Compartmentalizing intestinal epithelial cell toll-like receptors for immune surveillance

Cellular and Molecular Life Sciences

Volumn 72, Issue 17, 2015, Pages 3343-3353

  Yu, Shiyan ^a   Gao, Nan ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Intestinal epithelium; Microbe; Toll like receptor; Traffic

Indexed keywords

ADAPTOR PROTEIN; CD14 ANTIGEN; CHAPERONE; PROTEIN MD 2; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSMEMBRANE EMP24 DOMAIN CONTAINING PROTEIN; UNC93 HOMOLOG B1 PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; LY96 PROTEIN, HUMAN; TMED7 PROTEIN, HUMAN; UNC93B1 PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

CELL COMPARTMENTALIZATION; CELL MIGRATION; CROHN DISEASE; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; INTESTINE EPITHELIUM CELL; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS; BIOLOGICAL MODEL; CYTOLOGY; EPITHELIUM CELL; GENETICS; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY;

ANTIGENS, CD14; EPITHELIAL CELLS; HUMANS; IMMUNOLOGIC SURVEILLANCE; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; LYMPHOCYTE ANTIGEN 96; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; TOLL-LIKE RECEPTORS; VESICULAR TRANSPORT PROTEINS;

EID: 84938949551     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1931-1     Document Type: Review

References (122)

1. Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10(5):323-335
2. Kashyap PC et al (2013) Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proc Natl Acad Sci USA 110(42):17059-17064
3. Erkosar B et al (2013) Host-intestinal microbiota mutualism: "learning on the fly". Cell Host Microbe 13(1):8-14
4. Pickard JM et al (2014) Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514(7524):638-641
5. Brestoff JR, Artis D (2013) Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14(7):676-684
6. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121-141
7. Buffie CG, Pamer EG (2013) Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13(11):790-801
8. Maier L et al (2013) Microbiota-derived hydrogen fuels Salmonella typhimurium invasion of the gut ecosystem. Cell Host Microbe 14(6):641-651
9. Clemente JC et al (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148(6):1258-1270
10. Sekirov I et al (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859-904
11. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7(5):349-359
12. Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol 15(1):19-33
13. Mabbott NA et al (2013) Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 6(4):666-677
14. Wells JM et al (2011) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA 108(Suppl 1):4607-4614
15. Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10(2):131-144
16. Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14(3):141-153
17. Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34(5):637-650
18. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4(7):499-511
19. Kang JY et al (2009) Recognition of lipopeptide patterns by toll-like receptor 2-toll-like receptor 6 heterodimer. Immunity 31(6):873-884
20. Jin MS et al (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130(6):1071-1082
21. Koblansky AA et al (2013) Recognition of profilin by toll-like receptor 12 is critical for host resistance to Toxoplasma gondii. Immunity 38(1):119-130
22. Oldenburg M et al (2012) TLR13 recognizes bacterial 23S rRNA devoid of erythromycin resistance-forming modification. Science 337(6098):1111-1115
23. Rifkin IR et al (2005) Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 204:27-42
24. Rakoff-Nahoum S, Medzhitov R (2009) Toll-like receptors and cancer. Nat Rev Cancer 9(1):57-63
25. Zhang P et al (2009) Cutting edge: cardiac myosin activates innate immune responses through TLRs. J Immunol 183(1):27-31
26. Barton GM, Kagan JC (2009) A cell biological view of toll-like receptor function: regulation through compartmentalization. Nat Rev Immunol 9(8):535-542
27. Gay NJ et al (2014) Assembly and localization of toll-like receptor signalling complexes. Nat Rev Immunol 14(8):546-558
28. 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
29. O'Neill LA, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in toll-like receptor signalling. Nat Rev Immunol 7(5):353-364
30. Blasius AL, Beutler B (2010) Intracellular toll-like receptors. Immunity 32(3):305-315
31. Otte JM, Cario E, Podolsky DK (2004) Mechanisms of cross hyporesponsiveness to toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126(4):1054-1070
32. Cario E et al (2002) Commensal-associated molecular patterns induce selective toll-like receptor-trafficking from apical membrane to cytoplasmic compartments in polarized intestinal epithelium. Am J Pathol 160(1):165-173
33. Melmed G et al (2003) Human intestinal epithelial cells are broadly unresponsive to toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J Immunol 170(3):1406-1415
34. Lavelle EC et al (2010) The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 3(1):17-28
35. Fusunyan RD et al (2001) Evidence for an innate immune response in the immature human intestine: toll-like receptors on fetal enterocytes. Pediatr Res 49(4):589-593
36. Chabot S et al (2006) TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J Immunol 176(7):4275-4283
37. 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
38. Ortega-Cava CF et al (2003) Strategic compartmentalization of toll-like receptor 4 in the mouse gut. J Immunol 170(8):3977-3985
39. Hornef MW et al (2002) Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 195(5):559-570
40. Ortega-Cava CF et al (2006) Epithelial toll-like receptor 5 is constitutively localized in the mouse cecum and exhibits distinctive down-regulation during experimental colitis. Clin Vaccine Immunol 13(1):132-138
41. Gewirtz AT et al (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167(4):1882-1885
42. Rhee SH et al (2005) Pathophysiological role of toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci USA 102(38):13610-13615
43. Bambou JC et al (2004) In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 279(41):42984-42992
44. Barton GM, Kagan JC, Medzhitov R (2006) Intracellular localization of toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol 7(1):49-56
45. Onji M et al (2013) An essential role for the N-terminal fragment of toll-like receptor 9 in DNA sensing. Nat Commun 4:1949
46. Ewald SE et al (2008) The ectodomain of toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456(7222):658-662
47. Park B et al (2008) Proteolytic cleavage in an endolysosomal compartment is required for activation of toll-like receptor 9. Nat Immunol 9(12):1407-1414
48. Ewald SE et al (2011) Nucleic acid recognition by toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J Exp Med 208(4):643-651
49. Mouchess ML et al (2011) Transmembrane mutations in toll-like receptor 9 bypass the requirement for ectodomain proteolysis and induce fatal inflammation. Immunity 35(5):721-732
50. Lee J et al (2006) Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 8(12):1327-1336
51. Yu S et al (2014) TLR sorting by Rab11 endosomes maintains intestinal epithelial-microbial homeostasis. EMBO J 33(17):1882-1895
52. Rumio C et al (2004) Degranulation of Paneth cells via toll-like receptor 9. Am J Pathol 165(2):373-381
53. Rumio C et al (2012) Induction of Paneth cell degranulation by orally administered toll-like receptor ligands. J Cell Physiol 227(3):1107-1113
54. Schulz O, Pabst O (2013) Antigen sampling in the small intestine. Trends Immunol 34(4):155-161
55. De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9(4):273-284
56. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513-525
57. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91(1):119-149
58. Yu IM, Hughson FM (2010) Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 26:137-156
59. Takahashi K et al (2007) A protein associated with toll-like receptor (TLR) 4 (PRAT4A) is required for TLR-dependent immune responses. J Exp Med 204(12):2963-2976
60. Liu B et al (2010) Folding of toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat Commun 1:79
61. Yang Y et al (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26(2):215-226
62. Bonifacino JS (2014) Adaptor proteins involved in polarized sorting. J Cell Biol 204(1):7-17
63. Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10(9):597-608
64. Hsu VW, Bai M, Li J (2012) Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol 13(5):323-328
65. Hirokawa N et al (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10(10):682-696
66. Roberts AJ et al (2013) Functions and mechanics of dynein motor proteins. Nat Rev Mol Cell Biol 14(11):713-726
67. Hammer JA 3rd, Sellers JR (2012) Walking to work: roles for class V myosins as cargo transporters. Nat Rev Mol Cell Biol 13(1):13-26
68. Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10(11):765-777
69. Seabra MC, Coudrier E (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5(6):393-399
70. Hancock WO (2014) Bidirectional cargo transport: moving beyond tug of war. Nat Rev Mol Cell Biol 15(9):615-628
71. Ivanov II et al (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4(4):337-349
72. Martin-Belmonte F et al (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128(2):383-397
73. Rodriguez-Boulan E, Macara IG (2014) Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 15(4):225-242
74. Leifer CA et al (2006) Cytoplasmic targeting motifs control localization of toll-like receptor 9. J Biol Chem 281(46):35585-35592
75. Lee BL et al (2013) UNC93B1 mediates differential trafficking of endosomal TLRs. Elife 2:e00291
76. Ohno H (2006) Clathrin-associated adaptor protein complexes. J Cell Sci 119(Pt 18):3719-3721
77. Hase K et al (2013) AP-1B-mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. Gastroenterology 145(3):625-635
78. Takahashi D et al (2011) The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. Gastroenterology 141(2):621-632
79. Shafaq-Zadah M et al (2012) AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development 139(11):2061-2070
80. Setta-Kaffetzi N et al (2014) AP1S3 Mutations are associated with pustular psoriasis and impaired toll-like receptor 3 trafficking. Am J Hum Genet 94(5):790-797
81. Mantegazza AR et al (2012) Adaptor protein-3 in dendritic cells facilitates phagosomal toll-like receptor signaling and antigen presentation to CD4+ T cells. Immunity 36(5):782-794
82. Sasai M, Linehan MM, Iwasaki A (2010) Bifurcation of toll-like receptor 9 signaling by adaptor protein 3. Science 329(5998):1530-1534
83. Blasius AL et al (2010) Slc15a4, AP-3, and Hermansky-Pudlak syndrome proteins are required for toll-like receptor signaling in plasmacytoid dendritic cells. Proc Natl Acad Sci USA 107(46):19973-19978
84. Weisz OA, Rodriguez-Boulan E (2009) Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 122(Pt 23):4253-4266
85. Weber AN, Morse MA, Gay NJ (2004) Four N linked glycosylation sites in human toll-like receptor 2 cooperate to direct efficient biosynthesis and secretion. J Biol Chem 279(33):34589-34594
86. Sun J et al (2006) Structural and functional analyses of the human toll-like receptor 3. Role of glycosylation. J Biol Chem 281(16):11144-11151
87. Istomin AY, Godzik A (2009) Understanding diversity of human innate immunity receptors: analysis of surface features of leucine-rich repeat domains in NLRs and TLRs. BMC Immunol 10:48
88. Xu S et al (2011) A Rab11a-enriched subapical membrane compartment regulates a cytoskeleton-dependent transcytotic pathway in secretory epithelial cells of the lacrimal gland. J Cell Sci 124(Pt 20):3503-3514
89. Roland JT et al (2011) Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci USA 108(7):2789-2794
90. Husebye H et al (2010) The Rab11a GTPase controls toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33(4):583-596
91. Wang D et al (2010) Ras-related protein Rab10 facilitates TLR4 signaling by promoting replenishment of TLR4 onto the plasma membrane. Proc Natl Acad Sci USA 107(31):13806-13811
92. Schuck S et al (2007) Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8(1):47-60
93. Chen S et al (2014) SEC-10 and RAB-10 coordinate basolateral recycling of clathrin-independent cargo through endosomal tubules in Caenorhabditis elegans. Proc Natl Acad Sci USA 111(43):15432-15437
94. Tuma P, Hubbard AL (2003) Transcytosis: crossing cellular barriers. Physiol Rev 83(3):871-932
95. Su T et al (2010) A kinase cascade leading to Rab11-FIP5 controls transcytosis of the polymeric immunoglobulin receptor. Nat Cell Biol 12(12):1143-1153
96. Piper RC, Luzio JP (2007) Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr Opin Cell Biol 19(4):459-465
97. Chiang CY et al (2012) Cofactors required for TLR7- and TLR9-dependent innate immune responses. Cell Host Microbe 11(3):306-318
98. Husebye H et al (2006) Endocytic pathways regulate toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J 25(4):683-692
99. Mashukova A, Wald FA, Salas PJ (2011) Tumor necrosis factor alpha and inflammation disrupt the polarity complex in intestinal epithelial cells by a posttranslational mechanism. Mol Cell Biol 31(4):756-765
100. St Johnston D, Ahringer J (2010) Cell polarity in eggs and epithelia: parallels and diversity. Cell 141(5):757-774
101. Pasparakis M (2009) Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat Rev Immunol 9(11):778-788
102. Eyster KM (2007) The membrane and lipids as integral participants in signal transduction: lipid signal transduction for the non-lipid biochemist. Adv Physiol Educ 31(1):5-16
103. Kagan JC, Medzhitov R (2006) Phosphoinositide-mediated adaptor recruitment controls toll-like receptor signaling. Cell 125(5):943-955
104. Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93(3):1019-1137
105. Tabeta K et al (2006) The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via toll-like receptors 3, 7 and 9. Nat Immunol 7(2):156-164
106. Lee BL, Barton GM (2014) Trafficking of endosomal toll-like receptors. Trends Cell Biol 24(6):360-369
107. Brinkmann MM et al (2007) The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J Cell Biol 177(2):265-275
108. Kim J et al (2013) Acidic amino acid residues in the juxtamembrane region of the nucleotide-sensing TLRs are important for UNC93B1 binding and signaling. J Immunol 190(10):5287-5295
109. Itoh H et al (2011) UNC93B1 physically associates with human TLR8 and regulates TLR8-mediated signaling. PLoS One 6(12):e28500
110. Funami K et al (2004) The cytoplasmic 'linker region' in toll-like receptor 3 controls receptor localization and signaling. Int Immunol 16(8):1143-1154
111. Pohar J et al (2012) The role of UNC93B1 protein in surface localization of TLR3 receptor and in cell priming to nucleic acid agonists. J Biol Chem 288(1):442-454
112. Huh JW et al (2014) UNC93B1 is essential for the plasma membrane localization and signaling of toll-like receptor 5. Proc Natl Acad Sci USA 111(19):7072-7077
113. Qi R, Singh D, Kao CC (2012) Proteolytic processing regulates toll-like receptor 3 stability and endosomal localization. J Biol Chem 287(39):32617-32629
114. Pelka K et al (2014) Cutting edge: the UNC93B1 tyrosine-based motif regulates trafficking and TLR responses via separate mechanisms. J Immunol 193(7):3257-3261
115. Latz E et al (2002) Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem 277(49):47834-47843
116. Ishihara S et al (2004) Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 173(2):1406-1416
117. Lee CC, Avalos AM, Ploegh HL (2012) Accessory molecules for toll-like receptors and their function. Nat Rev Immunol 12(3):168-179
118. Zanoni I et al (2011) CD14 controls the LPS-induced endocytosis of toll-like receptor 4. Cell 147(4):868-880
119. Jiang Z et al (2005) CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6(6):565-570
120. Abreu MT et al (2002) TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 277(23):20431-20437
121. Frolova L et al (2008) Expression of toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem 56(3):267-274
122. Liaunardy-Jopeace A, Bryant CE, Gay NJ (2014) The COP II adaptor protein TMED7 is required to initiate and mediate the delivery of TLR4 to the plasma membrane. Sci Signal 7(336):ra70