Maternal high fiber diet during pregnancy and lactation influences regulatory T Cell differentiation in offspring in mice

Journal of Immunology

Volumn 199, Issue 10, 2017, Pages 3516-3524

  Nakajima, Akihito ^a   Kaga, Naoko ^a   Nakanishi, Yumiko ^b   Ohno, Hiroshi ^b   Miyamoto, Junki ^c   Kimura, Ikuo ^c   Hori, Shohei ^b,d   Sasaki, Takashi ^a   Hiramatsu, Keiichi ^a   Okumura, Ko ^a   Miyake, Sachiko ^a   Habu, Sonoko ^a   Watanabe, Sumio ^a  

^a JUNTENDO UNIVERSITY   (Japan)

^b Institute of Physical and Chemical Research   (Japan)

^c TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNE REGULATOR PROTEIN; BUTYRIC ACID; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 41; SHORT CHAIN FATTY ACID; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; GPCR41 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; VOLATILE FATTY ACID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; EMBRYO; FATTY ACID BLOOD LEVEL; FEMALE; FETUS; HIGH FIBER DIET; IMMUNITY; LACTATION; LYMPHOCYTE DIFFERENTIATION; MATERNAL NUTRITION; MICROBIOME; MICROENVIRONMENT; MOUSE; NEWBORN; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; THYMUS; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; DIETARY FIBER; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MATERNAL EXPOSURE; METABOLISM;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DIETARY FIBER; FATTY ACIDS, VOLATILE; FEMALE; LYMPHOCYTE ACTIVATION; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; PREGNANCY; RECEPTORS, G-PROTEIN-COUPLED; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 85033361476     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1700248     Document Type: Article

References (44)

1. Honda, K., and D. R. Littman. 2012. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 30: 759-795.
2. Rooks, M. G., and W. S. Garrett. 2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16: 341-352.
3. Brestoff, J. R., and D. Artis. 2013. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14: 676-684.
4. Koren, O., J. K. Goodrich, T. C. Cullender, A. Spor, K. Laitinen, H. K. Bäckhed, A. Gonzalez, J. J. Werner, L. T. Angenent, R. Knight, et al. 2012. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150: 470-480.
5. Gomez de Agüero, M., S. C. Ganal-Vonarburg, T. Fuhrer, S. Rupp, Y. Uchimura, H. Li, A. Steinert, M. Heikenwalder, S. Hapfelmeier, U. Sauer, et al. 2016. The maternal microbiota drives early postnatal innate immune development. Science 351: 1296-1302.
6. Buffington, S. A., G. V. Di Prisco, T. A. Auchtung, N. J. Ajami, J. F. Petrosino, and M. Costa-Mattioli. 2016. Microbial reconstitution reverses maternal dietinduced social and synaptic deficits in offspring. Cell 165: 1762-1775.
7. van de Pavert, S. A., M. Ferreira, R. G. Domingues, H. Ribeiro, R. Molenaar, L. Moreira-Santos, F. F. Almeida, S. Ibiza, I. Barbosa, G. Goverse, et al. 2014. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508: 123-127.
8. Nakajima, A., N. Negishi, H. Tsurui, N. Kadowaki-Ohtsuji, K. Maeda, M. Nanno, Y. Yamaguchi, N. Shimizu, H. Yagita, K. Okumura, and S. Habu. 2014. Commensal bacteria regulate thymic Aire expression. PLoS One 9: e105904.
9. Thorburn, A. N., C. I. McKenzie, S. Shen, D. Stanley, L. Macia, L. J. Mason, L. K. Roberts, C. H.Wong, R. Shim, R. Robert, et al. 2015. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat. Commun. 6: 7320.
10. Mathis, D., and C. Benoist. 2009. Aire. Annu. Rev. Immunol. 27: 287-312.
11. Maslowski, K. M., and C. R. Mackay. 2011. Diet, gut microbiota and immune responses. Nat. Immunol. 12: 5-9.
12. Furusawa, Y., Y. Obata, S. Fukuda, T. A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, T. Kato, et al. 2013. Commensal microbederived butyrate induces the differentiation of colonic regulatory T cells. Nature 504: 446-450.
13. Arpaia, N., C. Campbell, X. Fan, S. Dikiy, J. van der Veeken, P. deRoos, H. Liu, J. R. Cross, K. Pfeffer, P. J. Coffer, and A. Y. Rudensky. 2013. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504: 451-455.
14. Smith, P. M., M. R. Howitt, N. Panikov, M. Michaud, C. A. Gallini, M. Bohlooly-Y, J. N. Glickman, and W. S. Garrett. 2013. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341: 569-573.
15. Tanoue, T., K. Atarashi, and K. Honda. 2016. Development and maintenance of intestinal regulatory T cells. Nat. Rev. Immunol. 16: 295-309.
16. Liston, A., and D. H. Gray. 2014. Homeostatic control of regulatory T cell diversity. Nat. Rev. Immunol. 14: 154-165.
17. Yang, S., N. Fujikado, D. Kolodin, C. Benoist, and D. Mathis. 2015. Immune tolerance. Regulatory T cells generated early in life play a distinct role in maintaining self-Tolerance. Science 348: 589-594.
18. Curotto de Lafaille, M. A., and J. J. Lafaille. 2009. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30: 626-635.
19. Hsieh, C. S., H. M. Lee, and C. W. Lio. 2012. Selection of regulatory T cells in the thymus. Nat. Rev. Immunol. 12: 157-167.
20. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-Tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-Tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
21. Komatsu, N., M. E. Mariotti-Ferrandiz, Y. Wang, B. Malissen, H. Waldmann, and S. Hori. 2009. Heterogeneity of natural Foxp3+ T cells: A committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc. Natl. Acad. Sci. USA 106: 1903-1908.
22. Kimura, I., D. Inoue, T. Maeda, T. Hara, A. Ichimura, S. Miyauchi, M. Kobayashi, A. Hirasawa, and G. Tsujimoto. 2011. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc. Natl. Acad. Sci. USA 108: 8030-8035.
23. Gray, D. H., A. P. Chidgey, and R. L. Boyd. 2002. Analysis of thymic stromal cell populations using flow cytometry. J. Immunol. Methods 260: 15-28.
24. Osman, N., D. Adawi, S. Ahrné, B. Jeppsson, and G. Molin. 2008. Probiotics and blueberry attenuate the severity of dextran sulfate sodium (DSS)-induced colitis. Dig. Dis. Sci. 53: 2464-2473.
25. Ishikawa, D., T. Sasaki, T. Osada, K. Kuwahara-Arai, K. Haga, T. Shibuya, K. Hiramatsu, and S. Watanabe. 2017. Changes in intestinal microbiota following combination therapy with fecal microbial transplantation and antibiotics for ulcerative colitis. Inflamm. Bowel Dis. 23: 116-125.
26. Turner, S., K. M. Pryer, V. P. Miao, and J. D. Palmer. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46: 327-338.
27. Camacho, C., G. Coulouris, V. Avagyan, N. Ma, J. Papadopoulos, K. Bealer, and T. L. Madden. 2009. BLAST+: Architecture and applications. BMC Bioinformatics 10: 421.
28. Huson, D. H., S. Mitra, H. J. Ruscheweyh, N. Weber, and S. C. Schuster. 2011. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21: 1552-1560.
29. Marques, F. Z., E. Nelson, P. Y. Chu, D. Horlock, A. Fiedler, M. Ziemann, J. K. Tan, S. Kuruppu, N. W. Rajapakse, A. El-Osta, et al. 2016. High fibre diet and acetate supplementation change the gut microbiota and prevent the development of hypertension and heart failure in DOCA-salt hypertensive mice. Circulation. 135: 964-977.
30. Trompette, A., E. S. Gollwitzer, K. Yadava, A. K. Sichelstiel, N. Sprenger, C. Ngom-Bru, C. Blanchard, T. Junt, L. P. Nicod, N. L. Harris, and B. J. Marsland. 2014. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20: 159-166.
31. Clark, D. A. 2016. The importance of being a regulatory T cell in pregnancy. J. Reprod. Immunol. 116: 60-69.
32. Fontenot, J. D., J. L. Dooley, A. G. Farr, and A. Y. Rudensky. 2005. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202: 901-906.
33. Weiss, J. M., A. M. Bilate, M. Gobert, Y. Ding, M. A. Curotto de Lafaille, C. N. Parkhurst, H. Xiong, J. Dolpady, A. B. Frey, M. G. Ruocco, et al. 2012. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 209: 1723-1742, S1721.
34. Yadav, M., C. Louvet, D. Davini, J. M. Gardner, M. Martinez-Llordella, S. Bailey-Bucktrout, B. A. Anthony, F. M. Sverdrup, R. Head, D. J. Kuster, et al. 2012. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209: 1713-1722.
35. Nitta, T., I. Ohigashi, and Y. Takahama. 2013. The development of T lymphocytes in fetal thymus organ culture. Methods Mol. Biol. 946: 85-102.
36. Kimura, I., K. Ozawa, D. Inoue, T. Imamura, K. Kimura, T. Maeda, K. Terasawa, D. Kashihara, K. Hirano, T. Tani, et al. 2013. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4: 1829.
37. Lin, J., L. Yang, H. M. Silva, A. Trzeciak, Y. Choi, S. R. Schwab, M. L. Dustin, and J. J. Lafaille. 2016. Increased generation of Foxp3(+) regulatory T cells by manipulating antigen presentation in the thymus. Nat. Commun. 7: 10562.
38. Matsumoto, M., Y. Nishikawa, H. Nishijima, J. Morimoto, M. Matsumoto, and Y. Mouri. 2013. Which model better fits the role of aire in the establishment of self-Tolerance: The transcription model or the maturation model? Front. Immunol. 4: 210.
39. Aschenbrenner, K., L. M. DCruz, E. H. Vollmann, M. Hinterberger, J. Emmerich, L. K. Swee, A. Rolink, and L. Klein. 2007. Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat. Immunol. 8: 351-358.
40. Akiyama, T., Y. Shimo, H. Yanai, J. Qin, D. Ohshima, Y. Maruyama, Y. Asaumi, J. Kitazawa, H. Takayanagi, J. M. Penninger, et al. 2008. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-Tolerance. [Published erratum appears in 2013 Immunity 39: 796.] Immunity 29: 423-437.
41. Hikosaka, Y., T. Nitta, I. Ohigashi, K. Yano, N. Ishimaru, Y. Hayashi, M. Matsumoto, K. Matsuo, J. M. Penninger, H. Takayanagi, et al. 2008. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 29: 438-450.
42. Anderson, M. S., and M. A. Su. 2016. AIRE expands: new roles in immune tolerance and beyond. Nat. Rev. Immunol. 16: 247-258.
43. Guerau-de-Arellano, M., M. Martinic, C. Benoist, and D. Mathis. 2009. Neonatal tolerance revisited: A perinatal window for Aire control of autoimmunity. J. Exp. Med. 206: 1245-1252.
44. Singh, N., A. Gurav, S. Sivaprakasam, E. Brady, R. Padia, H. Shi, M. Thangaraju, P. D. Prasad, S. Manicassamy, D. H. Munn, et al. 2014. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40: 128-139.