Fatty acid-binding protein 3 regulates differentiation of IgM-producing plasma cells.
Acetylation
Animals
Cell Differentiation
/ genetics
Cells, Cultured
Fatty Acid Binding Protein 3
/ genetics
Gene Expression Regulation
Histones
/ metabolism
Immunoglobulin M
/ metabolism
Immunohistochemistry
Mice, Inbred C57BL
Mice, Knockout
Plasma Cells
/ metabolism
Positive Regulatory Domain I-Binding Factor 1
/ genetics
Reverse Transcriptase Polymerase Chain Reaction
Blimp-1
FABP3
histone acetylation
plasma cell
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
08
04
2020
revised:
26
05
2020
accepted:
09
06
2020
pubmed:
25
6
2020
medline:
27
7
2021
entrez:
25
6
2020
Statut:
ppublish
Résumé
Plasma cells (PCs), which aim to protect host health, produce various subsets of immunoglobulin (Ig) in response to extracellular pathogens. Blimp-1 (encoded by Prdm1)-a protein that is highly expressed by PCs-is important for PC functions, including the generation of Igs. Fatty acid-binding protein 3 (FABP3) is a carrier protein of polyunsaturated fatty acids (PUFAs) and participates in multiple cellular functions. Although the functions of FABP3 in neurons and cardiac myocytes are well-noted, their roles in immune cells remain to be fully elucidated. In this study, we demonstrate that FABP3 is expressed in activated B cells and that FABP3 promotes PC development and IgM secretion. Moreover, we provide the first evidence that FABP3 is necessary for Blimp-1 expression, by regulating the histone modification of its promoter region. Taken together, our findings reveal that FABP3 acts as a positive regulator of B-cell activation by controlling histone acetylation of the Blimp-1 gene, thereby playing a role in host defense against pathogens.
Substances chimiques
Fabp3 protein, mouse
0
Fatty Acid Binding Protein 3
0
Histones
0
Immunoglobulin M
0
Prdm1 protein, mouse
0
Positive Regulatory Domain I-Binding Factor 1
EC 2.1.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1130-1141Informations de copyright
© 2020 Federation of European Biochemical Societies.
Références
Akkaya M, Kwak K & Pierce SK (2019) B cell memory: building two walls of protection against pathogens. Nat Rev Immunol 20, 229-238.
Shapiro-Shelef M & Calame K (2005) Regulation of plasma-cell development. Nat Rev Immunol 5, 230-242.
Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG & Calame K (2003) Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19, 607-620.
Klein U, Casola S, Cattoretti G, Shen Q, Lia M, Mo T, Ludwig T, Rajewsky K & Dalla-Favera R (2006) Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol 7, 773-782.
Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, Yu X, Yang L, Tan BK, Rosenwald A et al. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93.
Tellier J & Nutt SL (2019) Plasma cells: The programming of an antibody-secreting machine. Eur J Immunol 49, 30-37.
Tellier J, Shi W, Minnich M, Liao Y, Crawford S, Smyth GK, Kallies A, Busslinger M & Nutt SL (2016) Blimp-1 controls plasma cell function through the regulation of immunoglobulin secretion and the unfolded protein response. Nat Immunol 17, 323-330.
O'Sullivan D, van der Windt GJ, Huang SC, Curtis JD, Chang CH, Buck MD, Qiu J, Smith AM, Lam WY, DiPlato LM et al. (2014) Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity 41, 75-88.
Pan Y, Tian T, Park CO, Lofftus SY, Mei S, Liu X, Luo C, O'Malley JT, Gehad A, Teague JE et al. (2017) Survival of tissue-resident memory T cells requires exogenous lipid uptake and metabolism. Nature 543, 252-256.
Jellusova J, Cato MH, Apgar JR, Ramezani-Rad P, Leung CR, Chen C, Richardson AD, Conner EM, Benschop RJ, Woodgett JR et al. (2017) Gsk3 is a metabolic checkpoint regulator in B cells. Nat Immunol 18, 303-312.
Caro-Maldonado A, Wang R, Nichols AG, Kuraoka M, Milasta S, Sun LD, Gavin AL, Abel ED, Kelsoe G, Green DR et al. (2014) Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J Immunol 192, 3626-3636.
Waters LR, Ahsan FM, Wolf DM, Shirihai O & Teitell MA (2018) Initial B cell activation induces metabolic reprogramming and mitochondrial remodeling. iScience 5, 99-109.
Kim JY, Lim K, Kim KH, Kim JH, Choi JS & Shim SC (2018) N-3 polyunsaturated fatty acids restore Th17 and Treg balance in collagen antibody-induced arthritis. PLoS One 13, e0194331.
Han SC, Koo DH, Kang NJ, Yoon WJ, Kang GJ, Kang HK & Yoo ES (2015) Docosahexaenoic acid alleviates atopic dermatitis by generating Tregs and IL-10/TGF-β-modified macrophages via a TGF-β-dependent mechanism. J Invest Dermatol 135, 1556-1564.
Han SC, Kang GJ, Ko YJ, Kang HK, Moon SW, Ann YS & Yoo ES (2012) Fermented fish oil suppresses T helper 1/2 cell response in a mouse model of atopic dermatitis via generation of CD4+CD25+Foxp3+ T cells. BMC Immunol 13, 44.
Islam A, Kagawa Y, Sharifi K, Ebrahimi M, Miyazaki H, Yasumoto Y, Kawamura S, Yamamoto Y, Sakaguti S, Sawada T et al. (2014) Fatty Acid Binding Protein 3 Is involved in n-3 and n-6 PUFA transport in mouse trophoblasts. J Nutr 144, 1509-1516.
Teague H, Harris M, Fenton J, Lallemand P, Shewchuk BM & Shaikh SR (2014) Eicosapentaenoic and docosahexaenoic acid ethyl esters differentially enhance B-cell activity in murine obesity. J Lipid Res 55, 1420-1433.
Ramon S, Gao F, Serhan CN & Phipps RP (2012) Specialized proresolving mediators enhance human B cell differentiation to antibody-secreting cells. J Immunol 189, 1036-1042.
Kosaraju R, Guesdon W, Crouch MJ, Teague HL, Sullivan EM, Karlsson EA, Schultz-Cherry S, Gowdy K, Bridges LC, Reese LR et al. (2017) B cell activity is impaired in human and mouse obesity and is responsive to an essential fatty acid upon murine influenza infection. J Immunol 198, 4738-4752.
Roper RL, Graf B & Phipps RP (2002) Prostaglandin E2 and cAMP promote B lymphocyte class switching to IgG1. Immunol Lett 84, 191-198.
Allman D & Pillai S (2008) Peripheral B cell subsets. Curr Opin Immunol 20, 149-157.
Moore SM, Holt VV, Malpass LR, Hines IN & Wheeler MD (2015) Fatty acid-binding protein 5 limits the anti-inflammatory response in murine macrophages. Mol Immunol 67, 265-275.
Teague H, Fhaner CJ, Harris M, Duriancik DM, Reid GE & Shaikh SR (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.
Rockett BD, Salameh M, Carraway K, Morrison K & Shaikh SR (2010) n-3 PUFA improves fatty acid composition, prevents palmitate-induced apoptosis, and differentially modifies B cell cytokine secretion in vitro and ex vivo. J Lipid Res 51, 1284-1297.
Crouch MJ, Kosaraju R, Guesdon W, Armstrong M, Reisdorph N, Jain R, Fenton J & Shaikh SR (2019) Frontline Science: A reduction in DHA-derived mediators in male obesity contributes toward defects in select B cell subsets and circulating antibody. J Leukoc Biol 106, 241-257.
Ramon S, Baker SF, Sahler JM, Kim N, Feldsott EA, Serhan CN, Martínez-Sobrido L, Topham DJ & Phipps RP (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.
Lam WY, Becker AM, Kennerly KM, Wong R, Curtis JD, Llufrio EM, McCommis KS, Fahrmann J, Pizzato HA, Nunley RM et al. (2016) Mitochondrial pyruvate import promotes long-term survival of antibody-secreting plasma cells. Immunity 45, 60-73.
Sandoval H, Kodali S & Wang J (2018) Regulation of B cell fate, survival, and function by mitochondria and autophagy. Mitochondrion 41, 58-65.
Jasiulionis MG (2018) Abnormal epigenetic regulation of immune system during aging. Front Immunol 9, 197.
Yamamoto Y, Kida H, Kagawa Y, Yasumoto Y, Miyazaki H, Islam A, Ogata M, Yanagawa Y, Mitsushima D, Fukunaga K et al. (2018) FABP3 in the anterior cingulate cortex modulates the methylation status of the glutamic acid decarboxylase. J Neurosci 38, 10411-10423.
Chen Z, Li S, Subramaniam S, Shyy JY & Chien S (2017) Epigenetic regulation: a new frontier for biomedical engineers. Annu Rev Biomed Eng 19, 195-219.
Allis CD & Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17, 487-500.
Kucharski R, Maleszka J, Foret S & Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827-1830.
González-Becerra K, Ramos-Lopez O, Barrón-Cabrera E, Riezu-Boj JI, Milagro FI, Martínez-López E & Martínez JA (2019) Fatty acids, epigenetic mechanisms and chronic diseases: a systematic review. Lipids Health Dis 18, 178.
Gerhauser C (2018) Impact of dietary gut microbial metabolites on the epigenome. Philos Trans R Soc Lond B Biol Sci 373, 20170359.
Romagnolo DF, Donovan MG, Doetschman TC & Selmin OI (2019) 6 Linoleic acid induces epigenetics alterations associated with colonic inflammation and cancer. Nutrients 11, 171.
Silva-Martínez GA, Rodríguez-Ríos D, Alvarado-Caudillo Y, Vaquero A, Esteller M, Carmona FJ, Moran S, Nielsen FC, Wickström-Lindholm M, Wrobel K et al. (2016) Arachidonic and oleic acid exert distinct effects on the DNA methylome. Epigenetics 11, 321-334.
Bernard MP & Phipps RP (2010) Inhibition of cyclooxygenase-2 impairs the expression of essential plasma cell transcription factors and human B-lymphocyte differentiation. Immunology 129, 87-96.
Garaeva AA, Kovaleva IE, Chumakov PM & Evstafieva AG (2016) Mitochondrial dysfunction induces SESN2 gene expression through Activating Transcription Factor 4. Cell Cycle 15, 64-71.
Cheung P, Allis CD & Sassone-Corsi P (2000) Signaling to chromatin through histone modifications. Cell 103, 263-271.
Kouzarides T (2007) Chromatin modifications and their function. Cell 128, 693-705.
Josefowicz SZ, Shimada M, Armache A, Li CH, Miller RM, Lin S, Yang A, Dill BD, Molina H, Park HS et al. (2016) Chromatin kinases act on transcription factors and histone tails in regulation of inducible transcription. Mol Cell 64, 347-361.
Binas B, Danneberg H, McWhir J, Mullins L & Clark AJ (1999) Requirement for the heart-type fatty acid binding protein in cardiac fatty acid utilization. FASEB J 13, 805-812.
Hanihara-Tatsuzawa F, Miura H, Kobayashi S, Isagawa T, Okuma A, Manabe I & MaruYama T (2014) Control of Toll-like receptor-mediated T cell-independent type 1 antibody responses by the inducible nuclear protein IκB-ζ. J Biol Chem 289, 30925-30936.