B‐1a lymphocytes attenuate insulin resistance
Open accessAbstract
Obesity-associated insulin resistance, a common precursor of type 2 diabetes, is characterized by chronic inflammation of tissues, including visceral adipose tissue (VAT). Here we show that B-1a cells, a subpopulation of B lymphocytes, are novel and important regulators of this process. B-1a cells are reduced in frequency in obese high-fat diet (HFD)-fed mice, and EGFP interleukin-10 (IL-10) reporter mice show marked reductions in anti-inflammatory IL-10 production by B cells in vivo during obesity. In VAT, B-1a cells are the dominant producers of B cell–derived IL-10, contributing nearly half of the expressed IL-10 in vivo. Adoptive transfer of B-1a cells into HFD-fed B cell–deficient mice rapidly improves insulin resistance and glucose tolerance through IL-10 and polyclonal IgM-dependent mechanisms, whereas transfer of B-2 cells worsens metabolic disease. Genetic knockdown of B cell–activating factor (BAFF) in HFD-fed mice or treatment with a B-2 cell–depleting, B-1a cell–sparing anti-BAFF antibody attenuates insulin resistance. These findings establish B-1a cells as a new class of immune regulators that maintain metabolic homeostasis and suggest manipulation of these cells as a potential therapy for insulin resistance.
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In mice fed a high-fat diet, adipose tissue B1 cells ameliorate disease attributable to their production of IL-10 and polyclonal IgM.
“In mice fed an HFD, adipose tissue B1 cells ameliorate disease attributable to their production of IL‐10 and polyclonal IgM( 51 ); however, a role for B1 cells in adipose tissue is yet to be confirmed in humans.”
From The Emerging Role of B Cells in the Pathogenesis of NAFLD (2021) · cites this paper as [51]
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Obesity is associated with macrophage accumulation in adipose tissue
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319246 · Cited by 10,041 · see citing works
Global estimates of the prevalence of diabetes for 2010 and 2030
Shaw, J. E., Sicree, R. A., & Zimmet, P. Z. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2009.10.007 · Cited by 7,216 · see citing works
Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319451 · Cited by 6,760 · see citing works
Obesity induces a phenotypic switch in adipose tissue macrophage polarization
Lumeng, C. N., Bodzin, J. L., & Saltiel, A. R. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29881 · Cited by 4,664 · see citing works
Hotamisligil, G. S., Peraldi, P., Budavari, A., Ellis, R., White, M. F., & Spiegelman, B. M. (1996) · Science · doi:10.1126/science.271.5249.665 · Cited by 2,630 · see citing works
Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Greenberg, A. S., & Obin, M. S. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500294-jlr200 · Cited by 2,529 · see citing works
Macrophage-specific PPARγ controls alternative activation and improves insulin resistance
Odegaard, J. I., Ricardo-Gonzalez, R. R., Goforth, M. H., Morel, C. R., Subramanian, V., Mukundan, L., Eagle, A. R., Vats, D., Brombacher, F., Ferrante, A. W., et al. (2007) · Nature · doi:10.1038/nature05894 · Cited by 2,107 · cited 1× · see citing works
“This finding is interesting, because several studies have intimately linked classically activated M1 macrophages with IR (10,31,39).”
BackgroundB cells regulate autoimmunity by provision of IL-10
Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D., & Anderton, S. M. (2002) · Nature Immunology · doi:10.1038/ni833 · Cited by 1,647 · see citing works
Fried, S. K., Bunkin, D. A., & Greenberg, A. S. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.3.4660 · Cited by 1,528 · see citing works
Normalization of obesity-associated insulin resistance through immunotherapy
Winer, S., Chan, Y., Paltser, G., Truong, D., Tsui, H., Bahrami, J., Dorfman, R., Wang, Y., Zielenski, J., Mastronardi, F., et al. (2009) · Nature Medicine · doi:10.1038/nm.2001 · Cited by 1,370 · see citing works
Self-citationMacrophage-mediated inflammation in metabolic disease
Chawla, A., Nguyen, K. D., & Goh, Y. P. S. (2011) · Nature reviews. Immunology · doi:10.1038/nri3071 · Cited by 1,314 · see citing works
Fried, S. K. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.3.847 · Cited by 1,146 · see citing works
PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells
Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S. E., Benoist, C., & Mathis, D. (2012) · Nature · doi:10.1038/nature11132 · Cited by 1,143 · see citing works
An Essential Role for BAFF in the Normal Development of B Cells Through a BCMA-Independent Pathway
Schiemann, B. J., Gommerman, J. L., Vora, K. A., Cachero, T. G., Shulga‐Morskaya, S., Dobles, M., Frew, E. M., & Scott, M. L. (2001) · Science · doi:10.1126/science.1061964 · Cited by 1,070 · see citing works
Winer, D. A., Winer, S., Shen, L., Wadia, P. P., Yantha, J., Paltser, G., Tsui, H., Wu, P., Davidson, M. G., Alonso, M. N., et al. (2011) · Nature Medicine · doi:10.1038/nm.2353 · Cited by 1,050 · see citing works
Self-citationThe double life of a B-1 cell: self-reactivity selects for protective effector functions
Baumgarth, N. (2011) · Nature Reviews Immunology · doi:10.1038/nri2901 · Cited by 969 · see citing works
Prevention of Arthritis by Interleukin 10–producing B Cells
Mauri, C., Gray, D., Mushtaq, N., & Londei, M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021293 · Cited by 858 · see citing works
Shaw, P. X., Hörkkö, S., Chang, M.-K., Curtiss, L. K., Palinski, W., Silverman, G. J., & Witztum, J. L. (2000) · Journal of Clinical Investigation · doi:10.1172/jci8472 · Cited by 674 · see citing works
Progenitors for Ly-1 B cells are distinct from progenitors for other B cells.
Hayakawa, K., Hardy, R. R., Herzenberg, L. A., & Herzenberg, L. A. (1985) · The Journal of Experimental Medicine · doi:10.1084/jem.161.6.1554 · Cited by 614 · see citing works
DeFuria, J., Belkina, A. C., Jagannathan-Bogdan, M., Snyder-Cappione, J., Carr, J. D., Nersesova, Y. R., Markham, D., Strissel, K. J., Watkins, A. A., Zhu, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215840110 · Cited by 521 · see citing works
Rosenfeld, M. E., Palinski, W., Ylä‐Herttuala, S., Butler, S. S., & Witztum, J. L. (1990) · Arteriosclerosis An Official Journal of the American Heart Association Inc · doi:10.1161/01.atv.10.3.336 · Cited by 474 · see citing works
Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans
Chou, M.-Y., Fogelstrand, L., Hartvigsen, K., Hansen, L. F., Woelkers, D., Shaw, P. X., Choi, J., Perkmann, T., Bäckhed, F., Miller, Y. I., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci36800 · Cited by 468 · see citing works
The half-lives of serum immunoglobulins in adult mice
Vieira, P., & Rajewsky, K. (1988) · European Journal of Immunology · doi:10.1002/eji.1830180221 · Cited by 449 · see citing works
Hong, E., Ko, H. J., Cho, Y.-R., Kim, H., Ma, Z., Yu, T. Y., Friedline, R. H., Kurt‐Jones, E. A., Finberg, R. W., Fischer, M. A., et al. (2009) · Diabetes · doi:10.2337/db08-1261 · Cited by 412 · see citing works
Aron‐Wisnewsky, J., Tordjman, J., Poitou, C., Darakhshan, F., Hugol, D., Basdevant, A., Aissat, A., Guerre-Millo, M., & Clément, K. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0925 · Cited by 379 · see citing works
Kyaw, T. S., Tay, C., Krishnamurthi, S., Kanellakis, P., Agrotis, A., Tipping, P. G., Bobik, A., & Toh, B. (2011) · Circulation Research · doi:10.1161/circresaha.111.248542 · Cited by 333 · see citing works
Enhanced B-1 Cell Development, But Impaired IgG Antibody Responses in Mice Deficient in Secreted IgM
Boes, M. L., Esau, C., Fischer, M. B., Schmidt, T., Carroll, M. C., & Chen, J. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.10.4776 · Cited by 323 · see citing works
Baumgarth, N., Herman, O. C., Jager, G. C., Brown, L. E., Herzenberg, L. A., & Herzenberg, L. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2250 · Cited by 320 · see citing works
Nonredundant Roles for B Cell-Derived IL-10 in Immune Counter-Regulation
Madan, R., Demircik, F., Surianarayanan, S., Allen, J. L., Divanovic, S., Trompette, A., Yogev, N., Gu, Y., Khodoun, M. V., Hildeman, D. A., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900185 · Cited by 295 · see citing works
Adipose natural regulatory B cells negatively control adipose tissue inflammation
Nishimura, S., Manabe, I., Takaki, S., Nagasaki, M., Otsu, M., Yamashita, H., Sugita, J., Yoshimura, K., Eto, K., Komuro, I., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.09.017 · Cited by 251 · see citing works
IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity
Ricardo-González, R. R., Eagle, A. R., Odegaard, J. I., Jouihan, H. A., Morel, C. R., Heredia, J. E., Mukundan, L., Wu, D., Locksley, R. M., & Chawla, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009152108 · Cited by 251 · see citing works
Schultz, O., Oberhauser, F., Saech, J., Rubbert-Roth, A., Hahn, M., Krone, W., & Laudes, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014328 · Cited by 244 · see citing works
Intestinal reperfusion injury is mediated by IgM and complement
Williams, J. P., Pechet, T. T. V., Weiser, M. R., Reid, R. R., Kobzik, L., Moore, F. D., Carroll, M. C., & Hechtman, H. B. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.86.3.938 · Cited by 240 · see citing works
Chen, Y., Park, Y., Patel, E. S., & Silverman, G. J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0804191 · Cited by 221 · see citing works
Kyaw, T. S., Tay, C., Hosseini, H., Kanellakis, P., Gadowski, T., Mackay, F., Tipping, P. G., Bobik, A., & Toh, B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029371 · Cited by 185 · see citing works
Macrophage polarization to a unique phenotype driven by B cells
Wong, S. C., Puaux, A., Chittezhath, M., Shalova, I. N., Kajiji, T., Wang, X., Abastado, J., Lam, K., & Biswas, S. K. (2010) · European Journal of Immunology · doi:10.1002/eji.200940288 · Cited by 184 · see citing works
Faria‐Neto, J. R., Chyu, K., Li, X., Dimayuga, P. C., Ferreira, C., Yano, J., Cercek, B., & Shah, P. K. (2006) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.11.033 · Cited by 182 · see citing works
BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact
Scholz, J. L., Crowley, J. E., Tomayko, M. M., Steinel, N. C., O'Neill, P. J., Quinn, W. J., Goenka, R., Miller, J. P., Cho, Y. H., Long, V., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807841105 · Cited by 179 · see citing works
Natural IgM in Immune Equilibrium and Harnessing Their Therapeutic Potential
Kaveri, S. V., Silverman, G. J., & Bayry, J. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102107 · Cited by 150 · see citing works
Griffin, D. O., & Rothstein, T. L. (2012) · Molecular Medicine · doi:10.2119/molmed.2012.00203 · Cited by 99 · see citing works
Wood, I. S., Wang, B., Jenkins, J. R., & Trayhurn, P. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.09.068 · Cited by 94 · see citing works
Popi, A. F., Lopes, J. D., & Mariano, M. (2004) · Immunology · doi:10.1111/j.1365-2567.2004.01969.x · Cited by 87 · see citing works
McLaughlin, T., Deng, A. C., Gonzales, O., Aillaud, M., Yee, G., Lamendola, C. A., Abbasi, F., Connolly, A. J., Sherman, A., Cushman, S. W., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1148-z · Cited by 67 · see citing works
B Cell‐Activating Factor Controls the Production of Adipokines and Induces Insulin Resistance
Hamada, M., Abe, M., Miyake, T., Kawasaki, K., Tada, F., Furukawa, S., Matsuura, B., Hiasa, Y., & Onji, M. (2011) · Obesity · doi:10.1038/oby.2011.165 · Cited by 49 · see citing works
B-1 cells temper endotoxemic inflammatory responses
Barbeiro, D. F., Barbeiro, H. V., Faintuch, J., Ariga, S. K. K., Mariano, M., Popi, A. F., de Souza, H. P., Velasco, I. T., & Soriano, F. G. (2010) · Immunobiology · doi:10.1016/j.imbio.2010.08.002 · Cited by 45 · see citing works
The Road From Obesity to Type 2 Diabetes
Ioannidis, I. (2008) · Angiology · doi:10.1177/0003319708318583 · Cited by 38 · see citing works
Kawasaki, K., Abe, M., Tada, F., Tokumoto, Y., Chen, S., Miyake, T., Furukawa, S., Matsuura, B., Hiasa, Y., & Onji, M. (2013) · Laboratory Investigation · doi:10.1038/labinvest.2012.176 · Cited by 36 · see citing works
Glucose impairs B-1 cell function in diabetes
Jennbacken, K., Ståhlman, S., Grahnemo, L., Wiklund, O., & Fogelstrand, L. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12148 · Cited by 35 · see citing works
Activation of adipose tissue macrophages in obese mice does not require lymphocytes
Behan, J. W., Ehsanipour, E. A., Sheng, X., Pramanik, R., Wang, X., Hsieh, Y., Kim, Y., & Mittelman, S. D. (2013) · Obesity · doi:10.1002/oby.20159 · Cited by 27 · see citing works
Ab initio study of MKr n 2+ (M = Cu, Ag, and Au, n = 1-6) clusters
Li, X. (2011) · Journal of Molecular Modeling · doi:10.1007/s00894-011-1138-9 · Cited by 18 · see citing works
Müller, N., Schulte, D. M., Hillebrand, S., Türk, K., Hampe, J., Schafmayer, C., Brosch, M., Schönfels, W. V., Ahrens, M., Zeuner, R. A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094282 · Cited by 11 · see citing works
Flagged first, then by citations
2 of the 53 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Adapting to obesity with adipose tissue inflammation
Reilly, S. M., & Saltiel, A. R. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2017.90 · Cited by 1,204 · see citing works
Metabolic Inflammation and Insulin Resistance in Obesity
Wu, H., & Ballantyne, C. M. (2020) · Circulation Research · doi:10.1161/circresaha.119.315896 · Cited by 1,059 · see citing works
Obesity, Inflammation, and Immune System in Osteoarthritis
Nedunchezhiyan, U., Varughese, I., Sun, A. R., Wu, X., Crawford, R., & Prasadam, I. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.907750 · Cited by 487 · see citing works
Role of innate and adaptive immunity in obesity-associated metabolic disease
McLaughlin, T., Ackerman, S. E., Shen, L., & Engleman, E. G. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88876 · Cited by 444 · see citing works
Self-citationImmunosuppressive Mechanisms of Regulatory B Cells
Catalán, D., Mansilla, M. A., Ferrier, A., Soto, L., Oļeiņika, K., Aguillón, J. C., & Aravena, O. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.611795 · Cited by 407 · see citing works
Karczewski, J., Śledzińska, E., Baturo, A., Jończyk, I., Maleszko, A., Maleszko, A., Samborski, P., Krasińska, B., & Dobrowolska, A. (2018) · European Cytokine Network · doi:10.1684/ecn.2018.0415 · Cited by 315 · see citing works
White adipose tissue dysfunction in obesity and aging
Reyes-Farias, M., Fos-Domenech, J., Serra, D., Herrero, L., & Sánchez-Infantes, D. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114723 · Cited by 250 · see citing works
Camell, C. D., Günther, P. S., Lee, A., Goldberg, E. L., Spadaro, O., Youm, Y., Bartke, A., Hubbard, G. B., Ikeno, Y., Ruddle, N. H., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.10.006 · Cited by 215 · see citing works
Barrow, F., Khan, S., Fredrickson, G., Wang, H., Dietsche, K., Parthiban, P., Robert, S., Kaiser, T., Winer, S., Herman, A., et al. (2021) · Hepatology · doi:10.1002/hep.31755 · Cited by 210 · see citing works
Self-citationGut-associated IgA+ immune cells regulate obesity-related insulin resistance
Luck, H., Khan, S. M., Kim, J. H., Copeland, J. K., Revelo, X. S., Tsai, S. J., Chakraborty, M., Cheng, K., Chan, Y. T., Nøhr, M. K., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11370-y · Cited by 204 · see citing works
Self-citationSzukiewicz, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129818 · Cited by 208 · see citing works
Commensal bacteria contribute to insulin resistance in aging by activating innate B1a cells
Bodogai, M., O’Connell, J., Kim, K., Kim, Y., Moritoh, K., Chen, C., Gusev, F., Vaughan, K., Shulzhenko, N., Mattison, J. A., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aat4271 · Cited by 182 · see citing works
Adipose Tissue Inflammation in the Pathogenesis of Type 2 Diabetes
Kohlgruber, A. C., & Lynch, L. (2015) · Current Diabetes Reports · doi:10.1007/s11892-015-0670-x · Cited by 157 · see citing works
Emerging concepts in intestinal immune control of obesity-related metabolic disease
Khan, S. M., Luck, H., Winer, S., & Winer, D. A. (2021) · Nature Communications · doi:10.1038/s41467-021-22727-7 · Cited by 151 · see citing works
Self-citationImmune and non-immune functions of adipose tissue leukocytes
Trim, W. V., & Lynch, L. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00635-7 · Cited by 147 · see citing works
Calvo, S. S.-C., Bharath, L. P., Pugh, G. H., SantaCruz-Calvo, L., Lenin, R. R., Lutshumba, J., Liu, R., Bachstetter, A. D., Zhu, B., & Nikolajczyk, B. S. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00575-1 · Cited by 141 · see citing works
Kosaraju, R., Guesdon, W., Crouch, M. J., Teague, H., Sullivan, E. M., Karlsson, E. A., Schultz‐Cherry, S., Gowdy, K. M., Bridges, L. C., Reese, L., et al. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601031 · Cited by 136 · see citing works
The Emerging Role of B Cells in the Pathogenesis of NAFLD
Barrow, F., Khan, S., Wang, H., & Revelo, X. S. (2021) · Hepatology · doi:10.1002/hep.31889 · Cited by 126 · see citing works
The Immune Landscape of Visceral Adipose Tissue During Obesity and Aging
Khan, S. M., Chan, Y. T., Revelo, X. S., & Winer, D. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00267 · Cited by 126 · see citing works
Self-citationHarmon, D. B., Srikakulapu, P., Kaplan, J. L., Oldham, S. N., McSkimming, C. C., Garmey, J. C., Perry, H. M., Kirby, J. L., Prohaska, T. A., Gonen, A., et al. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.116.307166 · Cited by 123 · see citing works
Type 2 Diabetes: How Much of an Autoimmune Disease?
de Candia, P., Prattichizzo, F., Garavelli, S., Rosa, V. D., Galgani, M., Rella, F. D., Spagnuolo, M. I., Colamatteo, A., Fusco, C., Micillo, T., et al. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00451 · Cited by 118 · see citing works
Wu, L., Dalal, R., Cao, C. D., Postoak, J. L., Yang, G., Zhang, Q., Wang, Z., Lal, H., & Kaer, L. V. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911464116 · Cited by 115 · see citing works
B Lymphocytes and Adipose Tissue Inflammation
Srikakulapu, P., & McNamara, C. A. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.312467 · Cited by 106 · see citing works
T-bet+ B cells accumulate in adipose tissue and exacerbate metabolic disorder during obesity
Hägglöf, T., Vanz, C., Kumagai, A., Dudley, E. A., Ortega, V., Siller, M., Parthasarathy, R., Keegan, J., Koenigs, A., Shute, T. J., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.07.002 · Cited by 88 · see citing works
Bojadzic, D., & Buchwald, P. (2018) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026618666180531092503 · Cited by 81 · see citing works
Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
Pindjáková, J., Sartini, C., Re, O. L., Rappa, F., Coupé, B., Lelouvier, B., Pazienza, V., & Vinciguerra, M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01157 · Cited by 81 · see citing works
AlZaim, I., Hammoud, S. H., Al-Koussa, H., Ghazi, A., Eid, A. H., & EL‐Yazbi, A. F. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.602088 · Cited by 76 · see citing works
Zhang, F., Jiang, W. W., Li, X., Qiu, X. Y., Wu, Z., Chi, Y. J., Cong, X., & Liu, Y. L. (2016) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12362 · Cited by 57 · see citing works
TRPV1: A Potential Therapeutic Target in Type 2 Diabetes and Comorbidities?
Gram, D. X., Holst, J. J., & SZALLASI, A. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.09.005 · Cited by 52 · see citing works
Caro-Gómez, E., Sierra, J. A., Escobar, J. S., Álvarez, R., Naranjo, M., Medina, S., Velásquez-Mejía, E. P., Tabares-Guevara, J. H., Jaramillo, J. C., León-Varela, Y. M., et al. (2019) · Nutrients · doi:10.3390/nu11030497 · Cited by 51 · see citing works
IgM Plasma Cells Reside in Healthy Skin and Accumulate with Chronic Inflammation
Wilson, R. P., McGettigan, S. E., Dang, V. D., Kumar, A., Cancro, M. P., Nikbakht, N., Stohl, W., & Debes, G. F. (2019) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2019.05.009 · Cited by 50 · see citing works
B cell contribution to immunometabolic dysfunction and impaired immune responses in obesity
Oļeiņika, K., Šlisere, B., Catalán, D., & Rosser, E. C. (2022) · Clinical & Experimental Immunology · doi:10.1093/cei/uxac079 · Cited by 52 · see citing works
Kien, C. L., Bunn, J. Y., Fukagawa, N. K., Anathy, V., Matthews, D. E., Crain, K. I., Ebenstein, D. B., Tarleton, E. K., Pratley, R. E., & Poynter, M. E. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.07.014 · Cited by 42 · see citing works
Chatzigeorgiou, A., & Chavakis, T. (2016) · Handbook of Experimental Pharmacology · doi:10.1007/164_2015_8 · Cited by 48 · see citing works
Circulating inflammatory cell profiling and periodontitis: A systematic review and meta-analysis
Irwandi, R. A., Kuswandani, S. O., Harden, S., Marletta, D., & D’Aiuto, F. (2022) · Journal of Leukocyte Biology · doi:10.1002/jlb.5ru1021-524r · Cited by 40 · see citing works
Adaptive Immunity and Antigen‐Specific Activation in Obesity‐Associated Insulin Resistance
Chng, M. H. Y., Alonso, M. N., Barnes, S. E., Nguyen, K. D., & Engleman, E. G. (2015) · Mediators of Inflammation · doi:10.1155/2015/593075 · Cited by 39 · see citing works
Self-citationOrchestration of the Adipose Tissue Immune Landscape by Adipocytes
Bradley, D. P., Deng, T., Shantaram, D., & Hsueh, W. A. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042222-024353 · Cited by 38 · see citing works
Interaction between IgA and gut microbiota and its role in controlling metabolic syndrome
Guo, J., Han, X., Huang, W., You, Y., & Zhan, J. (2020) · Obesity Reviews · doi:10.1111/obr.13155 · Cited by 37 · see citing works
Yang, Z., Chen, F., Zhang, Y., Ou, M., Tan, P., Xu, X., Li, Q., & Zhou, S. (2024) · MedComm · doi:10.1002/mco2.560 · Cited by 35 · see citing works
Carter, S., Miard, S., Caron, A., Sallé-Lefort, S., St‐Pierre, P., Anhê, F. F., Lavoie-Charland, É., Blais‐Lecours, P., Drolet, M., Lefebvre, J. S., et al. (2018) · Diabetes · doi:10.2337/db17-0558 · Cited by 35 · see citing works
Nakamura, Y., Abe, M., Kawasaki, K., Miyake, T., Watanabe, T., Yoshida, O., Hirooka, M., Matsuura, B., & Hiasa, Y. (2019) · Scientific Reports · doi:10.1038/s41598-018-37403-y · Cited by 34 · see citing works
Dwaib, H. S., AlZaim, I., Eid, A. H., Obeid, O., & EL‐Yazbi, A. F. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.626313 · Cited by 32 · see citing works
Tanigaki, K., Chambliss, K. L., Yuhanna, I. S., Sacharidou, A., Ahmed, M. H., Atochin, D. N., Huang, P. L., Shaul, P. W., & Mineo, C. (2016) · Diabetes · doi:10.2337/db15-1605 · Cited by 26 · see citing works
Amyloid fibrils activate B-1a lymphocytes to ameliorate inflammatory brain disease
Kurnellas, M. P., Ghosn, E., Schartner, J., Baker, J., Rothbard, J. J., Negrin, R. S., Herzenberg, L., Fathman, C., Steinman, L., & Rothbard, J. (2015) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1521206112 · Cited by 23 · see citing works
Immunopathology of adipose tissue during metabolic syndrome
Ghazarian, M., Luck, H., Revelo, X. S., Winer, S., & Winer, D. A. (2015) · Turkish Journal of Pathology · doi:10.5146/tjpath.2015.01323 · Cited by 23 · see citing works
Self-citationT cells accumulate in non-diabetic islets during ageing
Denroche, H. C., Miard, S., Sallé-Lefort, S., Picard, F., & Verchere, C. B. (2021) · Immunity & Ageing · doi:10.1186/s12979-021-00221-4 · Cited by 22 · see citing works
B Cell–Activating Factor Antagonism Attenuates the Growth of Experimental Abdominal Aortic Aneurysm
Spinosa, M., Montgomery, W. G., Lempicki, M. D., Srikakulapu, P., Johnsrude, M. J., McNamara, C. A., Upchurch, G. R., Ailawadi, G., Leitinger, N., & Meher, A. K. (2021) · American Journal Of Pathology · doi:10.1016/j.ajpath.2021.08.012 · Cited by 23 · see citing works
Exploring the Interplay between Fatty Acids, Inflammation, and Type 2 Diabetes
Nicholas, D., Mbongue, J. C., Garcia-Pérez, D., Sorensen, D. W., Bennit, H. R. F., León, M. A. D., & Langridge, W. H. R. (2024) · Immuno · doi:10.3390/immuno4010006 · Cited by 22 · see citing works
Olson, N. C., Doyle, M. F., Sitlani, C. M., de Boer, I. H., Rich, S. S., Huber, S. A., LANDAY, A. L., Tracy, R. P., Psaty, B. M., & Delaney, J. A. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa036 · Cited by 22 · see citing works
Adipose tissue lymphocytes and obesity
Gao, F., Litchfield, B., & Wu, H. (2023) · The Journal of Cardiovascular Aging · doi:10.20517/jca.2023.38 · Cited by 21 · see citing works
Deng, C., Xiang, Y., Tan, T., Ren, Z., Cao, C., Liu, B., Huang, G., Wang, X., & Zhou, Z. (2017) · Journal of Diabetes Research · doi:10.1155/2017/5052812 · Cited by 19 · see citing works
Role of antigen presentation in the production of pro-inflammatory cytokines in obese adipose tissue
Majdoubi, A., Kishta, O. A., & Thibodeau, J. (2016) · Cytokine · doi:10.1016/j.cyto.2016.01.023 · Cited by 19 · see citing works
Méndez-Frausto, G., Romero-Aguilera, G., Sánchez-Gutiérrez, R., García-Jacobo, R. E., Lara-Ramirez, E. E., Uresti‐Rivera, E. E., González‐Amaro, R., Enciso‐Moreno, J. A., & García-Hernández, M. H. (2021) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2021.108692 · Cited by 18 · see citing works
B cells in non-lymphoid tissues
Samiea, A., Celis, G., Yadav, R., Rodda, L. B., & Moreau, J. M. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01137-6 · Cited by 18 · see citing works
Neuroimmune regulation of white adipose tissues
Qian, X., Meng, X., Zhang, S., & Zeng, W. (2021) · FEBS Journal · doi:10.1111/febs.16213 · Cited by 16 · see citing works
Liu, W., Liu, T., Zhao, Q., Ma, J., Jiang, J., & Shi, H. (2023) · Stem Cells International · doi:10.1155/2023/9517826 · Cited by 19 · see citing works
Adaptive Immunity and Metabolic Health: Harmony Becomes Dissonant in Obesity and Aging
Bharath, L. P., Ip, B. C., & Nikolajczyk, B. S. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160042 · Cited by 17 · see citing works
Daley, A. D., & Bénézech, C. (2024) · Immunological Reviews · doi:10.1111/imr.13339 · Cited by 22 · see citing works
Similarities and Distinctions in the Effects of Metformin and Carbon Monoxide in Immunometabolism.
Park, J., Joe, Y., Ryter, S. W., Surh, Y., & Chung, H. (2019) · PubMed Central · doi:10.14348/molcells.2019.0016 · Cited by 16 · see citing works
Immunomodulation by helminths: Similar impact on type 1 and type 2 diabetes?
Surendar, J., Indulekha, K., Hoerauf, A. M., & Hübner, M. P. (2016) · Parasite Immunology · doi:10.1111/pim.12401 · Cited by 15 · see citing works
Wang, M., Zhou, M., Tan, Q., Yu, L., Dong, C., Liang, R., Liu, W., Zhang, Y., Li, M., Nie, X., et al. (2023) · Environmental Pollution · doi:10.1016/j.envpol.2023.121833 · Cited by 12 · see citing works
Noncanonical B Cells: Characteristics of Uncharacteristic B Cells
Haas, K. M. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200944 · Cited by 12 · see citing works
Pattarabanjird, T., Nguyen, A. T., McSkimming, C. C., Dinh, H. Q., Marshall, M. A., Ghosheh, Y., Gulati, R., Durant, C., Vallejo, J., Saigusa, R., et al. (2023) · Nature Cardiovascular Research · doi:10.1038/s44161-023-00356-1 · Cited by 11 · see citing works
Meher, A. K., & McNamara, C. A. (2024) · Immunological Reviews · doi:10.1111/imr.13342 · Cited by 11 · see citing works
Tipping the Scale: Atheroprotective IgM-Producing B Cells in Atherosclerosis
Ransegnola, B. P., Pattarabanjird, T., & McNamara, C. A. (2024) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.124.319847 · Cited by 11 · see citing works
Impact of obesity and SARS-CoV-2 infection: implications for host defence - a living review
Richter, F. C., Alrubayyi, A., Crespo, A. T., & Hulin-Curtis, S. L. (2021) · Oxford Open Immunology · doi:10.1093/oxfimm/iqab001 · Cited by 11 · see citing works
Immune activation induced by dysregulated lipid metabolism in the pathogenesis of type 2 diabetes
Yang, H., Yu, W., Mao, Q., & Zhao, L. (2025) · World Journal of Diabetes · doi:10.4239/wjd.v16.i12.114395 · Cited by 11 · see citing works
Klein, M., & Varga, I. (2018) · Inflammation · doi:10.1007/s10753-018-0798-3 · Cited by 10 · see citing works
Lempicki, M. D., Gray, J. A., Abuna, G. F., Murata, R. M., Divanovic, S., McNamara, C. A., & Meher, A. K. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1436900 · Cited by 9 · see citing works
The relationship between Schistosoma and glycolipid metabolism
Cai, Z., Deng, X., Zhao, L., Wang, X., Yang, L., & Yuan, G. (2021) · Microbial Pathogenesis · doi:10.1016/j.micpath.2021.105120 · Cited by 9 · see citing works
Teague, H., Harris, M., Whelan, J. T., Comstock, S. S., Fenton, J. I., & Shaikh, S. R. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.09.012 · Cited by 9 · see citing works
Immune cells in adipose tissue microenvironment under physiological and obese conditions
Jiang, Y., & Gong, F. (2023) · Endocrine · doi:10.1007/s12020-023-03521-5 · Cited by 8 · see citing works
Ho, P.-Y., Koh, Y., Lu, T., Liao, P., & Pan, M. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.3c05678 · Cited by 8 · see citing works
Obesity-associated Inflammation and Alloimmunity
Zhou, H., Gizlenci, M., Xiao, Y., Martin, F., Nakamori, K., Zicari, E. M., Sato, Y., & Tullius, S. G. (2024) · Transplantation · doi:10.1097/tp.0000000000005183 · Cited by 7 · see citing works
Helix-Loop-Helix Factor Id3 (Inhibitor of Differentiation 3)
Misiou, A., Garmey, J. C., Hensien, J. M., Harmon, D. B., Osinski, V., McSkimming, C. C., Marshall, M. A., Fischer, J. W., Grandoch, M., & McNamara, C. A. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.315588 · Cited by 6 · see citing works
The B side of B cells in NAFLD
Barrow, F., & Revelo, X. S. (2022) · Hepatology · doi:10.1002/hep.32481 · Cited by 6 · see citing works
Han, M., Wang, J., Guo, S., Zhu, H., Zhao, L., Wu, Z., Wu, Y., Guo, J., Liao, J., & Tang, Z. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.10.070 · Cited by 5 · see citing works
Weight and organ specific immune cell profiling of sleeve gastrectomy in mice
Harris, D. A., Subramaniam, R., Brenner, T. A., Tavakkoli, A., & Sheu, E. G. (2021) · Metabolism · doi:10.1016/j.metabol.2021.154729 · Cited by 5 · see citing works
Adipose tissue regulatory T cells: differentiation and function
Fooks, A. N., Beppu, L. Y., Frias, A. B., & D’Cruz, L. M. (2022) · International Reviews of Immunology · doi:10.1080/08830185.2022.2044808 · Cited by 5 · see citing works
Ashikawa, S., Komatsu, Y., Kawai, Y., Aoyama, K., Nakano, S., Cui, X., Hayakawa, M., Sakabe, N., Furukawa, N., Ikeda, K., et al. (2022) · Physiological Reports · doi:10.14814/phy2.15165 · Cited by 3 · see citing works
Adaptive Immunity and Metabolic Health: Harmony Becomes Dissonant in Obesity and Aging
Bharath, L. P., Ip, B. C., & Nikolajczyk, B. S. (2017) · Comprehensive physiology · doi:10.1002/j.2040-4603.2017.tb00780.x · Cited by 4 · see citing works
The Role of B Lymphocyte Subsets in Adipose Tissue Development, Metabolism, and Aging
Fernandez, N. C., & Shinoda, K. (2022) · Comprehensive physiology · doi:10.1002/cphy.c220006 · Cited by 4 · see citing works
Puente-Ruiz, S. C., Ide, L., Schuller, J., Ben-Kraiem, A., Hoffmann, A., Ghosh, A., Noé, F., Wolfrum, C., Krause, K., Gericke, M. T., et al. (2025) · iScience · doi:10.1016/j.isci.2025.112819 · Cited by 3 · see citing works
Shruthi, S., Mohan, V., Maradana, M. R., & Aravindhan, V. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.01.198 · Cited by 3 · see citing works
Mikame, M., Tsuno, N. H., Miura, Y., Kitazaki, H., Uchimura, D., Miyagi, T., Miyazaki, T., Onodera, T., Ohashi, W., Kameda, T., et al. (2023) · Immunohematology · doi:10.2478/immunohematology-2023-023 · Cited by 3 · see citing works
Ho, P.-Y., Lin, P., Koh, Y., Lin, W., Tang, K., Chen, Y., Weerawatanakorn, M., & Pan, M. (2024) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202400604 · Cited by 4 · see citing works
Interaction between adipocytes and B lymphocytes in human metabolic diseases
Stasevich, E. M., Zheremyan, E. A., Kuprash, D. V., & Schwartz, A. M. (2023) · Biochemistry (Moscow) · doi:10.31857/s0320972523020124 · Cited by 2 · see citing works
Zhao, B.-H., Yuan, T., Zhao, L., Ruze, A., Li, Q., Deng, A.-X., Hu, S., & Gao, X.-M. (2025) · BMJ Open · doi:10.1136/bmjopen-2025-099750 · Cited by 2 · see citing works
Geng, T., Feng, M., Wang, K., Wang, H., Gu, T., Hu, X., Li, J., Wang, H., Qi, S., Shangguan, W., et al. (2025) · The FASEB Journal · doi:10.1096/fj.202501027rr · Cited by 2 · see citing works
Obesity disrupts ILC2 metabolic and functional homeostasis by inhibiting mTORC1 signaling
Hu, L., Wang, D., Chen, Y., Qiu, J., Wang, H., Zhang, Y., Zhang, M. H., Su, X., Qiu, J., Sun, J., et al. (2026) · Cellular and Molecular Immunology · doi:10.1038/s41423-026-01389-9 · Cited by 2 · see citing works
Self-citationB1a Cell-IgM Axis Protects Against Hypertension by Blunting IFNγ+CD4+T Cells
Chen, X.-H., Lin, J., Zhang, Z.-B., Li, J.-Q., Chen, D.-R., Zhai, Y.-H., Xu, L., Guzik, T. J., & Gao, P. (2026) · Circulation Research · doi:10.1161/circresaha.125.328062 · Cited by 2 · see citing works
The Immunology of Adipose Tissue
Revelo, X. S., Luck, H., Winer, S., & Winer, D. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-374279-7.19008-3 · Cited by 2 · see citing works
Self-citationAging induces Nlrp3 inflammasome dependent adipose B cell expansion to impair metabolic homeostasisPreprint
Camell, C. D., Lee, A., Günther, P. S., Goldberg, E. L., Spadaro, O., Youm, Y., Bartke, A., Hubbard, G. B., Ikeno, Y., Ruddle, N. H., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/607192 · Cited by 2 · see citing works
Calvo, S. S.-C., SantaCruz-Calvo, L., & Nikolajczyk, B. S. (2020) · Immunometabolism · doi:10.20900/immunometab20200011 · Cited by 2 · see citing works
Interaction Between Adipocytes and B Lymphocytes in Human Metabolic Diseases
Stasevich, E. M., Zheremyan, E. A., Kuprash, D. V., & Schwartz, A. M. (2023) · Biochemistry (Moscow) · doi:10.1134/s0006297923020104 · Cited by 1 · see citing works
Yin, Y., Zhao, C., Hua, Y., Yang, F., Qiu, D., Yan, J., & Jin, X. (2025) · BioData Mining · doi:10.1186/s13040-025-00472-7 · Cited by 1 · see citing works
Bone marrow rewired: Trained immunity and clonal hematopoiesis in metabolic disease
Chronopoulos, J., Hajishengallis, G., & Chavakis, T. (2026) · Metabolism · doi:10.1016/j.metabol.2026.156603 · Cited by 2 · see citing works
The Role of B Lymphocyte Subsets in Adipose Tissue Development, Metabolism, and Aging
Fernandez, N. C., & Shinoda, K. (2022) · Comprehensive physiology · doi:10.1002/j.2040-4603.2022.tb00243.x · Cited by 1 · see citing works
The Role of the Intestinal Immune System in Diet-induced Obesity and Insulin Resistance
Luck, H. (2020) · TSpace (University of Toronto)
Berzofsky, J. A. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.734431272.793569295
- Authors
- Shen, L., Chng, M. H. Y., Alonso, M. N., Yuan, R., Winer, D. A., & Engleman, E. G.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Stanford Medicine (US)
- University Health Network (CA)
- Corresponding author
- Winer, Daniel A.
- Engleman, Edgar G.
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2014-09-22
- Volume
- 64
- Issue
- 2
- Pages
- 593-603
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC4303967
- OpenAlex
- W2105987065
- Cited by
- 109
- References
- 53
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 10 · 2023: 11 · 2022: 9 · 2021: 16 · 2020: 10 · 2019: 11 · 2018: 5 · 2017: 8 · 2016: 6 · 2015: 7
- FWCI
- 5.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Diabetes Association (119414, CS-5-12-3886, OG-3-12-3844)
- National Institutes of Health (1R01DK096038)
- Canadian Institutes of Health Research (119414)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- insulin resistance, obesity, type 2 diabetes, visceral adipose tissue, IL-10, BAFF, high-fat diet, glucose tolerance, adoptive transfer, B cell-deficient mice, anti-inflammatory regulation, metabolic homeostasis
- MeSH terms
- Animals, Blood Glucose, Dietary Fats, Female, Gene Expression Regulation, Humans, Immunoglobulin M, Insulin Resistance, Male, Mice, Inbred C57BL, Middle Aged, Obesity, B-Lymphocyte Subsets, Interleukin-10, Glucose Intolerance, Mice
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