CD91-dependent modulation of immune responses by heat shock proteins: A role in autoimmunity

Autoimmune Diseases

Volumn 1, Issue 1, 2012, Pages

  Binder, Robert J ^a   Zhou, Yu Jerry ^a   Messmer, Michelle N ^a   Pawaria, Sudesh ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEASOME; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; CELL INTERACTION; CELL MATURATION; HUMAN; IMMUNIZATION; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOTHERAPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TH1 CELL; TUMOR IMMUNITY;

EID: 84871397752     PISSN: None     EISSN: 20900430     Source Type: Journal    
DOI: 10.1155/2012/863041     Document Type: Review

References (106)

1. Lindquist S., Craig E. A., The heat-shock proteins. Annual Review of Genetics 1988 22 631 677 2-s2.0-0024151897 (Pubitemid 19156675)
2. Binder R. J., Heat-shock protein-based vaccines for cancer and infectious disease. Expert Review of Vaccines 2008 7 3 383 393 2-s2.0-42049087381 10.1586/14760584.7.3.383 (Pubitemid 351520026)
3. Wang X. Y., Kazim L., Repasky E. A., Subjeck J. R., Characterization of heat shock protein 110 and glucose-regulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine activity. Journal of Immunology 2001 166 1 490 497 2-s2.0-0035167866 (Pubitemid 32038468)
4. Manjili M. H., Henderson R., Wang X. Y., Chen X., Li Y., Repasky E., Kazim L., Subjeck J. R., Development of a recombinant HSP110-HER-2/neu vaccine using the chaperoning properties of HSP110. Cancer Research 2002 62 6 1737 1742 2-s2.0-0037086266 (Pubitemid 34408496)
5. Cresswell P., Ackerman A. L., Giodini A., Peaper D. R., Wearsch P. A., Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunological Reviews 2005 207 145 157 2-s2.0-26244455510 10.1111/j.0105-2896. 2005.00316.x (Pubitemid 41415014)
6. Srivastava P. K., Udono H., Blachere N. E., Li Z., Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 1994 39 2 93 98 2-s2.0-0028366212 (Pubitemid 23344809)
7. Binder R. J., Blachere N. E., Srivastava P. K., Heat shock protein-chaperoned peptides but not free peptides introduced into the cytosol are presented efficiently by major histocompatibility complex I molecules. Journal of Biological Chemistry 2001 276 20 17163 17171 2-s2.0-0035907379 10.1074/jbc.M011547200
8. Kunisawa J., Shastri N., Hsp90 α chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 2006 24 5 523 534 2-s2.0-33646575879 10.1016/j.immuni.2006.03. 015 (Pubitemid 43728158)
9. Callahan M. K., Garg M., Srivastava P. K., Heat-shock protein 90 associates with N-terminal extended peptides and is required for direct and indirect antigen presentation. Proceedings of the National Academy of Sciences of the United States of America 2008 105 5 1662 1667 2-s2.0-40349088739 10.1073/pnas.0711365105 (Pubitemid 351346571)
10. Villanueva M. S., Fischer P., Feen K., Pamer E. G., Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity 1994 1 6 479 489 2-s2.0-0028501143
11. Yewdell J. W., Reits E., Neefjes J., Making sense of mass destruction: quantitating MHC class I antigen presentation. Nature Reviews Immunology 2003 3 12 952 961 2-s2.0-0346521283 (Pubitemid 37521537)
12. Ménoret A., Peng P., Srivastava P. K., Association of peptides with heat shock protein gp96 occurs in vivo and not after cell lysis. Biochemical and Biophysical Research Communications 1999 262 3 813 818 2-s2.0-0344132066 10.1006/bbrc.1999.1306 (Pubitemid 29443740)
13. Peng P., Ménoret A., Srivastava P. K., Purification of immunogenic heat shock protein 70-peptide complexes by ADP-affinity chromatography. Journal of Immunological Methods 1997 204 1 13 21 2-s2.0-0342547302 10.1016/S0022-1759(97)00017-3 (Pubitemid 27192307)
14. Dick T. P., Ruppert T., Groettrup M., Kloetzel P. M., Kuehn L., Koszinowski U. H., Stevanović S., Schild H., Rammensee H. G., Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell 1996 86 2 253 262 2-s2.0-0030602834 10.1016/S0092-8674(00)80097-5 (Pubitemid 26286108)
15. Ishii T., Udono H., Yamano T., Ohta H., Uenaka A., Toshiro O., Hizuta A., Tanaka N., Srivastava P. K., Nakayama E., Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. Journal of Immunology 1999 162 3 1303 1309 2-s2.0-0033083413 (Pubitemid 29306999)
16. Stocki P., Morris N. J., Preisinger C., Wang X. N., Kolch W., Multhoff G., Dickinson A. M., Identification of potential HLA class i and class II epitope precursors associated with heat shock protein 70 (HSPA). Cell Stress and Chaperones 2010 15 5 729 741 2-s2.0-77955712821 10.1007/s12192-010-0184-z
17. Kropp L. E., Garg M., Binder R. J., Ovalbumin-derived precursor peptides are transferred sequentially from gp96 and calreticulin to MHC class I in the endoplasmic reticulum. Journal of Immunology 2010 184 10 5619 5627 2-s2.0-77954721411 10.4049/jimmunol.0902368
18. Nieland T. J. F., Tan M. C. A. A., Muijen M. M. V., Koning F., Kruisbeek A. M., Van Bleek G. M., Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proceedings of the National Academy of Sciences of the United States of America 1996 93 12 6135 6139 2-s2.0-0029892849 10.1073/pnas.93.12.6135 (Pubitemid 26190816)
19. Breloer M., Marti T., Fleischer B., von Bonin A., 1998Isolation of processed, H-2Kb-binding ovalbumin-derived peptides associated with the stress proteins HSP70 and gp96. European Journal of Immunology 1998 28 1016 1021 (Pubitemid 28116215)
20. Arnold D., Wahl C., Faath S., Rammensee H. G., Schild H., Influences of transporter associated with antigen processing (TAP) on the repertoire of peptides associated with the endoplasmic reticulum- resident stress protein gp96. Journal of Experimental Medicine 1997 186 3 461 466 2-s2.0-0030800342 10.1084/jem.186.3.461 (Pubitemid 27332905)
21. Li M., Davey G. M., Sutherland R. M., Kurts C., Lew A. M., Hirst C., Carbone F. R., Heath W. R., Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. Journal of Immunology 2001 166 10 6099 6103 2-s2.0-0035873381 (Pubitemid 32440737)
22. + T cells. Nature Immunology 2005 6 6 593 599 2-s2.0-20544433550 10.1038/ni1201 (Pubitemid 41710730)
23. Binder R. J., Han D. K., Srivastava P. K., CD91: a receptor for heat shock protein gp96. Nature Immunology 2000 1 2 151 155 2-s2.0-0034252620
24. Basu S., Binder R. J., Ramalingam T., Srivastava P. K., CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 2001 14 3 303 313 2-s2.0-0035070198 10.1016/S1074-7613(01)00111-X (Pubitemid 32289294)
25. Binder R. J., Hsp receptors: the cases of identity and mistaken identity. Current Opinion in Molecular Therapeutics 2009 11 1 62 71 2-s2.0-58849156936
26. Arnold-Schild D., Hanau D., Spehner D., Schmid C., Rammensee H. G., De La Salle H., Schild H., Cutting edge: receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. Journal of Immunology 1999 162 7 3757 3760 2-s2.0-0033120990 (Pubitemid 29314749)
27. Singh-Jasuja H., Toes R. E. M., Spee P., Münz C., Hilf N., Schoenberger S. P., Ricciardi-Castagnoli P., Neefjes J., Rammensee H. G., Arnold-Schild D., Schild H., Cross-presentation of glycoprotein 96-associated antigens: on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. Journal of Experimental Medicine 2000 191 11 1965 1974 2-s2.0-0034608387 10.1084/jem.191.11.1965 (Pubitemid 30390358)
28. Lipsker D., Ziylan U., Spehner D., Heat shock proteins 70 and 60 share common receptors which are expressed on human monocyte-derived but not epidermal dendritic cells. European Journal of Immunology 2002 32 322 332 (Pubitemid 34173323)
29. Berwin B., Rosser M. F. N., Brinker G., Nicchitta C. V., Transfer of GRP94(Gp96)-associated peptides onto endosomal MHC class I molecules. Traffic 2002 3 5 358 366 2-s2.0-0036237529 10.1034/j.1600-0854.2002.30505.x (Pubitemid 34461045)
30. Kurotaki T., Tamura Y., Ueda G., Oura J., Kutomi G., Hirohashi Y., Sahara H., Torigoe T., Hiratsuka H., Sunakawa H., Hirata K., Sato N., Efficient cross-presentation by heat shock protein 90-peptide complex-loaded dendritic cells via an endosomal pathway. Journal of Immunology 2007 179 3 1803 1813 2-s2.0-34548654412
31. Castellino F., Boucher P. E., Eichelberg K., Mayhew M., Rothman J. E., Houghton A. N., Germain R. N., Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. Journal of Experimental Medicine 2000 191 11 1957 1964 2-s2.0-0034608370 10.1084/jem.191.11.1957 (Pubitemid 30390357)
32. Ichiyanagi T., Imai T., Kajiwara C., Mizukami S., Nakai A., Nakayama T., Udono H., Essential role of endogenous heat shock protein 90 of dendritic cells in antigen cross-presentation. Journal of Immunology 2010 185 5 2693 2700 2-s2.0-78049374392 10.4049/jimmunol.1000821
33. Oura J., Tamura Y., Kamiguchi K., Kutomi G., Sahara H., Torigoe T., Himi T., Sato N., Extracellular heat shock protein 90 plays a role in translocating chaperoned antigen from endosome to proteasome for generating antigenic peptide to be cross-presented by dendritic cells. International Immunology 2011 23 4 223 237 2-s2.0-79953326945 10.1093/intimm/dxq475
34. + T cell effector function. Journal of Immunology 2004 172 10 6087 6092 2-s2.0-2442517310 (Pubitemid 38621211)
35. SenGupta D., Norris P. J., Suscovich T. J., Hassan-Zahraee M., Moffett H. F., Trocha A., Draenert R., Goulder P. J. R., Binder R. J., Levey D. L., Walker B. D., Srivastava P. K., Brander C., Heat shock protein-mediated cross-presentation of exogenous HIV antigen on HLA class I and class II. Journal of Immunology 2004 173 3 1987 1993 2-s2.0-3242811091 (Pubitemid 38971635)
36. + T cells. Journal of Immunology 2004 173 8 5130 5137 2-s2.0-6344276691 (Pubitemid 39387796)
37. Matsutake T., Sawamura T., Srivastava P. K., High efficiency CD91- and LOX-1-mediated re-presentation of gp96-chaperoned peptides by MHC II molecules. Cancer Immunity 2010 10 7 2-s2.0-78049357396
38. + T cells in vitro. Veterinary Research 2010 41 3 36 2-s2.0-77953145922 10.1051/vetres/ 2010008
39. Bendz H., Ruhland S. C., Pandya M. J., Hainzl O., Riegelsberger S., Bräuchle C., Mayer M. P., Buchner J., Issels R. D., Noessner E., Human heat shock protein 70 enhances tumor antigen presentation through complex formation and intracellular antigen delivery without innate immune signaling. Journal of Biological Chemistry 2007 282 43 31688 31702 2-s2.0-35748934798 10.1074/jbc.M704129200 (Pubitemid 350044903)
40. Huang Y., Biswas C., Klos Dehring D. A., The actin regulatory protein HS1 is required for antigen uptake and presentation by dendritic cells. The Journal of Immunology 2011 187 5952 5963
41. Zitzler S., Hellwig A., Hartl F. U., Wieland F., Diestelkötter- Bachert P., Distinct binding sites for the ATPase and substrate-binding domain of human Hsp70 on the cell surface of antigen presenting cells. Molecular Immunology 2008 45 15 3974 3983 2-s2.0-49449115065 10.1016/j.molimm.2008.06.022
42. Noessner E., Gastpar R., Milani V., Brandl A., Hutzler P. J. S., Kuppner M. C., Roos M., Kremmer E., Asea A., Calderwood S. K., Issels R. D., Tumor-derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. Journal of Immunology 2002 169 10 5424 5432 2-s2.0-0037111218 (Pubitemid 35291639)
43. + T cells by cytosolic mechanisms in dendritic cells versus vacuolar mechanisms in macrophages. Journal of Immunology 2004 172 9 5277 5286 2-s2.0-2142750909 (Pubitemid 38542025)
44. Binder R. J., Srivastava P. K., Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proceedings of the National Academy of Sciences of the United States of America 2004 101 16 6128 6133 2-s2.0-1942501656 10.1073/pnas.0308180101 (Pubitemid 38520539)
45. Robert J., Ramanayake T., Maniero G. D., Morales H., Chida A. S., Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. Journal of Immunology 2008 180 5 3176 3182 2-s2.0-49149084518
46. Tischer S., Basila M., Maecker-Kolhoff B., Heat shock protein 70/peptide complexes: potent mediators for the generation of antiviral T cells particularly with regard to low precursor frequencies. Journal of Translational Medicine 2011 9 175
47. + memory T cells. European Journal of Immunology 2010 40 4 986 997 2-s2.0-77951036167 10.1002/eji.200939738
48. Langelaar M. F. M., Hope J. C., Rutten V. P. M. G., Noordhuizen J. P. T. M., Van Eden W., Koets A. P., Mycobacterium avium ssp. paratuberculosis recombinant heat shock protein 70 interaction with different bovine antigen-presenting cells. Scandinavian Journal of Immunology 2005 61 3 242 250 2-s2.0-16244404934 10.1111/j.1365-3083.2005.01559.x (Pubitemid 40462774)
49. Berwin B., Hart J. P., Pizzo S. V., Nicchitta C. V., Cutting edge: CD91-independent cross-presentation of GRP94(gp96)-associated peptides. Journal of Immunology 2002 168 9 4282 4286 2-s2.0-0036569356 (Pubitemid 34441326)
50. Jockheck-Clark A. R., Bowers E. V., Totonchy M. B., Neubauer J., Pizzo S. V., Nicchitta C. V., Re-examination of CD91 function in GRP94 (glycoprotein 96) surface binding, uptake, and peptide cross-presentation. Journal of Immunology 2010 185 11 6819 6830 2-s2.0-78650667874 10.4049/jimmunol.1000448
51. Murshid A., Gong J., Calderwood S. K., Heat shock protein 90 mediates efficient antigen cross presentation through the scavenger receptor expressed by endothelial cells-I. Journal of Immunology 2010 185 5 2903 2917 2-s2.0-78049397567 10.4049/jimmunol.0903635
52. Walters J. J., Berwin B., Differential CD91 dependence for calreticulin and Pseudomonas exotoxin-A endocytosis. Traffic 2005 6 12 1173 1182 2-s2.0-27744555038 10.1111/j.1600-0854.2005.00351.x (Pubitemid 41632268)
53. Berwin B., Delneste Y., Lovingood R. V., Post S. R., Pizzo S. V., SREC-I, a type F scavenger receptor, is an endocytic receptor for calreticulin. Journal of Biological Chemistry 2004 279 49 51250 51257 2-s2.0-10944228434 10.1074/jbc.M406202200 (Pubitemid 40017869)
54. Delneste Y., Magistrelli G., Gauchat J. F., Haeuw J. F., Aubry J. P., Nakamura K., Kawakami-Honda N., Goetsch L., Sawamura T., Bonnefoy J. Y., Jeannin P., Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 2002 17 3 353 362 2-s2.0-18644364531 10.1016/S1074-7613(02)00388-6 (Pubitemid 35279555)
55. Berwin B., Hart J. P., Rice S., Gass C., Pizzo S. V., Post S. R., Nicchitta C. V., Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. The EMBO Journal 2003 22 22 6127 6136 2-s2.0-0345305789 10.1093/emboj/cdg572 (Pubitemid 37463255)
56. Tewalt E. F., Maynard J. C., Walters J. J., Schell A. M., Berwin B. L., Nicchitta C. V., Norbury C. C., Redundancy renders the glycoprotein 96 receptor scavenger receptor A dispensable for cross priming in vivo. Immunology 2008 125 4 480 491 2-s2.0-55449088718 10.1111/j.1365-2567.2008.02861.x
57. Facciponte J. G., Wang X. Y., Subjeck J. R., Hsp110 and Grp170, members of the Hsp70 superfamily, bind to scavenger receptor-A and scavenger receptor expressed by endothelial cell-I. European Journal of Immunology 2007 37 8 2268 2279 2-s2.0-34547882750 10.1002/eji.200737127 (Pubitemid 47250218)
58. Wassenberg J. J., Dezfulian C., Nicchitta C. V., Receptor mediated and fluid phase pathways for internalization of the ER Hsp90 chaperone GRP94 in murine macrophages. Journal of Cell Science 1999 112 13 2167 2175 2-s2.0-0032856673 (Pubitemid 29355431)
59. Li Z., Srivastava P. K., Tumor rejection antigen gp96/grp94 is an ATPase: implications for protein folding and antigen presentation. The EMBO Journal 1993 12 8 3143 3151 2-s2.0-0027208741 (Pubitemid 23232745)
60. Srivastava P. K., DeLeo A. B., Old L. J., Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proceedings of the National Academy of Sciences of the United States of America 1986 83 10 3407 3411 2-s2.0-0022534393 (Pubitemid 16043046)
61. Binder R. J., Kelly J. B., Vatner R. E., Srivastava P. K., Specific immunogenicity of heat shock protein gp96 derives from chaperoned antigenic peptides and not from contaminating proteins. Journal of Immunology 2007 179 11 7254 7261 2-s2.0-38849166048
62. Udono H., Srivastava P. K., Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. Journal of Immunology 1994 152 11 5398 5403 2-s2.0-0028301079 (Pubitemid 24152988)
63. + T cells in vivo. Proceedings of the National Academy of Sciences of the United States of America 1994 91 8 3077 3081 2-s2.0-0028261389 (Pubitemid 24130178)
64. Nair S., Wearsch P. A., Mitchell D. A., Wassenberg J. J., Gilboa E., Nicchitta C. V., Calreticulin displays in vivo peptide-binding activity and can elicit CTL responses against bound peptides. Journal of Immunology 1999 162 11 6426 6432 2-s2.0-0033152788 (Pubitemid 29309363)
65. Basu S., Srivastava P. K., Calreticulin, a peptide-binding chaperone of the endoplasmic reticulum, elicits tumor- and peptide-specific immunity. Journal of Experimental Medicine 1999 189 5 797 802 2-s2.0-0033103513 10.1084/jem.189.5.797 (Pubitemid 29189684)
66. Arnold D., Faath S., Rammensee H. G., Schild H., Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. Journal of Experimental Medicine 1995 182 3 885 889 2-s2.0-0029127770 10.1084/jem.182.3.885
67. Blachere N. E., Li Z., Chandawarkar R. Y., Suto R., Jaikaria N. S., Basu S., Udono H., Srivastava P. K., Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. Journal of Experimental Medicine 1997 186 8 1315 1322 2-s2.0-0030775140 10.1084/jem.186.8.1315 (Pubitemid 27469027)
68. Udono H., Yamano T., Kawabata Y., Ueda M., Yui K., Generation of cytotoxic T lymphocytes by MHC class I ligands fused to heat shock cognate protein 70. International Immunology 2001 13 10 1233 1242 2-s2.0-0034782206 (Pubitemid 32994523)
69. Navaratnam M., Deshpande M. S., Hariharan M. J., Zatechka D. S., Srikumaran S., Heat shock protein-peptide complexes elicit cytotoxic T-lymphocyte and antibody responses specific for bovine herpesvirus 1. Vaccine 2001 19 11-12 1425 1434 2-s2.0-0035825064 10.1016/S0264-410X(00)00381-9 (Pubitemid 32332727)
70. Jimbo J., Sato K., Hosoki T., Shindo M., Ikuta K., Torimoto Y., Kohgo Y., Induction of leukemia-specific antibodies by immunotherapy with leukemia-cell-derived heat shock protein 70. Cancer Science 2008 99 7 1427 1434 2-s2.0-44449140618 10.1111/j.1349-7006.2008.00829.x (Pubitemid 351761734)
71. Pawaria S., Binder R. J., CD91-dependent programming of T-helper cell responses following heat shock protein immunization. Nature Communications 2011 2 521 10.1038/ncomms1524
72. Gong X., Gai W., Xu J., Zhou W., Tien P., Glycoprotein 96-mediated presentation of human immunodeficiency virus type 1 (HIV-1)-specific human leukocyte antigen class I-restricted peptide and humoral immune responses to HIV-1 p24. Clinical and Vaccine Immunology 2009 16 11 1595 1600 2-s2.0-70350738619 10.1128/CVI.00160-09
73. Srivastava P., Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annual Review of Immunology 2002 20 395 425 2-s2.0-0036214288 10.1146/annurev.immunol.20.100301.064801 (Pubitemid 34293430)
74. Basu S., Binder R. J., Suto R., Anderson K. M., Srivastava P. K., Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF- B pathway. International Immunology 2000 12 11 1539 1546 2-s2.0-0033747044
75. Skeen M. J., Miller M. A., Shinnick T. M., Kirk Ziegler H., Regulation of murine macrophage IL-12 production: activation of macrophages in vivo, restimulation in vitro, and modulation by other cytokines. Journal of Immunology 1996 156 3 1196 1206 2-s2.0-0030051658 (Pubitemid 26048117)
76. Chen W., Syldath U., Bellmann K., Burkart V., Kolb H., Human 60-kDa heat-shock protein: a danger signal to the innate immune system. Journal of Immunology 1999 162 6 3212 3219 2-s2.0-0033559496 (Pubitemid 29313567)
77. Kol A., Bourcier T., Lichtman A. H., Libby P., Chlamydial and human heat shock protein 60s activate human vascular endothelium, smooth muscle cells, and macrophages. Journal of Clinical Investigation 1999 103 4 571 577 2-s2.0-0033557202 (Pubitemid 29094058)
78. Asea A., Kraeft S. K., Kurt-Jones E. A., Stevenson M. A., Chen L. B., Finberg R. W., Koo G. C., Calderwood S. K., HSP70 stimulates cytokine production through a CD 14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nature Medicine 2000 6 4 435 442 2-s2.0-0034113617 10.1038/74697 (Pubitemid 30208161)
79. Singh-Jasuja H., Scherer H. U., Hilf N., Arnold-Schild D., Rammensee H. G., Toes R. E. M., Schild H., The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. European Journal of Immunology 2000 30 2211 2215 (Pubitemid 30655760)
80. Ohashi K., Burkart V., Flohé S., Kolb H., Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. Journal of Immunology 2000 164 2 558 561 2-s2.0-0034650427 (Pubitemid 30043672)
81. + cells in vivo. Journal of Immunology 2000 165 11 6029 6035 2-s2.0-0034541171
82. Asea A., Kabingu E., Stevenson M. A., Calderwood S. K., HSP70 peptide-bearing and peptide-negative preparations act as chaperokines. Cell Stress Chaperones 2000 5 425 431 (Pubitemid 32057493)
83. Moroi Y., Mayhew M., Trcka J., Hoe M. H., Takechi Y., Hartl F. U., Rothman J. E., Houghton A. N., Induction of cellular immunity by immunization with novel hybrid peptides complexed to heat shock protein 70. Proceedings of the National Academy of Sciences of the United States of America 2000 97 7 3485 3490 2-s2.0-0034724336 10.1073/pnas.070550797 (Pubitemid 30183329)
84. Kuppner M. C., Gastpar R., Gelwer S., Nossner E., Ochmann O., Scharner A., Issels R. D., The role of heat shock protein (hsp70) in dendritic cell maturation: Hsp70 induces the maturation of immature dendritic cells but reduces DC differentiation from monocyte precursors. European Journal of Immunology 2001 31 1602 1609 (Pubitemid 32454709)
85. Wang Y., Kelly C. G., Karttunen J. T., Whittall T., Lehner P. J., Duncan L., MacAry P., Younson J. S., Singh M., Oehlmann W., Cheng G., Bergmeier L., Lehner T., Cd40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 2001 15 6 971 983 2-s2.0-18244367700 10.1016/S1074-7613(01)00242-4 (Pubitemid 34075377)
86. Somersan S., Larsson M., Fonteneau J. F., Basu S., Srivastava P., Bhardwaj N., Primary tumor tissue lysates are enriched in heat shock proteins and induce the maturation of human dendritic cells. Journal of Immunology 2001 167 9 4844 4852 2-s2.0-0035500779 (Pubitemid 33009712)
87. Vabulas R. M., Ahmad-Nejad P., Ghose S., Kirschning C. J., Issels R. D., Wagner H., HSP70 as endogenous stimulus of the toll/interleukin-1 receptor signal pathway. Journal of Biological Chemistry 2002 277 17 15107 15112 2-s2.0-0037177833 10.1074/jbc.M111204200 (Pubitemid 34952589)
88. Vabulas R. M., Braedel S., Hilf N., Singh-Jasuja H., Herter S., Ahmad-Nejad P., Kirschning C. J., Rammensee C. D. C. H. G., Wagner H., Schild H., The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the toll-like receptor 2/4 pathway. Journal of Biological Chemistry 2002 277 23 20847 20853 2-s2.0-0037036369 10.1074/jbc.M200425200 (Pubitemid 34967392)
89. Panjwani N. N., Popova L., Srivastava P. K., Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. Journal of Immunology 2002 168 6 2997 3003 2-s2.0-0037087398 (Pubitemid 34211681)
90. Wang Y., Kelly C. G., Singh M., McGowan E. G., Carrara A. S., Bergmeier L. A., Lehner T., Stimulation of Th1-polarizing cytokines, C-C chemokines, maturation of dendritic cells, and adjuvant function by the peptide binding fragment of heat shock protein 70. Journal of Immunology 2002 169 5 2422 2429 2-s2.0-0036721692 (Pubitemid 34920985)
91. Flohé S. B., Brüggemann J., Lendemans S., Nikulina M., Meierhoff G., Flohé S., Kolb H., Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype. Journal of Immunology 2003 170 5 2340 2348 2-s2.0-0345074067 (Pubitemid 36245620)
92. Millar D. G., Garza K. M., Odermatt B., Elford A. R., Ono N., Li Z., Ohashi P. S., Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nature Medicine 2003 9 12 1469 1476 2-s2.0-0347122087 10.1038/nm962 (Pubitemid 38004773)
93. Campisi J., Leem T. H., Fleshner M., Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 2003 8 272 286 (Pubitemid 37484722)
94. Wan T., Zhou X., Chen G., An H., Chen T., Zhang W., Liu S., Jiang Y., Yang F., Wu Y., Cao X., Novel heat shock protein Hsp70L1 activates dendritic cells and acts as a Th1 polarizing adjuvant. Blood 2004 103 5 1747 1754 2-s2.0-10744220813 10.1182/blood-2003-08-2828 (Pubitemid 38268968)
95. Cohen-Sfady M., Nussbaum G., Pevsner-Fischer M., Mor F., Carmi P., Zanin-Zhorov A., Lider O., Cohen I. R., Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. Journal of Immunology 2005 175 6 3594 3602 2-s2.0-24744442576 (Pubitemid 41292018)
96. Roelofs M. F., Boelens W. C., Joosten L. A. B., Abdollahi-Roodsaz S., Geurts J., Wunderink L. U., Schreurs B. W., Van Den Berg W. B., Radstake T. R. D. J., Identification of small heat shock protein B8 (HSP22) as a novel TLR4 ligand and potential involvement in the pathogenesis of rheumatoid arthritis. Journal of Immunology 2006 176 11 7021 7027 2-s2.0-33646882893 (Pubitemid 43787883)
97. Chen T., Guo J., Han C., Yang M., Cao X., 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. Journal of Immunology 2009 182 3 1449 1459 2-s2.0-63149158731
98. Huang Q. Q., Sobkoviak R., Jockheck-Clark A. R., Shi B., Mandelin A. M., Tak P. P., Haines G. K., Nicchitta C. V., Pope R. M., Heat shock protein 96 is elevated in rheumatoid arthritis and activates macrophages primarily via TLR2 signaling. Journal of Immunology 2009 182 8 4965 4973 2-s2.0-65249190995 10.4049/jimmunol.0801563
99. Martin C. A., Carsons S. E., Kowalewski R., Bernstein D., Valentino M., Santiago-Schwarz F., Aberrant extracellular and dendritic Cell (DC) surface expression of heat shock protein (hsp)70 in the rheumatoid joint: possible mechanisms of hsp/DC-mediated cross-priming. Journal of Immunology 2003 171 11 5736 5742 2-s2.0-0344585492 (Pubitemid 37467188)
100. Sedlackova L., Nguyen T. T. H., Zlacka D., Sosna A., Hromadnikova I., Cell surface and relative mRNA expression of heat shock protein 70 in human synovial cells. Autoimmunity 2009 42 1 17 24 2-s2.0-58149520329 10.1080/08916930802227466
101. Auger I., Escola J. M., Gorvel J. P., Roudier J., HLA-DR4 and HLA-DR10 motifs that carry susceptibility to rheumatoid arthritis bind 70-kD heat shock proteins. Nature Medicine 1996 2 3 306 310 2-s2.0-0029879122 10.1038/nm0396-306 (Pubitemid 26082011)
102. Chandawarkar R. Y., Wagh M. S., Srivastava P. K., The dual nature of specific immunological activity of tumor-derived gp96 preparations. Journal of Experimental Medicine 1999 189 9 1437 1442 2-s2.0-0345299172 10.1084/jem.189.9.1437 (Pubitemid 29227529)
103. Chandawarkar R. Y., Wagh M. S., Kovalchin J. T., Srivastava P., Immune modulation with high-dose heat-schock protein gp96: therapy of murine autoimmune diabetes and encephalomyelitis. International Immunology 2004 16 4 615 624 2-s2.0-1842854683 10.1093/intimm/dxh063 (Pubitemid 38489436)
104. Kovalchin J. T., Mendonca C., Wagh M. S., Wang R., Chandawarkar R. Y., In vivo treatment of mice with heat shock protein, gp96, improves survival of skin grafts with minor and major antigenic disparity. Transplant Immunology 2006 15 3 179 185 2-s2.0-31144460794 10.1016/j.trim.2005.07.003 (Pubitemid 43129384)
105. Liu Z., Li X., Qiu L., Zhang X., Chen L., Cao S., Wang F., Meng S., Treg suppress CTL responses upon immunization with HSP gp96. European Journal of Immunology 2009 39 11 3110 3120 2-s2.0-70449334144 10.1002/eji.200939593
106. Yan X., Zhang X., Wang Y., Li X., Wang S., Zhao B., Li Y., Ju Y., Chen L., Liu W., Meng S., Regulatory T-cell depletion synergizes with gp96-mediated cellular responses and antitumor activity. Cancer Immunology, Immunotherapy 2011 60 12 1763 1774 2-s2.0-79960558750 10.1007/s00262-011-1076-5