 2013). Previous studies have demonstrated that most brown adipocytes originate from precursor cells in embryonic mesodermal somites that can develop into skeletal muscle cells (Seale et al, 2008; Lepper and Fan, 2010; Sanchez-Gurmaches et al, 2012). Myogenic factor 5 (Myf5) and Pax expression is considered a selective marker of skeletal myoblast (Lepper and Fan, 2010; Sanchez-Gurmaches et al, 2012), and brown adipocyte precursor cells express a gene profile similar to that of muscle (Timmons et al, 2007); in addition, they possess related mitochondrial proteomes (Forner et al, 2009). Brown adipocytes in BAT are defined as cells containing multilocular lipid droplet, high mitochondrial content and the expression of brown adipocyte markers, including uncoupling protein-1 (Ucp1) (Kopecky et al, 1995; Bettini et al, 2019), cell deathinducing DNA fragmentation factor alpha-like effector A (Cidea) (Zhou et al, 2003; Toh et al, 2008), type II iodothyronine 5 deiodinase (Dio2) (Chan et al, 2019), cytochrome c oxidase polypeptide 7A1 (Cox7a1) and cytochrome c oxidase subunit VIIIb (Cox8b) (Chan et al, 2019) as well as transcriptional regulators, including PR domain zinc finger protein 16 (PRDM16) (Forner et al, 2009), peroxisome proliferatoractivated receptor-γ coactivator 1-α (Pgc-1α) (Hondares et al, 2006; Hallberg et al, 2008), and peroxisome proliferator-activated CCAAT/enlmnccr-binding protein B (C/EBPb) (Tanaka et al, 1997; Carmona et al, 2005; Karamanlidis et al, 2007) and receptor alpha (PPARα) (Tai et al, 1996; Siersbæk et al, 2012)
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