The salivary IgA flow rate is increased by high concentrations of short-chain fatty acids in the cecum of rats ingesting fructooligosaccharides

Nutrients

Volumn 8, Issue 8, 2016, Pages

  Yamamoto, Yuko ^a   Takahahi, Toru ^b   To, Masahiro ^a   Nakagawa, Yusuke ^a   Hayashi, Takashi ^a   Shimizu, Tomoko ^a   Kamata, Yohei ^a   Saruta, Juri ^a   Tsukinoki, Keiichi ^a  

^a KANAGAWA DENTAL COLLEGE   (Japan)

^b FUKUOKA WOMEN'S UNIVERSITY   (Japan)

Author keywords

Fructooligosaccharides; IgA; Rats; Saliva; Short chain fatty acid

Indexed keywords

BENZYLSULFONYL FLUORIDE; FRUCTOSE OLIGOSACCHARIDE; HORSERADISH PEROXIDASE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN A ANTIBODY; PENTOBARBITAL; PILOCARPINE; SALIVA PROTEIN; SHORT CHAIN FATTY ACID; TETRAMETHYLBENZIDINE; OLIGOSACCHARIDE; SECRETORY IMMUNOGLOBULIN; VOLATILE FATTY ACID;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CECUM; CONTROLLED STUDY; DIET RESTRICTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW RATE; FOOD INTAKE; MALE; MUCOSAL IMMUNITY; NEWBORN; NONHUMAN; RANDOMIZED CONTROLLED TRIAL; RAT; SALIVA; SUBMANDIBULAR GLAND; ANIMAL; BODY WEIGHT; EATING; FERMENTATION; IMMUNOLOGY; METABOLISM; POSTPRANDIAL STATE; SECRETION (PROCESS); SECRETION RATE; WISTAR RAT;

ANIMALS; BODY WEIGHT; CECUM; EATING; FATTY ACIDS, VOLATILE; FERMENTATION; IMMUNOGLOBULIN A, SECRETORY; MALE; OLIGOSACCHARIDES; POSTPRANDIAL PERIOD; RATS; RATS, WISTAR; SALIVA; SECRETORY RATE; SUBMANDIBULAR GLAND;

EID: 84983315635     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu8080500     Document Type: Article

References (47)

1. Kiyono, H.; Azegami, T. The mucosal immune system: From dentistry to vaccine development. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2015, 91, 423–439.
2. Diamond, G.; Beckloff, N.; Ryan, L.K. Host defense peptides in the oral cavity and the lung: Similarities and differences. J. Dent. Res. 2008, 87, 915–927.
3. Shimizu, K.; Sato, H.; Suga, Y.; Yamahira, S.; Toba, M.; Hamuro, K.; Kakumoto, K.; Kohda, N.; Akama, T.; Kono, I. et al. The effects of Lactobacillus pentosus strain b240 and appropriate physical training on salivary secretory IgA levels in elderly adults with low physical fitness: A randomized, double-blind, placebo-controlled trial. J. Clin. Biochem. Nutr. 2014, 54, 61–66.
4. Salvatori, O.; Puri, S.; Tati, S.; Edgerton, M. Innate immunity and saliva in Candida albicans-mediated oral diseases. J. Dent. Res. 2016, 95, 365–371.
5. Caballé-Serrano, J.; Cvikl, B.; Bosshardt, D.D.; Buser, D.; Lussi, A.; Gruber, R. Saliva suppresses osteoclastogenesis in murine bone marrow cultures. J. Dent. Res. 2015, 94, 192–200.
6. Dawes, C.; Pedersen, A.M.; Villa, A.; Ekström, J.; Proctor, G.B.; Vissink, A.; Aframian, D.; McGowan, R.; Aliko, A.; Narayana, N., et al. The functions of human saliva: A review sponsored by the World Workshop on Oral Medicine VI. Arch. Oral Biol. 2015, 60, 863–874.
7. Hanson, L.A.; Ahlstedt, S.; Andersson, B.; Carlsson, B.; Cole, M.F.; Cruz, J.R.; Dahlgren, U.; Ericsson, T.H.; Jalil, F.; Khan, S.R., et al. Mucosal immunity. Ann. N. Y. Acad. Sci. 1983, 409, 1–21.
8. Tomasi, T.B. The discovery of secretory IgA and the mucosal immune system. Immunol. Today 1992, 13, 416–418.
9. Oliver, S.J.; Laing, S.J.; Wilson, S.; Bilzon, J.L.; Walters, R.; Walsh, N.P. Salivary immunoglobulin A response at rest and after exercise following a 48 h period of fluid and/or energy restriction. Br. J. Nutr. 2007, 97, 1109–1116.
10. Isaacs, D.; Webster, A.D.; Valman, H.B. Immunoglobulin levels and function in pre-school children with recurrent respiratory infections. Clin. Exp. Immunol. 1984, 58, 335–340.
11. Ostergaard, P.A. Clinical and immunological features of transient IgA deficiency in children. Clin. Exp. Immunol. 1980, 40, 561–565.
12. Tenovuo, J.; Gråhn, E.; Lehtonen, O.P.; Hyyppä, T.; Karhuvaara, L.; Vilja, P. Antimicrobial factors in saliva: Ontogeny and relation to oral health. J. Dent. Res. 1987, 66, 475–479.
13. Tanida, T.; Ueta, E.; Tobiume, A.; Hamada, T.; Rao, F.; Osaki, T. Influence of aging on candidal growth and adhesion regulatory agents in saliva. J. Oral Pathol. Med. 2001, 30, 328–335.
14. Schley, P.D.; Field, C. The immune-enhancing effects of dietary fibres and prebiotics. Br. J. Nutr. 2002, 87, 221–230.
15. Nakamura, Y.; Nosaka, S.; Suzuki, M.; Nagafuchi, S.; Takahashi, T.; Yajima, T.; Takenouchi-Ohkubo, N.; Iwase, T. Moro, I. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin. Exp. Immunol. 2004, 137, 52–58.
16. Komura, M.; Fukuta, T.; Genda, T.; Hino, S.; Aoe, S.; Kawagishi, H.; Morita, T. A short-term ingestion of fructo-oligosaccharides increases immunoglobulin A and mucin concentrations in the rat cecum, but the effects are attenuated with the prolonged ingestion. Biosci. Biotechnol. Biochem. 2014, 78, 1592–1602.
17. Kato, T.; Fukuda, S.; Fujiwara, A.; Suda, W.; Hattori, M.; Kikuchi, J.; Ohno, H. Multiple omics uncovers host-gut microbial mutualism during prebiotic fructooligosaccharide supplementation. DNA Res. 2014, 21, 469–480.
18. Tezuka, H.; Abe, Y.; Asano, J.; Sato, T.; Liu, J.; Iwata, M.; Ohteki, T. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 2011, 34, 247–257.
19. Jinno, S.; Nakamura, Y.; Nagata, M.; Takahashi, T. 1-Kestose consumption during pregnancy and lactation increases the levels of IgA in the milk of lactating mice. Biosci. Biotechnol. Biochem. 2014, 78, 861–866.
20. Yamamoto, Y.; To, M.; Hayashi, T.; Shimizu, T.; Kamata, Y.; Saruta, J.; Takahashi, T.; Tsukinoki, K. Intake of indigestible carbohydrates influences IgA response and polymeric Ig receptor expression in the rat submandibular gland. Br. J. Nutr. 2015, 113, 1895–1902.
21. Frost, G.S.; Walton, G.E.; Swann, J.R.; Psichas, A.; Costabile, A.; Johnson, L.P.; Sponheimer, M.; Gibson, G.R.; Barraclough, T.G. Impacts of plant-based foods in ancestral hominin diets on the metabolism and function of gut microbiota in vitro. mBio 2014, 5, e00853-14.
22. Otles, S.; Ozgoz, S. Health effects of dietary fiber. Acta Sci. Pol. Technol. Aliment. 2014, 13, 191–202.
23. Cresci, A.; Orpianesi, C.; Silvi, S.; Mastrandrea, V.; Dolara, P. The effect of sucrose or starch-based diet on short-chain fatty acids and faecal microflora in rats. J. Appl. Microbiol. 1999, 86, 245–250.
24. Tsukahara, T.; Matsukawa, N.; Tomonaga, S.; Inoue, R.; Ushida, K.; Ochiai, K. High-sensitivity detection of short-chain fatty acids in porcine ileal, cecal, portal and abdominal blood by gas chromatography-mass spectrometry. Anim. Sci. J. 2014, 85, 494–498.
25. Maglogiannis, I.; Zafiropoulos, E.; Platis, A.; Lambrinoudakis, C. Risk analysis of a patient monitoring system using Bayesian Network modeling. J. Biomed. Inform. 2006, 39, 637–647.
26. Soto, E.J.; Gambino, L.O.; Mustafá, E.R. Free fatty acid receptor 3 is a key target of short chain fatty acid. What is the impact on the sympathetic nervous system? Channels 2014, 8, 169–171.
27. Kimura, I.; Ozawa, K.; Inoue, D.; Imamura, T.; Kimura, K.; Maeda, T.; Terasawa, K.; Kashihara, D.; Hirano, K.; Tani, T., et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 2013, 4, 1829.
28. Won, Y.J.; Lu, V.B.; Puhl, H.L.; Ikeda, S.R. β-Hydroxybutyrate modulates N-type calcium channels in rat sympathetic neurons by acting as an agonist for the G-protein-coupled receptor FFA3. J. Neurosci. 2013, 33, 19314–19325.
29. Kimura, I.; Inoue, D.; Maeda, T.; Hara, T.; Ichimura, A.; Miyauchi, S.; Kobayashi, M.; Hirasawa, A.; Tsujimoto, G. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc. Natl. Acad. Sci. USA 2011, 108, 8030–8035.
30. Nøhr, M.K.; Egerod, K.L.; Christiansen, S.H.; Gille, A.; Offermanns, S.; Schwartz, T.W.; Møller, M. Expression of the short chain fatty acid receptor GPR41/FFAR3 in autonomic and somatic sensory ganglia. Neuroscience 2015, 290, 126–137.
31. Sakata, T. Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: A possible explanation for trophic effects of fermentable fibre, gut microbes and luminal trophic factors. Br. J. Nutr. 1987, 58, 95–103.
32. Sakata, T.; von Engelhardt, W. Stimulatory effect of short chain fatty acids on the epithelial cell proliferation in rat large intestine. Comp. Biochem. Physiol. A Comp. Physiol. 1983, 74, 459–462.
33. Carpenter, G.H.; Garrett, J.R.; Hartley, R.H.; Proctor, G.B. The influence of nerves on the secretion of immunoglobulin A into submandibular saliva in rats. J. Physiol. 1998, 512, 567–573.
34. Carpenter, G.H.; Proctor, G.B.; Anderson, L.C.; Zhang, X.S.; Garrett, J.R. Immunoglobulin A secretion into saliva during dual sympathetic and parasympathetic nerve stimulation of rat submandibular glands. Exp. Physiol. 2000, 85, 281–286.
35. Liu, C.; Hashizume, T.; Kurita-Ochiai, T.; Fujihashi, K.; Yamamoto, M. Oral immunization with Porphyromonas gingivalis outer membrane protein and CpGoligodeoxynucleotides elicits T helper 1 and 2 cytokines for enhanced protective immunity. Mol. Oral Microbiol. 2010, 25, 178–189.
36. Kataoka, K.; Fujihashi, K.; Sekine, S.; Fukuiwa, T.; Kobayashi, R.; Suzuki, H.; Nagata, H.; Takatsu, K.; Shizukuishi, S.; McGhee, J.R., et al. Nasal cholera toxin elicits IL-5 and IL-5 receptor alpha-chain expressing B-1a B cells for innate mucosal IgA antibody responses. J. Immunol. 2007, 178, 6058–6065.
37. Clancy, R.L.; Cripps, A.W.; Husband, A.J.; Buckley, D. Specific immune response in the respiratory tract after administration of an oral polyvalent bacterial vaccine. Infect. Immun. 1983, 39, 491–496.
38. Proctor, G.B.; Carpenter, G.H.; Anderson, L.C.; Garrett, J.R. Nerve-evoked secretion of immunoglobulin A in relation to other proteins by parotid glands in anaesthetized rat. Exp. Physiol. 2000, 85, 511–518.
39. Kikuchi, H.; Sakata, T. Qualitative and quantitative estimation of soluble indigestible polysaccharides as substrate for hindgut fermentation by mini-scale batch culture. J. Nutr. Sci. Vitaminol. 1992, 38, 287–296.
40. Strugnell, R.A.; Wijburg, O.L. The role of secretory antibodies in infection immunity. Nat. Rev. Microbiol. 2010, 8, 656–667.
41. Lecerf, J.M.; Dépeint, F.; Clerc, E.; Dugenet, Y.; Niamba, C.N.; Rhazi, L.; Cayzeele, A.; Abdelnour, G.; Jaruga, A.; Younes, H., et al. Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties. Br. J. Nutr. 2012, 108, 1847–1858.
42. Şahin, A.; Aslan, A.; Baş, O.; İkinci, A.; Özyılmaz, C.; Sönmez, O.F.; Çolakoğlu, S.; Odacı, E. Deleterious impacts of a 900-MHz electromagnetic field on hippocampal pyramidal neurons of 8-week-old Sprague Dawley male rats. Brain Res. 2015, 1624, 232–238.
43. Romero, M.R.; Lozano, M.L.; Posada, C.; Rueda, P.A.; Roa, N.S.; Rodríguez, A. Immunoglobulin A, G and M levels in saliva in children between 3–12 years of age, healthy and with gingivitis. Acta Odontol. Latinoam. 2011, 24, 176–182.
44. Blay, G.L.; Michel, C.; Blottière, H.M.; Cherbut, C. Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. J. Nutr. 1999, 129, 2231–2235.
45. Han, K.H.; Kobayashi, Y.; Nakamura, Y.; Shimada, K.; Aritsuka, T.; Ohba, K.; Morita, T.; Fukushima, M. Comparison of the effects of longer chain inulins with different degrees of polymerization on colonic fermentation in a mixed culture of Swine fecal bacteria. J. Nutr. Sci. Vitaminol. 2014, 60, 206–212.
46. Schroeder, N.; Marquart, L.F.; Gallaher, D.D. The role of viscosity and fermentability of dietary fibers on satiety- and adiposity-related hormones in rats. Nutrients 2013, 5, 2093–2113.
47. Nakamura, S.; Tanabe, K.; Morita, S.; Hamaguchi, N.; Shimura, F.; Oku, T. Metabolism and bioavailability of newly developed dietary fiber materials, resistant glucan and hydrogenated resistant glucan, in rats and humans. Nutr. Metab. 2016, 13, 13.