View Item 

Show simple item record

Contrasting recruitment of skin- associated adipose depots during cold challenge of mouse and human
dc.contributor.authorKasza, Ildiko
dc.contributor.authorKühn, Jens-Peter
dc.contributor.authorVölzke, Henry
dc.contributor.authorHernando, Diego
dc.contributor.authorXu, Yaohui G.
dc.contributor.authorSiebert, John W.
dc.contributor.authorGibson, Angela L. F.
dc.contributor.authorYen, C. -L. Eric
dc.contributor.authorNelson, David W.
dc.contributor.authorMacDougald, Ormond A.
dc.contributor.authorRichardson, Nicole E.
dc.contributor.authorLamming, Dudley W.
dc.contributor.authorKern, Philip A.
dc.contributor.authorAlexander, C. M.
dc.date.accessioned2022-03-07T03:13:28Z
dc.date.available2023-03-06 22:13:26en
dc.date.available2022-03-07T03:13:28Z
dc.date.issued2022-02
dc.identifier.citationKasza, Ildiko; Kühn, Jens-Peter ; Völzke, Henry ; Hernando, Diego; Xu, Yaohui G.; Siebert, John W.; Gibson, Angela L. F.; Yen, C. -L. Eric ; Nelson, David W.; MacDougald, Ormond A.; Richardson, Nicole E.; Lamming, Dudley W.; Kern, Philip A.; Alexander, C. M. (2022). "Contrasting recruitment of skin- associated adipose depots during cold challenge of mouse and human." The Journal of Physiology 600(4): 847-868.
dc.identifier.issn0022-3751
dc.identifier.issn1469-7793
dc.identifier.urihttps://hdl.handle.net/2027.42/171880
dc.description.abstractMammalian skin impacts metabolic efficiency system- wide, controlling the rate of heat loss and consequent heat production. Here we compare the unique fat depots associated with mouse and human skin, to determine whether they have corresponding functions and regulation. For humans, we assay a skin- associated fat (SAF) body- wide depot to distinguish it from the subcutaneous fat pads characteristic of the abdomen and upper limbs. We show that the thickness of SAF is not related to general adiposity; it is much thicker (1.6- fold) in women than men, and highly subject- specific. We used molecular and cellular assays of β- adrenergic- induced lipolysis and found that dermal white adipose tissue (dWAT) in mice is resistant to lipolysis; in contrast, the body- wide human SAF depot becomes lipolytic, generating heat in response to β- adrenergic stimulation. In mice challenged to make more heat to maintain body temperature (either environmentally or genetically), there is a compensatory increase in thickness of dWAT: a corresponding β- adrenergic stimulation of human skin adipose (in vivo or in explant) depletes adipocyte lipid content. We summarize the regulation of skin- associated adipocytes by age, sex and adiposity, for both species. We conclude that the body- wide dWAT depot of mice shows unique regulation that enables it to be deployed for heat preservation; combined with the actively lipolytic subcutaneous mammary fat pads they enable thermal defence. The adipose tissue that covers human subjects produces heat directly, providing an alternative to the brown adipose tissues.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherheat production
dc.subject.otherdermal white adipose tissue
dc.subject.otherUCP1
dc.subject.otherthermogenesis
dc.subject.othersubcutaneous white adipose tissue
dc.subject.otherskin- associated fat
dc.subject.otherscWAT
dc.subject.otherobesity
dc.subject.otherlipolysis
dc.subject.otherdWAT
dc.subject.otherβ- adrenergic response
dc.subject.otherbrown adipose tissue
dc.titleContrasting recruitment of skin- associated adipose depots during cold challenge of mouse and human
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelPhysiology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/171880/1/tjp14623_am.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/171880/2/tjp14623.pdf
dc.identifier.doi10.1113/JP280922
dc.identifier.sourceThe Journal of Physiology
dc.identifier.citedreferenceQiao G, Chen M, Bucsek MJ, Repasky EA & Hylander BL ( 2018 ). Adrenergic signaling: a targetable checkpoint limiting development of the antitumor immune response. Front Immunol 9, 164.
dc.identifier.citedreferenceKuhn JP, Meffert P, Heske C, Kromrey ML, Schmidt CO, Mensel B, Volzke H, Lerch MM, Hernando D, Mayerle J & Reeder SB ( 2017 ). Prevalence of fatty liver disease and hepatic iron overload in a northeastern german population by using quantitative MR imaging. Radiology 284, 706 - 716.
dc.identifier.citedreferenceLangin D, Dicker A, Tavernier G, Hoffstedt J, Mairal A, Ryden M, Arner E, Sicard A, Jenkins CM, Viguerie N, van Harmelen V, Gross RW, Holm C & Arner P ( 2005 ). Adipocyte lipases and defect of lipolysis in human obesity. Diabetes 54, 3190 - 3197.
dc.identifier.citedreferenceLee MJ, Wu Y & Fried SK ( 2013 ). Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med 34, 1 - 11.
dc.identifier.citedreferenceLiu D, Bordicchia M, Zhang C, Fang H, Wei W, Li JL, Guilherme A, Guntur K, Czech MP & Collins S ( 2016 ). Activation of mTORC1 is essential for beta- adrenergic stimulation of adipose browning. J Clin Invest 126, 1704 - 1716.
dc.identifier.citedreferenceLoh NY, Neville MJ, Marinou K, Hardcastle SA, Fielding BA, Duncan EL, McCarthy MI, Tobias JH, Gregson CL, Karpe F & Christodoulides C ( 2015 ). LRP5 regulates human body fat distribution by modulating adipose progenitor biology in a dose- and depot- specific fashion. Cell Metab 21, 262 - 273.
dc.identifier.citedreferenceLu Y, Day FR, Gustafsson S, Buchkovich ML, Na J, Bataille V, Cousminer DL, Dastani Z, Drong AW, Esko T, Evans DM, Falchi M, Feitosa MF, Ferreira T, Hedman AK, Haring R, Hysi PG, Iles MM, Justice AE, Kanoni S, Lagou V, Li R, Li X, Locke A, Lu C, Magi R, Perry JR, Pers TH, Qi Q, Sanna M, Schmidt EM, Scott WR, Shungin D, Teumer A, Vinkhuyzen AA, Walker RW, Westra HJ, Zhang M, Zhang W, Zhao JH, Zhu Z, Afzal U, Ahluwalia TS, Bakker SJ, Bellis C, Bonnefond A, Borodulin K, Buchman AS, Cederholm T, Choh AC, Choi HJ, Curran JE, de Groot LC, De Jager PL, Dhonukshe- Rutten RA, Enneman AW, Eury E, Evans DS, Forsen T, Friedrich N, Fumeron F, Garcia ME, Gartner S, Han BG, Havulinna AS, Hayward C, Hernandez D, Hillege H, Ittermann T, Kent JW, Kolcic I, Laatikainen T, Lahti J, Mateo Leach I, Lee CG, Lee JY, Liu T, Liu Y, Lobbens S, Loh M, Lyytikainen LP, Medina- Gomez C, Michaelsson K, Nalls MA, Nielson CM, Oozageer L, Pascoe L, Paternoster L, Polasek O, Ripatti S, Sarzynski MA, Shin CS, Narancic NS, Spira D, Srikanth P, Steinhagen- Thiessen E, Sung YJ, Swart KM, Taittonen L, Tanaka T, Tikkanen E, van der Velde N, van Schoor NM, Verweij N, Wright AF, Yu L, Zmuda JM, Eklund N, Forrester T, Grarup N, Jackson AU, Kristiansson K, Kuulasmaa T, Kuusisto J, Lichtner P, Luan J, Mahajan A, Mannisto S, Palmer CD, Ried JS, Scott RA, Stancakova A, Wagner PJ, Demirkan A, Doring A, Gudnason V, Kiel DP, Kuhnel B, Mangino M, McKnight B, Menni C, O’Connell JR, Oostra BA, Shuldiner AR, Song K, Vandenput L, van Duijn CM, Vollenweider P, White CC, Boehnke M, Boettcher Y, Cooper RS, Forouhi NG, Gieger C, Grallert H, Hingorani A, Jorgensen T, Jousilahti P, Kivimaki M, Kumari M, Laakso M, Langenberg C, Linneberg A, Luke A, McKenzie CA, Palotie A, Pedersen O, Peters A, Strauch K, Tayo BO, Wareham NJ, Bennett DA, Bertram L, Blangero J, Bluher M, Bouchard C, Campbell H, Cho NH, Cummings SR, Czerwinski SA, Demuth I, Eckardt R, Eriksson JG, Ferrucci L, Franco OH, Froguel P, Gansevoort RT, Hansen T, Harris TB, Hastie N, Heliovaara M, Hofman A, Jordan JM, Jula A, Kahonen M, Kajantie E, Knekt PB, Koskinen S, Kovacs P, Lehtimaki T, Lind L, Liu Y, Orwoll ES, Osmond C, Perola M, Perusse L, Raitakari OT, Rankinen T, Rao DC, Rice TK, Rivadeneira F, Rudan I, Salomaa V, Sorensen TI, Stumvoll M, Tonjes A, Towne B, Tranah GJ, Tremblay A, Uitterlinden AG, van der Harst P, Vartiainen E, Viikari JS, Vitart V, Vohl MC, Volzke H, Walker M, Wallaschofski H, Wild S, Wilson JF, Yengo L, Bishop DT, Borecki IB, Chambers JC, Cupples LA, Dehghan A, Deloukas P, Fatemifar G, Fox C, Furey TS, Franke L, Han J, Hunter DJ, Karjalainen J, Karpe F, Kaplan RC, Kooner JS, McCarthy MI, Murabito JM, Morris AP, Bishop JA, North KE, Ohlsson C, Ong KK, Prokopenko I, Richards JB, Schadt EE, Spector TD, Widen E, Willer CJ, Yang J, Ingelsson E, Mohlke KL, Hirschhorn JN, Pospisilik JA, Zillikens MC, Lindgren C, Kilpelainen TO & Loos RJ ( 2016 ). New loci for body fat percentage reveal link between adiposity and cardiometabolic disease risk. Nat Commun 7, 10495.
dc.identifier.citedreferenceManolopoulos KN, Karpe F & Frayn KN ( 2010 ). Gluteofemoral body fat as a determinant of metabolic health. Int J Obes 34, 949 - 959.
dc.identifier.citedreferenceMills EL, Pierce KA, Jedrychowski MP, Garrity R, Winther S, Vidoni S, Yoneshiro T, Spinelli JB, Lu GZ, Kazak L, Banks AS, Haigis MC, Kajimura S, Murphy MP, Gygi SP, Clish CB & Chouchani ET ( 2018 ). Accumulation of succinate controls activation of adipose tissue thermogenesis. Nature 560, 102 - 106.
dc.identifier.citedreferenceMottillo EP, Balasubramanian P, Lee YH, Weng C, Kershaw EE & Granneman JG ( 2014 ). Coupling of lipolysis and de novo lipogenesis in brown, beige, and white adipose tissues during chronic beta3- adrenergic receptor activation. J Lipid Res 55, 2276 - 2286.
dc.identifier.citedreferenceNeess D, Bek S, Bloksgaard M, Marcher AB, Faergeman NJ & Mandrup S ( 2013 ). Delayed hepatic adaptation to weaning in ACBP- /- mice is caused by disruption of the epidermal barrier. Cell Rep 5, 1403 - 1412.
dc.identifier.citedreferenceNeess D, Kruse V, Marcher AB, Waede MR, Vistisen J, Moller PM, Petersen R, Brewer JR, Ma T, Colleluori G, Severi I, Cinti S, Gerhart- Hines Z, Mandrup S & Faergeman NJ ( 2020 ). Epidermal Acyl- CoA- binding protein is indispensable for systemic energy homeostasis. Mol Metab 44, 101144.
dc.identifier.citedreferenceNicu C, Pople J, Bonsell L, Bhogal R, Ansell DM & Paus R ( 2018 ). A guide to studying human dermal adipocytes in situ. Exp Dermatol 27, 589 - 602.
dc.identifier.citedreferenceOgasawara J, Izawa T, Sakurai T, Sakurai T, Shirato K, Ishibashi Y, Ishida H, Ohno H & Kizaki T ( 2015 ). The molecular mechanism underlying continuous exercise training- induced adaptive changes of lipolysis in white adipose cells. J Obes 2015, 473430.
dc.identifier.citedreferencePerez- Chirinos Buxade C, Sola- Perez T, Castizo- Olier J, Carrasco- Marginet M, Roy A, Marfell- Jones M & Irurtia A ( 2018 ). Assessing subcutaneous adipose tissue by simple and portable field instruments: skinfolds versus a- mode ultrasound measurements. PLoS One 13, e0205226.
dc.identifier.citedreferencePinnick KE, Nicholson G, Manolopoulos KN, McQuaid SE, Valet P, Frayn KN, Denton N, Min JL, Zondervan KT, Fleckner J, Mol PC, McCarthy MI, Holmes CC & Karpe F ( 2014 ). Distinct developmental profile of lower- body adipose tissue defines resistance against obesity- associated metabolic complications. Diabetes 63, 3785 - 3797.
dc.identifier.citedreferenceRivera- Gonzalez GC, Shook BA, Andrae J, Holtrup B, Bollag K, Betsholtz C, Rodeheffer MS & Horsley V ( 2016 ). Skin adipocyte stem cell self- renewal is regulated by a PDGFA/AKT- signaling axis. Cell Stem Cell 19, 738 - 751.
dc.identifier.citedreferenceSampath H, Flowers MT, Liu X, Paton CM, Sullivan R, Chu K, Zhao M & Ntambi JM ( 2009 ). Skin- specific deletion of stearoyl- CoA desaturase- 1 alters skin lipid composition and protects mice from high fat diet- induced obesity. J Biol Chem 284, 19961 - 19973.
dc.identifier.citedreferenceSampath H & Ntambi JM ( 2014 ). Role of stearoyl- CoA desaturase- 1 in skin integrity and whole body energy balance. J Biol Chem 289, 2482 - 2488.
dc.identifier.citedreferenceSbarbati A, Accorsi D, Benati D, Marchetti L, Orsini G, Rigotti G & Panettiere P ( 2010 ). Subcutaneous adipose tissue classification. Eur J Histochem 54, 48.
dc.identifier.citedreferenceScheller EL, Khandaker S, Learman BS, Cawthorn WP, Anderson LM, Pham HA, Robles H, Wang Z, Li Z, Parlee SD, Simon BR, Mori H, Bree AJ, Craft CS & MacDougald OA ( 2019 ). Bone marrow adipocytes resist lipolysis and remodeling in response to beta- adrenergic stimulation. Bone 118, 32 - 41.
dc.identifier.citedreferenceShih MY, Kane MA, Zhou P, Yen CL, Streeper RS, Napoli JL & Farese RV, Jr ( 2009 ). Retinol esterification by DGAT1 is essential for retinoid homeostasis in murine skin. J Biol Chem 284, 4292 - 4299.
dc.identifier.citedreferenceSmith GI, Mittendorfer B & Klein S ( 2019 ). Metabolically healthy obesity: facts and fantasies. J Clin Invest 129, 3978 - 3989.
dc.identifier.citedreferenceSmith SR, Lovejoy JC, Greenway F, Ryan D, deJonge L, de la Bretonne J, Volafova J & Bray GA ( 2001 ). Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism 50, 425 - 435.
dc.identifier.citedreferenceSpeakman JR ( 2013 ). Measuring energy metabolism in the mouse - theoretical, practical, and analytical considerations. Front Physiol 4, 34.
dc.identifier.citedreferenceStorchle P, Muller W, Sengeis M, Lackner S, Holasek S & Furhapter- Rieger A ( 2018 ). Measurement of mean subcutaneous fat thickness: eight standardised ultrasound sites compared to 216 randomly selected sites. Sci Rep 8, 16268.
dc.identifier.citedreferenceTian XY, Ganeshan K, Hong C, Nguyen KD, Qiu Y, Kim J, Tangirala RK, Tonotonoz P & Chawla A ( 2016 ). Thermoneutral housing accelerates metabolic inflammation to potentiate atherosclerosis but not insulin resistance. Cell Metab 23, 165 - 178.
dc.identifier.citedreferenceTschop MH, Speakman JR, Arch JR, Auwerx J, Bruning JC, Chan L, Eckel RH, Farese RV, Jr., Galgani JE, Hambly C, Herman MA, Horvath TL, Kahn BB, Kozma SC, Maratos- Flier E, Muller TD, Munzberg H, Pfluger PT, Plum L, Reitman ML, Rahmouni K, Shulman GI, Thomas G, Kahn CR & Ravussin E ( 2012 ). A guide to analysis of mouse energy metabolism. Nat Methods 9, 57 - 63.
dc.identifier.citedreferencevan der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, Hansen J, Jorgensen JA, Wu J, Mottaghy FM, Schrauwen P & van Marken Lichtenbelt WD ( 2013 ). Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 123, 3395 - 3403.
dc.identifier.citedreferencevan Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P & Teule GJ ( 2009 ). Cold- activated brown adipose tissue in healthy men. N Engl J Med 360, 1500 - 1508.
dc.identifier.citedreferenceVerboven K, Wouters K, Gaens K, Hansen D, Bijnen M, Wetzels S, Stehouwer CD, Goossens GH, Schalkwijk CG, Blaak EE & Jocken JW ( 2018 ). Abdominal subcutaneous and visceral adipocyte size, lipolysis and inflammation relate to insulin resistance in male obese humans. Sci Rep 8, 4677.
dc.identifier.citedreferenceVillarroya F & Giralt M ( 2015 ). The beneficial effects of brown fat transplantation: further evidence of an endocrine role of brown adipose tissue. Endocrinology 156, 2368 - 2370.
dc.identifier.citedreferenceVolzke H, Alte D, Schmidt CO, Radke D, Lorbeer R, Friedrich N, Aumann N, Lau K, Piontek M, Born G, Havemann C, Ittermann T, Schipf S, Haring R, Baumeister SE, Wallaschofski H, Nauck M, Frick S, Arnold A, Junger M, Mayerle J, Kraft M, Lerch MM, Dorr M, Reffelmann T, Empen K, Felix SB, Obst A, Koch B, Glaser S, Ewert R, Fietze I, Penzel T, Doren M, Rathmann W, Haerting J, Hannemann M, Ropcke J, Schminke U, Jurgens C, Tost F, Rettig R, Kors JA, Ungerer S, Hegenscheid K, Kuhn JP, Kuhn J, Hosten N, Puls R, Henke J, Gloger O, Teumer A, Homuth G, Volker U, Schwahn C, Holtfreter B, Polzer I, Kohlmann T, Grabe HJ, Rosskopf D, Kroemer HK, Kocher T, Biffar R, John U & Hoffmann W ( 2011 ). Cohort profile: the study of health in Pomerania. Int J Epidemiol 40, 294 - 307.
dc.identifier.citedreferenceWajchenberg BL ( 2000 ). Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21, 697 - 738.
dc.identifier.citedreferenceWalker GE, Marzullo P, Ricotti R, Bona G & Prodam F ( 2014 ). The pathophysiology of abdominal adipose tissue depots in health and disease. Horm Mol Biol Clin Investig 19, 57 - 74.
dc.identifier.citedreferenceWang GX, Zhao XY & Lin JD ( 2015 ). The brown fat secretome: metabolic functions beyond thermogenesis. Trends Endocrinol Metab 26, 231 - 237.
dc.identifier.citedreferenceWu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P & Spiegelman BM ( 2012 ). Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366 - 376.
dc.identifier.citedreferenceYoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kawai Y, Iwanaga T & Saito M ( 2013 ). Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 123, 3404 - 3408.
dc.identifier.citedreferenceYoneshiro T, Matsushita M, Nakae S, Kameya T, Sugie H, Tanaka S & Saito M ( 2016 ). Brown adipose tissue is involved in the seasonal variation of cold- induced thermogenesis in humans. Am J Physiol Regul Integr Comp Physiol, 310, R999 - R1009, ajpregu 00057 02015.
dc.identifier.citedreferenceZhang Z, Shao M, Hepler C, Zi Z, Zhao S, An YA, Zhu Y, Ghaben AL, Wang MY, Li N, Onodera T, Joffin N, Crewe C, Zhu Q, Vishvanath L, Kumar A, Xing C, Wang QA, Gautron L, Deng Y, Gordillo R, Kruglikov I, Kusminski CM, Gupta RK & Scherer PE ( 2019 ). Dermal adipose tissue has high plasticity and undergoes reversible dedifferentiation in mice. J Clin Invest 129, 5327 - 5342.
dc.identifier.citedreferenceZwick RK, Guerrero- Juarez CF, Horsley V & Plikus MV ( 2018 ). Anatomical, physiological, and functional diversity of adipose tissue. Cell Metab 27, 68 - 83.
dc.identifier.citedreferenceAlexander CM, Kasza I, Yen CL, Reeder SB, Hernando D, Gallo RL, Jahoda CA, Horsley V & MacDougald OA ( 2015 ). Dermal white adipose tissue: a new component of the thermogenic response. J Lipid Res 56, 2061 - 2069.
dc.identifier.citedreferenceBartelt A & Heeren J ( 2014 ). Adipose tissue browning and metabolic health. Nat Rev Endocrinol 10, 24 - 36.
dc.identifier.citedreferenceBerry DC, Jiang Y, Arpke RW, Close EL, Uchida A, Reading D, Berglund ED, Kyba M & Graff JM ( 2017 ). Cellular aging contributes to failure of cold- induced beige adipocyte formation in old mice and humans. Cell Metab 25, 166 - 181.
dc.identifier.citedreferenceCannon B & Nedergaard J ( 2009 ). Thermogenesis challenges the adipostat hypothesis for body- weight control. Proc Nutr Soc 68, 401 - 407.
dc.identifier.citedreferenceCappellano G, Morandi EM, Rainer J, Grubwieser P, Heinz K, Wolfram D, Bernhard D, Lobenwein S, Pierer G & Ploner C ( 2018 ). Human macrophages preferentially infiltrate the superficial adipose tissue. Int J Mol Sci 1404, 19.
dc.identifier.citedreferenceChen KY, Cypess AM, Laughlin MR, Haft CR, Hu HH, Bredella MA, Enerback S, Kinahan PE, Lichtenbelt W, Lin FI, Sunderland JJ, Virtanen KA & Wahl RL ( 2016 ). Brown adipose reporting criteria in imaging STudies (BARCIST 1.0): Recommendations for standardized FDG- PET/CT experiments in humans. Cell Metab 24, 210 - 222.
dc.identifier.citedreferenceChondronikola M & Sidossis LS ( 2019 ). Brown and beige fat: From molecules to physiology. Biochim Biophys Acta Mol Cell Biol Lipids 1864, 91 - 103.
dc.identifier.citedreferenceChouchani ET, Kazak L & Spiegelman BM ( 2019 ). New advances in adaptive thermogenesis: UCP1 and beyond. Cell Metab 29, 27 - 37.
dc.identifier.citedreferenceDriskell RR, Jahoda CA, Chuong CM, Watt FM & Horsley V ( 2014 ). Defining dermal adipose tissue. Exp Dermatol 23, 629 - 631.
dc.identifier.citedreferenceElattar S & Satyanarayana A ( 2015 ). Can brown fat win the battle against white fat?. J Cell Physiol 230, 2311 - 2317.
dc.identifier.citedreferenceEnevoldsen LH, Simonsen L, Stallknecht B, Galbo H & Bulow J ( 2001 ). In vivo human lipolytic activity in preperitoneal and subdivisions of subcutaneous abdominal adipose tissue. Am J Physiol Endocrinol Metab 281, E1110 - E1114.
dc.identifier.citedreferenceFabbiano S, Suarez- Zamorano N, Rigo D, Veyrat- Durebex C, Stevanovic Dokic A, Colin DJ & Trajkovski M ( 2016 ). Caloric restriction leads to browning of white adipose tissue through type 2 immune signaling. Cell Metab 24, 434 - 446.
dc.identifier.citedreferenceFinlin BS, Confides AL, Zhu B, Boulanger MC, Memetimin H, Taylor KW, Johnson ZR, Westgate PM, Dupont- Versteegden EE & Kern PA ( 2019 ). Adipose tissue mast cells promote human adipose beiging in response to cold. Sci Rep 9, 8658.
dc.identifier.citedreferenceFinlin BS, Memetimin H, Confides AL, Kasza I, Zhu B, Vekaria HJ, Harfmann B, Jones KA, Johnson ZR, Westgate PM, Alexander CM, Sullivan PG, Dupont- Versteegden EE & Kern PA ( 2018 ). Human adipose beiging in response to cold and mirabegron. JCI Insight 3.
dc.identifier.citedreferenceFinlin BS, Zhu B, Confides AL, Westgate PM, Harfmann BD, Dupont- Versteegden EE & Kern PA ( 2017 ). Mast cells promote seasonal white adipose beiging in humans. Diabetes 66, 1237 - 1246.
dc.identifier.citedreferenceFruhbeck G, Mendez- Gimenez L, Fernandez- Formoso JA, Fernandez S & Rodriguez A ( 2014 ). Regulation of adipocyte lipolysis. Nutr Res Rev 27, 63 - 93.
dc.identifier.citedreferenceGiles DA, Moreno- Fernandez ME, Stankiewicz TE, Graspeuntner S, Cappelletti M, Wu D, Mukherjee R, Chan CC, Lawson MJ, Klarquist J, Sunderhauf A, Softic S, Kahn CR, Stemmer K, Iwakura Y, Aronow BJ, Karns R, Steinbrecher KA, Karp CL, Sheridan R, Shanmukhappa SK, Reynaud D, Haslam DB, Sina C, Rupp J, Hogan SP & Divanovic S ( 2017 ). Thermoneutral housing exacerbates nonalcoholic fatty liver disease in mice and allows for sex- independent disease modeling. Nat Med 23, 829 - 838.
dc.identifier.citedreferenceGrove KL, Fried SK, Greenberg AS, Xiao XQ & Clegg DJ ( 2010 ). A microarray analysis of sexual dimorphism of adipose tissues in high- fat- diet- induced obese mice. Int J Obes 34, 989 - 1000.
dc.identifier.citedreferenceHanssen MJ, van der Lans AA, Brans B, Hoeks J, Jardon KM, Schaart G, Mottaghy FM, Schrauwen P & van Marken Lichtenbelt WD ( 2016 ). Short- term cold acclimation recruits brown adipose tissue in obese humans. Diabetes 65, 1179 - 1189.
dc.identifier.citedreferenceHarms M & Seale P ( 2013 ). Brown and beige fat: development, function and therapeutic potential. Nat Med 19, 1252 - 1263.
dc.identifier.citedreferenceIkeda K, Kang Q, Yoneshiro T, Camporez JP, Maki H, Homma M, Shinoda K, Chen Y, Lu X, Maretich P, Tajima K, Ajuwon KM, Soga T & Kajimura S ( 2017 ). UCP1- independent signaling involving SERCA2b- mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat Med 23, 1454 - 1465.
dc.identifier.citedreferenceKajimura S, Spiegelman BM & Seale P ( 2015 ). Brown and beige fat: physiological roles beyond heat generation. Cell Metab 22, 546 - 559.
dc.identifier.citedreferenceKarastergiou K & Fried SK ( 2013 ). Multiple adipose depots increase cardiovascular risk via local and systemic effects. Curr Atheroscler Rep 15, 361.
dc.identifier.citedreferenceKarastergiou K & Fried SK ( 2017 ). Cellular mechanisms driving sex differences in adipose tissue biology and body shape in humans and mouse models. Adv Exp Med Biol 1043, 29 - 51.
dc.identifier.citedreferenceKarastergiou K, Smith SR, Greenberg AS & Fried SK ( 2012 ). Sex differences in human adipose tissues - the biology of pear shape. Biol Sex Differ 3, 13.
dc.identifier.citedreferenceKasza I, Adler D, Nelson DW, Eric Yen CL, Dumas S, Ntambi JM, MacDougald OA, Hernando D, Porter WP, Best FA & Alexander CM ( 2019 ). Evaporative cooling provides a major metabolic energy sink. Mol Metab 27, 47 - 61.
dc.identifier.citedreferenceKasza I, Hernando D, Roldan- Alzate A, Alexander CM & Reeder SB ( 2016 ). Thermogenic profiling using magnetic resonance imaging of dermal and other adipose tissues. JCI Insight 1, e87146.
dc.identifier.citedreferenceKasza I, Suh Y, Wollny D, Clark RJ, Roopra A, Colman RJ, MacDougald OA, Shedd TA, Nelson DW, Yen MI, Yen CL & Alexander CM ( 2014 ). Syndecan- 1 is required to maintain intradermal fat and prevent cold stress. PLoS Genet 10, e1004514.
dc.identifier.citedreferenceKazak L, Rahbani JF, Samborska B, Lu GZ, Jedrychowski MP, Lajoie M, Zhang S, Ramsay LC, Dou FY, Tenen D, Chouchani ET, Dzeja P, Watson IR, Tsai L, Rosen ED & Spiegelman BM ( 2019 ). Ablation of adipocyte creatine transport impairs thermogenesis and causes diet- induced obesity. Nat Metab 1, 360 - 370.
dc.identifier.citedreferenceKeipert S & Jastroch M ( 2014 ). Brite/beige fat and UCP1 - is it thermogenesis?. Biochim Biophys Acta 1837, 1075 - 1082.
dc.identifier.citedreferenceKeipert S, Lutter D, Schroeder BO, Brandt D, Stahlman M, Schwarzmayr T, Graf E, Fuchs H, de Angelis MH, Tschop MH, Rozman J & Jastroch M ( 2020 ). Endogenous FGF21- signaling controls paradoxical obesity resistance of UCP1- deficient mice. Nat Commun 11, 624.
dc.identifier.citedreferenceKelley DE, Thaete FL, Troost F, Huwe T & Goodpaster BH ( 2000 ). Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance. Am J Physiol Endocrinol Metab 278, E941 - E948.
dc.identifier.citedreferenceKern PA, Finlin BS, Zhu B, Rasouli N, McGehee RE, Jr., Westgate PM & Dupont- Versteegden EE ( 2014 ). The effects of temperature and seasons on subcutaneous white adipose tissue in humans: evidence for thermogenic gene induction. J Clin Endocrinol Metab 99, E2772 - E2779.
dc.identifier.citedreferenceKershaw EE & Flier JS ( 2004 ). Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89, 2548 - 2556.
dc.identifier.citedreferenceKruglikov IL & Scherer PE ( 2016a ). Dermal adipocytes and hair cycling: is spatial heterogeneity a characteristic feature of the dermal adipose tissue depot?. Exp Dermatol 25, 258 - 262.
dc.identifier.citedreferenceKruglikov IL & Scherer PE ( 2016b ). Dermal adipocytes: from irrelevance to metabolic targets?. Trends Endocrinol Metab 27, 1 - 10.
dc.identifier.citedreferenceKruse V, Neess D & Faergeman NJ ( 2017 ). The significance of epidermal lipid metabolism in whole- body physiology. Trends Endocrinol Metab 28, 669 - 683.
dc.working.doiNOen
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
tjp14623_am.pdf
Size:
3.942MB
Format:
PDF
View/Open
Name:
tjp14623.pdf
Size:
6.161MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.