Mode of Bioenergetic Metabolism during B Cell Differentiation in the Intestine Determines the Distinct Requirement for Vitamin B1

Cell Reports

Volumn 13, Issue 1, 2015, Pages 122-131

  Kunisawa, Jun ^a,b,c,d   Sugiura, Yuki ^e,f   Wake, Taichi ^b   Nagatake, Takahiro ^a   Suzuki, Hidehiko ^a   Nagasawa, Risa ^a,b   Shikata, Shiori ^a,b   Honda, Kurara ^e,f   Hashimoto, Eri ^a,b   Suzuki, Yuji ^b   Setou, Mitsutoshi ^b,g,h   Suematsu, Makoto ^e   Kiyono, Hiroshi ^b,f,i  

^a Health and Nutrition   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^g HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^h UNIVERSITY OF HONG KONG   (Hong Kong)

ⁱ UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; THIAMINE; ANTIBODY; IMMUNOGLOBULIN M;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN ANTIBODY REACTION; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; BIOENERGY; CELL METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; DIETARY INTAKE; ENERGY METABOLISM; FEMALE; GLYCOLYSIS; INTESTINAL TISSUE; INTESTINE CELL; LAMINA PROPRIA; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PEYER PATCH; PLASMA CELL; PRIORITY JOURNAL; ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; HUMORAL IMMUNITY; IMMUNOLOGY; INTESTINE MUCOSA; LYMPH NODE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; METABOLISM; MUCOSAL IMMUNITY; PATHOLOGY; VITAMIN DEFICIENCY;

ANIMALS; ANTIBODIES; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CITRIC ACID CYCLE; FEMALE; GLYCOLYSIS; IMMUNITY, HUMORAL; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; INTESTINAL MUCOSA; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED BALB C; PEYER'S PATCHES; PLASMA CELLS; THIAMINE; VITAMIN B DEFICIENCY;

EID: 84943259720     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.063     Document Type: Article

References (49)

1. Atkinson D.E. The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 1968, 7:4030-4034.
2. Barrientos A., Moraes C.T. Titrating the effects of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 1999, 274:16188-16197.
3. Blair D., Dufort F.J., Chiles T.C. Protein kinase Cβ is critical for the metabolic switch to glycolysis following B-cell antigen receptor engagement. Biochem. J. 2012, 448:165-169.
4. Caro-Maldonado A., Wang R., Nichols A.G., Kuraoka M., Milasta S., Sun L.D., Gavin A.L., Abel E.D., Kelsoe G., Green D.R., Rathmell J.C. Metabolic reprogramming is required for antibody production that is suppressed in anergic but exaggerated in chronically BAFF-exposed B cells. J. Immunol. 2014, 192:3626-3636.
5. Cerutti A., Chen K., Chorny A. Immunoglobulin responses at the mucosal interface. Annu. Rev. Immunol. 2011, 29:273-293.
6. Chappell J.B., Greville G.D. Effects of oligomycin on respiration and swelling of isolated liver mitochondria. Nature 1961, 190:502-504.
7. Doughty C.A., Bleiman B.F., Wagner D.J., Dufort F.J., Mataraza J.M., Roberts M.F., Chiles T.C. Antigen receptor-mediated changes in glucose metabolism in B lymphocytes: role of phosphatidylinositol 3-kinase signaling in the glycolytic control of growth. Blood 2006, 107:4458-4465.
8. Dufort F.J., Bleiman B.F., Gumina M.R., Blair D., Wagner D.J., Roberts M.F., Abu-Amer Y., Chiles T.C. Cutting edge: IL-4-mediated protection of primary B lymphocytes from apoptosis via Stat6-dependent regulation of glycolytic metabolism. J. Immunol. 2007, 179:4953-4957.
9. Dutta B., Huang W., Molero M., Kekuda R., Leibach F.H., Devoe L.D., Ganapathy V., Prasad P.D. Cloning of the human thiamine transporter, a member of the folate transporter family. J. Biol. Chem. 1999, 274:31925-31929.
10. Everts B., Amiel E., Huang S.C., Smith A.M., Chang C.H., Lam W.Y., Redmann V., Freitas T.C., Blagih J., van der Windt G.J., et al. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKε supports the anabolic demands of dendritic cell activation. Nat. Immunol. 2014, 15:323-332.
11. Fox C.J., Hammerman P.S., Thompson C.B. Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 2005, 5:844-852.
12. Frank R.A., Leeper F.J., Luisi B.F. Structure, mechanism and catalytic duality of thiamine-dependent enzymes. Cell. Mol. Life Sci. 2007, 64:892-905.
13. Frauwirth K.A., Riley J.L., Harris M.H., Parry R.V., Rathmell J.C., Plas D.R., Elstrom R.L., June C.H., Thompson C.B. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002, 16:769-777.
14. Gohda M., Kunisawa J., Miura F., Kagiyama Y., Kurashima Y., Higuchi M., Ishikawa I., Ogahara I., Kiyono H. Sphingosine 1-phosphate regulates the egress of IgA plasmablasts from Peyer's patches for intestinal IgA responses. J. Immunol. 2008, 180:5335-5343.
15. Haimovich B., Reddell M.T., Calvano J.E., Calvano S.E., Macor M.A., Coyle S.M., Lowry S.F. A novel model of common Toll-like receptor 4- and injury-induced transcriptional themes in human leukocytes. Crit. Care 2010, 14:R177.
16. Hall J.A., Grainger J.R., Spencer S.P., Belkaid Y. The role of retinoic acid in tolerance and immunity. Immunity 2011, 35:13-22.
17. Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
18. + regulatory T cells in the colon. J. Immunol. 2012, 189:2869-2878.
19. Kunisawa J., Kurashima Y., Higuchi M., Gohda M., Ishikawa I., Ogahara I., Kim N., Shimizu M., Kiyono H. Sphingosine 1-phosphate dependence in the regulation of lymphocyte trafficking to the gut epithelium. J. Exp. Med. 2007, 204:2335-2348.
20. Kunisawa J., Hashimoto E., Ishikawa I., Kiyono H. A pivotal role of vitamin B9 in the maintenance of regulatory T cells in vitro and in vivo. PLoS ONE 2012, 7:e32094.
21. Kunisawa J., Kurashima Y., Kiyono H. Gut-associated lymphoid tissues for the development of oral vaccines. Adv. Drug Deliv. Rev. 2012, 64:523-530.
22. + plasma cells mediate robust early-phase intestinal IgA responses in mice. Nat Commun. 2013, 4:1772.
23. Kunisawa J., Hashimoto E., Inoue A., Nagasawa R., Suzuki Y., Ishikawa I., Shikata S., Arita M., Aoki J., Kiyono H. Regulation of intestinal IgA responses by dietary palmitic acid and its metabolism. J. Immunol. 2014, 193:1666-1671.
24. Kunisawa J., Arita M., Hayasaka T., Harada T., Iwamoto R., Nagasawa R., Shikata S., Nagatake T., Suzuki H., Hashimoto E., et al. Dietary ω3 fatty acid exerts anti-allergic effect through the conversion to 17,18-epoxyeicosatetraenoic acid in the gut. Sci. Rep. 2015, 5:9750.
25. Kurashima Y., Amiya T., Fujisawa K., Shibata N., Suzuki Y., Kogure Y., Hashimoto E., Otsuka A., Kabashima K., Sato S., et al. The enzyme Cyp26b1 mediates inhibition of mast cell activation by fibroblasts to maintain skin-barrier homeostasis. Immunity 2014, 40:530-541.
26. Larkin J.R., Zhang F., Godfrey L., Molostvov G., Zehnder D., Rabbani N., Thornalley P.J. Glucose-induced down regulation of thiamine transporters in the kidney proximal tubular epithelium produces thiamine insufficiency in diabetes. PLoS ONE 2012, 7:e53175.
27. Le A., Lane A.N., Hamaker M., Bose S., Gouw A., Barbi J., Tsukamoto T., Rojas C.J., Slusher B.S., Zhang H., et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab. 2012, 15:110-121.
28. Manz R.A., Radbruch A. Plasma cells for a lifetime?. Eur. J. Immunol. 2002, 32:923-927.
29. Mathis D., Shoelson S.E. Immunometabolism: an emerging frontier. Nat. Rev. Immunol. 2011, 11:81.
30. + T cell subsets. J. Immunol. 2011, 186:3299-3303.
31. Moon J.S., Jin W.J., Kwak J.H., Kim H.J., Yun M.J., Kim J.W., Park S.W., Kim K.S. Androgen stimulates glycolysis for de novo lipid synthesis by increasing the activities of hexokinase 2 and 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 2 in prostate cancer cells. Biochem. J. 2011, 433:225-233.
32. Mora J.R., Iwata M., von Andrian U.H. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 2008, 8:685-698.
33. Murata K. Actions of two types of thiaminase on thiamin and its analogues. Ann. N Y Acad. Sci. 1982, 378:146-156.
34. O'Neill L.A., Hardie D.G. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 2013, 493:346-355.
35. Obata T., Shibata N., Goto Y., Ishikawa I., Sato S., Kunisawa J., Kiyono H. Critical role of dendritic cells in T cell retention in the interfollicular region of Peyer's patches. J. Immunol. 2013, 191:942-948.
36. Pabst O. New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 2012, 12:821-832.
37. Pearce E.L., Pearce E.J. Metabolic pathways in immune cell activation and quiescence. Immunity 2013, 38:633-643.
38. Pearce E.L., Walsh M.C., Cejas P.J., Harms G.M., Shen H., Wang L.S., Jones R.G., Choi Y. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009, 460:103-107.
39. Pearce E.L., Poffenberger M.C., Chang C.H., Jones R.G. Fueling immunity: insights into metabolism and lymphocyte function. Science 2013, 342:1242454.
40. Rajgopal A., Edmondnson A., Goldman I.D., Zhao R. SLC19A3 encodes a second thiamine transporter ThTr2. Biochim. Biophys. Acta 2001, 1537:175-178.
41. Spencer S.P., Belkaid Y. Dietary and commensal derived nutrients: shaping mucosal and systemic immunity. Curr. Opin. Immunol. 2012, 24:379-384.
42. Spencer S.P., Wilhelm C., Yang Q., Hall J.A., Bouladoux N., Boyd A., Nutman T.B., Urban J.F., Wang J., Ramalingam T.R., et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 2014, 343:432-437.
43. Stammati A., Zanetti C., Pizzoferrato L., Quattrucci E., Tranquilli G.B. In vitro model for the evaluation of toxicity and antinutritional effects of sulphites. Food Addit. Contam. 1992, 9:551-560.
44. Sugiura Y., Taguchi R., Setou M. Visualization of spatiotemporal energy dynamics of hippocampal neurons by mass spectrometry during a kainate-induced seizure. PLoS ONE 2011, 6:e17952.
45. + T cell memory development. Immunity 2012, 36:68-78.
46. van der Windt G.J., O'Sullivan D., Everts B., Huang S.C., Buck M.D., Curtis J.D., Chang C.H., Smith A.M., Ai T., Faubert B., et al. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc. Natl. Acad. Sci. USA 2013, 110:14336-14341.
47. Wang R., Green D.R. Metabolic reprogramming and metabolic dependency in T cells. Immunol. Rev. 2012, 249:14-26.
48. Webb M.E., Marquet A., Mendel R.R., Rébeillé F., Smith A.G. Elucidating biosynthetic pathways for vitamins and cofactors. Nat. Prod. Rep. 2007, 24:988-1008.
49. Zahr N.M., Kaufman K.L., Harper C.G. Clinical and pathological features of alcohol-related brain damage. Nat. Rev. Neurol. 2011, 7:284-294.