Administration of the stress protein gp96 prolongs rat cardiac allograft survival, modifies rejection-associated inflammatory events, and induces a state of peripheral T-cell hyporesponsiveness

Cell Stress and Chaperones

Volumn 12, Issue 1, 2007, Pages 71-82

  Slack, Laura K ^a   Muthana, Munitta ^a   Hopkinson, Kay ^a   Suvarna, S Kim ^b   Espigares, Elena ^c   Mirza, Shabana ^a   Fairburn, Barbara ^a   Pockley, A Graham ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b NORTHERN GENERAL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; INTERLEUKIN 10; INTERLEUKIN 4; PHOSPHATE BUFFERED SALINE; CYTOKINE; ENDOPLASMIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CARDIAC GRAFT REJECTION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; GRAFT SURVIVAL; HEART TRANSPLANTATION; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; INFLAMMATION; NONHUMAN; PALPATION; PRIORITY JOURNAL; RAT; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; ALLOTRANSPLANTATION; ANIMAL; CYTOLOGY; DRUG EFFECT; GRAFT REJECTION; HEART MUSCLE; IMMUNOLOGY; LEUKOCYTE; METHODOLOGY; ORGAN SIZE; PATHOLOGY; RAT STRAIN; SECRETION; SPLEEN; T LYMPHOCYTE;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

ANIMALS; ANTIGENS, CD3; CYTOKINES; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; INFLAMMATION; LEUKOCYTES; MEMBRANE GLYCOPROTEINS; MYOCARDIUM; ORGAN SIZE; RATS; RATS, INBRED STRAINS; SPLEEN; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 34250826696     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1379/CSC-237R.1     Document Type: Article

References (63)

1. Arnold-Schild D, Hanau D, Spehner D, Schmid C, Rammensee HG, de la Salle H, Schild H. 1999. Receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J Immunol 162: 3757-3760.
2. Banerjee PP, Vinay DS, Mathew A, et al. 2002. Evidence that glycoprotein 96 (B2), a stress protein, functions as a Th2-specific costimulatory molecule. J Immunol 169: 3507-3518.
3. Basu S, Srivastava P. 1999. Calreticulin, a peptide-binding chaperone of the endoplasmic reticulum, elicits tumor- and peptide-specific immunity. J Exp Med 189: 797-802.
4. Berwin B, Hart JP, Pizzo SV, Nicchitta CV. 2002. CD91-independent cross-presentation of grp94(gp96)-associated peptides. J Immunol 168: 4282-4286.
5. Binder RJ, Han DK, Srivastava PK. 2000. CD91: a receptor for heat shock protein gp96. Nat Immunol 1: 151-155.
6. Binder RJ, Srivastava PK. 2004. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci U S A 101: 6128-6133.
7. + T cells. Nat Immunol 6: 593-599.
8. Binder RJ, Vatner R, Srivastava P. 2004. The heat-shock protein receptors: some answers and more questions. Tissue Antigens 64:442-451.
9. Brenan M, Puklavec M. 1992. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 175: 1457-1465.
10. Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J. 2003. Regulatory T cells selectively express Toll-like receptors and are activated by lipopolysaccharide. J Exp Med 197: 403-411.
11. Castellino F, Boucher PE, Eichelberg K, Mayhew M, Rothman JE, Houghton AN, Germain RN. 2000. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct pathways. J Exp Med 191: 1957-1964.
12. Chai JG, Bartok I, Chandler P, Vendetti S, Antoniou A, Dyson J, Lechler R. 1999. Anergic T cells act as suppressor cells in vitro and in vivo. Eur J Immunol 29: 686-692.
13. Chandawarkar RY, Wagh MS, Kovalchin JT, Srivastava P. 2004. Immune modulation with high-dose heat-shock protein gp96: therapy of murine autoimmune diabetes and encephalomyelitis. Int Immunol 16: 615-624.
14. Chandawarkar RY, Wagh MS, Srivastava PK. 1999. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J Exp Med 189: 1437-1442.
15. Ciubotariu R, Liu Z, Colovai AI, et al. 1998. Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts. J Clin Investig 101: 398-405.
16. Cohen-Sfady M, Nussbaum G, Pevsner-Fischer M, Mor F, Carmi P, Zanin-Zhorov A, Lider O, Cohen IR. 2005. Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J Immunol 175: 3594-3602.
17. Dijkstra CD, Dopp EA, Joling P, Kraal G. 1985. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54: 589-599.
18. + T cell effector function. J Immunol 172:6087-6092.
19. Fairburn B, Muthana M, Hopkinson K, et al. 2006. Analysis of purified gp96 preparations from rat and mouse livers using 2-D gel electrophoresis and tandem mass spectrometry. Biochimie 88: 1165-1174.
20. + T cells. Curr Opin Immunol 15: 690-696.
21. Gething MJ, Sambrook J. 1992. Protein folding in the cell. Nature 355:33-45.
22. Hornick PI, Mason PD, Baker RJ, et al. 2000. Significant frequencies of T cells with indirect anti-donor specificity in heart graft recipients with chronic rejection. Circulation 101: 2405-2410.
23. Hornick PI, Mason D, Yacoub MH, Rose ML, Batchelor R, Lechler RI. 1998. Assessment of the contribution that direct allorecognition makes to the progression of chronic cardiac transplant rejection in humans. Circulation 97: 1257-1263.
24. - and Type I IFN-producing cells that exhibit selective expression of Toll-like receptors 7 and 9 and strong responsiveness to CpG. J Immunol 172: 7485-7494.
25. + naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 162: 5317-5326.
26. + Th1 cells pro-inflammatory or anti-inflammatory? The ratio of IL-10 to IFN-γ or IL-2 determines their function. Int Immunol 7: 1287-1294.
27. Klein L, Khazaie K, von Boehmer H. 2003. In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc Natl Acad Sci U S A 100: 8886-8891.
28. Koizumi H, Konoeda Y, Kobayashi S, Koizumi H, Tamaki T, Tanioka Y. 1996. Comparison of methods to evaluate acute rejection in heterotopic heart transplantation in rats. Exp Anim 45: 217-225.
29. Kovalchin JT, Mendonca C, Wagh MS, Wang R, Chandawarkar RY. 2006a. In vivo treatment of mice with heat shock protein, gp96, improves survival of skin grafts with minor and major antigenic disparity. Transplant Immunol 15: 179-185.
30. Kovalchin JT, Wang R, Wagh MS, Azoulay J, Sanders M, Chandawarkar RY. 2006b. In vivo delivery of heat shock protein 70 accelerates wound healing by upregulating macrophage-mediated phagocytosis. Wound Repair Regen 14: 129-137.
31. Krasinskas AM, Eiref SD, McLean AD, Kreisel D, Gelman AE, Popma SH, Moore JS, Rosengard BR. 2000. Replacement of graft-resident donor-type antigen presenting cells alters the tempo and pathogenesis of murine cardiac allograft rejection. Transplantation 70: 514-521.
32. + regulatory T cells: evidence for in vivo inhibition of effector cell proliferation. J Immunol 172: 6539-6544.
33. Lee RS, Yamada K, Houser SL, Womer KL, Maloney ME, Rose HS, Sayegh MH, Madsen JC. 2001. Indirect antigen recognition of allopeptides promotes the development of cardiac allograft vasculopathy. Proc Natl Acad Sci U S A 98: 3276-3281.
34. Lombardi G, Sidhu S, Batchelor R, Lechler R. 1994. Anergic T cells as suppressor cells in vitro. Science 264: 1587-1589.
35. + T cells. Cell Stress Chaperones 11: 364-378.
36. Muthana M, Fairburn B, Mirza S, Slack LK, Pockley AG. 2004. Systematic evaluation of the conditions required for the generation of immature rat bone marrow-derived dendritic cells and their phenotypic and functional characterization. J Immunol Methods 294: 165-179.
37. Nair S, Wearsch PA, Mitchell DA, Wassenberg JJ, Gilboa E, Nicchitta CV. 1999. Calreticulin displays in vivo peptide-binding activity and can elicit CTL responses against bound peptides. J Immunol 162: 6426-6432.
38. Norbury CC. 2006. Drinking a lot is good for dendritic cells. Immunology 117: 443-451.
39. Ogita K, Hopkinson K, Nakao M, Wood RFM, Pockley AG. 2000. Stress responses in graft and native intestine after rat heterotopic small bowel transplantation. Transplantation 69: 2273-2277.
40. Ohashi K, Burkart V, Flohé S, Kolb H. 2000. Heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J Immunol 164: 558-561.
41. Pêche H, Heslan M, Usal C, Amigorena S, Cuturi MC. 2003. Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection. Transplantation 76: 1503-1510.
42. Reid SD, Uff CR, Saeed I, Ross J, Wood RFM, Pockley AG. 1995. Differential adhesion molecule expression in rat small bowel allograft rejection. Transplantation 60: 989-992.
43. SenGupta D, Norris PJ, Suscovich TJ, et al. 2004. Heat shock protein-mediated cross-presentation of exogenous HIV antigen on HLA class I and class II. J Immunol 173: 1987-1993.
44. + suppressor T cells: more questions than answers. Nat Rev Immunol 2: 389-400.
45. Singh-Jasuja H, Toes REM, Spee P, et al. 2000. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex molecules requires receptor-mediated endocytosis. J Exp Med 191: 1965-1974.
46. Srivastava PK. 1997. Purification of heat shock protein-peptide complexes for use in vaccination against cancers and intracellular pathogens. Methods 12: 165-171.
47. Stewart S, Winters GL, Fishbein MC, et al. 2005. Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J Heart Lung Transplant 24: 1710-1720.
48. + naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/ suppressive state. Int Immunol 10: 1969-1980.
49. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188: 287-296.
50. Trinité B, Voisine C, Yagita H, Josien R. 2000. A subset of cytolytic dendritic cells in rat. J Immunol 165: 4202-4208.
51. Udono H, Srivastava PK. 1994. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90 and hsp70. J Immunol 152: 5398-5403.
52. Uff CR, Reid SD, Wood RFM, Pockley AG. 1995. CD44 expression in rejecting rat small bowel allografts. Transplantation 60: 985-989.
53. Vabulas RM, Ahmad-Nejad P, da Costa C, Miethke T, Kirschning CJ, Hacker H, Wagner H. 2001. Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 276: 31332-31339.
54. Vabulas RM, Braedel S, Hilf N, et al. 2002a. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 277: 20847-20853.
55. Vabulas RM, Wagner H, Schild H. 2002b. Heat shock proteins as ligands of Toll-like receptors. Curr Top Microbiol Immunol 270: 169-184.
56. van Denderen B, Peche H, Gagne K, Usal C, Cuturi M, Soulillou J. 2001. Identification of immunodominant donor MHC peptides following rejection and donor strain transfusion-induced tolerance of heart allografts in adult rats. Eur J Immunol 31: 1333-1339.
57. Vendetti S, Chai JG, Dyson J, Simpson E, Lombardi G, Lechler R. 2000. Anergic T cells inhibit the antigen-presenting function of dendritic cells. J Immunol 165: 1175-1181.
58. Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y. 2004. Regulatory T cells and organ transplantation. Semin Immunol 16: 119-126.
59. Wood KJ, Sakaguchi S. 2003. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 3: 199-210.
60. Xiu D, Uchida H, To H, Sugimoto K, Kasahara K, Nagai H, Fujimura A, Kobayashi E. 2001. Simplified method of heterotopic rat heart transplantation using the cuff technique: application to sublethal dose protocol of methotrexate on allograft survival. Microsurgery 21: 16-21.
61. Young D, Romain E, Moreno C, O'Brien R, Born W. 1993. Molecular chaperones and the immune system response. Philos Trans R Soc Lond 339: 363-367.
62. + regulatory T cell function via innate TLR2 signaling J Clin Invest 116: 2022-2032.
63. Zanin-Zhorov A, Nussbaum G, Franitza S, Cohen IR, Lider O. 2003. T cells respond to heat shock protein 60 via TLR2: activation of adhesion and inhibition of chemokine receptors. FASEB J 17: 1567-1569.