Loss of toll-like receptor 2 and 4 leads to differential induction of endoplasmic reticulum stress and proapoptotic responses in the intestinal epithelium under conditions of chronic inflammation

Journal of Proteome Research

Volumn 8, Issue 10, 2009, Pages 4406-4417

  Messlik, Anja ^a   Schmechel, Silke ^a   Kisling, Sigrid ^a   Bereswill, Stefan ^b   Heimesaat, Markus M ^b   Fischer, Andre ^b   Göbel, Ulf ^b   Haller, Dirk ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Endoplasmic reticulum (ER) stress; Epithelial cell proteome; Experimental colitis; Inflammatory bowel diseases; Interleukin 10 (IL 10) deficient mice; Intestinal epithelial cells; Intestinal homeostasis; Maldi tof mass spectrometry; Toll like receptor (TLR)

Indexed keywords

CASPASE 3; CHAPERONE; INTERLEUKIN 10; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ISOLATION; CELLULAR STRESS RESPONSE; CHRONIC INFLAMMATION; COLITIS; CONTROLLED STUDY; CROSS BREEDING; DISSOCIATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME DEGRADATION; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; HOMEOSTASIS; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN TARGETING; PROTEOMICS; STEADY STATE; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; CHRONIC DISEASE; COLITIS; COLON; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOPLASMIC RETICULUM; HISTOCYTOCHEMISTRY; INFLAMMATION; INTERLEUKIN-10; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEOMICS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

BACTERIA (MICROORGANISMS); MUS;

EID: 70349972786     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr9000465     Document Type: Article

References (39)

1. Abreu, M. T.; Fukata, M.; Arditi, M. TLR signaling in the gut in health and disease. J. Immunol. 2005, 174 (8), 4453-4460 (Pubitemid 40504521)
2. Cario, E. Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut 2005, 54 (8), 1182-1193 (Pubitemid 41025918)
3. Carneiro, L. A.; Travassos, L. H.; Philpott, D. J. Innate immune recognition of microbes through Nod1 and Nod2: implications for disease. Microbes Infect. 2004, 6 (6), 609-616
4. Schwandner, R.; et al. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 1999, 274 (25), 17406-17409 (Pubitemid 129519082)
5. Yoshimura, A.; et al. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 1999, 163 (1), 1-5.
6. Poltorak, A.; et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282 (5396), 2085-2088
7. Xu, Y.; et al. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 2000, 408 (6808), 111-115
8. O'Neill, L. A.; Fitzgerald, K. A.; Bowie, A. G. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol. 2003, 24 (6), 286-290
9. Akira, S.; Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4 (7), 499-511.
10. Kawai, T.; Akira, S. TLR signaling. Semin. Immunol. 2007, 19 (1), 24-32.
11. Kuhn, R.; et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75 (2), 263-274 (Pubitemid 23320290)
12. Sellon, R. K.; et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 1998, 66 (11), 5224-5231
13. Strober, W.; Fuss, I. J.; Blumberg, R. S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002, 20, 495-549.
14. Rakoff-Nahoum, S.; Hao, L.; Medzhitov, R. Role of toll-like receptors in spontaneous commensal-dependent colitis. Immunity 2006, 25 (2), 319-329 (Pubitemid 44224143)
15. Rakoff-Nahoum, S.; et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118 (2), 229-241
16. Sundberg, J. P.; et al. Spontaneous, heritable colitis in a new substrain of C3H/HeJ mice. Gastroenterology 1994, 107 (6), 1726-1735
17. Mahler, M.; et al. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am. J. Physiol. 1998, 274 (3 Pt 1), G544-51.
18. Schnare, M.; et al. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2001, 2 (10), 947-950 (Pubitemid 32976167)
19. Frank, D. N.; et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (34), 13780-13785
20. Heimesaat, M. M.; et al. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J Immunol 2006, 177 (12), 8785-8795
21. Heimesaat, M. M.; et al. Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS ONE 2007, 2 (7), e662.
22. Szegezdi, E.; et al. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7 (9), 880-885 (Pubitemid 44523966)
23. Endo, M.; et al. The ER stress pathway involving CHOP is activated in the lungs of LPS-treated mice. J. Biochem. 2005, 138 (4), 501-507
24. Endo, M.; et al. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 2006, 176 (10), 6245-6253
25. Shkoda, A.; et al. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 2007, 132 (1), 190-207. (Pubitemid 46108743)
26. Heimesaat, M. M.; et al. Exacerbation of murine ileitis by Toll-like receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli. Gut 2007, 56 (7), 941-948
27. Rath, H. C.; et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLAB27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 1996, 98 (4), 945-953
28. Ruiz, P. A.; et al. IL-10 gene-deficient mice lack TGF-beta/Smad signaling and fail to inhibit proinflammatory gene expression in intestinal epithelial cells after the colonization with colitogenic Enterococcus faecalis. J. Immunol. 2005, 174 (5), 2990-2999
29. Yoshida, H. ER stress and diseases. FEBS J. 2007, 274 (3), 630-658
30. Rutkowski, D. T.; et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006, 4 (11), e374.
31. Malhotra, J. D.; Kaufman, R. J. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007, 18 (6), 16-31.
32. Shearwin-Whyatt, L. M.; Kumar, S. Caspases in developmental cell death. IUBMB Life 1999, 48 (2), 143-150
33. Kumar, S. Mechanisms mediating caspase activation in cell death. Cell Death Differ. 1999, 6 (11), 1060-1066
34. Grossmann, J.; et al. Induction of apoptosis before shedding of human intestinal epithelial cells. Am. J. Gastroenterol. 2002, 97 (6), 1421-1428 (Pubitemid 34664787)
35. Seimon, T. A.; et al. Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (52), 19794-19799
36. Zhao, Q.; et al. A mitochondrial specific stress response in mammalian cells. EMBO J. 2002, 21 (17), 4411-4419 (Pubitemid 34984328)
37. Martinus, R. D.; et al. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur. J. Biochem. 1996, 240 (1), 98-103.
38. Yoneda, T.; et al. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci. 2004, 117 (Pt 18), 4055-4066
39. Horibe, T.; Hoogenraad, N. J. The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response. PLoS ONE 2007, 2 (9), e835.