Epithelial Cells Orchestrate the Functions of Dendritic Cells in Intestinal Homeostasis

Tianming Li; Mei Liu; Siyu Sun; Xuying Liu; Dongyan Liu*

Tianming Li, Mei Liu, Siyu Sun, Xuying Liu and Dongyan Liu*

Volume1-Issue7
Dates: Received: 2020-11-13 | Accepted: 2020-11-23 | Published: 2020-11-24
Pages: 343-352

Abstract

The gastrointestinal tract represents the largest mucosal membrane surface and is the one of the most complex human organs. The intestinal barrier dysfunction contributes to systemic immune activation. The mucosal immune system has extremely arduous tasks to resist invaders and promote tolerance of food antigens and the microbiota. The intestinal mucosal immune system fulfills these tasks through complex interactions between immune cells and the local microenvironment in intestine. Intestinal Epithelial Cells (IECs) play important roles in these complex interactions. IECs not only constitute the first barrier of the intestine but also are crucial for integrating external and internal signals and for coordinating the ensuing immune response. Dendritic Cells (DCs) play key roles in shaping the intestinal immune response by their ability to coordinate protective immunity and immune tolerance in the host. DCs are pivotal actors in the connection between innate and adaptive immune responses. The IECs coordinate with the DCs in immune recognition, tolerance and host defense mechanisms. In this review, we will summarize how IECs orchestrate intestinal DCs in intestinal homeostasis and diseases.

FullText HTML FullText PDF DOI: 10.37871/jbres1165

Certificate of Publication

Copyright

How to cite this article

Li T, Liu M, Sun S, Liu X, Liu D. Epithelial Cells Orchestrate the Functions If Dendritic Cells in Intestinal Homeostasis. J Biomed Res Environ Sci. 2020 Nov 24; 1(7): 343-352. doi: 10.37871/jbres1165, Article ID: jbres1165

Subject area(s)

Immunotherapy

Immunology

Pediatrics

University/Institute

China Medical University

References

Adachi T, Kakuta S, Aihara Y, Kamiya T, Watanabe Y, Osakabe N, Hazato N, Miyawaki A, Yoshikawa S, Usami T, Karasuyama H, Kimoto-Nira H, Hirayama K, Tsuji NM. Visualization of Probiotic-Mediated Ca2+ Signaling in Intestinal Epithelial Cells In vivo. Front Immunol. 2016 Dec 16;7:601. doi: 10.3389/fimmu.2016.00601. PMID: 28018362; PMCID: PMC5159486.
Nakamura T. Recent progress in organoid culture to model intestinal epithelial barrier functions. International Immunology. 2019 Feb;31(1):13-21
Crawley SW, Mooseker MS, Tyska MJ. Shaping the intestinal brush border. J Cell Biol. 2014 Nov 24;207(4):441-51. doi: 10.1083/jcb.201407015. PMID: 25422372; PMCID: PMC4242837.
Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nature reviews. Gastroenterology & hepatology. 2013 Jun;10:352-361.
Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nature Reviews Immunologyl. 2014 Mar; 14(3):141-153.
Taupin DR, Kinoshita K, Podolsky DK. Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):799-804. doi: 10.1073/pnas.97.2.799. PMID: 10639160; PMCID: PMC15411.
Power KA, Lepp D, Zarepoor L, Jennifer MM, Wenqing W, Rong T, Ronghua L. Dietary flaxseed modulates the colonic microenvironment in healthy C57Bl/6 male mice which may alter susceptibility to gut-associated diseases. Journal Nuture Biochemal 2016 Feb;28:61-69. doi: 10.1016/j.jnutbio.2015.09.028.
McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, Newberry RD, Miller MJ. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature. 2012 Mar 14;483(7389):345-9. doi: 10.1038/nature10863. PMID: 22422267; PMCID: PMC3313460.
Bel S, Pendse M, Wang Y, Li Y, Ruhn KA, Hassell B, Leal T, Winter SE, Xavier RJ, Hooper LV. Paneth cells secrete lysozyme via secretory autophagy during bacterial infection of the intestine. Science. 2017 Sep 8;357(6355):1047-1052. doi: 10.1126/science.aal4677. Epub 2017 Jul 27. PMID: 28751470; PMCID: PMC5702267. .
Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000 Aug;1(2):113-8. doi: 10.1038/77783. PMID: 11248802.
Gerbe F, Legraverend C, Jay P. The intestinal epithelium tuft cells: specification and function. Cell Mol Life Sci. 2012 Sep;69(17):2907-17. doi: 10.1007/s00018-012-0984-7. Epub 2012 Apr 19. PMID: 22527717; PMCID: PMC3417095.
Worthington JJ. The intestinal immunoendocrine axis: novel cross-talk between enteroendocrine cells and the immune system during infection and inflammatory disease. Biochemical Society transaction 2015 Aug;43(4):727-733.
Hansson GC, Johansson ME. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes. 2010 Jan;1(1):51-54. doi: 10.4161/gmic.1.1.10470. PMID: 21327117; PMCID: PMC3035142.
Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Büller HA, Dekker J, Van Seuningen I, Renes IB, Einerhand AW. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006 Jul;131(1):117-29. doi: 10.1053/j.gastro.2006.04.020. PMID: 16831596.
Velcich A, Yang W, Heyer J, Fragale A, Nicholas C, Viani S, Kucherlapati R, Lipkin M, Yang K, Augenlicht L. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science. 2002 Mar 1;295(5560):1726-9. doi: 10.1126/science.1069094. PMID: 11872843.
Roda G, Sartini A, Zambon E, Calafiore A, Marocchi M, Caponi A, Belluzzi A, Roda E. Intestinal epithelial cells in inflammatory bowel diseases. World J Gastroenterol. 2010 Sep 14;16(34):4264-71. doi: 10.3748/wjg.v16.i34.4264. PMID: 20818809; PMCID: PMC2937106.
Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol. 2004 Dec;4(12):953-64. doi: 10.1038/nri1499. PMID: 15573130.
Hansson GC. Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol. 2012 Feb;15(1):57-62. doi: 10.1016/j.mib.2011.11.002. Epub 2011 Dec 14. PMID: 22177113; PMCID: PMC3716454.
Muñoz-Wolf N, Lavelle EC. Innate Immune Receptors. Methods Mol Biol. 2016;1417:1-43. doi: 10.1007/978-1-4939-3566-6_1. PMID: 27221479.
Patel RM, Lin PW. Developmental biology of gut-probiotic interaction. Gut Microbes. 2010 May-Jun;1(3):186-95. doi: 10.4161/gmic.1.3.12484. Epub 2010 May 26. PMID: 21327024; PMCID: PMC3023598.
Walsh D, Carthy McJ, Driscoll OC, Silvia M. Pattern recognition receptors--molecular orchestrators of inflammation in inflammatory bowel disease. Cytokine & growth factor reviews 2013 Apr;24:91-104. doi: 10.1016/j.cytogfr.2012.09.003.
Chan YK, Gack MU. RIG-I-like receptor regulation in virus infection and immunity. Curr Opin Virol. 2015 Jun;12:7-14. doi: 10.1016/j.coviro.2015.01.004. Epub 2015 Jan 30. PMID: 25644461; PMCID: PMC5076476.
Suthar MS, Ramos HJ, Brassil MM, Netland J, Chappell CP, Blahnik G, McMillan A, Diamond MS, Clark EA, Bevan MJ, Gale M Jr. The RIG-I-like receptor LGP2 controls CD8(+) T cell survival and fitness. Immunity. 2012 Aug 24;37(2):235-48. doi: 10.1016/j.immuni.2012.07.004. Epub 2012 Jul 26. PMID: 22841161; PMCID: PMC3910444.
Chiang JJ, Davis ME, Gack MU. Regulation of RIG-I-like receptor signaling by host and viral proteins. Cytokine Growth Factor Rev. 2014 Oct;25(5):491-505. doi: 10.1016/j.cytogfr.2014.06.005. Epub 2014 Jun 21. PMID: 25023063; PMCID: PMC7108356.
Errett JS, Gale M. Emerging complexity and new roles for the RIG-I-like receptors in innate antiviral immunity. Virol Sin. 2015 Jun;30(3):163-73. doi: 10.1007/s12250-015-3604-5. Epub 2015 May 20. PMID: 25997992; PMCID: PMC7090589.
Lee MS, Kim YJ. Pattern-recognition receptor signaling initiated from extracellular, membrane, and cytoplasmic space. Mol Cells. 2007 Feb 28;23(1):1-10. PMID: 17464205.
Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011;29:707-35. doi: 10.1146/annurev-immunol-031210-101405. PMID: 21219188; PMCID: PMC4067317.
Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jéhanno M, Viala J, Tedin K, Taha MK, Labigne A, Zähringer U, Coyle AJ, DiStefano PS, Bertin J, Sansonetti PJ, Philpott DJ. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science. 2003 Jun 6;300(5625):1584-7. doi: 10.1126/science.1084677. PMID: 12791997.
Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003 Mar 14;278(11):8869-72. doi: 10.1074/jbc.C200651200. Epub 2003 Jan 13. PMID: 12527755.
Natividad JM, Petit V, Huang X, de Palma G, Jury J, Sanz Y, Philpott D, Garcia Rodenas CL, McCoy KD, Verdu EF. Commensal and probiotic bacteria influence intestinal barrier function and susceptibility to colitis in Nod1-/-; Nod2-/- mice. Inflamm Bowel Dis. 2012 Aug;18(8):1434-46. doi: 10.1002/ibd.22848. Epub 2011 Dec 11. PMID: 22162005.
Germain A, Guéant RM, Chamaillard M, Allen PB, Bresler L, Guéant JL, Peyrin-Biroulet L. NOD2 gene variant is a risk factor for postoperative complications in patients with Crohn’s disease: A genetic association study. Surgery. 2016 Jul;160(1):74-80. doi: 10.1016/j.surg.2016.01.013. Epub 2016 Mar 2. PMID: 26946932.
Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, Huot L, Grandjean T, Bressenot A, Delanoye-Crespin A, Gaillot O, Schreiber S, Lemoine Y, Ryffel B, Hot D, Nùñez G, Chen G, Rosenstiel P, Chamaillard M. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013 Feb;123(2):700-11. doi: 10.1172/JCI62236. Epub 2013 Jan 2. PMID: 23281400; PMCID: PMC3561825.
Rescigno M. Intestinal dendritic cells. Adv Immunol. 2010;107:109-38. doi: 10.1016/B978-0-12-381300-8.00004-6. PMID: 21034972.
Karrich JJ, Romera-Hernández M, Papazian N, Veenbergen S, Cornelissen F, Aparicio-Domingo P, Stenhouse FH, Peddie CD, Hoogenboezem RM, den Hollander CWJ, Gaskell T, Medley T, Boon L, Blackburn CC, Withers DR, Samsom JN, Cupedo T. Expression of Plet1 controls interstitial migration of murine small intestinal dendritic cells. Eur J Immunol. 2019 Feb;49(2):290-301. doi: 10.1002/eji.201847671. Epub 2018 Dec 14. PMID: 30537036; PMCID: PMC6492104.
Bain CC, Mowat AM. Intestinal macrophages - specialised adaptation to a unique environment. Eur J Immunol. 2011 Sep;41(9):2494-8. doi: 10.1002/eji.201141714. PMID: 21952804.
Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, Grip O, Guilliams M, Malissen B, Agace WW, Mowat AM. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 2013 May;6(3):498-510. doi: 10.1038/mi.2012.89. Epub 2012 Sep 19. PMID: 22990622; PMCID: PMC3629381.
Tamoutounour S, Henri S, Lelouard H, de Bovis B, de Haar C, van der Woude CJ, Woltman AM, Reyal Y, Bonnet D, Sichien D, Bain CC, Mowat AM, Reis e Sousa C, Poulin LF, Malissen B, Guilliams M. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur J Immunol. 2012 Dec;42(12):3150-66. doi: 10.1002/eji.201242847. Epub 2012 Oct 17. PMID: 22936024.
Cerovic V, Houston SA, Scott CL, Aumeunier A, Yrlid U, Mowat AM, Milling SW. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 2013 Jan;6(1):104-13. doi: 10.1038/mi.2012.53. Epub 2012 Jun 20. PMID: 22718260.
Zigmond E, Jung S. Intestinal macrophages: well educated exceptions from the rule. Trends Immunol. 2013 Apr;34(4):162-8. doi: 10.1016/j.it.2013.02.001. Epub 2013 Mar 13. PMID: 23477922.
Satpathy AT, Briseño CG, Lee JS, Ng D, Manieri NA, Kc W, Wu X, Thomas SR, Lee WL, Turkoz M, McDonald KG, Meredith MM, Song C, Guidos CJ, Newberry RD, Ouyang W, Murphy TL, Stappenbeck TS, Gommerman JL, Nussenzweig MC, Colonna M, Kopan R, Murphy KM. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat Immunol. 2013 Sep;14(9):937-48. doi: 10.1038/ni.2679. Epub 2013 Aug 4. PMID: 23913046; PMCID: PMC3788683.
Bain CC, Mowat AM. Macrophages in intestinal homeostasis and inflammation. Immunol Rev. 2014 Jul;260(1):102-17. doi: 10.1111/imr.12192. PMID: 24942685; PMCID: PMC4141699.
Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, Chu FF, Randolph GJ, Rudensky AY, Nussenzweig M. In vivo analysis of dendritic cell development and homeostasis. Science. 2009 Apr 17;324(5925):392-7. doi: 10.1126/science.1170540. Epub 2009 Mar 12. PMID: 19286519; PMCID: PMC2803315.
Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, Cumano A, Geissmann F. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science. 2006 Jan 6;311(5757):83-7. doi: 10.1126/science.1117729. Epub 2005 Dec 1. Erratum in: Science. 2006 Mar 3;311(5765):1242. PMID: 16322423.
Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010 Feb 5;327(5966):656-61. doi: 10.1126/science.1178331. Erratum in: Science. 2010 Dec 3;330(6009):1319. PMID: 20133564; PMCID: PMC2887389.
Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, Liu K, Jakubzick C, Ingersoll MA, Leboeuf M, Stanley ER, Nussenzweig M, Lira SA, Randolph GJ, Merad M. Origin of the lamina propria dendritic cell network. Immunity. 2009 Sep 18;31(3):513-25. doi: 10.1016/j.immuni.2009.08.010. Epub 2009 Sep 10. PMID: 19733489; PMCID: PMC2778256.
Bogunovic M, Mortha A, Muller PA, Merad M. Mononuclear phagocyte diversity in the intestine. Immunol Res. 2012 Dec;54(1-3):37-49. doi: 10.1007/s12026-012-8323-5. PMID: 22562804.
Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, Fehling HJ, Hardt WD, Shakhar G, Jung S. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009 Sep 18;31(3):502-12. doi: 10.1016/j.immuni.2009.06.025. Epub 2009 Sep 3. PMID: 19733097.
Tussiwand R, Lee WL, Murphy TL, Mashayekhi M, KC W, Albring JC, Satpathy AT, Rotondo JA, Edelson BT, Kretzer NM, Wu X, Weiss LA, Glasmacher E, Li P, Liao W, Behnke M, Lam SS, Aurthur CT, Leonard WJ, Singh H, Stallings CL, Sibley LD, Schreiber RD, Murphy KM. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature. 2012 Oct 25;490(7421):502-7. doi: 10.1038/nature11531. Epub 2012 Sep 19. PMID: 22992524; PMCID: PMC3482832.
Tamura T, Tailor P, Yamaoka K, Kong HJ, Tsujimura H, O’Shea JJ, Singh H, Ozato K. IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J Immunol. 2005 Mar 1;174(5):2573-81. doi: 10.4049/jimmunol.174.5.2573. PMID: 15728463.
Jackson JT, Hu Y, Liu R, Masson F, D’Amico A, Carotta S, Xin A, Camilleri MJ, Mount AM, Kallies A, Wu L, Smyth GK, Nutt SL, Belz GT. Id2 expression delineates differential checkpoints in the genetic program of CD8α+ and CD103+ dendritic cell lineages. EMBO J. 2011 May 17;30(13):2690-704. doi: 10.1038/emboj.2011.163. PMID: 21587207; PMCID: PMC3155298..
Bajaña S, Roach K, Turner S, Paul J, Kovats S. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J Immunol. 2012 Oct 1;189(7):3368-77. doi: 10.4049/jimmunol.1102613. Epub 2012 Aug 29. PMID: 22933627; PMCID: PMC3448873.
Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT, Ng D, Klinakis A, Charo IF, Jung S, Gommerman JL, Ivanov II, Liu K, Merad M, Reizis B. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity. 2011 Nov 23;35(5):780-91. doi: 10.1016/j.immuni.2011.08.013. Epub 2011 Oct 20. PMID: 22018469; PMCID: PMC3225703.
Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, Vyas JM, Boes M, Ploegh HL, Fox JG, Littman DR, Reinecker HC. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005 Jan 14;307(5707):254-8. doi: 10.1126/science.1102901. PMID: 15653504.
Farache J, Koren I, Milo I, Gurevich I, Kim KW, Zigmond E, Furtado GC, Lira SA, Shakhar G. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity. 2013 Mar 21;38(3):581-95. doi: 10.1016/j.immuni.2013.01.009. Epub 2013 Feb 7. PMID: 23395676; PMCID: PMC4115273.
Cerovic V, Bain CC, Mowat AM, Milling SW. Intestinal macrophages and dendritic cells: what’s the difference? Trends Immunol. 2014 Jun;35(6):270-7. doi: 10.1016/j.it.2014.04.003. Epub 2014 Apr 30. PMID: 24794393.
Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998 Mar 19;392(6673):245-52. doi: 10.1038/32588. PMID: 9521319.
Jaensson E, Uronen-Hansson H, Pabst O, Eksteen B, Tian J, Coombes JL, Berg PL, Davidsson T, Powrie F, Johansson-Lindbom B, Agace WW. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med. 2008 Sep 1;205(9):2139-49. doi: 10.1084/jem.20080414. Epub 2008 Aug 18. PMID: 18710932; PMCID: PMC2526207.
Pabst O, Bernhardt G. The puzzle of intestinal lamina propria dendritic cells and macrophages. Eur J Immunol. 2010 Aug;40(8):2107-11. doi: 10.1002/eji.201040557. PMID: 20853495.
Worbs T, Bode U, Yan S, Hoffmann MW, Hintzen G, Bernhardt G, Förster R, Pabst O. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med. 2006 Mar 20;203(3):519-27. doi: 10.1084/jem.20052016. Epub 2006 Mar 13. PMID: 16533884; PMCID: PMC2118247.
Wilson NS, Young LJ, Kupresanin F, Naik SH, Vremec D, Heath WR, Akira S, Shortman K, Boyle J, Maraskovsky E, Belz GT, Villadangos JA. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol Cell Biol. 2008 Feb;86(2):200-5. doi: 10.1038/sj.icb.7100125. Epub 2007 Nov 20. PMID: 18026177.
Scott CL, Aumeunier AM, Mowat AM. Intestinal CD103+ dendritic cells: master regulators of tolerance? Trends Immunol. 2011 Sep;32(9):412-9. doi: 10.1016/j.it.2011.06.003. Epub 2011 Aug 2. PMID: 21816673.
Rescigno M, Di Sabatino A. Dendritic cells in intestinal homeostasis and disease. J Clin Invest. 2009 Sep;119(9):2441-50. doi: 10.1172/JCI39134. Epub 2009 Sep 1. PMID: 19729841; PMCID: PMC2735931.
Iliev ID, Spadoni I, Mileti E, Matteoli G, Sonzogni A, Sampietro GM, Foschi D, Caprioli F, Viale G, Rescigno M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut. 2009 Nov;58(11):1481-9. doi: 10.1136/gut.2008.175166. Epub 2009 Jun 30. PMID: 19570762.
Iliev ID, Mileti E, Matteoli G, Chieppa M, Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2009 Jul;2(4):340-50. doi: 10.1038/mi.2009.13. Epub 2009 Apr 22. PMID: 19387433.
Coombes JL, Siddiqui KR, Arancibia-Cárcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med. 2007 Aug 6;204(8):1757-64. doi: 10.1084/jem.20070590. Epub 2007 Jul 9. PMID: 17620361; PMCID: PMC2118683.
Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol. 2005 May;6(5):507-14. doi: 10.1038/ni1192. Epub 2005 Apr 10. Erratum in: Nat Immunol. 2015 Mar;16(3):326. PMID: 15821737.
Spadoni I, Iliev ID, Rossi G, Rescigno M. Dendritic cells produce TSLP that limits the differentiation of Th17 cells, fosters Treg development, and protects against colitis. Mucosal Immunol. 2012 Mar;5(2):184-93. doi: 10.1038/mi.2011.64. Epub 2012 Jan 11. PMID: 22236997.
Kornete M, Piccirillo CA. Functional crosstalk between dendritic cells and Foxp3(+) regulatory T cells in the maintenance of immune tolerance. Front Immunol. 2012 Jun 22;3:165. doi: 10.3389/fimmu.2012.00165. PMID: 22737152; PMCID: PMC3381230.
Wittkopf N, Neurath MF, Becker C. Immune-epithelial crosstalk at the intestinal surface. J Gastroenterol. 2014 Mar;49(3):375-87. doi: 10.1007/s00535-013-0929-4. Epub 2014 Jan 28. PMID: 24469679.
Rescigno M, Lopatin U, Chieppa M. Interactions among dendritic cells, macrophages, and epithelial cells in the gut: implications for immune tolerance. Curr Opin Immunol. 2008 Dec;20(6):669-75. doi: 10.1016/j.coi.2008.09.007. Epub 2008 Oct 22. PMID: 18852045.
Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol. 2010;108:111-65. doi: 10.1016/B978-0-12-380995-7.00004-5. PMID: 21056730; PMCID: PMC3050492.
Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1(Suppl 1):4607-14. doi: 10.1073/pnas.1000092107. Epub 2010 Sep 8. PMID: 20826446; PMCID: PMC3063605.
Lampen A, Meyer S, Arnhold T, Nau H. Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. J Pharmacol Exp Ther. 2000 Dec;295(3):979-85. PMID: 11082432.
Bimczok D, Kao JY, Zhang M, Cochrun S, Mannon P, Peter S, Wilcox CM, Mönkemüller KE, Harris PR, Grams JM, Stahl RD, Smith PD, Smythies LE. Human gastric epithelial cells contribute to gastric immune regulation by providing retinoic acid to dendritic cells. Mucosal Immunol. 2015 May;8(3):533-44. doi: 10.1038/mi.2014.86. Epub 2014 Sep 24. PMID: 25249167; PMCID: PMC4372513.
Hurst RJ, Else KJ. The retinoic acid-producing capacity of gut dendritic cells and macrophages is reduced during persistent T. muris infection. Parasite Immunol. 2013 Jul;35(7-8):229-33. doi: 10.1111/pim.12032. PMID: 23495720; PMCID: PMC3757314.
Zeng R, Oderup C, Yuan R, Lee M, Habtezion A, Hadeiba H, Butcher EC. Retinoic acid regulates the development of a gut-homing precursor for intestinal dendritic cells. Mucosal Immunol. 2013 Jul;6(4):847-56. doi: 10.1038/mi.2012.123. Epub 2012 Dec 12. PMID: 23235743; PMCID: PMC3612556.
Bakdash G, Vogelpoel LT, van Capel TM, Kapsenberg ML, de Jong EC. Retinoic acid primes human dendritic cells to induce gut-homing, IL-10-producing regulatory T cells. Mucosal Immunol. 2015 Mar;8(2):265-78. doi: 10.1038/mi.2014.64. Epub 2014 Jul 16. PMID: 25027601.
Hanabuchi S, Watanabe N, Liu YJ. TSLP and immune homeostasis. Allergol Int. 2012 Mar;61(1):19-25. doi: 10.2332/allergolint.11-RAI-0394. Epub 2012 Jan 25. PMID: 22270070; PMCID: PMC3652583.
Chen X, Song CH, Feng BS, Li TL, Li P, Zheng PY, Chen XM, Xing Z, Yang PC. Intestinal epithelial cell-derived integrin αβ6 plays an important role in the induction of regulatory T cells and inhibits an antigen-specific Th2 response. J Leukoc Biol. 2011 Oct;90(4):751-9. doi: 10.1189/jlb.1210696. Epub 2011 Jul 1. PMID: 21724807.
Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU, Chen K, He B, Cassis L, Bigas A, Cols M, Comerma L, Huang B, Blander JM, Xiong H, Mayer L, Berin C, Augenlicht LH, Velcich A, Cerutti A. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science. 2013 Oct 25;342(6157):447-53. doi: 10.1126/science.1237910. Epub 2013 Sep 26. PMID: 24072822; PMCID: PMC4005805.
Ruane DT, Lavelle EC. The role of CD103⁺ dendritic cells in the intestinal mucosal immune system. Front Immunol. 2011 Jul 1;2:25. doi: 10.3389/fimmu.2011.00025. PMID: 22566815; PMCID: PMC3342356.
Kayama H, Takeda K. Regulation of intestinal homeostasis by innate and adaptive immunity. Int Immunol. 2012 Nov;24(11):673-80. doi: 10.1093/intimm/dxs094. Epub 2012 Sep 7. PMID: 22962437.
Taylor BC, Zaph C, Troy AE, Du Y, Guild KJ, Comeau MR, Artis D. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J Exp Med. 2009 Mar 16;206(3):655-67. doi: 10.1084/jem.20081499. Epub 2009 Mar 9. PMID: 19273626; PMCID: PMC2699121.
Kushwah R, Hu J. Role of dendritic cells in the induction of regulatory T cells. Cell Biosci. 2011 May 24;1(1):20. doi: 10.1186/2045-3701-1-20. PMID: 21711933; PMCID: PMC3125210.
Sharma MD, Hou DY, Liu Y, Koni PA, Metz R, Chandler P, Mellor AL, He Y, Munn DH. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood. 2009 Jun 11;113(24):6102-11. doi: 10.1182/blood-2008-12-195354. Epub 2009 Apr 14. PMID: 19366986; PMCID: PMC2699232.
Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, Mellor AL. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol. 2009 Aug 15;183(4):2475-83. doi: 10.4049/jimmunol.0900986. Epub 2009 Jul 27. PMID: 19635913; PMCID: PMC3677163.
Mann ER, Li X. Intestinal antigen-presenting cells in mucosal immune homeostasis: crosstalk between dendritic cells, macrophages and B-cells. World J Gastroenterol. 2014 Aug 7;20(29):9653-64. doi: 10.3748/wjg.v20.i29.9653. PMID: 25110405; PMCID: PMC4123356.
Cerutti A, Chen K, Chorny A. Immunoglobulin responses at the mucosal interface. Annu Rev Immunol. 2011;29:273-93. doi: 10.1146/annurev-immunol-031210-101317. PMID: 21219173; PMCID: PMC3064559.
Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, Cerutti A. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol. 2002 Sep;3(9):822-9. doi: 10.1038/ni829. Epub 2002 Aug 5. PMID: 12154359; PMCID: PMC4621779.
He B, Xu W, Santini PA, Polydorides AD, Chiu A, Estrella J, Shan M, Chadburn A, Villanacci V, Plebani A, Knowles DM, Rescigno M, Cerutti A. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity. 2007 Jun;26(6):812-26. doi: 10.1016/j.immuni.2007.04.014. PMID: 17570691.
Gutzeit C, Magri G, Cerutti A. Intestinal IgA production and its role in host-microbe interaction. Immunol Rev. 2014 Jul;260(1):76-85. doi: 10.1111/imr.12189. PMID: 24942683; PMCID: PMC4174397.
Schneider P. The role of APRIL and BAFF in lymphocyte activation. Curr Opin Immunol. 2005 Jun;17(3):282-9. doi: 10.1016/j.coi.2005.04.005. PMID: 15886118.
Mora JR, Iwata M, Eksteen B, Song SY, Junt T, Senman B, Otipoby KL, Yokota A, Takeuchi H, Ricciardi-Castagnoli P, Rajewsky K, Adams DH, von Andrian UH. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science. 2006 Nov 17;314(5802):1157-60. doi: 10.1126/science.1132742. PMID: 17110582.
Di Caro V, Phillips B, Engman C, Harnaha J, Trucco M, Giannoukakis N. Retinoic acid-producing, ex-vivo-generated human tolerogenic dendritic cells induce the proliferation of immunosuppressive B lymphocytes. Clin Exp Immunol. 2013 Nov;174(2):302-17. doi: 10.1111/cei.12177. PMID: 23865694; PMCID: PMC3828834.
Mora JR, von Andrian UH. Role of retinoic acid in the imprinting of gut-homing IgA-secreting cells. Semin Immunol. 2009 Feb;21(1):28-35. doi: 10.1016/j.smim.2008.08.002. Epub 2008 Sep 18. PMID: 18804386; PMCID: PMC2663412.
Seo GY, Jang YS, Kim HA, Lee MR, Park MH, Park SR, Lee JM, Choe J, Kim PH. Retinoic acid, acting as a highly specific IgA isotype switch factor, cooperates with TGF-β1 to enhance the overall IgA response. J Leukoc Biol. 2013 Aug;94(2):325-35. doi: 10.1189/jlb.0313128. Epub 2013 Jun 6. PMID: 23744644.
Mantis NJ, Rol N, Corthésy B. Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011 Nov;4(6):603-11. doi: 10.1038/mi.2011.41. Epub 2011 Oct 5. PMID: 21975936; PMCID: PMC3774538.
Gutzeit C, Magri G, Cerutti A. Intestinal IgA production and its role in host-microbe interaction. Immunol Rev. 2014 Jul;260(1):76-85. doi: 10.1111/imr.12189. PMID: 24942683; PMCID: PMC4174397.
Boyaka PN. Inducing Mucosal IgA: A Challenge for Vaccine Adjuvants and Delivery Systems. J Immunol. 2017 Jul 1;199(1):9-16. doi: 10.4049/jimmunol.1601775. PMID: 28630108; PMCID: PMC5719502.
Ren W, Wang K, Yin J, Chen S, Liu G, Tan B, Wu G, Bazer FW, Peng Y, Yin Y. Glutamine-Induced Secretion of Intestinal Secretory Immunoglobulin A: A Mechanistic Perspective. Front Immunol. 2016 Nov 24;7:503. doi: 10.3389/fimmu.2016.00503. PMID: 27933057; PMCID: PMC5121228.
Wu M, Xiao H, Liu G, Chen S, Tan B, Ren W, Bazer FW, Wu G, Yin Y. Glutamine promotes intestinal SIgA secretion through intestinal microbiota and IL-13. Mol Nutr Food Res. 2016 Jul;60(7):1637-48. doi: 10.1002/mnfr.201600026. Epub 2016 Apr 24. PMID: 27005687.
Zheng T, Zhang B, Chen C, Ma J, Meng D, Huang J, Hu R, Liu X, Otsu K, Liu AC, Li H, Yin Z, Huang G. Protein kinase p38α signaling in dendritic cells regulates colon inflammation and tumorigenesis. Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):E12313-E12322. doi: 10.1073/pnas.1814705115. Epub 2018 Dec 12. PMID: 30541887; PMCID: PMC6310843.
Laffont S, Siddiqui KR, Powrie F. Intestinal inflammation abrogates the tolerogenic properties of MLN CD103+ dendritic cells. Eur J Immunol. 2010 Jul;40(7):1877-83. doi: 10.1002/eji.200939957. PMID: 20432234; PMCID: PMC6108414.
Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13722-7. doi: 10.1073/pnas.241308598. PMID: 11717433; PMCID: PMC61108.
Uematsu S, Fujimoto K, Jang MH, Yang BG, Jung YJ, Nishiyama M, Sato S, Tsujimura T, Yamamoto M, Yokota Y, Kiyono H, Miyasaka M, Ishii KJ, Akira S. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol. 2008 Jul;9(7):769-76. doi: 10.1038/ni.1622. Epub 2008 May 30. PMID: 18516037.
Jie Z, Yang JY, Gu M, Wang H, Xie X, Li Y, Liu T, Zhu L, Shi J, Zhang L, Zhou X, Joo D, Brightbill HD, Cong Y, Lin D, Cheng X, Sun SC. NIK signaling axis regulates dendritic cell function in intestinal immunity and homeostasis. Nat Immunol. 2018 Nov;19(11):1224-1235. doi: 10.1038/s41590-018-0206-z. Epub 2018 Sep 24. PMID: 30250187; PMCID: PMC6195481.
Wenzel UA, Jonstrand C, Hansson GC, Wick MJ. CD103+ CD11b+ Dendritic Cells Induce Th17 T Cells in Muc2-Deficient Mice with Extensively Spread Colitis. PLoS One. 2015 Jun 29;10(6):e0130750. doi: 10.1371/journal.pone.0130750. PMID: 26121642; PMCID: PMC4487685.
Yao Y, Levings MK, Steiner TS. ATP conditions intestinal epithelial cells to an inflammatory state that promotes components of DC maturation. Eur J Immunol. 2012 Dec;42(12):3310-21. doi: 10.1002/eji.201142213. Epub 2012 Oct 26. PMID: 22987503.
Bowcutt R, Bramhall M, Logunova L, Wilson J, Booth C, Carding SR, Grencis R, Cruickshank S. A role for the pattern recognition receptor Nod2 in promoting recruitment of CD103+ dendritic cells to the colon in response to Trichuris muris infection. Mucosal Immunol. 2014 Sep;7(5):1094-105. doi: 10.1038/mi.2013.125. Epub 2014 Jan 22. PMID: 24448097; PMCID: PMC4074062.
Nakahashi-Oda C, Udayanga KG, Nakamura Y, Nakazawa Y, Totsuka N, Miki H, Iino S, Tahara-Hanaoka S, Honda S, Shibuya K, Shibuya A. Apoptotic epithelial cells control the abundance of Treg cells at barrier surfaces. Nat Immunol. 2016 Apr;17(4):441-50. doi: 10.1038/ni.3345. Epub 2016 Feb 8. PMID: 26855029.
Evans C, Dalgleish AG, Kumar D. Review article: immune suppression and colorectal cancer. Aliment Pharmacol Ther. 2006 Oct 15;24(8):1163-77. doi: 10.1111/j.1365-2036.2006.03075.x. PMID: 17014575.