B cell activity is impaired in human and mouse obesity and is responsive to an essential fatty acid upon murine influenza infection

Journal of Immunology

Volumn 198, Issue 12, 2017, Pages 4738-4752

  Kosaraju, Rasagna ^a,b   Guesdon, William ^a,b   Crouch, Miranda J ^a,b   Teague, Heather L ^a,b,f   Sullivan, E Madison ^a,b   Karlsson, Erik A ^c   Schultz Cherry, Stacey ^c   Gowdy, Kymberly ^a   Bridges, Lance C ^a,b,g   Reese, Lauren R ^a,b   Neufer, P Darrell ^a,b   Armstrong, Michael ^d   Reisdorph, Nichole ^d   Milner, J Justin ^e   Beck, Melinda ^e,h   Shaikh, S R ^a,b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e University of North Carolina   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g Arkansas Colleges of Health Education   (United States)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAKPOINT CLUSTER REGION PROTEIN; CD59 ANTIGEN; DOCOSAHEXAENOIC ACID; ESSENTIAL FATTY ACID; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 6; TOLL LIKE RECEPTOR 9; 10,17-DIHYDROXYDOCOSA-4,7,11,13,15,19-HEXAENOIC ACID; 14-HYDROXYDOCOSAHEXAENOIC ACID; 17-HYDROXY-4,7,10,13,15,19-DOCOSAHEXAENOIC ACID; TLR9 PROTEIN, HUMAN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; INFLUENZA; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; ANIMAL; BLOOD; COMPLICATION; DISEASE MODEL; IMMUNOLOGY; INFLUENZA A VIRUS; LYMPHOCYTE ACTIVATION; METABOLISM; ORTHOMYXOVIRUS INFECTION; SECRETION (PROCESS); WESTERN DIET;

ANIMALS; B-LYMPHOCYTES; DIET, WESTERN; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, ESSENTIAL; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN M; INFLUENZA A VIRUS; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MICE; OBESITY; ORTHOMYXOVIRIDAE INFECTIONS; TOLL-LIKE RECEPTOR 9;

EID: 85020396044     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1601031     Document Type: Article

References (75)

1. McGill, H. C., Jr., C. A. McMahan, E. E. Herderick, A. W. Zieske, G. T. Malcom, R. E. Tracy, and J. P. Strong, Pathobiological Determinants of Atherosclerosis in Youth (PDAY) Research Group. 2002. Obesity accelerates the progression of coronary atherosclerosis in young men. Circulation 105: 2712-2718.
2. Quante, M., A. Dietrich, A. ElKhal, and S. G. Tullius. 2015. Obesity-related immune responses and their impact on surgical outcomes. Int. J. Obes. 39: 877-883.
3. Allott, E. H., and S. D. Hursting. 2015. Obesity and cancer: mechanistic insights from transdisciplinary studies. Endocr. Relat. Cancer 22: R365-R386.
4. Karlsson, E. A., and M. A. Beck. 2010. The burden of obesity on infectious disease. Exp. Biol. Med. (Maywood) 235: 1412-1424.
5. Furukawa, S., T. Fujita, M. Shimabukuro, M. Iwaki, Y. Yamada, Y. Nakajima, O. Nakayama, M. Makishima, M. Matsuda, and I. Shimomura. 2004. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114: 1752-1761.
6. Dixit, V. D. 2008. Adipose-immune interactions during obesity and caloric restriction: reciprocal mechanisms regulating immunity and health span. J. Leukoc. Biol. 84: 882-892.
7. Mishra, A. K., V. Dubey, and A. R. Ghosh. 2016. Obesity: an overview of possible role(s) of gut hormones, lipid sensing and gut microbiota. Metabolism 65: 48-65.
8. Lee, B. C., and J. Lee. 2014. Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance. Biochim. Biophys. Acta 1842: 446-462.
9. Weisberg, S. P., D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante, Jr. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112: 1796-1808.
10. Weber, D. J., W. A. Rutala, G. P. Samsa, J. E. Santimaw, and S. M. Lemon. 1985. Obesity as a predictor of poor antibody response to hepatitis B plasma vaccine. JAMA 254: 3187-3189.
11. Huttunen, R., and J. Syrjänen. 2013. Obesity and the risk and outcome of infection. Int. J. Obes. 37: 333-340.
12. Genoni, G., F. Prodam, A. Marolda, E. Giglione, I. Demarchi, S. Bellone, and G. Bona. 2014. Obesity and infection: two sides of one coin. Eur. J. Pediatr. 173: 25-32.
13. Sheridan, P. A., H. A. Paich, J. Handy, E. A. Karlsson, M. G. Hudgens, A. B. Sammon, L. A. Holland, S. Weir, T. L. Noah, and M. A. Beck. 2012. Obesity is associated with impaired immune response to influenza vaccination in humans. Int. J. Obes. 36: 1072-1077.
14. Zhai, X., G. Qian, Y. Wang, X. Chen, J. Lu, Y. Zhang, Q. Huang, and Q. Wang. 2016. Elevated B cell activation is associated with type 2 diabetes development in obese subjects. Cell. Physiol. Biochem. 38: 1257-1266.
15. Arai, S., N. Maehara, Y. Iwamura, S. Honda, K. Nakashima, T. Kai, M. Ogishi, K. Morita, J. Kurokawa, M. Mori, et al. 2013. Obesity-associated autoantibody production requires AIM to retain the immunoglobulin M immune complex on follicular dendritic cells. Cell Rep. 3: 1187-1198.
16. Milner, J. J., P. A. Sheridan, E. A. Karlsson, S. Schultz-Cherry, Q. Shi, and M. A. Beck. 2013. Diet-induced obese mice exhibit altered heterologous immunity during a secondary 2009 pandemic H1N1 infection. J. Immunol. 191: 2474-2485.
17. Farnsworth, C. W., C. T. Shehatou, R. Maynard, K. Nishitani, S. L. Kates, M. J. Zuscik, E. M. Schwarz, J. L. Daiss, and R. A. Mooney. 2015. A humoral immune defect distinguishes the response to Staphylococcus aureus infections in mice with obesity and type 2 diabetes from that in mice with type 1 diabetes. Infect. Immun. 83: 2264-2274.
18. Rothaeusler, K., and N. Baumgarth. 2010. B-cell fate decisions following influenza virus infection. Eur. J. Immunol. 40: 366-377.
19. Shaikh, S. R., K. M. Haas, M. A. Beck, and H. Teague. 2015. The effects of dietinduced obesity on B cell function. Clin. Exp. Immunol. 179: 90-99.
20. Frasca, D., F. Ferracci, A. Diaz, M. Romero, S. Lechner, and B. B. Blomberg. 2016. Obesity decreases B cell responses in young and elderly individuals. Obesity (Silver Spring) 24: 615-625.
21. Ying, W., A. Tseng, R. C. Chang, H. Wang, Y. L. Lin, S. Kanameni, T. Brehm, A. Morin, B. Jones, T. Splawn, et al. 2016. miR-150 regulates obesity-associated insulin resistance by controlling B cell functions. Sci. Rep. 6: 20176.
22. Winer, D. A., S. Winer, L. Shen, P. P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M. G. Davidson, M. N. Alonso, et al. 2011. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17: 610-617.
23. Shen, L., M. H. Chng, M. N. Alonso, R. Yuan, D. A. Winer, and E. G. Engleman. 2015. B-1a lymphocytes attenuate insulin resistance. Diabetes 64: 593-603.
24. Harmon, D. B., P. Srikakulapu, J. L. Kaplan, S. N. Oldham, C. McSkimming, J. C. Garmey, H. M. Perry, J. L. Kirby, T. A. Prohaska, A. Gonen, 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.
25. Nishimura, S., I. Manabe, S. Takaki, M. Nagasaki, M. Otsu, H. Yamashita, J. Sugita, K. Yoshimura, K. Eto, I. Komuro, et al. 2013. Adipose natural regulatory B cells negatively control adipose tissue inflammation. Cell Metab. 18: 759-766.
26. Nicholas, D. A., and B. S. Nikolajczyk. 2016. B cells shed light on diminished vaccine responses in obesity. Obesity (Silver Spring) 24: 551.
27. Madhumitha, H., V. Mohan, N. P. Kumar, R. Pradeepa, S. Babu, and V. Aravindhan. 2015. Impaired Toll-like receptor signalling in peripheral B cells from newly diagnosed type-2 diabetic subjects. Cytokine 76: 253-259.
28. DeFuria, J., A. C. Belkina, M. Jagannathan-Bogdan, J. Snyder-Cappione, J. D. Carr, Y. R. Nersesova, D. Markham, K. J. Strissel, A. A. Watkins, M. Zhu, 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.
29. Sheridan, P. A., H. A. Paich, J. Handy, E. A. Karlsson, S. Schultz-Cherry, M. Hudgens, S.Weir, T. Noah, and M. A. Beck. 2015. The antibody response to influenza vaccination is not impaired in type 2 diabetics. Vaccine 33: 3306-3313.
30. Calder, P. C. 2015. Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim Biophys Acta 1851: 469-484.
31. Micallef, M., I. Munro, M. Phang, and M. Garg. 2009. Plasma n-3 polyunsaturated fatty acids are negatively associated with obesity. Br. J. Nutr. 102: 1370-1374.
32. Yu, Y., Z. Cai, J. Zheng, J. Chen, X. Zhang, X. F. Huang, and D. Li. 2012. Serum levels of polyunsaturated fatty acids are low in Chinese men with metabolic syndrome, whereas serum levels of saturated fatty acids, zinc, and magnesium are high. Nutr. Res. 32: 71-77.
33. Albert, B. B., J. G. Derraik, C. M. Brennan, J. B. Biggs, G. C. Smith, M. L. Garg, D. Cameron-Smith, P. L. Hofman, and W. S. Cutfield. 2014. Higher omega-3 index is associated with increased insulin sensitivity and more favourable metabolic profile in middle-aged overweight men. Sci. Rep. 4: 6697.
34. Teague, H., C. J. Fhaner, M. Harris, D. M. Duriancik, G. E. Reid, and S. R. Shaikh. 2013. n-3 PUFAs enhance the frequency of murine B-cell subsets and restore the impairment of antibody production to a T-independent antigen in obesity. J. Lipid Res. 54: 3130-3138.
35. Gurzell, E. A., H. Teague, M. Harris, J. Clinthorne, S. R. Shaikh, and J. I. Fenton. 2013. DHA-enriched fish oil targets B cell lipid microdomains and enhances ex vivo and in vivo B cell function. J. Leukoc. Biol. 93: 463-470.
36. Wong, J. Y., H. Kelly, C. M. Cheung, E. Y. Shiu, P. Wu, M. Y. Ni, D. K. M. Ip, and B. J. Cowling. 2015. Hospitalization fatality risk of influenza A(H1N1) pdm09: a systematic review and meta-analysis. Am. J. Epidemiol. 182: 294-301.
37. Serhan, C. N. 2014. Pro-resolving lipid mediators are leads for resolution physiology. Nature 510: 92-101.
38. Buckley, C. D., D. W. Gilroy, and C. N. Serhan. 2014. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 40: 315-327.
39. Teague, H., M. Harris, J. Fenton, P. Lallemand, B. M. Shewchuk, and S. R. Shaikh. 2014. Eicosapentaenoic and docosahexaenoic acid ethyl esters differentially enhance B-cell activity in murine obesity. J. Lipid Res. 55: 1420-1433.
40. Bradberry, J. C., and D. E. Hilleman. 2013. Overview of omega-3 fatty acid therapies. P&T 38: 681-691.
41. Ramon, S., F. Gao, C. N. Serhan, and R. P. Phipps. 2012. Specialized proresolving mediators enhance human B cell differentiation to antibody-secreting cells. J. Immunol. 189: 1036-1042.
42. 2 emission in nonmenopausal women. Am. J. Physiol. Endocrinol. Metab. 300: E528-E535.
43. Rockett, B. D., M. Harris, and S. Raza Shaikh. 2012. High dose of an n-3 polyunsaturated fatty acid diet lowers activity of C57BL/6 mice. Prostaglandins Leukot. Essent. Fatty Acids 86: 137-140.
44. Karlsson, E. A., V. A. Meliopoulos, C. Savage, B. Livingston, A. Mehle, and S. Schultz-Cherry. 2015. Visualizing real-time influenza virus infection, transmission and protection in ferrets. Nat. Commun. 6: 6378.
45. Deems, R., M. W. Buczynski, R. Bowers-Gentry, R. Harkewicz, and E. A. Dennis. 2007. Detection and quantitation of eicosanoids via high performance liquid chromatography-electrospray ionization-mass spectrometry. Methods Enzymol. 432: 59-82.
46. Yang, Y., C. Cruickshank, M. Armstrong, S. Mahaffey, R. Reisdorph, and N. Reisdorph. 2013. New sample preparation approach for mass spectrometrybased profiling of plasma results in improved coverage of metabolome. J. Chromatogr. A 1300: 217-226.
47. Shaikh, S. R., B. D. Rockett, M. Salameh, and K. Carraway. 2009. Docosahexaenoic acid modifies the clustering and size of lipid rafts and the lateral organization and surface expression of MHC class I of EL4 cells. J. Nutr. 139: 1632-1639.
48. Mazzucchelli, R., and S. K. Durum. 2007. Interleukin-7 receptor expression: intelligent design. Nat. Rev. Immunol. 7: 144-154.
49. Goetz, C. A., I. R. Harmon, J. J. O'Neil, M. A. Burchill, T. M. Johanns, and M. A. Farrar. 2005. Restricted STAT5 activation dictates appropriate thymic B versus T cell lineage commitment. J. Immunol. 174: 7753-7763.
50. Matthias, P., and A. G. Rolink. 2005. Transcriptional networks in developing and mature B cells. Nat. Rev. Immunol. 5: 497-508.
51. Shapiro-Shelef, M., K. I. Lin, D. Savitsky, J. Liao, and K. Calame. 2005. Blimp-1 is required for maintenance of long-lived plasma cells in the bone marrow. J. Exp. Med. 202: 1471-1476.
52. Oh, D. Y., S. Talukdar, E. J. Bae, T. Imamura, H. Morinaga, W. Fan, P. Li, W. J. Lu, S. M. Watkins, and J. M. Olefsky. 2010. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142: 687-698.
53. Garcia-Bates, T. M., C. J. Baglole, M. P. Bernard, T. I. Murant, P. J. Simpson- Haidaris, and R. P. Phipps. 2009. Peroxisome proliferator-activated receptor g ligands enhance human B cell antibody production and differentiation. J. Immunol. 183: 6903-6912.
54. Ramon, S., S. F. Baker, J. M. Sahler, N. Kim, E. A. Feldsott, C. N. Serhan, L. Martínez-Sobrido, D. J. Topham, and R. P. Phipps. 2014. The specialized proresolving mediator 17-HDHA enhances the antibody-mediated immune response against influenza virus: a new class of adjuvant? J. Immunol. 193: 6031-6040.
55. Colas, R. A., M. Shinohara, J. Dalli, N. Chiang, and C. N. Serhan. 2014. Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. Am. J. Physiol. Cell Physiol. 307: C39-C54.
56. Skarke, C., N. Alamuddin, J. A. Lawson, X. Li, J. F. Ferguson, M. P. Reilly, and G. A. FitzGerald. 2015. Bioactive products formed in humans from fish oils. J. Lipid Res. 56: 1808-1820.
57. Frasca, D., A. Diaz, M. Romero, A. M. Landin, and B. B. Blomberg. 2014. High TNF-α levels in resting B cells negatively correlate with their response. Exp. Gerontol. 54: 116-122.
58. Chan, M. E., B. J. Adler, D. E. Green, and C. T. Rubin. 2012. Bone structure and B-cell populations, crippled by obesity, are partially rescued by brief daily exposure to low-magnitude mechanical signals. FASEB J. 26: 4855-4863.
59. Clark, M. R., M. Mandal, K. Ochiai, and H. Singh. 2014. Orchestrating B cell lymphopoiesis through interplay of IL-7 receptor and pre-B cell receptor signalling. Nat. Rev. Immunol. 14: 69-80.
60. Burrows, T., C. E. Collins, and M. L. Garg. 2011. Omega-3 index, obesity and insulin resistance in children. Int. J. Pediatr. Obes. 6: e532-e539.
61. Balas, L., M. Guichardant, T. Durand, and M. Lagarde. 2014. Confusion between protectin D1 (PD1) and its isomer protectin DX (PDX). An overview on the dihydroxy-docosatrienes described to date. Biochimie 99: 1-7.
62. Clària, J., J. Dalli, S. Yacoubian, F. Gao, and C. N. Serhan. 2012. Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J. Immunol. 189: 2597-2605.
63. Spite, M., J. Clària, and C. N. Serhan. 2014. Resolvins, specialized proresolving lipid mediators, and their potential roles in metabolic diseases. Cell Metab. 19: 21-36.
64. Titos, E., B. Rius, C. López-Vicario, J. Alcaraz-Quiles, V. García-Alonso, A. Lopategi, J. Dalli, J. J. Lozano, V. Arroyo, S. Delgado, et al. 2016. Signaling and immunoresolving actions of resolvin D1 in inflamed human visceral adipose tissue. J. Immunol. 197: 3360-3370.
65. Neuhofer, A., M. Zeyda, D. Mascher, B. K. Itariu, I. Murano, L. Leitner, E. E. Hochbrugger, P. Fraisl, S. Cinti, C. N. Serhan, and T. M. Stulnig. 2013. Impaired local production of proresolving lipid mediators in obesity and 17- HDHA as a potential treatment for obesity-associated inflammation. Diabetes 62: 1945-1956.
66. Tang, Y., M. J. Zhang, J. Hellmann, M. Kosuri, A. Bhatnagar, and M. Spite. 2013. Proresolution therapy for the treatment of delayed healing of diabetic wounds. Diabetes 62: 618-627.
67. Karlsson, E. A., T. Hertz, C. Johnson, A. Mehle, F. Krammer, and S. Schultz- Cherry. 2016. Obesity outweighs protection conferred by adjuvanted influenza vaccination. MBio 7: e01144-16.
68. Morita, M., K. Kuba, A. Ichikawa, M. Nakayama, J. Katahira, R. Iwamoto, T. Watanebe, S. Sakabe, T. Daidoji, S. Nakamura, et al. 2013. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 153: 112-125.
69. Coulombe, F., J. Jaworska, M. Verway, F. Tzelepis, A. Massoud, J. Gillard, G. Wong, G. Kobinger, Z. Xing, C. Couture, et al. 2014. Targeted prostaglandin E2 inhibition enhances antiviral immunity through induction of type I interferon and apoptosis in macrophages. Immunity 40: 554-568.
70. Tam, V. C., O. Quehenberger, C. M. Oshansky, R. Suen, A. M. Armando, P. M. Treuting, P. G. Thomas, E. A. Dennis, and A. Aderem. 2013. Lipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation. Cell 154: 213-227.
71. Yog, R., R. Barhoumi, D. N. McMurray, and R. S. Chapkin. 2010. n-3 polyunsaturated fatty acids suppress mitochondrial translocation to the immunologic synapse and modulate calcium signaling in T cells. J. Immunol. 184: 5865-5873.
72. Teague, H., B. D. Rockett, M. Harris, D. A. Brown, and S. R. Shaikh. 2013. Dendritic cell activation, phagocytosis and CD69 expression on cognate T cells are suppressed by n-3 long-chain polyunsaturated fatty acids. Immunology 139: 386-394.
73. Kim, N., S. Ramon, T. H. Thatcher, C. F. Woeller, P. J. Sime, and R. P. Phipps. 2016. Specialized proresolving mediators (SPMs) inhibit human B-cell IgE production. Eur. J. Immunol. 46: 81-91.
74. Hariri, N., and L. Thibault. 2010. High-fat diet-induced obesity in animal models. Nutr. Res. Rev. 23: 270-299.
75. Milner, J. J., J. Rebeles, S. Dhungana, D. A. Stewart, S. C. J. Sumner, M. H. Meyers, P. Mancuso, and M. A. Beck. 2015. Obesity increases mortality and modulates the lung metabolome during pandemic H1N1 influenza virus infection in mice. J. Immunol. 194: 4846-4859.