Skip to main content

Advertisement

SpringerLink
Log in

Differential modulation in the functions of intestinal dendritic cells by long- and medium-chain fatty acids

  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

Although dendritic cells (DCs) play significant roles in intestinal immune responses, little is known regarding the direct effects of luminal foods on DC functions in the intestinal mucosa. In this study, we examined the effects of fatty acids (FAs) with various chain length on the phagocytic function, antigen presentation, and chemotaxis of intestinal DCs.

Methods

DCs obtained from the thoracic duct lymph of mesenteric lymphadenectomized rats were cultured with long [arachidonic acid (AA) or oleic acid] or medium (octanoic acid) chain FAs with interleukin-4 and granulocyte macrophage-colony stimulating factor. Tumor necrosis factor-α was added in the maturation group. Phagocytic function was examined by the intake of fluorescent microbeads. The expression of cell surface molecules was determined by immunocytochemistry or fluorescence-activated cell sorting (FACS). Antigen presentation ability was evaluated by coincubating keyhole limpet hemocyanin (KLH)-sensitized spleen lymphocytes and KLH-pulsed DCs. Migratory ability of DCs toward the chemokines CC chemokine ligand (CCL) 20 and CCL21 was also assessed.

Results

There was a maturation-induced decrease in phagocytic function, and an increased expression of major histocompatibility complex (MHC) class II molecules. Exposure of DCs to both long- and medium-chain FAs maintained phagocytic ability. The expression of MHC class II molecules was significantly suppressed only by long-chain FAs. The expression of costimulatory factors was suppressed only by AA. Long- but not medium-chain FAs suppressed the antigen presentation ability of DCs induced by maturation. Chemotactic ability of mature DCs toward CCL21 was abrogated only by long-chain FAs.

Conclusions

The data suggest that intraluminal exposure to long- and medium-chain FAs may differentially modulate the immune functions of intestinal DCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Y Tsuzuki S Miura I Kurose M Suematsu H Higuchi T Shigematsu et al. (1997) ArticleTitleEnhanced lymphocyte interaction in postcapillary venules of Peyer's patches during fat absorption in rats Gastroenterology 112 813–25 Occurrence Handle10.1053/gast.1997.v112.pm9041243 Occurrence Handle1:STN:280:DyaK2s7ptlKmug%3D%3D Occurrence Handle9041243

    Article  CAS  PubMed  Google Scholar 

  2. H Yoshida S Miura H Kishikawa M Hirokawa H Nakamizo RC Nakatsumi et al. (2001) ArticleTitleFatty acids enhance GRO/CINC-1 and interleukin-6 production in rat intestinal epithelial cells J Nutr 131 2943–50 Occurrence Handle1:CAS:528:DC%2BD3MXosVykt78%3D Occurrence Handle11694623

    CAS  PubMed  Google Scholar 

  3. A Andoh H Takaya Y Araki T Tsujikawa Y Fujiyama T Bamba (2000) ArticleTitleMedium- and long-chain fatty acids differentially modulate interleukin-8 secretion in human fetal intestinal epithelial cells J Nutr 130 2636–40 Occurrence Handle1:CAS:528:DC%2BD3cXnvVOlsbg%3D Occurrence Handle11053499

    CAS  PubMed  Google Scholar 

  4. D Breitfeld L Ohl E Kremmer J Ellwart F Sallusto M Lipp et al. (2000) ArticleTitleFollicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production J Exp Med 192 1545–52 Occurrence Handle10.1084/jem.192.11.1545 Occurrence Handle1:CAS:528:DC%2BD3cXosF2ntrw%3D Occurrence Handle11104797

    Article  CAS  PubMed  Google Scholar 

  5. GJ Dougherty S Murdoch N Hogg (1988) ArticleTitleThe function of human intercellular adhesion molecule-1 (ICAM-1) in the generation of an immune response Eur J Immunol 18 35–9 Occurrence Handle1:CAS:528:DyaL1cXhsVyks7g%3D Occurrence Handle3257922

    CAS  PubMed  Google Scholar 

  6. BL Kelsall CA Biron O Sharma PM Kaye (2002) ArticleTitleDendritic cells at the host–pathogen interface Nat Immunol 3 699–702 Occurrence Handle10.1038/ni0802-699 Occurrence Handle1:CAS:528:DC%2BD38Xls1SntbY%3D Occurrence Handle12145651

    Article  CAS  PubMed  Google Scholar 

  7. CA Janeway SuffixJr PJ Conrad EA Lerner J Babich P Wettstein DB Murphy (1984) ArticleTitleMonoclonal antibodies specific for Ia glycoproteins raised by immunization with activated T cells: possible role of T cell-bound Ia antigens as targets of immunoregulatory T cells J Immunol 132 662–7 Occurrence Handle6228596

    PubMed  Google Scholar 

  8. SY Tseng M Otsuji K Gorski X Huang JE Slansky SI Pai et al. (2001) ArticleTitleB7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells J Exp Med 193 839–46 Occurrence Handle10.1084/jem.193.7.839 Occurrence Handle1:CAS:528:DC%2BD3MXisVyhurg%3D Occurrence Handle11283156

    Article  CAS  PubMed  Google Scholar 

  9. A Iwasaki BL Kelsall (2000) ArticleTitleLocalization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine J Exp Med 191 1381–94 Occurrence Handle10.1084/jem.191.8.1381 Occurrence Handle1:CAS:528:DC%2BD3cXislSitbo%3D Occurrence Handle10770804

    Article  CAS  PubMed  Google Scholar 

  10. M Rescigno G Rotta B Valzasina P Ricciardi-Castagnoli (2001) ArticleTitleDendritic cells shuttle microbes across gut epithelial monolayers Immunobiology 204 572–81 Occurrence Handle10.1078/0171-2985-00094 Occurrence Handle1:STN:280:DC%2BD387hsVShuw%3D%3D Occurrence Handle11846220

    Article  CAS  PubMed  Google Scholar 

  11. M Rescigno M Urbano B Valzasina M Francolini G Rotta R Bonasio et al. (2001) ArticleTitleDendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria Nat Immunol 2 361–7 Occurrence Handle10.1038/86373 Occurrence Handle1:CAS:528:DC%2BD3MXis1aktbo%3D Occurrence Handle11276208

    Article  CAS  PubMed  Google Scholar 

  12. MC Udey RD Peck AP Pentland GF Schreiner JB Lefkowith (1991) ArticleTitleAntigen-presenting cells in essential fatty acid-deficient murine epidermis: keratinocytes bearing class II (Ia) antigens may potentiate the accessory cell function of Langerhans cells J Invest Dermatol 96 950–8 Occurrence Handle10.1111/1523-1747.ep12475701 Occurrence Handle1:CAS:528:DyaK3MXltlemtbs%3D Occurrence Handle1828477

    Article  CAS  PubMed  Google Scholar 

  13. D Hwang (1989) ArticleTitleEssential fatty acids and immune response FASEB J 3 2052–61 Occurrence Handle1:CAS:528:DyaL1MXkslGqurk%3D Occurrence Handle2501132

    CAS  PubMed  Google Scholar 

  14. P Sanderson GG MacPherson CH Jenkins PC Calder (1997) ArticleTitleDietary fish oil diminishes the antigen presentation activity of rat dendritic cells J Leukoc Biol 62 771–7 Occurrence Handle1:CAS:528:DyaK2sXnvFSqtrw%3D Occurrence Handle9400818

    CAS  PubMed  Google Scholar 

  15. P Sanderson F Thies PC Calder (2000) ArticleTitleExtracellular release of free fatty acids by rat T lymphocytes is stimulus-dependent and is affected by dietary lipid manipulation Cell Biochem Funct 18 47–58 Occurrence Handle10.1002/(SICI)1099-0844(200001/03)18:1<47::AID-CBF848>3.0.CO;2-8 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Smsb0%3D Occurrence Handle10686583

    Article  CAS  PubMed  Google Scholar 

  16. JL Bollman JC Cain JH Grindlay (1948) ArticleTitleTechniques for collection of lymph from liver, small intestine, or thoracic duct of the rat J Lab Clin Med 33 1349–52 Occurrence Handle18886337 Occurrence Handle1:STN:280:DyaH1c%2FjtVSrtg%3D%3D

    PubMed  CAS  Google Scholar 

  17. SC Knight J Farrant A Bryant AJ Edwards S Burman A Lever et al. (1986) ArticleTitleNon-adherent, low-density cells from human peripheral blood contain dendritic cells and monocytes, both with veiled morphology Immunology 57 595–603 Occurrence Handle1:STN:280:DyaL287ms1KltQ%3D%3D Occurrence Handle3007336

    CAS  PubMed  Google Scholar 

  18. EJ Bates A Ferrante DP Harvey A Poulos (1993) ArticleTitlePolyunsaturated fatty acids increase neutrophil adherence and integrin receptor expression J Leukoc Biol 53 420–6 Occurrence Handle1:CAS:528:DyaK3sXlsF2jt7s%3D Occurrence Handle8097761

    CAS  PubMed  Google Scholar 

  19. P Yaqoob EA Newsholme PC Calder (1994) ArticleTitleThe effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation Immunology 82 603–10 Occurrence Handle1:CAS:528:DyaK2MXkvVSjtw%3D%3D Occurrence Handle7835924

    CAS  PubMed  Google Scholar 

  20. K Kusugami T Ando M Ohsuga A Imada M Shinoda T Konagaya et al. (1997) ArticleTitleMucosal chemokine activity in Helicobacter pylori infection J Clin Gastroenterol 25 Suppl 1 S203–10 Occurrence Handle10.1097/00004836-199700001-00032 Occurrence Handle1:STN:280:DyaK1c7ktVaktA%3D%3D Occurrence Handle9479649

    Article  CAS  PubMed  Google Scholar 

  21. S Basak A Harui M Stolina S Sharma K Mitani S Dubinett et al. (2002) ArticleTitleIncreased dendritic cell number and function following continuous in vivo infusion of granulocyte macrophage-colony-stimulating factor and interleukin-4 Blood 99 2869–79 Occurrence Handle10.1182/blood.V99.8.2869 Occurrence Handle1:CAS:528:DC%2BD38XivV2jsr0%3D Occurrence Handle11929777

    Article  CAS  PubMed  Google Scholar 

  22. Y Hara S Miura S Komoto T Ogino S Koseki H Fujimori et al. (2000) ArticleTitleEffect of fatty acids of different chain length on interferon-gamma production from intraepithelial lymphocyte Gastroenterology 118 A557 Occurrence Handle10.1016/S0016-5085(00)82361-6

    Article  Google Scholar 

  23. MK Matyszak JL Young JS Gaston (2002) ArticleTitleUptake and processing of Chlamydia trachomatis by human dendritic cells Eur J Immunol 32 742–51 Occurrence Handle10.1002/1521-4141(200203)32:3<742::AID-IMMU742>3.0.CO;2-9 Occurrence Handle1:CAS:528:DC%2BD38Xitl2ns70%3D Occurrence Handle11870618

    Article  CAS  PubMed  Google Scholar 

  24. N Haicheur E Bismuth S Bosset O Adotevi G Warnier V Lacabanne et al. (2000) ArticleTitleThe B subunit of Shiga toxin fused to a tumor antigen elicits CTL and targets dendritic cells to allow MHC class I-restricted presentation of peptides derived from exogenous antigens J Immunol 165 3301–8 Occurrence Handle1:CAS:528:DC%2BD3cXmslyntLw%3D Occurrence Handle10975847

    CAS  PubMed  Google Scholar 

  25. CC Leslie (1997) ArticleTitleProperties and regulation of cytosolic phospholipase A2 J Biol Chem 272 16709–12 Occurrence Handle10.1074/jbc.272.27.16709 Occurrence Handle1:CAS:528:DyaK2sXksVentb8%3D Occurrence Handle9201969

    Article  CAS  PubMed  Google Scholar 

  26. H Harizi M Juzan V Pitard JF Moreau N Gualde (2002) ArticleTitleCyclooxygenase-2-issued prostaglandin E(2) enhances the production of endogenous IL-10, which down-regulates dendritic cell functions J Immunol 168 2255–63 Occurrence Handle1:CAS:528:DC%2BD38XhvVegsrs%3D Occurrence Handle11859113

    CAS  PubMed  Google Scholar 

  27. HK Takahashi H Iwagaki T Yoshino S Mori T Morichika H Itoh et al. (2002) ArticleTitleProstaglandin E(2) inhibits IL-18-induced ICAM-1 and B7.2 expression through EP2/EP4 receptors in human peripheral blood mononuclear cells J Immunol 168 4446–54 Occurrence Handle1:CAS:528:DC%2BD38Xjt12jtrg%3D Occurrence Handle11970988

    CAS  PubMed  Google Scholar 

  28. B Canque S Camus M Yagello JC Gluckman (1998) ArticleTitleIL-4 and CD40 ligation affect differently the differentiation, maturation, and function of human CD34+ cell-derived CD1a+CD14- and CD1a-CD14+ dendritic cell precursors in vitro J Leukoc Biol 64 235–44 Occurrence Handle1:CAS:528:DyaK1cXltFyls74%3D Occurrence Handle9715264

    CAS  PubMed  Google Scholar 

  29. AA Nash BM Dutia JP Stewart AJ Davison (2001) ArticleTitleNatural history of murine gamma-herpesvirus infection Philos Trans R Soc Lond B Biol Sci 356 569–79 Occurrence Handle1:CAS:528:DC%2BD3MXltFWgtrk%3D Occurrence Handle11313012 Occurrence Handle10.1098/rstb.2000.0779

    Article  CAS  PubMed  Google Scholar 

  30. L Liu EJ Usherwood MA Blackman DL Woodland (1999) ArticleTitleT-cell vaccination alters the course of murine herpesvirus 68 infection and the establishment of viral latency in mice J Virol 73 9849–57 Occurrence Handle1:CAS:528:DyaK1MXnsV2mtrs%3D Occurrence Handle10559297

    CAS  PubMed  Google Scholar 

  31. RK Pai D Askew WH Boom CV Harding (2002) ArticleTitleRegulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator J Immunol 169 1326–33 Occurrence Handle1:CAS:528:DC%2BD38XlslWhsbo%3D Occurrence Handle12133955

    CAS  PubMed  Google Scholar 

  32. H Kobayashi S Miura H Nagata Y Tsuzuki R Hokari T Ogino et al. (2004) ArticleTitleIn situ demonstration of dendritic cell migration from rat intestine to mesenteric lymph nodes: relationships to maturation and role of chemokines J Leukoc Biol 75 434–42 Occurrence Handle10.1189/jlb.0603250 Occurrence Handle1:CAS:528:DC%2BD2cXis1ehs74%3D Occurrence Handle14673014

    Article  CAS  PubMed  Google Scholar 

  33. R Forster A Schubel D Breitfeld E Kremmer I Renner-Muller E Wolf et al. (1999) ArticleTitleCCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs Cell 99 23–33 Occurrence Handle10.1016/S0092-8674(00)80059-8 Occurrence Handle1:CAS:528:DyaK1MXmsleqs7o%3D Occurrence Handle10520991

    Article  CAS  PubMed  Google Scholar 

  34. F Boisleve S Kerdine-Romer N Rougier-Larzat M Pallardy (2004) ArticleTitleNickel and DNCB induce CCR7 expression on human dendritic cells through different signalling pathways: role of TNF-alpha and MAPK J Invest Dermatol 123 494–502 Occurrence Handle10.1111/j.0022-202X.2004.23229.x Occurrence Handle1:CAS:528:DC%2BD2cXnsValt7c%3D Occurrence Handle15304089

    Article  CAS  PubMed  Google Scholar 

  35. R Shoda K Matsueda S Yamato N Umeda (1996) ArticleTitleEpidemiologic analysis of Crohn disease in Japan: increased dietary intake of n-6 polyunsaturated fatty acids and animal protein related to the increased incidence of Crohn disease in Japan Am J Clin Nutr 63 741–5 Occurrence Handle1:STN:280:DyaK283gsV2msQ%3D%3D Occurrence Handle8615358

    CAS  PubMed  Google Scholar 

  36. N Sakamoto S Kono K Wakai Y Fukuda M Satomi T Shimoyama et al. (2005) ArticleTitleEpidemiology Group of the Research Committee on Inflammatory Bowel Disease in Japan Inflamm Bowel Dis 11 154–63 Occurrence Handle10.1097/00054725-200502000-00009 Occurrence Handle15677909

    Article  PubMed  Google Scholar 

  37. B Johansson-Lindbom M Svensson MA Wurbel B Malissen G Marquez W Agace (2003) ArticleTitleSelective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant J Exp Med 198 963–9 Occurrence Handle10.1084/jem.20031244 Occurrence Handle1:CAS:528:DC%2BD3sXnsV2ntb8%3D Occurrence Handle12963696

    Article  CAS  PubMed  Google Scholar 

  38. JR Mora MR Bono N Manjunath W Weninger LL Cavanagh M Rosemblatt et al. (2003) ArticleTitleSelective imprinting of gut-homing T cells by Peyer's patch dendritic cells Nature 424 88–93 Occurrence Handle10.1038/nature01726 Occurrence Handle1:CAS:528:DC%2BD3sXltVelsLs%3D Occurrence Handle12840763

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Second Department of Internal Medicine, National Defense Medical College, 3-2 Namiki, Tokorozawa, 359-8513, Japan

    Yoshikazu Tsuzuki, Jyunichi Miyazaki, Koji Matsuzaki, Yoshikiyo Okada, Ryota Hokari, Atsushi Kawaguchi, Shigeaki Nagao, Kazuro Itoh & Soichiro Miura

Authors
  1. Yoshikazu Tsuzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jyunichi Miyazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koji Matsuzaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoshikiyo Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ryota Hokari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Atsushi Kawaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shigeaki Nagao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kazuro Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Soichiro Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsuzuki, Y., Miyazaki, J., Matsuzaki, K. et al. Differential modulation in the functions of intestinal dendritic cells by long- and medium-chain fatty acids. J Gastroenterol 41, 209–216 (2006). https://doi.org/10.1007/s00535-005-1747-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-005-1747-0

Key words

Search

Navigation