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Cited by 171Adipose Tissue and MetabolismAdipokines, Inflammation, and Metabolic DiseasesCardiovascular Disease and Adiposity

Cellular heterogeneity in adipose tissues

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Corvera, Silvia·2021·Annual Review of Physiology
DOI 10.1146/annurev-physiol-031620-095446PMC PMC8091658
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Abstract

Adipose tissue depots in distinct anatomical locations mediate key aspects of metabolism, including energy storage, nutrient release, and thermogenesis. Although adipocytes make up more than 90% of adipose tissue volume, they represent less than 50% of its cellular content. Here, I review recent advances in genetic lineage tracing and transcriptomics that reveal the identities of the heterogeneous cell populations constituting mouse and human adipose tissues. In addition to mature adipocytes and their progenitors, these include endothelial and various immune cell types that together orchestrate adipose tissue development and functions. One salient finding is the identification of progenitor subtypes that can modulate adipogenic capacity through paracrine mechanisms. Another is the description of fate trajectories of monocyte/macrophages, which can respond maladaptively to nutritional and thermogenic stimuli, leading to metabolic disease. These studies have generated an extraordinary source of publicly available data that can be leveraged to explore commonalities and differences among experimental models, providing new insights into adipose tissues and their role in metabolic disease.

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  • In obesity, adipose tissue undergoes significant remodeling, expanding substantially to enhance storage capacity, orchestrated by diverse cell types including adipocytes, preadipocytes, endothelial cells, and immune cells.

    “In obesity, adipose tissue undergoes a significant remodeling process, expanding substantially to enhance its storage capacity. This process is orchestrated through coordinated actions among diverse cell types, including adipocytes, preadipocytes, endothelial cells, and various immune cells (Corvera, 2021).”

    From Robust single-nucleus RNA sequencing reveals depot-specific cell population dynamics in adipose tissue remodeling during obesity (2025) · cites this paper as Corvera, 2021

    The Introduction identifies adipocytes as energy-storing cells, and the section on morphological and functional evidence describes white adipose tissue storing energy through adipocyte hypertrophy. The progenitor, endothelial-cell, and immune-cell sections document these cell types and changes associated with obesogenic diets. They do not establish that coordinated action among all four cell types drives substantial expansion specifically to increase storage capacity in obesity; page numbers are unavailable in our copy. (LLM, conf=0.84)

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  1. [1]Ottaviani E, Malagoli D, Franceschi C. 2011. The evolution of the adipose tissue: a neglected enigma. Gen. Comp. Endocrinol. 174: 1– 4 21781968
  2. [2]Gesta S, Tseng YH, Kahn CR. 2007. Developmental origin of fat: tracking obesity to its source. Cell 131: 242– 56 17956727
  3. [3]Gimble J, Guilak F. 2003. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5: 362– 69 14578098
  4. [4]Yamamoto N, Akamatsu H, Hasegawa S, Yamada T, Nakata S, 2007. Isolation of multipotent stem cells from mouse adipose tissue. J. Dermatol. Sci. 48: 43– 52 17644316
  5. [5]Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, 2001. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7: 211– 28 11304456
  6. [6]Ferrante AW Jr. 2013. Macrophages, fat, and the emergence of immunometabolism. J. Clin. Investig. 123: 4992– 93 24292661 PMC3859415
  7. [7]Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Investig. 112: 1796– 808 14679176 PMC296995
  8. [8]Eto H, Suga H, Matsumoto D, Inoue K, Aoi N, 2009. Characterization of structure and cellular components of aspirated and excised adipose tissue. Plast. Reconstr. Surg. 124: 1087– 97 19935292
  9. [9]Chen G, Ning B, Shi T. 2019. Single-cell RNA-seq technologies and related computational data analysis. Front. Genet. 10: 317 31024627 PMC6460256
  10. [10]Efremova M, Vento-Tormo R, Park JE, Teichmann SA, James KR. 2020. Immunology in the era of single-cell technologies. Annu. Rev. Immunol. 38: 727– 57 32075461
  11. [11]Natarajan KN, Miao Z, Jiang M, Huang X, Zhou H, 2019. Comparative analysis of sequencing technologies for single-cell transcriptomics. Genome Biol. 20: 70 30961669 PMC6454680
  12. [12]Shinde P, Mohan L, Kumar A, Dey K, Maddi A, 2018. Current trends of microfluidic single-cell technologies. Int. J. Mol. Sci. 19: 3143 PMC6213733 30322072
  13. [15]Napolitano L, Gagne HT. 1963. Lipid-depleted white adipose cells: an electron microscope study. Anat. Rec. 147: 273– 93 14065939
  14. [16]Napolitano L, McNary JE, Kloep LP. 1965. The release of free fatty acids from brown and white adipose tissues after incubation with ACTH or epinephrine. Metabolism 14: 1076– 83 4284423
  15. [17]Napolitano LM. 1965. Observations on the fine structure of adipose cells. Ann. N. Y. Acad. Sci. 131: 34– 42 5216974
  16. [18]Slavin BG, Ballard KW. 1978. Morphological studies on the adrenergic innervation of white adipose tissue. Anat. Rec. 191: 377– 89 677491
  17. [19]Alexander G, Stevens D. 1980. Sympathetic innervation and the development of structure and function of brown adipose tissue: studies on lambs chemically sympathectomized in utero with 6-hydroxydopamine. J. Dev. Physiol. 2: 119– 37 7204907
  18. [20]Davis V 1980. The structure and function of brown adipose tissue in the neonate. J. Obstet. Gynecol. Neonatal Nurs. 9: 368– 72 6906468
  19. [21]Hausman GJ, Richardson RL. 1983. Cellular and vascular development in immature rat adipose tissue. J. Lipid Res. 24: 522– 32 6875377
  20. [22]Pond CM, Mattacks CA. 1985. Cellular structure of adipose tissue in birds. J. Morphol. 185: 195– 202 29969869
  21. [23]Marchington JM, Mattacks CA, Pond CM. 1989. Adipose tissue in the mammalian heart and pericardium: structure, foetal development and biochemical properties. Comp. Biochem. Physiol. B 94: 225– 32 2591189
  22. [24]Cinti S 1999. Adipose tissues and obesity. Ital. J. Anat. Embryol. 104: 37– 51 10450668
  23. [25]Suter ER. 1969. The fine structure of brown adipose tissue. I. Cold-induced changes in the rat. J. Ultra- struct. Res. 26: 216– 41 5776618
  24. [26]Salans LB, Dougherty JW. 1971. The effect of insulin upon glucose metabolism by adipose cells of different size. Influence of cell lipid and protein content, age, and nutritional state. J. Clin. Investig. 50: 1399– 410 5090056 PMC292078
  25. [27]Gliemann J, Vinten J. 1974. Lipogenesis and insulin sensitivity of single fat cells. J. Physiol. 236: 499– 516 4362702 PMC1350846
  26. [28]Varlamov O, Somwar R, Cornea A, Kievit P, Grove KL, Roberts CT Jr. 2010. Single-cell analysis of insulin-regulated fatty acid uptake in adipocytes. Am. J. Physiol. Endocrinol. Metab. 299: E486– 96 20570821 PMC2944284
  27. [29]Hagberg CE, Li Q, Kutschke M, Bhowmick D, Kiss E, 2018. Flow cytometry of mouse and human adipocytes for the analysis of browning and cellular heterogeneity. Cell Rep. 24: 2746– 56.e5 30184507 PMC6137819
  28. [30]Sanchez-Gurmaches J, Guertin DA. 2014. Adipocytes arise from multiple lineages that are heterogeneously and dynamically distributed. Nat. Commun. 5: 4099 24942009 PMC4066194
  29. [31]Chi J, Wu Z, Choi CHJ, Nguyen L, Tegegne S, 2018. Three-dimensional adipose tissue imaging reveals regional variation in beige fat biogenesis and PRDM16-dependent sympathetic neurite density. Cell Metab. 27: 226– 36.e3 29320703
  30. [32]Ebke LA, Nestor-Kalinoski AL, Slotterbeck BD, Al-Dieri AG, Ghosh-Lester S, 2014. Tight association between macrophages and adipocytes in obesity: implications for adipocyte preparation. Obesity 22: 1246– 55 24376179 PMC3980195
  31. [33]Tran KV, Gealekman O, Frontini A, Zingaretti MC, Morroni M, 2012. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 15: 222– 29 22326223 PMC3278718
  32. [34]Rajbhandari P, Arneson D, Hart SK, Ahn IS, Diamante G, 2019. Single cell analysis reveals immune cell–adipocyte crosstalk regulating the transcription of thermogenic adipocytes. eLife 8: e49501 31644425 PMC6837845
  33. [35]Janke J, Engeli S, Gorzelniak K, Luft FC, Sharma AM. 2002. Mature adipocytes inhibit in vitro differentiation of human preadipocytes via angiotensin type 1 receptors. Diabetes 51: 1699– 707 12031955
  34. [36]Min SY, Kady J, Nam M, Rojas-Rodriguez R, Berkenwald A, 2016. Human ‘brite/beige’ adipocytes develop from capillary networks, and their implantation improves metabolic homeostasis in mice. Nat. Med. 22: 312– 18 26808348 PMC4777633
  35. [37]Rojas-Rodriguez R, Lujan-Hernandez J, Min SY, DeSouza T, Teebagy P, 2019. Generation of functional human adipose tissue in mice from primed progenitor cells. Tissue Eng. A 25: 842– 54 PMC6590775 30306830
  36. [38]Song A, Dai W, Jang MJ, Medrano L, Li Z, 2020. Low- and high-thermogenic brown adipocyte subpopulations coexist in murine adipose tissue. J. Clin. Investig. 130: 247– 57 31573981 PMC6934193
  37. [39]Lee KY, Luong Q, Sharma R, Dreyfuss JM, Ussar S, Kahn CR. 2019. Developmental and functional heterogeneity of white adipocytes within a single fat depot. EMBO J. 38: e99291 30530479 PMC6356065
  38. [41]Czech MP. 2020. Mechanisms of insulin resistance related to white, beige, and brown adipocytes. Mol. Metab. 34: 27– 42 32180558 PMC6997501
  39. [42]Spaethling JM, Sanchez-Alavez M, Lee J, Xia FC, Dueck H, 2016. Single-cell transcriptomics and functional target validation of brown adipocytes show their complex roles in metabolic homeostasis. FASEB J. 30: 81– 92 26304220
  40. [43]Kazak L, Chouchani ET, Jedrychowski MP, Erickson BK, Shinoda K, 2015. A creatine-driven substrate cycle enhances energy expenditure and thermogenesis in beige fat. Cell 163: 643– 55 26496606 PMC4656041
  41. [44]Kazak L, Chouchani ET, Lu GZ, Jedrychowski MP, Bare CJ, 2017. Genetic depletion of adipocyte creatine metabolism inhibits diet-induced thermogenesis and drives obesity. Cell Metab. 26: 660– 71.e3 28844881 PMC5629120
  42. [45]Sun W, Dong H, Balaz M, Slyper M, Drokhlyansky E, 2020. Single-nucleus RNA-Seq reveals a new type of brown adipocyte regulating thermogenesis. bioRxiv 2020.01.20.890327. 10.1101/2020.01.20.890327 · DOI
  43. [47]Wu H, Kirita Y, Donnelly EL, Humphreys BD. 2019. Advantages of single-nucleus over single-cell RNA sequencing of adult kidney: rare cell types and novel cell states revealed in fibrosis. J. Am. Soc. Nephrol. 30: 23– 32 30510133 PMC6317600
  44. [48]Roesler A, Kazak L. 2020. UCP1-independent thermogenesis. Biochem. J. 477: 709– 25 32059055
  45. [49]Ikeda K, Kang Q, Yoneshiro T, Camporez JP, Maki H, 2017. UCP1-independent signaling involving SERCA2b-mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat. Med. 23: 1454– 65 29131158 PMC5727902
  46. [50]Zheng B, Cao B, Li G, Huard J. 2006. Mouse adipose–derived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng. 12: 1891– 901 16889519
  47. [51]Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, 2008. White fat progenitor cells reside in the adipose vasculature. Science 322: 583– 86 18801968 PMC2597101
  48. [52]Rodeheffer MS, Birsoy K, Friedman JM. 2008. Identification of white adipocyte progenitor cells in vivo. Cell 135: 240– 49 18835024
  49. [53]Smith NC, Fairbridge NA, Pallegar NK, Christian SL. 2015. Dynamic upregulation of CD24 in pre-adipocytes promotes adipogenesis. Adipocyte 4: 89– 100 26167413 PMC4496983
  50. [55]Min SY, Desai A, Yang Z, Sharma A, DeSouza T, 2019. Diverse repertoire of human adipocyte subtypes develops from transcriptionally distinct mesenchymal progenitor cells. PNAS 116: 17970– 79 31420514 PMC6731669
  51. [56]Burl RB, Ramseyer VD, Rondini EA, Pique-Regi R, Lee YH, Granneman JG. 2018. Deconstructing adipogenesis induced by β3-adrenergic receptor activation with single-cell expression profiling. Cell Metab. 28: 300– 9.e4 29937373 PMC6082711
  52. [58]Rennert RC, Januszyk M, Sorkin M, Rodrigues M, Maan ZN, 2016. Microfluidic single–cell transcriptional analysis rationally identifies novel surface marker profiles to enhance cell-based therapies. Nat. Commun. 7: 11945 27324848 PMC5512622
  53. [59]Hepler C, Shan B, Zhang Q, Henry GH, Shao M, 2018. Identification of functionally distinct fibro-inflammatory and adipogenic stromal subpopulations in visceral adipose tissue of adult mice. eLife 7: e39636 30265241 PMC6167054
  54. [60]Vishvanath L, MacPherson KA, Hepler C, Wang QA, Shao M, 2016. Pdgfrβ+ mural preadipocytes contribute to adipocyte hyperplasia induced by high-fat-diet feeding and prolonged cold exposure in adult mice. Cell Metab. 23: 350– 59 26626462 PMC4749445
  55. [61]Marcelin G, Ferreira A, Liu Y, Atlan M, Aron-Wisnewsky J, 2017. A PDGFRα-mediated switch toward CD9high adipocyte progenitors controls obesity-induced adipose tissue fibrosis. Cell Metab. 25: 673– 85 28215843
  56. [62]Kim YJ, Yu JM, Joo HJ, Kim HK, Cho HH, 2007. Role of CD9 in proliferation and proangiogenic action of human adipose-derived mesenchymal stem cells. Pflügers Arch. 455: 283– 96 17668233
  57. [63]Cho DS, Lee B, Doles JD. 2019. Refining the adipose progenitor cell landscape in healthy and obese visceral adipose tissue using single-cell gene expression profiling. Life Sci. Alliance 2. 10.26508/lsa.201900561 PMC6878222 31767614 · DOI
  58. [64]Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, 2002. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 13: 4279– 95 12475952 PMC138633
  59. [65]Schaffler A, Buchler C. 2007. Concise review: adipose tissue–derived stromal cells—basic and clinical implications for novel cell-based therapies. Stem Cells 25: 818– 27 17420225
  60. [66]Osathanon T, Subbalekha K, Sastravaha P, Pavasant P. 2012. Notch signalling inhibits the adipogenic differentiation of single-cell-derived mesenchymal stem cell clones isolated from human adipose tissue. Cell Biol. Int. 36: 1161– 70 22974058
  61. [67]Acosta JR, Joost S, Karlsson K, Ehrlund A, Li X, 2017. Single cell transcriptomics suggest that human adipocyte progenitor cells constitute a homogeneous cell population. Stem Cell Res. Ther. 8: 250 29116032 PMC5678572
  62. [68]Vijay J, Gauthier MF, Biswell RL, Louiselle DA, Johnston JJ, 2020. Single-cell analysis of human adipose tissue identifies depot and disease specific cell types. Nat. Metab. 2: 97– 109 32066997 PMC7025882
  63. [69]Tchkonia T, Lenburg M, Thomou T, Giorgadze N, Frampton G, 2007. Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. Endocrinol. Metab. 292: E298– 307 16985259
  64. [70]Zhang Z, Shao M, Hepler C, Zi Z, Zhao S, 2019. Dermal adipose tissue has high plasticity and undergoes reversible dedifferentiation in mice. J. Clin. Investig. 129: 5327– 42 31503545 PMC6877341
  65. [71]Maurizi G, Poloni A, Mattiucci D, Santi S, Maurizi A, 2017. Human white adipocytes convert into “rainbow” adipocytes in vitro. J. Cell Physiol. 232: 2887– 99 27987321
  66. [72]Wolock SL, Krishnan I, Tenen DE, Matkins V, Camacho V, 2019. Mapping distinct bone marrow niche populations and their differentiation paths. Cell Rep. 28: 302– 11.e5 31291568 PMC6684313
  67. [73]Zhong L, Yao L, Tower RJ, Wei Y, Miao Z, 2020. Single cell transcriptomics identifies a unique adipose lineage cell population that regulates bone marrow environment. eLife 9: e54695 32286228 PMC7220380
  68. [74]Baccin C, Al-Sabah J, Velten L, Helbling PM, Grunschlager F, 2020. Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat. Cell Biol. 22: 38– 48 31871321 PMC7610809
  69. [75]Chang L, Milton H, Eitzman DT, Chen YE. 2013. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ. J. 77: 11– 18 23207957
  70. [76]Chang L, Villacorta L, Li R, Hamblin M, Xu W, 2012. Loss of perivascular adipose tissue on peroxisome proliferator-activated receptor-gamma deletion in smooth muscle cells impairs intravascular thermoregulation and enhances atherosclerosis. Circulation 126: 1067– 78 22855570 PMC3493564
  71. [77]Gu W, Nowak WN, Xie Y, Le Bras A, Hu Y, 2019. Single-cell RNA-sequencing and metabolomics analyses reveal the contribution of perivascular adipose tissue stem cells to vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 39: 2049– 66 31340667 PMC6766361
  72. [78]Pan XX, Ruan CC, Liu XY, Kong LR, Ma Y, 2019. Perivascular adipose tissue-derived stromal cells contribute to vascular remodeling during aging. Aging Cell 18: e12969 31087498 PMC6612678
  73. [79]Tran KV, Fitzgibbons T, Min SY, DeSouza T, Corvera S. 2018. Distinct adipocyte progenitor cells are associated with regional phenotypes of perivascular aortic fat in mice. Mol. Metab. 9: 199– 206 29396370 PMC5869733
  74. [80]Lindhorst A, Bechmann I, Gericke M. 2020. Unspecific DNA recombination in AdipoqCre–ERT2-mediated knockout approaches in transgenic mice is sex-, age- and genotype-dependent. Adipocyte 9: 1– 6 31842670 PMC6959310
  75. [81]Jiang Y, Berry DC, Jo A, Tang W, Arpke RW, 2017. A PPARγ transcriptional cascade directs adipose progenitor cell-niche interaction and niche expansion. Nat. Commun. 8: 15926 28649987 PMC5490270
  76. [82]Park J, Kim M, Sun K, An YA, Gu X, Scherer PE. 2017. VEGF-A-expressing adipose tissue shows rapid beiging and enhanced survival after transplantation and confers IL-4-independent metabolic improvements. Diabetes 66: 1479– 90 28254844 PMC5440018
  77. [83]Hill DA, Lim HW, Kim YH, Ho WY, Foong YH, 2018. Distinct macrophage populations direct inflammatory versus physiological changes in adipose tissue. PNAS 115: E5096– 105 29760084 PMC5984532
  78. [84]Sharma M, Schlegel M, Brown EJ, Sansbury BE, Weinstock A, 2019. Netrin-1 alters adipose tissue macrophage fate and function in obesity. Immunometabolism 1: e190010 31428465 PMC6699780
  79. [86]Weinstock A, Brown EJ, Garabedian ML, Pena S, Sharma M, 2019. Single-cell RNA sequencing of visceral adipose tissue leukocytes reveals that caloric restriction following obesity promotes the accumulation of a distinct macrophage population with features of phagocytic cells. Immunometabolism 1: e190008 31396408 PMC6687332
  80. [87]Li C, Menoret A, Farragher C, Ouyang Z, Bonin C, 2019. Single cell transcriptomics-based Mac–Spectrum reveals novel macrophage activation signatures in diseases. JCI Insight 5: e126453 PMC6542613 30990466
  81. [88]Liu LF, Craig CM, Tolentino LL, Choi O, Morton J, 2017. Adipose tissue macrophages impair preadipocyte differentiation in humans. PLOS ONE 12: e0170728 28151993 PMC5289462
  82. [89]Cipolletta D, Kolodin D, Benoist C, Mathis D. 2011. Tissular T(regs): a unique population of adipose-tissue-resident Foxp3+CD4+ T cells that impacts organismal metabolism. Semin. Immunol. 23: 431– 37 21724410
  83. [90]Vasanthakumar A, Chisanga D, Blume J, Gloury R, Britt K, 2020. Sex-specific adipose tissue imprinting of regulatory T cells. Nature 579: 581– 85 32103173 PMC7241647
  84. [91]Kalin S, Becker M, Ott VB, Serr I, Hosp F, 2017. A Stat6/Pten axis links regulatory T cells with adipose tissue function. Cell Metab. 26: 475– 92.e7 28877454 PMC5627977
  85. [92]Setiady YY, Coccia JA, Park PU. 2010. In vivo depletion of CD4+FOXP3+ Treg cells by the PC61 anti-CD25 monoclonal antibody is mediated by FcγRIII+ phagocytes. Eur. J. Immunol. 40: 780– 86 20039297
  86. [93]Crewe C, Joffin N, Rutkowski JM, Kim M, Zhang F, 2018. An endothelial-to-adipocyte extracellular vesicle axis governed by metabolic state. Cell 175: 695– 708.e13 30293865 PMC6195477
  87. [94]Romacho T, Sell H, Indrakusuma I, Roehrborn D, Castaneda TR, 2020. DPP4 deletion in adipose tissue improves hepatic insulin sensitivity in diet-induced obesity. Am. J. Physiol. Endocrinol. Metab. 318: E590– 99 31891536
  88. [95]Zhong J, Rao X, Rajagopalan S. 2013. An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis 226: 305– 14 23083681
  89. [96]Glastonbury CA, Couto Alves A, El-Sayed Moustafa JS, Small KS. 2019. Cell-type heterogeneity in adipose tissue is associated with complex traits and reveals disease-relevant cell-specific eQTLs. Am. J. Hum. Genet. 104: 1013– 24 31130283 PMC6556877

Authors
Corvera, S.
Affiliations
University of Massachusetts Chan Medical School (US)
Corresponding author
Corvera, Silvia
ORCID
Corvera, Silvia
Venue
Annual Review of Physiology
Publisher
Annual Reviews
Published
2021-02-10
Volume
83
Issue
1
Pages
257-278
ISSN
  • 0066-4278 (ISSN-L)
  • 1545-1585
DOI
10.1146/annurev-physiol-031620-095446
PMC
PMC8091658
OpenAlex
W3126946264
Cited by
171
References
98
Citations by year
2026: 31 · 2025: 39 · 2024: 37 · 2023: 34 · 2022: 24 · 2021: 6
FWCI
3.40
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Physiology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK089101, R01DK123028)
Topics
  • Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
  • Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
Keywords
adipose tissue, cellular heterogeneity, adipocytes, adipose tissue development, endothelial cells, immune cells, paracrine signaling, thermogenesis, energy storage, metabolic disorders, lineage tracing, transcriptomics
MeSH terms
Adipose Tissue, Animals, Humans, Adipocytes, Thermogenesis, Adipogenesis

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