Shifts of Immune Cell Populations Differ in Response to Different Effectors of Beige Remodeling of Adipose Tissue

Overview

Journal iScience

Publisher Cell Press

Date 2020 Dec 9

PMID 33294778

Citations 13

Authors

Nabil Rabhi

Anna C Belkina

Kathleen Desevin

Briana Noel Cortez

Stephen R Farmer

Affiliations

Soon will be listed here.

Abstract

White adipose tissue (WAT) is a dynamic tissue, which responds to environmental stimuli and dietary cues by changing its morphology and metabolic capacity. The ability of WAT to undergo a beige remodeling has become an appealing strategy to combat obesity and its comorbidities. Here, by using single-cell RNA sequencing, we provide a comprehensive atlas of the cellular dynamics during beige remodeling. We reveal drastic changes both in the overall cellular composition and transcriptional states of individual cell subtypes between Adrb3- and cold-induced beiging. Moreover, we demonstrate that cold induces a myeloid to lymphoid shift of the immune compartment compared to Adrb3 activation. Further analysis showed that, Adrb3 stimulation leads to activation of the interferon/Stat1 pathways favoring infiltration of myeloid immune cells, while repression of this pathway by cold promotes lymphoid immune cell recruitment. These findings highlight that pharmacological mimetics may not provide the same beneficial effects as physiological stimuli.

Citing Articles

Mesenchymal stromal cells as conductors of adipose tissue remodeling.

Cannavino J, Gupta R Genes Dev. 2023; 37(17-18):781-800.

PMID: 37798016 PMC: 10620058. DOI: 10.1101/gad.351069.123.

Cold-Induced Reprogramming of Subcutaneous White Adipose Tissue Assessed by Single-Cell and Single-Nucleus RNA Sequencing.

Liu Q, Long Q, Zhao J, Wu W, Lin Z, Sun W Research (Wash D C). 2023; 6:0182.

PMID: 37398933 PMC: 10308956. DOI: 10.34133/research.0182.

Thermogenic adipose tissue in energy regulation and metabolic health.

Xue S, Lee D, Berry D Front Endocrinol (Lausanne). 2023; 14:1150059.

PMID: 37020585 PMC: 10067564. DOI: 10.3389/fendo.2023.1150059.

Adipose tissue at single-cell resolution.

Maniyadath B, Zhang Q, Gupta R, Mandrup S Cell Metab. 2023; 35(3):386-413.

PMID: 36889280 PMC: 10027403. DOI: 10.1016/j.cmet.2023.02.002.

The Single-Cell Revelation of Thermogenic Adipose Tissue.

Qi Y, Hui X Mol Cells. 2022; 45(10):673-684.

PMID: 36254709 PMC: 9589375. DOI: 10.14348/molcells.2022.0092.

References

Rajbhandari P, Arneson D, Hart S, Ahn I, Diamante G, Santos L . Single cell analysis reveals immune cell-adipocyte crosstalk regulating the transcription of thermogenic adipocytes. Elife. 2019; 8. PMC: 6837845. DOI: 10.7554/eLife.49501. View

Naka T, Tsutsui H, Fujimoto M, Kawazoe Y, Kohzaki H, Morita Y . SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-gamma and IL-4 signaling in vivo. Immunity. 2001; 14(5):535-45. DOI: 10.1016/s1074-7613(01)00132-7. View

Cannon B, Nedergaard J . Brown adipose tissue: function and physiological significance. Physiol Rev. 2004; 84(1):277-359. DOI: 10.1152/physrev.00015.2003. View

Ravasi T, Suzuki H, Cannistraci C, Katayama S, Bajic V, Tan K . An atlas of combinatorial transcriptional regulation in mouse and man. Cell. 2010; 140(5):744-52. PMC: 2836267. DOI: 10.1016/j.cell.2010.01.044. View

Wahle M, Neumann R, Moritz F, Krause A, Buttgereit F, Baerwald C . Beta2-adrenergic receptors mediate the differential effects of catecholamines on cytokine production of PBMC. J Interferon Cytokine Res. 2005; 25(7):384-94. DOI: 10.1089/jir.2005.25.384. View

Patsouris D, Qi P, Abdullahi A, Stanojcic M, Chen P, Parousis A . Burn Induces Browning of the Subcutaneous White Adipose Tissue in Mice and Humans. Cell Rep. 2015; 13(8):1538-44. PMC: 4662886. DOI: 10.1016/j.celrep.2015.10.028. View

Hepler C, Shan B, Zhang Q, Henry G, Shao M, Vishvanath L . Identification of functionally distinct fibro-inflammatory and adipogenic stromal subpopulations in visceral adipose tissue of adult mice. Elife. 2018; 7. PMC: 6167054. DOI: 10.7554/eLife.39636. View

Sharp L, Shinoda K, Ohno H, Scheel D, Tomoda E, Ruiz L . Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One. 2012; 7(11):e49452. PMC: 3500293. DOI: 10.1371/journal.pone.0049452. View

Vishvanath L, MacPherson K, Hepler C, Wang Q, Shao M, Spurgin S . Pdgfrβ+ Mural Preadipocytes Contribute to Adipocyte Hyperplasia Induced by High-Fat-Diet Feeding and Prolonged Cold Exposure in Adult Mice. Cell Metab. 2015; 23(2):350-9. PMC: 4749445. DOI: 10.1016/j.cmet.2015.10.018. View

10.

Berbee J, Boon M, Khedoe P, Bartelt A, Schlein C, Worthmann A . Brown fat activation reduces hypercholesterolaemia and protects from atherosclerosis development. Nat Commun. 2015; 6:6356. PMC: 4366535. DOI: 10.1038/ncomms7356. View

11.

Su A, Wiltshire T, Batalov S, Lapp H, Ching K, Block D . A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A. 2004; 101(16):6062-7. PMC: 395923. DOI: 10.1073/pnas.0400782101. View

12.

Sun K, Kusminski C, Scherer P . Adipose tissue remodeling and obesity. J Clin Invest. 2011; 121(6):2094-101. PMC: 3104761. DOI: 10.1172/JCI45887. View

13.

Sidossis L, Porter C, Saraf M, Borsheim E, Radhakrishnan R, Chao T . Browning of Subcutaneous White Adipose Tissue in Humans after Severe Adrenergic Stress. Cell Metab. 2015; 22(2):219-27. PMC: 4541608. DOI: 10.1016/j.cmet.2015.06.022. View

14.

Eto H, Suga H, Matsumoto D, Inoue K, Aoi N, Kato H . Characterization of structure and cellular components of aspirated and excised adipose tissue. Plast Reconstr Surg. 2009; 124(4):1087-1097. DOI: 10.1097/PRS.0b013e3181b5a3f1. View

15.

Merrick D, Sakers A, Irgebay Z, Okada C, Calvert C, Morley M . Identification of a mesenchymal progenitor cell hierarchy in adipose tissue. Science. 2019; 364(6438). PMC: 6816238. DOI: 10.1126/science.aav2501. View

16.

Burl R, Ramseyer V, Rondini E, Pique-Regi R, Lee Y, Granneman J . Deconstructing Adipogenesis Induced by β3-Adrenergic Receptor Activation with Single-Cell Expression Profiling. Cell Metab. 2018; 28(2):300-309.e4. PMC: 6082711. DOI: 10.1016/j.cmet.2018.05.025. View

17.

Kahn C, Wang G, Lee K . Altered adipose tissue and adipocyte function in the pathogenesis of metabolic syndrome. J Clin Invest. 2019; 129(10):3990-4000. PMC: 6763230. DOI: 10.1172/JCI129187. View

18.

Petruzzelli M, Schweiger M, Schreiber R, Campos-Olivas R, Tsoli M, Allen J . A switch from white to brown fat increases energy expenditure in cancer-associated cachexia. Cell Metab. 2014; 20(3):433-47. DOI: 10.1016/j.cmet.2014.06.011. View

19.

Nguyen K, Qiu Y, Cui X, Goh Y, Mwangi J, David T . Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature. 2011; 480(7375):104-8. PMC: 3371761. DOI: 10.1038/nature10653. View

20.

Jeschke M, Gauglitz G, Kulp G, Finnerty C, Williams F, Kraft R . Long-term persistance of the pathophysiologic response to severe burn injury. PLoS One. 2011; 6(7):e21245. PMC: 3138751. DOI: 10.1371/journal.pone.0021245. View