Heat Shock Protein gp96 Is a Master Chaperone for Toll-like Receptors and Is Important in the Innate Function of Macrophages

Immunity

Volumn 26, Issue 2, 2007, Pages 215-226

  Yang, Yi ^a   Liu, Bei ^a   Dai, Jie ^a   Srivastava, Pramod K ^a   Zammit, David J ^a   Lefrançois, Leo ^a   Li, Zihai ^a  

^a UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

CHAPERONE; CYTOKINE; GAMMA INTERFERON; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; ENDOTOXEMIA; INFECTION SENSITIVITY; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN INTERACTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEAT-SHOCK PROTEINS; IMMUNOPRECIPITATION; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MOLECULAR CHAPERONES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTORS;

EID: 33847260278     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2006.12.005     Document Type: Article

References (50)

1. Akira S., and Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 4 (2004) 499-511
2. Argon Y., and Simen B.B. GRP94, an ER chaperone with protein and peptide binding properties. Semin. Cell Dev. Biol. 10 (1999) 495-505
3. Barton G.M., Kagan J.C., and Medzhitov R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol. 7 (2006) 49-56
4. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., and Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
5. Beutler B., Milsark I.W., and Cerami A.C. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229 (1985) 869-871
6. Cabanes D., Sousa S., Cebria A., Lecuit M., Garcia-del Portillo F., and Cossart P. Gp96 is a receptor for a novel Listeria monocytogenes virulence factor, Vip, a surface protein. EMBO J. 24 (2005) 2827-2838
7. Chuang T.H., and Ulevitch R.J. Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat. Immunol. 5 (2004) 495-502
8. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., and Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8 (1999) 265-277
9. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., Diamond M.S., and Colonna M. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103 (2006) 8459-8464
10. Hawn T.R., Wu H., Grossman J.M., Hahn B.H., Tsao B.P., and Aderem A. A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 102 (2005) 10593-10597
11. Ishii K.J., Coban C., Kato H., Takahashi K., Torii Y., Takeshita F., Ludwig H., Sutter G., Suzuki K., Hemmi H., et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7 (2006) 40-48
12. Iwasaki A., and Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5 (2004) 987-995
13. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O., and Akira S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23 (2005) 19-28
14. Kozutsumi Y., Segal M., Normington K., Gething M.J., and Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332 (1988) 462-464
15. Kuznetsov G., Bush K.T., Zhang P.L., and Nigam S.K. Perturbations in maturation of secretory proteins and their association with endoplasmic reticulum chaperones in a cell culture model for epithelial ischemia. Proc. Natl. Acad. Sci. USA 93 (1996) 8584-8589
16. Lakso M., Pichel J.G., Gorman J.R., Sauer B., Okamoto Y., Lee E., Alt F.W., and Westphal H. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93 (1996) 5860-5865
17. Laroux F.S., Romero X., Wetzler L., Engel P., and Terhorst C. Cutting edge: MyD88 controls phagocyte NADPH oxidase function and killing of gram-negative bacteria. J. Immunol. 175 (2005) 5596-5600
18. Latz E., Schoenemeyer A., Visintin A., Fitzgerald K.A., Monks B.G., Knetter C.F., Lien E., Nilsen N.J., Espevik T., and Golenbock D.T. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5 (2004) 190-198
19. Lee A.S., Delegeane A., and Scharff D. Highly conserved glucose-regulated protein in hamster and chicken cells: preliminary characterization of its cDNA clone. Proc. Natl. Acad. Sci. USA 78 (1981) 4922-4925
20. Li Z., and Srivastava P.K. Tumor rejection antigen gp96/grp94 is an ATPase: implications for protein folding and antigen presentation. EMBO J. 12 (1993) 3143-3151
21. Liew F.Y., Xu D., Brint E.K., and O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5 (2005) 446-458
22. Liu B., Dai J., Zheng H., Stoilova D., Sun S., and Li Z. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc. Natl. Acad. Sci. USA 100 (2003) 15824-15829
23. Liu B., Yang Y., Dai J., Medzhitov R., Freudenberg M.A., Zhang P.L., and Li Z. TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J. Immunol. 177 (2006) 6880-6888
24. Loo M.A., Jensen T.J., Cui L., Hou Y., Chang X.B., and Riordan J.R. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 17 (1998) 6879-6887
25. Medzhitov R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1 (2001) 135-145
26. Melnick J., Dul J.L., and Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370 (1994) 373-375
27. Meunier L., Usherwood Y.K., Chung K.T., and Hendershot L.M. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13 (2002) 4456-4469
28. Nishiya T., Kajita E., Miwa S., and Defranco A.L. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements. J. Biol. Chem. 280 (2005) 37107-37117
29. Nomura F., Akashi S., Sakao Y., Sato S., Kawai T., Matsumoto M., Nakanishi K., Kimoto M., Miyake K., Takeda K., and Akira S. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J. Immunol. 164 (2000) 3476-3479
30. Novak A., Guo C., Yang W., Nagy A., and Lobe C.G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28 (2000) 147-155
31. O'Neill L.A., Fitzgerald K.A., and Bowie A.G. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol. 24 (2003) 286-290
32. Pamer E.G. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4 (2004) 812-823
33. Pasare C., and Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299 (2003) 1033-1036
34. Pasare C., and Medzhitov R. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 21 (2004) 733-741
35. Pope C., Kim S.K., Marzo A., Masopust D., Williams K., Jiang J., Shen H., and Lefrancois L. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166 (2001) 3402-3409
36. Randow F., and Seed B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat. Cell Biol. 3 (2001) 891-896
37. Roach J.C., Glusman G., Rowen L., Kaur A., Purcell M.K., Smith K.D., Hood L.E., and Aderem A. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 102 (2005) 9577-9582
38. Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., and Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2 (2001) 947-950
39. Shortman K., and Liu Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2 (2002) 151-161
40. Srivastava P.K., DeLeo A.B., and Old L.J. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc. Natl. Acad. Sci. USA 83 (1986) 3407-3411
41. Stoilova D., Dai J., de Crom R., van Haperen R., and Li Z. Haplosufficiency or functional redundancy of a heat shock protein gp96 gene in the adaptive immune response. Cell Stress Chaperones 5 (2000) 395
42. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., Mudd S., Mann N., Sovath S., Goode J., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7 (2006) 156-164
43. Takeda K., and Akira S. Toll-like receptors in innate immunity. Int. Immunol. 17 (2005) 1-14
44. Vandenbroeck K., Martens E., and Alloza I. Multi-chaperone complexes regulate the folding of interferon-gamma in the endoplasmic reticulum. Cytokine 33 (2006) 264-273
45. Vogen S., Gidalevitz T., Biswas C., Simen B.B., Stein E., Gulmen F., and Argon Y. Radicicol-sensitive peptide binding to the N-terminal portion of GRP94. J. Biol. Chem. 277 (2002) 40742-40750
46. Wang T., Chuang T.H., Ronni T., Gu S., Du Y.C., Cai H., Sun H.Q., Yin H.L., and Chen X. Flightless I homolog negatively modulates the TLR pathway. J. Immunol. 176 (2006) 1355-1362
47. Yang Y., and Li Z. Roles of heat shock protein gp96 in the ER quality control: redundant or unique function?. Mol. Cells 20 (2005) 173-182
48. Yarovinsky F., Zhang D., Andersen J.F., Bannenberg G.L., Serhan C.N., Hayden M.S., Hieny S., Sutterwala F.S., Flavell R.A., Ghosh S., and Sher A. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308 (2005) 1626-1629
49. Ye M., Iwasaki H., Laiosa C.V., Stadtfeld M., Xie H., Heck S., Clausen B., Akashi K., and Graf T. Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity 19 (2003) 689-699
50. Zheng H., and Li Z. Cutting edge: cross-presentation of cell-associated antigens to MHC class I molecule is regulated by a major transcription factor for heat shock proteins. J. Immunol. 173 (2004) 5929-5933