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Interaction Between Adipocytes and B Lymphocytes in Human Metabolic Diseases

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Abstract

Diseases associated with the disorders of carbohydrate and lipid metabolism are widespread in the modern world. Interaction between the cells of adipose tissue – adipocytes – and immune system cells is an essential factor in pathogenesis of such diseases. Long-term increase in the glucose and fatty acid levels leads to adipocyte hypertrophy and increased expression of pro-inflammatory cytokines and adipokines by these cells. As a result, immune cells acquire a pro-inflammatory phenotype, and new leukocytes are recruited. Inflammation of adipose tissue leads to insulin resistance and stimulates formation of atherosclerotic plaques and development of autoimmunity. New studies show that different groups of B lymphocytes play an essential role in regulation of adipose tissue inflammation. Decrease in the number of B-2 lymphocytes suppresses development of a number of metabolic diseases, whereas decreased numbers of the regulatory B lymphocytes and B-1 lymphocytes are associated with more severe pathology. Recent studies showed that adipocytes influence B lymphocyte activity both directly and by altering activity of other immune cells. These findings provide better understanding of the molecular mechanisms of human pathologies associated with impaired carbohydrate and lipid metabolism, such as type 2 diabetes mellitus.

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Abbreviations

AT:

adipose tissue

IFNγ:

interferon gamma

IL:

interleukin

TGFβ:

transforming growth factor beta

TNF:

tumor necrosis factor

References

  1. Shen, H., Kreisel, D., and Goldstein, D. R. (2013) Processes of sterile inflammation, J. Immunol., 191, 2857-2863, https://doi.org/10.4049/jimmunol.1301539.

    Article  CAS  PubMed  Google Scholar 

  2. Srikakulapu, P., and McNamara, C. A. (2020) B lymphocytes and adipose tissue inflammation, Arterioscler. Thromb. Vasc. Biol., 40, 1110-1122, https://doi.org/10.1161/ATVBAHA.119.312467.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Song, J., and Deng, T. (2020) The adipocyte and adaptive immunity, Front. Immunol., 11, 593058, https://doi.org/10.3389/fimmu.2020.593058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Frühbeck, G. (2008) Overview of adipose tissue and its role in obesity and metabolic disorders, Methods Mol. Biol., 456, 1-22, https://doi.org/10.1007/978-1-59745-245-8_1.

    Article  PubMed  Google Scholar 

  5. Ansel, K. M., Harris, R. B. S., and Cyster, J. G. (2002) CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity, Immunity, 16, 67-76, https://doi.org/10.1016/S1074-7613(01)00257-6.

    Article  CAS  PubMed  Google Scholar 

  6. Benoit, M., Desnues, B., and Mege, J.-L. (2008) Macrophage polarization in bacterial infections, J. Immunol., 181, 3733-3739, https://doi.org/10.4049/jimmunol.181.6.3733.

    Article  CAS  PubMed  Google Scholar 

  7. Mancuso, P. (2016) The role of adipokines in chronic inflammation, ImmunoTargets Ther., 5, 47-56, https://doi.org/10.2147/ITT.S73223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wong, S.-C., Puaux, A.-L., Chittezhath, M., Shalova, I., Kajiji, T. S., Wang, X., et al. (2010) Macrophage polarization to a unique phenotype driven by B cells, Eur. J. Immunol., 40, 2296-2307, https://doi.org/10.1002/eji.200940288.

    Article  CAS  PubMed  Google Scholar 

  9. Harmon, D. B., Srikakulapu, P., Kaplan, J. L., Oldham, S. N., McSkimming, C., Garmey, J. C., et al. (2016) Protective role for B-1b B cells and IgM in obesity-associated inflammation, glucose intolerance, and insulin resistance, Arterioscler. Thromb. Vasc. Biol., 36, 682-691, https://doi.org/10.1161/ATVBAHA.116.307166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Miller, Y. I., Choi, S.-H., Wiesner, P., Fang, L., Harkewicz, R., Hartvigsen, K., et al. (2011) Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity, Circ. Res., 108, 235-248, https://doi.org/10.1161/CIRCRESAHA.110.223875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Srikakulapu, P., Upadhye, A., Drago, F., Perry, H. M., Bontha, S. V., McSkimming, C., et al. (2021) Chemokine receptor-6 promotes B-1 cell trafficking to perivascular adipose tissue, local IgM production and atheroprotection, Front. Immunol., 12, 636013, https://doi.org/10.3389/fimmu.2021.636013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ying, W., Wollam, J., Ofrecio, J. M., Bandyopadhyay, G., El Ouarrat, D., Lee, Y. S., et al. (2017) Adipose tissue B2 cells promote insulin resistance through leukotriene LTB4/LTB4R1 signaling, J. Clin. Invest., 127, 1019-1030, https://doi.org/10.1172/JCI90350.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Werz, O., Gerstmeier, J., Libreros, S., De la Rosa, X., Werner, M., Norris, P. C., et al. (2018) Human macrophages differentially produce specific resolvin or leukotriene signals that depend on bacterial pathogenicity, Nat. Commun., 9, 59, https://doi.org/10.1038/s41467-017-02538-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. DeFuria, J., Belkina, A. C., Jagannathan-Bogdan, M., Snyder-Cappione, J., Carr, J. D., Nersesova, Y. R., et al. (2013) B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile, Proc. Natl. Acad. Sci. USA, 110, 5133-5138, https://doi.org/10.1073/pnas.1215840110.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhai, X., Qian, G., Wang, Y., Chen, X., Lu, J., Zhang, Y., et al. (2016) Elevated B cell activation is associated with type 2 diabetes development in obese subjects, Cell. Physiol. Biochem., 38, 1257-1266, https://doi.org/10.1159/000443073.

    Article  CAS  PubMed  Google Scholar 

  16. Arkatkar, T., Du, S. W., Jacobs, H. M., Dam, E. M., Hou, B., Buckner, J. H., et al. (2017) B cell-derived IL-6 initiates spontaneous germinal center formation during systemic autoimmunity, J. Exp. Med., 214, 3207-3217, https://doi.org/10.1084/jem.20170580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wueest, S., Laesser, C. I., Böni-Schnetzler, M., Item, F., Lucchini, F. C., Borsigova, M., et al. (2018) IL-6-type cytokine signaling in adipocytes induces intestinal GLP-1 secretion, Diabetes, 67, 36-45, https://doi.org/10.2337/db17-0637.

    Article  CAS  PubMed  Google Scholar 

  18. Akbari, M., and Hassan-Zadeh, V. (2018) IL-6 signalling pathways and the development of type 2 diabetes, Inflammopharmacology, 26, 685-698, https://doi.org/10.1007/s10787-018-0458-0.

    Article  CAS  PubMed  Google Scholar 

  19. Gómez-Touriño, I., Camiña-Darriba, F., Otero-Romero, I., Rodríguez, M. A., Hernández-Fernández, A., González-Fernández, A., et al. (2010) Autoantibodies to glial fibrillary acid protein and S100beta in diabetic patients, Diabet. Med., 27, 246-248, https://doi.org/10.1111/j.1464-5491.2009.02911.x.

    Article  CAS  PubMed  Google Scholar 

  20. Pietropaolo, M., Barinas-Mitchell, E., Pietropaolo, S. L., Kuller, L. H., and Trucco, M. (2000) Evidence of islet cell autoimmunity in elderly patients with type 2 diabetes, Diabetes, 49, 32-38, https://doi.org/10.2337/diabetes.49.1.32.

    Article  CAS  PubMed  Google Scholar 

  21. Turner, R., Stratton, I., Horton, V., Manley, S., Zimmet, P., Mackay, I. R., et al. (1997) UKPDS 25: autoantibodies to islet-cell cytoplasm and glutamic acid decarboxylase for prediction of insulin requirement in type 2 diabetes. UK Prospective Diabetes Study Group, Lancet (London, England), 350, 1288-1293, https://doi.org/10.1016/S0140-6736(97)03062-6.

    Article  CAS  PubMed  Google Scholar 

  22. Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R. S., and Bhan, A. K. (2002) Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation, Immunity, 16, 219-230, https://doi.org/10.1016/S1074-7613(02)00274-1.

    Article  CAS  PubMed  Google Scholar 

  23. Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D., and Anderton, S. M. (2002) B cells regulate autoimmunity by provision of IL-10, Nat. Immunol., 3, 944-950, https://doi.org/10.1038/ni833.

    Article  CAS  PubMed  Google Scholar 

  24. Tian, J., Zekzer, D., Hanssen, L., Lu, Y., Olcott, A., and Kaufman, D. L. (2001) Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice, J. Immunol., 167, 1081-1089, https://doi.org/10.4049/jimmunol.167.2.1081.

    Article  CAS  PubMed  Google Scholar 

  25. Parekh, V. V., Prasad, D. V. R., Banerjee, P. P., Joshi, B. N., Kumar, A., and Mishra, G. C. (2003) B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1, J. Immunol., 170, 5897-5911, https://doi.org/10.4049/jimmunol.170.12.5897.

    Article  CAS  PubMed  Google Scholar 

  26. Wang, R.-X., Yu, C.-R., Dambuza, I. M., Mahdi, R. M., Dolinska, M. B., Sergeev, Y. V., et al. (2014) Interleukin-35 induces regulatory B cells that suppress autoimmune disease, Nat. Med., 20, 633-641, https://doi.org/10.1038/nm.3554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Asadullah, K., Sterry, W., and Volk, H. D. (2003) Interleukin-10 therapy – review of a new approach, Pharmacol. Rev., 55, 241-269, https://doi.org/10.1124/pr.55.2.4.

    Article  CAS  PubMed  Google Scholar 

  28. Shang, J., Zha, H., and Sun, Y. (2020) Phenotypes, functions, and clinical relevance of regulatory B cells in cancer, Front. Immunol., 11, 582657, https://doi.org/10.3389/fimmu.2020.582657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jansen, K., Cevhertas, L., Ma, S., Satitsuksanoa, P., Akdis, M., and van de Veen, W. (2021) Regulatory B cells, A to Z, Allergy, 76, 2699-2715, https://doi.org/10.1111/all.14763.

    Article  CAS  PubMed  Google Scholar 

  30. Nishimura, S., Manabe, I., Takaki, S., Nagasaki, M., Otsu, M., Yamashita, H., et al. (2013) Adipose natural regulatory B cells negatively control adipose tissue inflammation, Cell Metab., 18, 759-766, https://doi.org/10.1016/j.cmet.2013.09.017.

    Article  CAS  PubMed  Google Scholar 

  31. Ghazarian, M., Luck, H., Revelo, X. S., Winer, S., and Winer, D. A. (2015) Immunopathology of adipose tissue during metabolic syndrome, Turk Patoloji Derg., 31 Suppl 1, 172-180, https://doi.org/10.5146/tjpath.2015.01323.

    Article  PubMed  Google Scholar 

  32. Garcia, S. G., Sandoval-Hellín, N., Clos-Sansalvador, M., Carreras-Planella, L., Morón-Font, M., Guerrero, D., et al. (2022) Mesenchymal stromal cells induced regulatory B cells are enriched in extracellular matrix genes and IL-10 independent modulators, Front. Immunol., 13, 957797, https://doi.org/10.3389/fimmu.2022.957797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shen, L., Chng, M. H. Y., Alonso, M. N., Yuan, R., Winer, D. A., and Engleman, E. G. (2015) B-1a lymphocytes attenuate insulin resistance, Diabetes, 64, 593-603, https://doi.org/10.2337/db14-0554.

    Article  CAS  PubMed  Google Scholar 

  34. Capasso, M., Rashed Alyahyawi, A., and Spear, S. (2015) Metabolic control of B cells: more questions than answers, Front. Immunol., 6, 80, https://doi.org/10.3389/fimmu.2015.00080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Fasshauer, M., and Blüher, M. (2015) Adipokines in health and disease, Trends Pharmacol. Sci., 36, 461-470, https://doi.org/10.1016/j.tips.2015.04.014.

    Article  CAS  PubMed  Google Scholar 

  36. Reiche, M. E., Poels, K., Bosmans, L. A., Vos, W. G., Van Tiel, C. M., Gijbels, M. J. J., et al. (2022) Adipocytes control haematopoiesis and inflammation through CD40 signaling, Haematologica, https://doi.org/10.3324/haematol.2022.281482.

    Article  PubMed  Google Scholar 

  37. Szumilas, K., Szumilas, P., Słuczanowska-Głąbowska, S., Zgutka, K., and Pawlik, A. (2020) Role of adiponectin in the pathogenesis of rheumatoid arthritis, Int. J. Mol. Sci., 21, 8265, https://doi.org/10.3390/ijms21218265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bennett, B. D., Solar, G. P., Yuan, J. Q., Mathias, J., Thomas, G. R., and Matthews, W. (1996) A role for leptin and its cognate receptor in hematopoiesis, Curr. Biol., 6, 1170-1180, https://doi.org/10.1016/S0960-9822(02)70684-2.

    Article  CAS  PubMed  Google Scholar 

  39. Claycombe, K., King, L. E., and Fraker, P. J. (2008) A role for leptin in sustaining lymphopoiesis and myelopoiesis, Proc. Natl. Acad. Sci. USA, 105, 2017-2021, https://doi.org/10.1073/pnas.0712053105.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lam, Q. L. K., Wang, S., Ko, O. K. H., Kincade, P. W., and Lu, L. (2010) Leptin signaling maintains B-cell homeostasis via induction of Bcl-2 and Cyclin D1, Proc. Natl. Acad. Sci. USA, 107, 13812-13817, https://doi.org/10.1073/pnas.1004185107.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gupta, S., Agrawal, S., and Gollapudi, S. (2013) Increased activation and cytokine secretion in B cells stimulated with leptin in aged humans, Immun. Ageing, 10, 3, https://doi.org/10.1186/1742-4933-10-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Frasca, D., Diaz, A., Romero, M., and Blomberg, B. B. (2020) Leptin induces immunosenescence in human B cells, Cell. Immunol., 348, 103994, https://doi.org/10.1016/j.cellimm.2019.103994.

    Article  CAS  PubMed  Google Scholar 

  43. Chen, J., Tan, B., Karteris, E., Zervou, S., Digby, J., Hillhouse, E. W., et al. (2006) Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines, Diabetologia, 49, 1292-1302, https://doi.org/10.1007/s00125-006-0194-7.

    Article  CAS  PubMed  Google Scholar 

  44. Zhang, K., Guo, Y., Ge, Z., Zhang, Z., Da, Y., Li, W., et al. (2017) Adiponectin suppresses T helper 17 Cell differentiation and limits autoimmune CNS inflammation via the SIRT1/PPARγ/RORγt pathway, Mol. Neurobiol., 54, 4908-4920, https://doi.org/10.1007/s12035-016-0036-7.

    Article  CAS  PubMed  Google Scholar 

  45. Li, W., Geng, L., Liu, X., Gui, W., and Qi, H. (2019) Recombinant adiponectin alleviates abortion in mice by regulating Th17/Treg imbalance via p38MAPK-STAT5 pathway, Biol. Reprod., 100, 1008-1017, https://doi.org/10.1093/biolre/ioy251.

    Article  PubMed  Google Scholar 

  46. Tsang, J. Y. S., Li, D., Ho, D., Peng, J., Xu, A., Lamb, J., et al. (2011) Novel immunomodulatory effects of adiponectin on dendritic cell functions, Int. Immunopharmacol., 11, 604-609, https://doi.org/10.1016/j.intimp.2010.11.009.

    Article  CAS  PubMed  Google Scholar 

  47. Cheng, X., Folco, E. J., Shimizu, K., and Libby, P. (2012) Adiponectin induces pro-inflammatory programs in human macrophages and CD4+ T cells, J. Biol. Chem., 287, 36896-36904, https://doi.org/10.1074/jbc.M112.409516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tsao, T.-S., Tomas, E., Murrey, H. E., Hug, C., Lee, D. H., Ruderman, N. B., et al. (2003) Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways, J. Biol. Chem., 278, 50810-50817, https://doi.org/10.1074/jbc.M309469200.

    Article  CAS  PubMed  Google Scholar 

  49. Pang, T. T. L., and Narendran, P. (2008) The distribution of adiponectin receptors on human peripheral blood mononuclear cells, Ann. N. Y. Acad. Sci., 1150, 143-145, https://doi.org/10.1196/annals.1447.021.

    Article  PubMed  Google Scholar 

  50. Yokota, T., Meka, C. S. R., Kouro, T., Medina, K. L., Igarashi, H., Takahashi, M., et al. (2003) Adiponectin, a fat cell product, influences the earliest lymphocyte precursors in bone marrow cultures by activation of the cyclooxygenase-prostaglandin pathway in stromal cells, J. Immunol., 171, 5091-5099, https://doi.org/10.4049/jimmunol.171.10.5091.

    Article  CAS  PubMed  Google Scholar 

  51. Chimen, M., McGettrick, H. M., Apta, B., Kuravi, S. J., Yates, C. M., Kennedy, A., et al. (2015) Homeostatic regulation of T cell trafficking by a B cell-derived peptide is impaired in autoimmune and chronic inflammatory disease, Nat. Med., 21, 467-475, https://doi.org/10.1038/nm.3842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Obeid, S., Wankell, M., Charrez, B., Sternberg, J., Kreuter, R., Esmaili, S., et al. (2017) Adiponectin confers protection from acute colitis and restricts a B cell immune response, J. Biol. Chem., 292, 6569-6582, https://doi.org/10.1074/jbc.M115.712646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Che, N., Sun, X., Gu, L., Wang, X., Shi, J., Sun, Y., et al. (2021) Adiponectin enhances B-cell proliferation and differentiation via activation of Akt1/STAT3 and exacerbates collagen-induced arthritis, Front. Immunol., 12, 626310, https://doi.org/10.3389/fimmu.2021.626310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fukuhara, A., Matsuda, M., Nishizawa, M., Segawa, K., Tanaka, M., Kishimoto, K., et al. (2005) Visfatin: a protein secreted by visceral fat that mimics the effects of insulin, Science, 307, 426-430, https://doi.org/10.1126/science.1097243.

    Article  CAS  PubMed  Google Scholar 

  55. Samal, B., Sun, Y., Stearns, G., Xie, C., Suggs, S., and McNiece, I. (1994) Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor, Mol. Cell. Biol., 14, 1431-1437, https://doi.org/10.1128/mcb.14.2.1431-1437.1994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Moschen, A. R., Kaser, A., Enrich, B., Mosheimer, B., Theurl, M., Niederegger, H., et al. (2007) Visfatin, an adipocytokine with proinflammatory and immunomodulating properties, J. Immunol., 178, 1748-1758, https://doi.org/10.4049/jimmunol.178.3.1748.

    Article  CAS  PubMed  Google Scholar 

  57. Craxton, A., Magaletti, D., Ryan, E. J., and Clark, E. A. (2003) Macrophage- and dendritic cell – dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF, Blood, 101, 4464-4471, https://doi.org/10.1182/blood-2002-10-3123.

    Article  CAS  PubMed  Google Scholar 

  58. Müller, N., Schulte, D. M., Hillebrand, S., Türk, K., Hampe, J., Schafmayer, C., et al. (2014) B Lymphocyte Stimulator (BLyS) is expressed in human adipocytes in vivo and is related to obesity but not to insulin resistance, PLoS One, 9, e94282, https://doi.org/10.1371/journal.pone.0094282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chan, C. C., Harley, I. T. W., Pfluger, P. T., Trompette, A., Stankiewicz, T. E., Allen, J. L., et al. (2021) A BAFF/APRIL axis regulates obesogenic diet-driven weight gain, Nat. Commun., 12, 2911, https://doi.org/10.1038/s41467-021-23084-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kim, B., and Hyun, C.-K. (2020) B-cell-activating factor depletion ameliorates aging-dependent insulin resistance via enhancement of thermogenesis in adipose tissues, Int. J. Mol. Sci., 21, 5121, https://doi.org/10.3390/ijms21145121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Apostolopoulos, V., de Courten, M. P. J., Stojanovska, L., Blatch, G. L., Tangalakis, K., and de Courten, B. (2016) The complex immunological and inflammatory network of adipose tissue in obesity, Mol. Nutr. Food Res., 60, 43-57, https://doi.org/10.1002/mnfr.201500272.

    Article  CAS  PubMed  Google Scholar 

  62. Biondi, G., Marrano, N., Borrelli, A., Rella, M., Palma, G., Calderoni, I., et al. (2022) Adipose tissue secretion pattern influences β-cell wellness in the transition from obesity to type 2 diabetes, Int. J. Mol. Sci., 23, 5522, https://doi.org/10.3390/ijms23105522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Spencer, N. F., and Daynes, R. A. (1997) IL-12 directly stimulates expression of IL-10 by CD5+ B cells and IL-6 by both CD5+ and CD5– B cells: possible involvement in age-associated cytokine dysregulation, Int. Immunol., 9, 745-754, https://doi.org/10.1093/intimm/9.5.745.

    Article  CAS  PubMed  Google Scholar 

  64. Figueiró, F., Muller, L., Funk, S., Jackson, E. K., Battastini, A. M. O., and Whiteside, T. L. (2016) Phenotypic and functional characteristics of CD39high human regulatory B cells (Breg), Oncoimmunology, 5, e1082703, https://doi.org/10.1080/2162402X.2015.1082703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Giraldez, M. D., Carneros, D., Garbers, C., Rose-John, S., and Bustos, M. (2021) New insights into IL-6 family cytokines in metabolism, hepatology and gastroenterology, Nat. Rev. Gastroenterol. Hepatol., 18, 787-803, https://doi.org/10.1038/s41575-021-00473-x.

    Article  CAS  PubMed  Google Scholar 

  66. Kalliolias, G. D., and Ivashkiv, L. B. (2016) TNF biology, pathogenic mechanisms and emerging therapeutic strategies, Nat. Rev. Rheumatol., 12, 49-62, https://doi.org/10.1038/nrrheum.2015.169.

    Article  CAS  PubMed  Google Scholar 

  67. Chen, X., Xun, K., Chen, L., and Wang, Y. (2009) TNF-α, a potent lipid metabolism regulator, Cell Biochem. Funct., 27, 407-416, https://doi.org/10.1002/cbf.1596.

    Article  CAS  PubMed  Google Scholar 

  68. Hotamisligil, G. S., Budavari, A., Murray, D., and Spiegelman, B. M. (1994) Reduced tyrosine kinase activity of the insulin receptor in obesity-diabetes. Central role of tumor necrosis factor-alpha, J. Clin. Invest., 94, 1543-1549, https://doi.org/10.1172/JCI117495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Coppack, S. W. (2001) Pro-inflammatory cytokines and adipose tissue, Proc. Nutr. Soc., 60, 349-356, https://doi.org/10.1079/PNS2001110.

    Article  CAS  PubMed  Google Scholar 

  70. Song, M., Meng, L., Liu, X., and Yang, Y. (2021) Feprazone prevents free fatty acid (FFA)-induced endothelial inflammation by mitigating the activation of the TLR4/MyD88/NF-κB pathway, ACS Omega, 6, 4850-4856, https://doi.org/10.1021/acsomega.0c05826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Xu, Y., Wu, K., Han, S., Ding, S., Lu, G., Lin, Z., et al. (2020) Astilbin combined with lipopolysaccharide induces IL-10-producing regulatory B cells via the STAT3 signalling pathway, Biomed. Pharmacother., 129, 110450, https://doi.org/10.1016/j.biopha.2020.110450.

    Article  CAS  PubMed  Google Scholar 

  72. Wang, K., Tao, L., Su, J., Zhang, Y., Zou, B., Wang, Y., et al. (2017) TLR4 supports the expansion of FasL+CD5+CD1dhi regulatory B cells, which decreases in contact hypersensitivity, Mol. Immunol., 87, 188-199, https://doi.org/10.1016/j.molimm.2017.04.016.

    Article  CAS  PubMed  Google Scholar 

  73. McLaughlin, T., Ackerman, S. E., Shen, L., and Engleman, E. (2017) Role of innate and adaptive immunity in obesity-associated metabolic disease, J. Clin. Invest., 127, 5-13, https://doi.org/10.1172/JCI88876.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Xiao, Y., Deng, C., and Zhou, Z. (2021) The multiple roles of B lymphocytes in the onset and treatment of type 1 diabetes: interactions between B lymphocytes and T cells, J. Diabetes Res., 2021, 6581213, https://doi.org/10.1155/2021/6581213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Fernandez, N. C., and Shinoda, K. (2022) The role of B lymphocyte subsets in adipose tissue development, metabolism, and aging, Compr. Physiol., 12, 4133-4145, https://doi.org/10.1002/cphy.c220006.

    Article  PubMed  Google Scholar 

  76. Karl, M., Hasselwander, S., Zhou, Y., Reifenberg, G., Kim, Y. O., Park, K.-S., et al. (2022) Dual roles of B lymphocytes in mouse models of diet-induced nonalcoholic fatty liver disease, Hepatology, 76, 1135-1149, https://doi.org/10.1002/hep.32428.

    Article  CAS  PubMed  Google Scholar 

  77. Kim, Y. H., Choi, B. H., Cheon, H. G., Do, M. S. (2009) B cell activation factor (BAFF) is a novel adipokine that links obesity and inflammation, Exp. Mol. Med., 41, 208-216, https://doi.org/10.3858/emm.2009.41.3.024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Francisco, V., Pino, J., Gonzalez-Gay, M. A., Mera, A., Lago, F., Gómez, R., et al. (2018) Adipokines and inflammation: is it a question of weight? Br. J. Pharmacol., 175, 1569-1579, https://doi.org/10.1111/bph.14181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Dludla, P. V., Nkambule, B. B., Mazibuko-Mbeje, S. E., Nyambuya, T. M., Mxinwa, V., Mokgalaboni, K., et al. (2021) Adipokines as a therapeutic target by metformin to improve metabolic function: a systematic review of randomized controlled trials, Pharmacol. Res., 163, 105219, https://doi.org/10.1016/j.phrs.2020.105219.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Alina Ustiugova for her help in writing the text.

Funding

This work was supported by the Russian Science Foundation (project no. 22-14-00398).

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Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    Ekaterina M. Stasevich, Elina A. Zheremyan, Dmitriy V. Kuprash & Anton M. Schwartz

  2. Moscow Institute of Physics and Technology, 141701, Moscow, Russia

    Anton M. Schwartz

  3. Department of Human Biology, University of Haifa, Haifa, Israel

    Anton M. Schwartz

Authors
  1. Ekaterina M. Stasevich
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  2. Elina A. Zheremyan
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  3. Dmitriy V. Kuprash
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  4. Anton M. Schwartz
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Contributions

Ekaterina M. Stasevich – writing the test, creating the illustration; Elina A. Zheremyan – writing the text; Dmitry V. Kuprash – editing the text of the article; Anton M. Schwartz – formulating the idea of the article and writing the text.

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Correspondence to Anton M. Schwartz.

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The authors declare no conflicts of interest in financial or any other sphere. This article does not contain any studies involving human participants or animals performed by any of the authors.

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Stasevich, E.M., Zheremyan, E.A., Kuprash, D.V. et al. Interaction Between Adipocytes and B Lymphocytes in Human Metabolic Diseases. Biochemistry Moscow 88, 280–288 (2023). https://doi.org/10.1134/S0006297923020104

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  • DOI: https://doi.org/10.1134/S0006297923020104

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