Intracellular heat shock protein-70 negatively regulates TLR4 signaling in the newborn intestinal epithelium

Journal of Immunology

Volumn 188, Issue 9, 2012, Pages 4543-4557

  Afrazi, Amin ^a,b   Sodhi, Chhinder P ^a,b   Good, Misty ^a,b   Jia, Hongpeng ^a,b   Siggers, Richard ^a,b   Yazji, Ibrahim ^a,b   Ma, Congrong ^a,b   Neal, Matthew D ^a,b   Prindle, Thomas ^a,b   Grant, Zachary S ^a,b   Branca, Maria F ^a,b   Ozolek, John ^a,b   Chang, Eugene B ^c   Hackam, David J ^a,b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELASTROL; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG MECHANISM; DRUG TARGETING; GENE OVEREXPRESSION; IN VIVO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM; INTRACELLULAR SPACE; MOUSE; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

ANIMALS; APOPTOSIS; ENTEROCOLITIS, NECROTIZING; FEMALE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INFANT, NEWBORN; INTESTINAL MUCOSA; LIPOPOLYSACCHARIDES; MALE; MICE; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84860324915     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103114     Document Type: Article

References (65)

1. Neu, J., and W. A. Walker. 2011. Necrotizing enterocolitis. N. Engl. J. Med. 364: 255-264.
2. Afrazi, A., C. P. Sodhi, W. Richardson, M. Neal, M. Good, R. Siggers, and D. J. Hackam. 2011. New insights into the pathogenesis and treatment of necrotizing enterocolitis: Toll-like receptors and beyond. Pediatr. Res. 69: 183-188.
3. Leaphart, C. L., J. C. Cavallo, S. C. Gribar, S. Cetin, J. Li, M. F. Branca, T. D. Dubowski, C. P. Sodhi, and D. J. Hackam. 2007. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J. Immunol. 179: 4808-4820.
4. Sodhi, C. P., X. H. Shi, W. M. Richardson, Z. S. Grant, R. A. Shapiro, T. J. Prindle, Jr., M. Branca, A. Russo, S. C. Gribar, C. Ma, and D. J. Hackam. 2010. Toll-like receptor-4 inhibits enterocyte proliferation via impaired beta-catenin signaling in necrotizing enterocolitis. Gastroenterology 138: 185-196.
5. Jilling, T., D. Simon, J. Lu, F. J. Meng, D. Li, R. Schy, R. B. Thomson, A. Soliman, M. Arditi, and M. S. Caplan. 2006. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J. Immunol. 177: 3273-3282. (Pubitemid 44277847)
6. Wolfs, T. G., J. P. Derikx, C. M. Hodin, J. Vanderlocht, A. Driessen, A. P. de Bruïne, C. L. Bevins, F. Lasitschka, N. Gassler, W. G. van Gemert, and W. A. Buurman. 2010. Localization of the lipopolysaccharide recognition complex in the human healthy and inflamed premature and adult gut. Inflamm. Bowel Dis. 16: 68-75.
7. Richardson, W. M., C. P. Sodhi, A. Russo, R. H. Siggers, A. Afrazi, S. C. Gribar, M. D. Neal, S. Dai, T. J. Prindle, Jr., M. Branca, et al. 2010. Nucleotide-binding oligomerization domain-2 inhibits toll-like receptor-4 signaling in the intestinal epithelium. Gastroenterology 139: 904-917.e1-6.
8. Gabai, V. L., A. B. Meriin, D. D. Mosser, A. W. Caron, S. Rits, V. I. Shifrin, and M. Y. Sherman. 1997. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 272: 18033-18037. (Pubitemid 27306383)
9. Jiang, B., P. Liang, G. Deng, Z. Tu, M. Liu, and X. Xiao. 2011. Increased stability of Bcl-2 in HSP70-mediated protection against apoptosis induced by oxidative stress. Cell Stress Chaperones 16: 143-152.
10. Tanaka, K., and T. Mizushima. 2009. Protective role of HSF1 and HSP70 against gastrointestinal diseases. Int. J. Hyperthermia 25: 668-676.
11. Jiang, B., K. Wang, P. Liang, W. Xiao, H. Wang, and X. Xiao. 2009. ATP-binding domain of heat shock protein 70 is essential for its effects on the inhibition of the release of the second mitochondria-derived activator of caspase and apoptosis in C2C12 cells. FEBS J. 276: 2615-2624.
12. Carrizo, L. C., C. M. Ruete, W. A. Manucha, D. R. Ciocca, and P. G. Vallés. 2006. Heat shock protein 70 expression is associated with inhibition of renal tubule epithelial cell apoptosis during recovery from low-protein feeding. Cell Stress Chaperones 11: 309-324. (Pubitemid 46905766)
13. Didelot, C., E. Schmitt, M. Brunet, L. Maingret, A. Parcellier, and C. Garrido. 2006. Heat shock proteins: endogenous modulators of apoptotic cell death. Handb. Exp. Pharmacol: 171-198.
14. Beere, H. M., and D. R. Green. 2001. Stress management - heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol. 11: 6-10. (Pubitemid 32056181)
15. Joly, A. L., G. Wettstein, G. Mignot, F. Ghiringhelli, and C. Garrido. 2010. Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J. Innate Immun. 2: 238-247.
16. Tao, Y., J. Hart, L. Lichtenstein, L. J. Joseph, M. J. Ciancio, S. Hu, E. B. Chang, and M. Bissonnette. 2009. Inducible heat shock protein 70 prevents multifocal flat dysplastic lesions and invasive tumors in an inflammatory model of colon cancer. Carcinogenesis 30: 175-182.
17. Hu, S., X. Zhu, J. R. Triggs, Y. Tao, Y. Wang, L. Lichtenstein, M. Bissonnette, M. W. Musch, and E. B. Chang. 2009. Inflammation-induced, 3'UTR-dependent translational inhibition of Hsp70 mRNA impairs intestinal homeostasis. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G1003-G1011.
18. Gribar, S. C., C. P. Sodhi, W. M. Richardson, R. J. Anand, G. K. Gittes, M. F. Branca, A. Jakub, X. H. Shi, S. Shah, J. A. Ozolek, and D. J. Hackam. 2009. Reciprocal expression and signaling of TLR4 and TLR9 in the pathogenesis and treatment of necrotizing enterocolitis. J. Immunol. 182: 636-646.
19. Radulescu, A., N. A. Zorko, X. Yu, and G. E. Besner. 2009. Preclinical neonatal rat studies of heparin-binding EGF-like growth factor in protection of the intestines from necrotizing enterocolitis. Pediatr. Res. 65: 437-442.
20. Leaphart, C. L., F. Qureshi, S. Cetin, J. Li, T. Dubowski, C. Baty, D. Beer-Stolz, F. Guo, S. A. Murray, and D. J. Hackam. 2007. Interferon-gamma inhibits intestinal restitution by preventing gap junction communication between enterocytes. [Published erratum appears in 2007 Gastroenterology 133: 1746.] Gastroenterology 132: 2395-2411. (Pubitemid 46890858)
21. Cetin, S., H. R. Ford, L. R. Sysko, C. Agarwal, J. Wang, M. D. Neal, C. Baty, G. Apodaca, and D. J. Hackam. 2004. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J. Biol. Chem. 279: 24592-24600. (Pubitemid 38725326)
22. Ding, L. A., and J. S. Li. 2003. Effects of glutamine on intestinal permeability and bacterial translocation in TPN-rats with endotoxemia. World J. Gastroenterol. 9: 1327-1332.
23. Siggers, R. H., and D. J. Hackam. 2011. The role of innate immune-stimulated epithelial apoptosis during gastrointestinal inflammatory diseases. Cell. Mol. Life Sci. 68: 3623-3634.
24. Khailova, L., S. K. Mount Patrick, K. M. Arganbright, M. D. Halpern, T. Kinouchi, and B. Dvorak. 2010. Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G1118-G1127.
25. Jilling, T., J. Lu, M. Jackson, and M. S. Caplan. 2004. Intestinal epithelial apoptosis initiates gross bowel necrosis in an experimental rat model of neonatal necrotizing enterocolitis. Pediatr. Res. 55: 622-629. (Pubitemid 38405849)
26. Houry, W. A. 2001. Chaperone-assisted protein folding in the cell cytoplasm. Curr. Protein Pept. Sci. 2: 227-244. (Pubitemid 32798793)
27. Naylor, D. J., and F. U. Hartl. 2001. Contribution of molecular chaperones to protein folding in the cytoplasm of prokaryotic and eukaryotic cells. Biochem. Soc. Symp. 45-68. (Pubitemid 33658552)
28. Brinker, A., C. Scheufler, F. Von Der Mulbe, B. Fleckenstein, C. Herrmann, G. Jung, I. Moarefi, and F. U. Hartl. 2002. Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 3 Hop 3 Hsp90 complexes. J. Biol. Chem. 277: 19265-19275. (Pubitemid 34967430)
29. Liu, F. H., S. J. Wu, S. M. Hu, C. D. Hsiao, and C. Wang. 1999. Specific interaction of the 70-kDa heat shock cognate protein with the tetratricopeptide repeats. J. Biol. Chem. 274: 34425-34432. (Pubitemid 129511788)
30. Scheufler, C., A. Brinker, G. Bourenkov, S. Pegoraro, L. Moroder, H. Bartunik, F. U. Hartl, and I. Moarefi. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101: 199-210. (Pubitemid 32004747)
31. Freeman, B. C., M. P. Myers, R. Schumacher, and R. I. Morimoto. 1995. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14: 2281-2292.
32. McDonough, H., and C. Patterson. 2003. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8: 303-308. (Pubitemid 38222876)
33. Ballinger, C. A., P. Connell, Y. Wu, Z. Hu, L. J. Thompson, L. Y. Yin, and C. Patterson. 1999. Identification of CHIP, a novel tetratricopeptide repeatcontaining protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 19: 4535-4545. (Pubitemid 29242026)
34. Murata, S., Y. Minami, M. Minami, T. Chiba, and K. Tanaka. 2001. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2: 1133-1138. (Pubitemid 34055961)
35. Qian, S. B., H. McDonough, F. Boellmann, D. M. Cyr, and C. Patterson. 2006. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440: 551-555.
36. Dickinson, E., R. Tuncer, E. Nadler, P. Boyle, S. Alber, S. Watkins, and H. Ford. 1999. NOX, a novel nitric oxide scavenger, reduces bacterial translocation in rats after endotoxin challenge. Am. J. Physiol. 277: G1281-G1287. (Pubitemid 30046031)
37. Unno, N., H. Wang, M. J. Menconi, S. H. Tytgat, V. Larkin, M. Smith, M. J. Morin, A. Chavez, R. A. Hodin, and M. P. Fink. 1997. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology 113: 1246-1257. (Pubitemid 27418978)
38. Cetin, S., C. L. Leaphart, J. Li, I. Ischenko, M. Hayman, J. Upperman, R. Zamora, S. Watkins, H. R. Ford, J. Wang, and D. J. Hackam. 2007. Nitric oxide inhibits enterocyte migration through activation of RhoA-GTPase in a SHP-2-dependent manner. Am. J. Physiol. Gastrointest. Liver Physiol. 292: G1347-G1358. (Pubitemid 47084651)
39. Westerheide, S. D., J. D. Bosman, B. N. Mbadugha, T. L. Kawahara, G. Matsumoto, S. Kim, W. Gu, J. P. Devlin, R. B. Silverman, and R. I. Morimoto. 2004. Celastrols as inducers of the heat shock response and cytoprotection. J. Biol. Chem. 279: 56053-56060. (Pubitemid 40066613)
40. Trott, A., J. D. West, L. Klaić, S. D. Westerheide, R. B. Silverman, R. I. Morimoto, and K. A. Morano. 2008. Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol. Biol. Cell 19: 1104-1112. (Pubitemid 351481823)
41. Paimela, T., J. M. Hyttinen, J. Viiri, T. Ryhänen, R. O. Karjalainen, A. Salminen, and K. Kaarniranta. 2011. Celastrol regulates innate immunity response via NF-κB and Hsp70 in human retinal pigment epithelial cells. Pharmacol. Res. 64: 501-508.
42. Kalmar, B., and L. Greensmith. 2009. Activation of the heat shock response in a primary cellular model of motoneuron neurodegeneration-evidence for neuroprotective and neurotoxic effects. Cell. Mol. Biol. Lett. 14: 319-335.
43. Morgan, J. A., L. Young, and W. McGuire. 2011. Pathogenesis and prevention of necrotizing enterocolitis. Curr. Opin. Infect. Dis. 24: 183-189.
44. Chow, A. M., R. Steel, and R. L. Anderson. 2009. Hsp72 chaperone function is dispensable for protection against stress-induced apoptosis. Cell Stress Chaperones 14: 253-263.
45. Jiang, J., C. A. Ballinger, Y. Wu, Q. Dai, D. M. Cyr, J. Höhfeld, and C. Patterson. 2001. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 276: 42938-42944.
46. Meacham, G. C., C. Patterson, W. Zhang, J. M. Younger, and D. M. Cyr. 2001. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 3: 100-105. (Pubitemid 32114840)
47. Dai, Q., C. Zhang, Y. Wu, H. McDonough, R. A. Whaley, V. Godfrey, H. H. Li, N. Madamanchi, W. Xu, L. Neckers, et al. 2003. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 22: 5446-5458. (Pubitemid 37279954)
48. Asea, A., M. Rehli, E. Kabingu, J. A. Boch, O. Bare, P. E. Auron, M. A. Stevenson, and S. K. Calderwood. 2002. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277: 15028-15034. (Pubitemid 34952579)
49. Vabulas, R. M., P. Ahmad-Nejad, S. Ghose, C. J. Kirschning, R. D. Issels, and H. Wagner. 2002. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277: 15107-15112. (Pubitemid 34952589)
50. Pockley, A. G., M. Muthana, and S. K. Calderwood. 2008. The dual immunoregulatory roles of stress proteins. Trends Biochem. Sci. 33: 71-79.
51. Chase, M. A., D. S. Wheeler, K. M. Lierl, V. S. Hughes, H. R. Wong, and K. Page. 2007. Hsp72 induces inflammation and regulates cytokine production in airway epithelium through a TLR4- and NF-kappaB-dependent mechanism. J. Immunol. 179: 6318-6324.
52. Chen, T., J. Guo, C. Han, M. Yang, and X. Cao. 2009. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J. Immunol. 182: 1449-1459.
53. Gong, J., B. Zhu, A. Murshid, H. Adachi, B. Song, A. Lee, C. Liu, and S. K. Calderwood. 2009. T cell activation by heat shock protein 70 vaccine requires TLR signaling and scavenger receptor expressed by endothelial cells-1. J. Immunol. 183: 3092-3098.
54. Retzlaff, C., Y. Yamamoto, P. S. Hoffman, H. Friedman, and T. W. Klein. 1994. Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect. Immun. 62: 5689-5693. (Pubitemid 24365021)
55. Wheeler, D. S., M. A. Chase, A. P. Senft, S. E. Poynter, H. R. Wong, and K. Page. 2009. Extracellular Hsp72, an endogenous DAMP, is released by virally infected airway epithelial cells and activates neutrophils via Toll-like receptor (TLR)-4. Respir. Res. 10: 31.
56. Tsan, M. F., and B. Gao. 2009. Heat shock proteins and immune system. J. Leukoc. Biol. 85: 905-910.
57. Wallin, R. P., A. Lundqvist, S. H. Moré, A. von Bonin, R. Kiessling, and H. G. Ljunggren. 2002. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23: 130-135. (Pubitemid 34178294)
58. Bausinger, H., D. Lipsker, U. Ziylan, S. Manié, J. P. Briand, J. P. Cazenave, S. Muller, J. F. Haeuw, C. Ravanat, H. de la Salle, and D. Hanau. 2002. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur. J. Immunol. 32: 3708-3713. (Pubitemid 36032655)
59. Gao, B., and M. F. Tsan. 2003. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor alpha release by murine macrophages. J. Biol. Chem. 278: 174-179. (Pubitemid 36043559)
60. Henderson, B., S. K. Calderwood, A. R. Coates, I. Cohen, W. van Eden, T. Lehner, and A. G. Pockley. 2010. Caught with their PAMPs down? The extracellular signalling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 15: 123-141.
61. van Wijk, F., and B. Prakken. 2010. Heat shock proteins: Darwinistic immune modulation on dangerous grounds. J. Leukoc. Biol. 88: 431-434.
62. Fukata, M., K. S. Michelsen, R. Eri, L. S. Thomas, B. Hu, K. Lukasek, C. C. Nast, J. Lechago, R. Xu, Y. Naiki, et al. 2005. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 288: G1055-G1065. (Pubitemid 40563149)
63. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
64. Fukata, M., Y. Hernandez, D. Conduah, J. Cohen, A. Chen, K. Breglio, T. Goo, D. Hsu, R. Xu, and M. T. Abreu. 2009. Innate immune signaling by Toll-like receptor-4 (TLR4) shapes the inflammatory microenvironment in colitisassociated tumors. Inflamm. Bowel Dis. 15: 997-1006.
65. Hornef, M. W., B. H. Normark, A. Vandewalle, and S. Normark. 2003. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J. Exp. Med. 198: 1225-1235. (Pubitemid 37323387)