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Host-Recognition of Pathogens and Commensals in the Mammalian Intestine

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Book cover Between Pathogenicity and Commensalism

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 358))

Abstract

To peacefully coexist with the microbial inhabitants of the intestine, mammals have evolved elaborate and interconnected regulatory mechanisms to maintain immune homeostasis in the face of potential infection and tissue damage by pathogenic microorganisms. Physical barriers, antimicrobial factors and secretory antibodies act in concert to keep microbes at a distance from the epithelium and initiate repair mechanisms in the event of damage. Commensal bacteria are not ignored but dynamically controlled via many complex overlapping and intertwined mechanisms involving intestinal epithelial cells (IECs) and signals from the microbiota. Polarized IECs play a decisive role in homeostasis by regulating the expression and activity of the pattern-recognition receptors (PRRs), in different compartments of the intestine. The differential signaling and expression of receptors on apical and basal membranes of the epithelium also plays its part in distinguishing commensals from harmful invaders. In steady state conditions macrophages and dendritic cells (DCs) in the lamina propria (LP) are conditioned by environmental factors to induce immune tolerance. The distinction between pathogen and non-pathogen is linked to the ability of pathogens to invade and cause damage to the host cells and tissues. This induces local inflammatory responses and the attraction of capillary leukocytes by chemokines released from colonized and invaded epithelial cells. This bypasses the tolerogenic mechanisms controlling the responses of resident DCs and macrophages leading to pathogen killing and adaptive immune responses. Research on this topic has important implications for the development of novel therapeutic approaches to treat or prevent inflammatory bowel disease (IBD), inflammation-related cancer and other gut-related diseases and disorders.

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Abbreviations

GIT:

Gastrointestinal tract

SI:

Small intestine

LP:

Lamina propria

M cell:

Microfold cell

GALT:

Gut-associated lymphoid tissue

DSS:

Dextran sodium sulphate

TFF3:

Trefoil factor 3

IECs:

Intestinal epithelial cells

APC:

Antigen presenting cell

TJ:

Tight junction

EPEC:

Enteropathogenic Escherichia coli

PRR:

Pattern recognition receptor

HD:

Human α-defensin

MMP:

Matrix metalloprotease

HBD-1:

Beta-defensin-1

MBD-2:

Murine β-defensin 2

DC:

Dendritic cell

sIgA:

Secretory immunoglobulin A

MLNs:

Mesenteric lymph nodes

TGF-β:

Transforming growth factor-β

RA:

Retinoic acid

J chain:

‘joining’ chain

pIg:

Polymeric-immunoglobulin

VH :

Variable region

BAFF:

B cell-activating factor

APRIL:

A B cell proliferation-inducing ligand

LPS:

Lipopolysaccharide

MAMPs:

Microbe-associated molecular patterns

TLRs:

Toll-like receptors

NLRs:

Nod-like receptors

LRR:

Leucine-rich repeat

TIR:

Toll-interleukin 1 receptor

CARD:

Caspase recruitment domain

NOD:

Nucleotide-binding oligomerization domain

PG:

Peptidoglycan

MyD88:

Myeloid differentiation primary response gene 88

MAPK:

Mitogen-activated protein kinase

NF-κB:

Nuclear factor κB

IKK:

IκB kinase

IL:

Interleukin

IFN:

Interferon

TNF:

Tumor necrosis factor

MCP-1 or CCL-2:

Monocyte chemotactic protein-1

PPARγ:

Peroxisome proliferator-activated receptor-γ

TOLLIP:

Toll-interacting protein

TSLP:

Thymic stromal lymphopoietin

IDO:

Indoleamine 2,3 dioxygenase

IBD:

Inflammatory bowel disease

AMPs:

Antimicrobial peptides

PP:

Peyer's patch

FAE:

Follicle-associated epithelium

References

  • Abreu MT, Vora P, Faure E, Thomas LS, Arnold ET, Arditi M (2001) Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J Immunol 167(3):1609–1616

    PubMed  CAS  Google Scholar 

  • Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, Logan SM, Aderem A (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci U S A 102(26):9247–9252. doi:0502040102[pii]10.1073/pnas.0502040102

    Article  PubMed  CAS  Google Scholar 

  • Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, Carter BD, Pozzi A, Abel TW, Dermody TS (2009) Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5(1):59–71. doi:S1931-3128(08)00398-3[pii]10.1016/j.chom.2008.12.001

    Article  PubMed  CAS  Google Scholar 

  • Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, Yagita H, Ishii N, Evans R, Honda K, Takeda K (2008) ATP drives lamina propria T(H)17 cell differentiation. Nature 455(7214):808–812. doi:nature07240[pii]10.1038/nature07240

    Article  PubMed  CAS  Google Scholar 

  • Batista FD, Harwood NE (2009) The who, how and where of antigen presentation to B cells. Nat Rev Immunol 9(1):15–27. doi:nri2454[pii]10.1038/nri2454

    Article  PubMed  CAS  Google Scholar 

  • Batista FD, Iber D, Neuberger MS (2001) B cells acquire antigen from target cells after synapse formation. Nature 411(6836):489–494. doi:10.1038/3507809935078099[pii]

    Article  PubMed  CAS  Google Scholar 

  • Beau I, Cotte-Laffitte J, Amsellem R, Servin AL (2007) A protein kinase A-dependent mechanism by which rotavirus affects the distribution and mRNA level of the functional tight junction-associated protein, occludin, in human differentiated intestinal Caco-2 cells. J Virol 81(16):8579–8586. doi:JVI.00263-07[pii]10.1128/JVI.00263-07

    Article  PubMed  CAS  Google Scholar 

  • Bergelson JM (2009) Intercellular junctional proteins as receptors and barriers to virus infection and spread. Cell Host Microbe 5(6):517–521. doi:S1931-3128(09)00176-0[pii]10.1016/j.chom.2009.05.009

    Article  PubMed  CAS  Google Scholar 

  • Bergtold A, Desai DD, Gavhane A, Clynes R (2005) Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23(5):503–514. doi:S1074-7613(05)00309-2[pii]10.1016/j.immuni.2005.09.013

    Article  PubMed  CAS  Google Scholar 

  • Bettelli E, Korn T, Kuchroo VK (2007) Th17: the third member of the effector T cell trilogy. Curr Opin Immunol 19(6):652–657. doi:S0952-7915(07)00133-1[pii]10.1016/j.coi.2007.07.020

    Article  PubMed  CAS  Google Scholar 

  • Biragyn A, Surenhu M, Yang D, Ruffini PA, Haines BA, Klyushnenkova E, Oppenheim JJ, Kwak LW (2001) Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J Immunol 167(11):6644–6653

    PubMed  CAS  Google Scholar 

  • Biragyn A, Belyakov IM, Chow YH, Dimitrov DS, Berzofsky JA, Kwak LW (2002) DNA vaccines encoding human immunodeficiency virus-1 glycoprotein 120 fusions with proinflammatory chemoattractants induce systemic and mucosal immune responses. Blood 100(4):1153–1159. doi:10.1182/blood-2002-01-0086

    Article  PubMed  CAS  Google Scholar 

  • 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 (2009) Origin of the lamina propria dendritic cell network. Immunity 31(3):513–525. doi:S1074-7613(09)00368-9[pii]10.1016/j.immuni.2009.08.010

    Article  PubMed  CAS  Google Scholar 

  • Brandl K, Plitas G, Schnabl B, DeMatteo RP, Pamer EG (2007) MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 204(8):1891–1900. doi:jem.20070563[pii]10.1084/jem.20070563

    Article  PubMed  CAS  Google Scholar 

  • Burger-van Paassen N, Vincent A, Puiman PJ, van der Sluis M, Bouma J, Boehm G, van Goudoever JB, van Seuningen I, Renes IB (2009) The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J 420(2):211–219. doi:BJ20082222[pii]10.1042/BJ20082222

    Article  PubMed  CAS  Google Scholar 

  • Cario E, Podolsky DK (2000) Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68(12):7010–7017

    Article  PubMed  CAS  Google Scholar 

  • Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK (2000) Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing toll-like receptors. J Immunol 164(2):966–972. doi:ji_v164n2p966[pii]

    PubMed  CAS  Google Scholar 

  • Cario E, Gerken G, Podolsky DK (2007) Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132(4):1359–1374. doi:S0016-5085(07)00415-5[pii]10.1053/j.gastro.2007.02.056

    Article  PubMed  CAS  Google Scholar 

  • Cash HL, Whitham CV, Behrendt CL, Hooper LV (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313(5790):1126–1130. doi:313/5790/1126[pii]10.1126/science.1127119

    Article  PubMed  CAS  Google Scholar 

  • Chabot S, Wagner JS, Farrant S, Neutra MR (2006) TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J Immunol 176(7):4275–4283. doi:176/7/4275[pii]

    PubMed  CAS  Google Scholar 

  • Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, Fukase K, Kusumoto S, Valvano MA, Foster SJ, Mak TW, Nunez G, Inohara N (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4(7):702–707. doi:10.1038/ni945ni945[pii]

    Article  PubMed  CAS  Google Scholar 

  • Chieppa M, Rescigno M, Huang AY, Germain RN (2006) Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 203(13):2841–2852. doi:jem.20061884[pii]10.1084/jem.20061884

    Article  PubMed  CAS  Google Scholar 

  • Collier-Hyams LS, Zeng H, Sun J, Tomlinson AD, Bao ZQ, Chen H, Madara JL, Orth K, Neish AS (2002) Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 169(6):2846–2850

    PubMed  CAS  Google Scholar 

  • Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F (2007) 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 204(8):1757–1764. doi:jem.20070590[pii]10.1084/jem.20070590

    Article  PubMed  CAS  Google Scholar 

  • Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8(10):1086–1094. doi:ni1511[pii]10.1038/ni1511

    Article  PubMed  CAS  Google Scholar 

  • Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54 (Pt 5):1469–1476. doi:10.1099/ijs.0.02873-054/5/1469 [pii]

  • Fagarasan S, Honjo T (2000) T-Independent immune response: new aspects of B cell biology. Science 290(5489):89–92. doi:8882[pii]

    Article  PubMed  CAS  Google Scholar 

  • Fernandez MI, Pedron T, Tournebize R, Olivo-Marin JC, Sansonetti PJ, Phalipon A (2003) Anti-inflammatory role for intracellular dimeric immunoglobulin a by neutralization of lipopolysaccharide in epithelial cells. Immunity 18(6):739–749. doi:S1074761303001225[pii]

    Article  PubMed  CAS  Google Scholar 

  • Funderburg N, Lederman MM, Feng Z, Drage MG, Jadlowsky J, Harding CV, Weinberg A, Sieg SF (2007) Human -defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc Natl Acad Sci U S A 104(47):18631–18635. doi:0702130104[pii]10.1073/pnas.0702130104

    Article  PubMed  CAS  Google Scholar 

  • Furrie E, Macfarlane S, Thomson G, Macfarlane GT (2005) Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115(4):565–574. doi:IMM2200[pii]10.1111/j.1365-2567.2005.02200.x

    Article  PubMed  CAS  Google Scholar 

  • Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, Eberl G, Snel J, Kelly D, Cerf-Bensussan N (2009) The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31(4):677–689. doi:S1074-7613(09)00404-X[pii]10.1016/j.immuni.2009.08.020

    Article  PubMed  CAS  Google Scholar 

  • Garabedian EM, Roberts LJ, McNevin MS, Gordon JI (1997) Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J Biol Chem 272(38):23729–23740

    Article  PubMed  CAS  Google Scholar 

  • Garcia JR, Jaumann F, Schulz S, Krause A, Rodriguez-Jimenez J, Forssmann U, Adermann K, Kluver E, Vogelmeier C, Becker D, Hedrich R, Forssmann WG, Bals R (2001) Identification of a novel, multifunctional beta-defensin (human beta-defensin 3) with specific antimicrobial activity. Its interaction with plasma membranes of Xenopus oocytes and the induction of macrophage chemoattraction. Cell Tissue Res 306 (2):257–264. doi:10.1007/s004410100433

    Google Scholar 

  • Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167(4):1882–1885

    PubMed  CAS  Google Scholar 

  • Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, Viala J, Tedin K, Taha MK, Labigne A, Zahringer U, Coyle AJ, DiStefano PS, Bertin J, Sansonetti PJ, Philpott DJ (2003a) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300 (5625):1584–1587. doi:10.1126/science.1084677300/5625/1584 [pii]

    Google Scholar 

  • Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ (2003b) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278 (11):8869–8872. doi:10.1074/jbc.C200651200

    Google Scholar 

  • Guerry P (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15(10):456–461. doi:S0966-842X(07)00174-6[pii]10.1016/j.tim.2007.09.006

    Article  PubMed  CAS  Google Scholar 

  • Harder J, Bartels J, Christophers E, Schroder JM (2001) Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276(8):5707–5713. doi:10.1074/jbc.M008557200M008557200[pii]

    Article  PubMed  CAS  Google Scholar 

  • Hart AL, Al-Hassi HO, Rigby RJ, Bell SJ, Emmanuel AV, Knight SC, Kamm MA, Stagg AJ (2005) Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 129(1):50–65. doi:S0016508505008838[pii]

    Article  PubMed  CAS  Google Scholar 

  • Hooper LV, Stappenbeck TS, Hong CV, Gordon JI (2003) Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4(3):269–273. doi:10.1038/ni888[pii]

    Article  PubMed  CAS  Google Scholar 

  • Hugdahl MB, Beery JT, Doyle MP (1988) Chemotactic behavior of Campylobacter jejuni. Infect Immun 56(6):1560–1566

    PubMed  CAS  Google Scholar 

  • Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Almer S, Tysk C, O’Morain CA, Gassull M, Binder V, Finkel Y, Cortot A, Modigliani R, Laurent-Puig P, Gower-Rousseau C, Macry J, Colombel JF, Sahbatou M, Thomas G (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 411(6837):599–603. doi:10.1038/3507910735079107[pii]

    Article  PubMed  CAS  Google Scholar 

  • Hume ME, Nisbet DJ, DeLoach JR (1997) In vitro 14C-amino acid fermentation by CF3, a characterized continuous-flow competitive exclusion culture of caecal bacteria. J Appl Microbiol 83(2):236–242

    Article  PubMed  CAS  Google Scholar 

  • Iliev ID, Spadoni I, Mileti E, Matteoli G, Sonzogni A, Sampietro GM, Foschi D, Caprioli F, Viale G, Rescigno M (2009) Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58(11):1481–1489. doi:gut.2008.175166[pii]10.1136/gut.2008.175166

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki A, Kelsall BL (2001) Unique functions of CD11b+ , CD8 alpha+ , and double-negative Peyer’s patch dendritic cells. J Immunol 166(8):4884–4890

    PubMed  CAS  Google Scholar 

  • Janssens S, Beyaert R (2002) A universal role for MyD88 in TLR/IL-1R-mediated signaling. Trends Biochem Sci 27(9):474–482. doi:S096800040202145X[pii]

    Article  PubMed  CAS  Google Scholar 

  • Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105(39):15064–15069. doi:0803124105[pii]10.1073/pnas0803124105

    Article  PubMed  CAS  Google Scholar 

  • Johansson ME, Gustafsson JK, Sjoberg KE, Petersson J, Holm L, Sjovall H, Hansson GC (2010) Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS One 5 (8):e12238. doi:e12238 [pii] 10.1371/journal.pone.0012238

  • Johansson-Lindbom B, Svensson M, Wurbel MA, Malissen B, Marquez G, Agace W (2003) Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 198(6):963–969. doi:10.1084/jem.20031244jem.20031244[pii]

    Article  PubMed  CAS  Google Scholar 

  • John LJ, Fromm M, Schulzke JD (2011) Epithelial barriers in intestinal inflammation. antioxid redox signal. doi:10.1089/ars.2011.3892

  • Kadioglu A, Weiser JN, Paton JC, Andrew PW (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6(4):288–301. doi:nrmicro1871[pii]10.1038/nrmicro1871

    Article  PubMed  CAS  Google Scholar 

  • Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298(6):G851–G859. doi:ajpgi.00327.2009[pii]10.1152/ajpgi.00327.2009

    Article  PubMed  CAS  Google Scholar 

  • Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11(5):373–384. doi:ni.1863[pii]10.1038/ni.1863

    Article  PubMed  CAS  Google Scholar 

  • Keilbaugh SA, Shin ME, Banchereau RF, McVay LD, Boyko N, Artis D, Cebra JJ, Wu GD (2005) Activation of RegIIIbeta/gamma and interferon gamma expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut. Gut 54(5):623–629. doi:54/5/623[pii]10.1136/gut.2004.056028

    Article  PubMed  CAS  Google Scholar 

  • Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S, Conway S (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5(1):104–112. doi:10.1038/ni1018ni1018[pii]

    Article  PubMed  CAS  Google Scholar 

  • Klotman ME, Chang TL (2006) Defensins in innate antiviral immunity. Nat Rev Immunol 6(6):447–456. doi:nri1860[pii]10.1038/nri1860

    Article  PubMed  CAS  Google Scholar 

  • Lai Y, Gallo RL (2009) AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 30(3):131–141. doi:S1471-4906(09)00005-2[pii]10.1016/j.it.2008.12.003

    Article  PubMed  CAS  Google Scholar 

  • Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, Dermody TS, Nusrat A, Parkos CA (2007) JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204(13):3067–3076. doi:jem.20071416[pii]10.1084/jem.20071416

    Article  PubMed  CAS  Google Scholar 

  • Lebeis SL, Bommarius B, Parkos CA, Sherman MA, Kalman D (2007) TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J Immunol 179(1):566–577. doi:179/1/566[pii]

    PubMed  CAS  Google Scholar 

  • Lee A, O’Rourke JL, Barrington PJ, Trust TJ (1986) Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect Immun 51(2):536–546

    PubMed  CAS  Google Scholar 

  • Lee J, Mo JH, Katakura K, Alkalay I, Rucker AN, Liu YT, Lee HK, Shen C, Cojocaru G, Shenouda S, Kagnoff M, Eckmann L, Ben-Neriah Y, Raz E (2006) Maintenance of colonic homeostasis by distinctive apical TLR9 signaling in intestinal epithelial cells. Nat Cell Biol 8(12):1327–1336. doi:ncb1500[pii]10.1038/ncb1500

    Article  PubMed  CAS  Google Scholar 

  • Liu AY, Destoumieux D, Wong AV, Park CH, Valore EV, Liu L, Ganz T (2002) Human beta-defensin-2 production in keratinocytes is regulated by interleukin-1, bacteria, and the state of differentiation. J Invest Dermatol 118(2):275–281. doi:1651[pii]10.1046/j.0022-202x.2001.01651.x

    Article  PubMed  CAS  Google Scholar 

  • Macpherson AJ, Uhr T (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303(5664):1662–1665. doi:10.1126/science.1091334303/5664/1662[pii]

    Article  PubMed  CAS  Google Scholar 

  • Macpherson AJ, Hunziker L, McCoy K, Lamarre A (2001) IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect 3(12):1021–1035. doi:S1286457901014605[pii]

    Article  PubMed  CAS  Google Scholar 

  • Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P (2008) The immune geography of IgA induction and function. Mucosal Immunol 1(1):11–22. doi:mi20076[pii]10.1038/mi.2007.6

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, Kagnoff MF, Eckmann L, Karin M (2005) Nod2 mutation in Crohn’s disease potentiates NF-kappaB activity and IL-1beta processing. Science 307(5710):734–738. doi:307/5710/734[pii]0.1126/science.1103685

    Article  PubMed  CAS  Google Scholar 

  • Mashimo H, Wu DC, Podolsky DK, Fishman MC (1996) Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274(5285):262–265

    Article  PubMed  CAS  Google Scholar 

  • Matteoli G, Mazzini E, Iliev ID, Mileti E, Fallarino F, Puccetti P, Chieppa M, Rescigno M (2010) Gut CD103 + dendritic cells express indoleamine 2, 3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction. Gut 59(5):595–604. doi:59/5/595[pii]10.1136/gut.2009.185108

    Article  PubMed  CAS  Google Scholar 

  • Mazanec MB, Coudret CL, Fletcher DR (1995) Intracellular neutralization of influenza virus by immunoglobulin A anti-hemagglutinin monoclonal antibodies. J Virol 69(2):1339–1343

    PubMed  CAS  Google Scholar 

  • McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A 92(5):1664–1668

    Article  PubMed  CAS  Google Scholar 

  • McNeil NI (1984) The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39(2):338–342

    PubMed  CAS  Google Scholar 

  • Mestecky J, Russell MW, Elson CO (1999) Intestinal IgA: novel views on its function in the defence of the largest mucosal surface. Gut 44(1):2–5

    Article  PubMed  CAS  Google Scholar 

  • 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 (2006) Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314(5802):1157–1160. doi:314/5802/1157[pii]10.1126/science.1132742

    Article  PubMed  CAS  Google Scholar 

  • Mosmann TR, Coffman RL (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 7:145–173. doi:10.1146/annurev.iy.07.040189.001045

    Article  PubMed  CAS  Google Scholar 

  • Munn DH, Mellor AL (2007) Indoleamine 2, 3-dioxygenase and tumor-induced tolerance. J Clin Invest 117(5):1147–1154. doi:10.1172/JCI31178

    Article  PubMed  CAS  Google Scholar 

  • Neish AS, Gewirtz AT, Zeng H, Young AN, Hobert ME, Karmali V, Rao AS, Madara JL (2000) Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289(5484):1560–1563. doi:8795[pii]

    Article  PubMed  CAS  Google Scholar 

  • Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, Danese S, Huth M, Nikolaev A, Neufert C, Madison B, Gumucio D, Neurath MF, Pasparakis M (2007) Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446(7135):557–561. doi:nature05698[pii]10.1038/nature05698

    Article  PubMed  CAS  Google Scholar 

  • Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, Vyas JM, Boes M, Ploegh HL, Fox JG, Littman DR, Reinecker HC (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307(5707):254–258. doi:307/5707/254[pii]10.1126/science.1102901

    Article  PubMed  CAS  Google Scholar 

  • O’Hara JR, Buret AG (2008) Mechanisms of intestinal tight junctional disruption during infection. Front Biosci 13:7008–7021. doi:3206[pii]

    PubMed  Google Scholar 

  • Olson TS, Reuter BK, Scott KG, Morris MA, Wang XM, Hancock LN, Burcin TL, Cohn SM, Ernst PB, Cominelli F, Meddings JB, Ley K, Pizarro TT (2006) The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med 203(3):541–552. doi:jem.20050407[pii]10.1084/jem.20050407

    Article  PubMed  CAS  Google Scholar 

  • Pazgier M, Hoover DM, Yang D, Lu W, Lubkowski J (2006) Human beta-defensins. Cell Mol Life Sci 63(11):1294–1313. doi:10.1007/s00018-005-5540-2

    Article  PubMed  CAS  Google Scholar 

  • Peterson DA, McNulty NP, Guruge JL, Gordon JI (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2(5):328–339. doi:S1931-3128(07)00246-6[pii]10.1016/j.chom.2007.09.013

    Article  PubMed  CAS  Google Scholar 

  • Philpott DJ, McKay DM, Sherman PM, Perdue MH (1996) Infection of T84 cells with enteropathogenic Escherichia coli alters barrier and transport functions. Am J Physiol 270(4 Pt 1),:G634–G645

    PubMed  CAS  Google Scholar 

  • Podolsky DK, Gerken G, Eyking A, Cario E (2009) Colitis-associated variant of TLR2 causes impaired mucosal repair because of TFF3 deficiency. Gastroenterology 137(1):209–220. doi:S0016-5085(09)00378-3[pii]10.1053/j.gastro.2009.03.007

    Article  PubMed  CAS  Google Scholar 

  • Powrie F, Read S, Mottet C, Uhlig H, Maloy K (2003) Control of immune pathology by regulatory T cells. Novartis Found Symp 252:92–98 discussion 98–105, 106–114

    Article  PubMed  CAS  Google Scholar 

  • Radhakrishnan GK, Yu Q, Harms JS, Splitter GA (2009) Brucella TIR domain-containing protein mimics properties of the toll-like receptor adaptor protein TIRAP. J Biol Chem 284(15):9892–9898. doi:M805458200[pii]10.1074/jbc.M805458200

    Article  PubMed  CAS  Google Scholar 

  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118(2):229–241. doi:10.1016/j.cell.2004.07.002S0092867404006610[pii]

    Article  PubMed  CAS  Google Scholar 

  • Raschperger E, Thyberg J, Pettersson S, Philipson L, Fuxe J, Pettersson RF (2006) The coxsackie- and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp Cell Res 312(9):1566–1580. doi:S0014-4827(06)00023-1[pii]10.1016/j.yexcr.2006.01.025

    Article  PubMed  CAS  Google Scholar 

  • Rescigno M (2010) Intestinal dendritic cells. Adv Immunol 107:109–138. doi:B978-0-12-381300-8.00004-6[pii]10.1016/B978-0-12-381300-8.00004-6

    Article  PubMed  CAS  Google Scholar 

  • Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P (2001) Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 204(5):572–581

    Article  PubMed  CAS  Google Scholar 

  • Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M (2005) Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 6(5):507–514. doi:ni1192[pii]10.1038/ni1192

    Article  PubMed  CAS  Google Scholar 

  • Rohrl J, Yang D, Oppenheim JJ, Hehlgans T (2010) Human beta-defensin 2 and 3 and their mouse orthologs induce chemotaxis through interaction with CCR2. J Immunol 184(12):6688–6694. doi:jimmunol.0903984[pii]10.4049/jimmunol.0903984

    Article  PubMed  CAS  Google Scholar 

  • Rumio C, Besusso D, Palazzo M, Selleri S, Sfondrini L, Dubini F, Menard S, Balsari A (2004) Degranulation of paneth cells via toll-like receptor 9. Am J Pathol 165(2):373–381. doi:S0002-9440(10)63304-4[pii]10.1016/S0002-9440(10)63304-4

    Article  PubMed  CAS  Google Scholar 

  • Salazar-Gonzalez RM, Niess JH, Zammit DJ, Ravindran R, Srinivasan A, Maxwell JR, Stoklasek T, Yadav R, Williams IR, Gu X, McCormick BA, Pazos MA, Vella AT, Lefrancois L, Reinecker HC, McSorley SJ (2006) CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer’s patches. Immunity 24(5):623–632. doi:S1074-7613(06)00215-9[pii]10.1016/j.immuni.2006.02.015

    Article  PubMed  CAS  Google Scholar 

  • Salzman NH, Ghosh D, Huttner KM, Paterson Y, Bevins CL (2003) Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422(6931):522–526. doi:10.1038/nature01520nature01520[pii]

    Article  PubMed  CAS  Google Scholar 

  • Salzman NH, Underwood MA, Bevins CL (2007) Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol 19(2):70–83. doi:S1044-5323(07)00032-2[pii]10.1016/j.smim.2007.04.002

    Article  PubMed  CAS  Google Scholar 

  • Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E, Teggatz P, Barman M, Hayward M, Eastwood D, Stoel M, Zhou Y, Sodergren E, Weinstock GM, Bevins CL, Williams CB, Bos NA (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11(1):76–83. doi:ni.1825[pii]10.1038/ni.1825

    Article  PubMed  CAS  Google Scholar 

  • Sato A, Hashiguchi M, Toda E, Iwasaki A, Hachimura S, Kaminogawa S (2003) CD11b + Peyer’s patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J Immunol 171(7):3684–3690

    PubMed  CAS  Google Scholar 

  • Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459(7244):262–265. doi:nature07935[pii]10.1038/nature07935

    Article  PubMed  CAS  Google Scholar 

  • Schilling JD, Martin SM, Hung CS, Lorenz RG, Hultgren SJ (2003) Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 100(7):4203–4208. doi:10.1073/pnas.07364731000736473100[pii]

    Article  PubMed  CAS  Google Scholar 

  • Schroeder BO, Wu Z, Nuding S, Groscurth S, Marcinowski M, Beisner J, Buchner J, Schaller M, Stange EF, Wehkamp J (2011) Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature 469(7330):419–423. doi:nature09674[pii]10.1038/nature09674

    Article  PubMed  CAS  Google Scholar 

  • Shroff KE, Meslin K, Cebra JJ (1995) Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect Immun 63(10):3904–3913

    PubMed  CAS  Google Scholar 

  • Simonovic I, Rosenberg J, Koutsouris A, Hecht G (2000) Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2(4):305–315. doi:cmi55[pii]

    Article  PubMed  CAS  Google Scholar 

  • Smith PD, Ochsenbauer-Jambor C, Smythies LE (2005) Intestinal macrophages: unique effector cells of the innate immune system. Immunol Rev 206:149–159. doi:IMR288[pii]10.1111/j.0105-2896.2005.00288.x

    Article  PubMed  CAS  Google Scholar 

  • Sonnenburg JL, Angenent LT, Gordon JI (2004) Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5(6):569–573. doi:10.1038/ni1079ni1079[pii]

    Article  PubMed  CAS  Google Scholar 

  • Sorensen OE, Thapa DR, Rosenthal A, Liu L, Roberts AA, Ganz T (2005) Differential regulation of beta-defensin expression in human skin by microbial stimuli. J Immunol 174(8):4870–4879. doi:174/8/4870[pii]

    PubMed  CAS  Google Scholar 

  • Stappenbeck TS (2009) Paneth cell development, differentiation, and function: new molecular cues. Gastroenterology 137(1):30–33. doi:S0016-5085(09)00778-1[pii]10.1053/j.gastro.2009.05.013

    Article  PubMed  CAS  Google Scholar 

  • Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, Meddings JB, Abraham C, Turner JR (2009) Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136(2):551–563. doi:S0016-5085(08)01979-3[pii]10.1053/j.gastro.2008.10.081

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Fagarasan S (2008) How host-bacterial interactions lead to IgA synthesis in the gut. Trends Immunol 29(11):523–531. doi:S1471-4906(08)00221-4[pii]10.1016/j.it.2008.08.001

    Article  PubMed  CAS  Google Scholar 

  • Takata T, Fujimoto S, Amako K (1992) Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract. Infect Immun 60(9):3596–3600

    PubMed  CAS  Google Scholar 

  • Tezuka H, Abe Y, Iwata M, Takeuchi H, Ishikawa H, Matsushita M, Shiohara T, Akira S, Ohteki T (2007) Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448(7156):929–933. doi:nature06033[pii]10.1038/nature06033

    Article  PubMed  CAS  Google Scholar 

  • Tien MT, Girardin SE, Regnault B, Le Bourhis L, Dillies MA, Coppee JY, Bourdet-Sicard R, Sansonetti PJ, Pedron T (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176(2):1228–1237. doi:176/2/1228[pii]

    PubMed  CAS  Google Scholar 

  • Tsuji M, Suzuki K, Kitamura H, Maruya M, Kinoshita K, Ivanov II, Itoh K, Littman DR, Fagarasan S (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29(2):261–271. doi:S1074-7613(08)00303-8[pii]10.1016/j.immuni.2008.05.014

    Article  PubMed  CAS  Google Scholar 

  • Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, Yamamoto M, Kato H, Sougawa N, Matsui H, Kuwata H, Hemmi H, Coban C, Kawai T, Ishii KJ, Takeuchi O, Miyasaka M, Takeda K, Akira S (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7(8):868–874. doi:ni1362[pii]10.1038/ni1362

    Article  PubMed  CAS  Google Scholar 

  • Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV (2008) Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 105(52):20858–20863. doi:0808723105[pii]10.1073/pnas.0808723105

    Article  PubMed  CAS  Google Scholar 

  • Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Buller HA, Dekker J, Van Seuningen I, Renes IB, Einerhand AW (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131(1):117–129. doi:S0016-5085(06)00762-1[pii]10.1053/j.gastro.2006.04.020

    Article  PubMed  CAS  Google Scholar 

  • Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, Fehling HJ, Hardt WD, Shakhar G, Jung S (2009) Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31(3):502–512. doi:S1074-7613(09)00362-8[pii]10.1016/j.immuni.2009.06.025

    Article  PubMed  CAS  Google Scholar 

  • Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5(11):1166–1174. doi:ni1131[pii]10.1038/ni1131

    Article  PubMed  CAS  Google Scholar 

  • Vijay-Kumar M, Sanders CJ, Taylor RT, Kumar A, Aitken JD, Sitaraman SV, Neish AS, Uematsu S, Akira S, Williams IR, Gewirtz AT (2007) Deletion of TLR5 results in spontaneous colitis in mice. J Clin Invest 117(12):3909–3921. doi:10.1172/JCI33084

    PubMed  CAS  Google Scholar 

  • Vongsa RA, Zimmerman NP, Dwinell MB (2009) CCR6 regulation of the actin cytoskeleton orchestrates human beta defensin-2- and CCL20-mediated restitution of colonic epithelial cells. J Biol Chem 284(15):10034–10045. doi:M805289200[pii]10.1074/jbc.M805289200

    Article  PubMed  CAS  Google Scholar 

  • Vora P, Youdim A, Thomas LS, Fukata M, Tesfay SY, Lukasek K, Michelsen KS, Wada A, Hirayama T, Arditi M, Abreu MT (2004) Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 173(9):5398–5405. doi:173/9/5398[pii]

    PubMed  CAS  Google Scholar 

  • Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaeffeler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr, Fellermann K, Ganz T, Stange EF, Bevins CL (2005) Reduced Paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci USA 102(50):18129–18134. doi:0505256102[pii]10.1073/pnas.0505256102

    Article  PubMed  CAS  Google Scholar 

  • Weintraub A, Zahringer U, Wollenweber HW, Seydel U, Rietschel ET (1989) Structural characterization of the lipid A component of Bacteroides fragilis strain NCTC 9343 lipopolysaccharide. Eur J Biochem 183(2):425–431

    Article  PubMed  CAS  Google Scholar 

  • Weller S, Braun MC, Tan BK, Rosenwald A, Cordier C, Conley ME, Plebani A, Kumararatne DS, Bonnet D, Tournilhac O, Tchernia G, Steiniger B, Staudt LM, Casanova JL, Reynaud CA, Weill JC (2004) Human blood IgM “memory” B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104(12):3647–3654. doi:10.1182/blood-2004-01-03462004-01-0346[pii]

    Article  PubMed  CAS  Google Scholar 

  • Wells JM, Kostantinov S, Konings I, Karczewski J (2008) Effects of probiotic and commensals on epithelial barrier function. Int J Probiotics Prebiotics 3(3):127–132

    Google Scholar 

  • Wells JM, Rossi O, Meijerink M, van Baarlen P (2010) Microbes and health sackler colloquium: epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci U S A. doi:1000092107 [pii] 10.1073/pnas.1000092107

  • Ye D, Ma I, Ma TY (2006) Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 290(3):G496–G504. doi:290/3/G496[pii]10.1152/ajpgi.00318.2005

    Article  PubMed  CAS  Google Scholar 

  • Yen TH, Wright NA (2006) The gastrointestinal tract stem cell niche. Stem Cell Rev 2(3):203–212. doi:SCR:2:3:203[pii]10.1007/s12015-006-0048-1

    Article  PubMed  CAS  Google Scholar 

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  1. Host-Microbe Interactomics Group, Wageningen University and Research Centre, 338, 6700, AH Wageningen, The Netherlands

    Oriana Rossi, Peter van Baarlen & Jerry M. Wells

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  1. Oriana Rossi
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  2. Peter van Baarlen
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  3. Jerry M. Wells
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  1. , Institut für Hygiene, Universitätsklinikum Münster, Robert-Koch-Str. 41, Münster, 48149, Germany

    Ulrich Dobrindt

  2. , Nationale Akademie der Wissenschaften, Deutsche Akademie der Naturforscher Leop, Emil-Abderhalden-Str. 37, Halle, 06108, Germany

    Jörg H. Hacker

  3. , Section of Microbiology, Immunology and, Lund University, Sölvegatan 23, Lund, 22362, Sweden

    Catharina Svanborg

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Rossi, O., van Baarlen, P., Wells, J.M. (2011). Host-Recognition of Pathogens and Commensals in the Mammalian Intestine . In: Dobrindt, U., Hacker, J., Svanborg, C. (eds) Between Pathogenicity and Commensalism. Current Topics in Microbiology and Immunology, vol 358. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2011_191

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