Heat-shock proteins in stromal joint tissues: Innocent bystanders or disease-initiating proteins?

Rheumatology (United Kingdom)

Volumn 53, Issue 2, 2014, Pages 223-232

  Lambrecht, Stijn ^a   Juchtmans, Nele ^a   Elewaut, Dirk ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Arthritis; Connective; Osteoarthritis; Stress response; Tissue inflammation

Indexed keywords

CHAPERONIN 60; EARLY PREGNANCY FACTOR; GLUCOSE REGULATED PROTEIN 78; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 22; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 47; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; SMALL HEAT SHOCK PROTEIN;

ARTHROPATHY; CONNECTIVE TISSUE; HUMAN; JOINT; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STROMAL JOINT TISSUE;

ARTHRITIS; CONNECTIVE; OSTEOARTHRITIS; STRESS RESPONSE; TISSUE INFLAMMATION;

CONNECTIVE TISSUE; HEAT-SHOCK PROTEINS; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; JOINT DISEASES; MOLECULAR CHAPERONES;

EID: 84892543889     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/ket277     Document Type: Review

References (107)

1. Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell 2010;40: 253-66.
2. Ellis RJ, van der Vies SM, Hemmingsen SM. The molecular chaperone concept. Biochem Soc Symp 1989;55:145-53.
3. Stetler RA, Gan Y, Zhang W et al. Heat shock proteins: cellular and molecular mechanisms in the central nervous system. Prog Neurobiol 2010;92:184-211.
4. Kampinga HH, Hageman J, Vos MJ et al. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009;14:105-11.
5. van Eden W, Thole JE, van der Zee R et al. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 1988;331:171-3.
6. Zlacka D, Vavrincova P, Hien Nguyen TT et al. Frequency of anti-hsp60, -65 and -70 antibodies in sera of patients with juvenile idiopathic arthritis. J Autoimmun 2006;27: 81-8.
7. Bodman-Smith MD, Corrigall VM, Berglin E et al. Antibody response to the human stress protein BiP in rheumatoid arthritis. Rheumatology 2004;43:1283-7.
8. Erlandsson Harris H, Liljestrom M, Klareskog L. Characteristics of synovial fluid effusion in collageninduced arthritis (CIA) in the DA rat: a comparison of histology and antibody reactivities in an experimental chronic arthritis model and rheumatoid arthritis (RA). Clin Exp Immunol 1997;107:480-4.
9. Billingham ME, Carney S, Butler R et al. A mycobacterial 65-kD heat shock protein induces antigen-specific suppression of adjuvant arthritis, but is not itself arthritogenic. J Exp Med 1990;171:339-44.
10. Shields AM, Panayi GS, Corrigall VM. A new-age for biologic therapies: long-term drug-free therapy with BiP? Front Immunol 2012;3:17.
11. Van Eden W, Wick G, Albani S et al. Stress, heat shock proteins, and autoimmunity: how immune responses to heat shock proteins are to be used for the control of chronic inflammatory diseases. Ann N Y Acad Sci 2007; 1113:217-37.
12. Shields AM, Thompson SJ, Panayi GS et al. Pro-resolution immunological networks: binding immunoglobulin protein and other resolution-associated molecular patterns. Rheumatology 2012;51:780-8.
13. Chen B, Piel WH, Gui L et al. The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 2005;86:627-37.
14. Rao DV, Watson K, Jones GL. Age-related attenuation in the expression of the major heat shock proteins in human peripheral lymphocytes. Mech Ageing Dev 1999;107: 105-18.
15. Richter K, Buchner J. Hsp90: chaperoning signal transduction. J Cell Physiol 2001;188:281-90.
16. Basso AD, Solit DB, Chiosis G et al. Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 2002;277:39858-66.
17. Yoshida M, Xia Y. Heat shock protein 90 as an endogenous protein enhancer of inducible nitric-oxide synthase. J Biol Chem 2003;278:36953-8.
18. Hashiramoto A, Murata M, Kawazoe T et al. Heat shock protein 90 maintains the tumour-like character of rheumatoid synovial cells by stabilizing integrin-linked kinase, extracellular signal-regulated kinase and protein kinase B. Rheumatology 2011;50: 852-61.
19. Boehm AK, Seth M, Mayr KG et al. Hsp90 mediates insulin-like growth factor 1 and interleukin-1beta signaling in an age-dependent manner in equine articular chondrocytes. Arthritis Rheum 2007;56:2335-43.
20. Fan Z, Tardif G, Hum D et al. Hsp90{beta} and p130(cas): novel regulatory factors of MMP-13 expression in human osteoarthritic chondrocytes. Ann Rheum Dis 2009;68: 976-82.
21. Gorska M, Popowska U, Sielicka-Dudzin A et al. Geldanamycin and its derivatives as Hsp90 inhibitors. Front Biosci 2012;17:2269-77.
22. Kimura H, Yukitake H, Tajima Y et al. ITZ-1, a client-selective Hsp90 inhibitor, efficiently induces heat shock factor 1 activation. Chem Biol 2010;17:18-27.
23. Terauchi R, Takahashi KA, Arai Y et al. Hsp70 prevents nitric oxide-induced apoptosis in articular chondrocytes. Arthritis Rheum 2003;48:1562-8.
24. Rice JW, Veal JM, Fadden RP et al. Small molecule inhibitors of Hsp90 potently affect inflammatory disease pathways and exhibit activity in models of rheumatoid arthritis. Arthritis Rheum 2008;58:3765-75.
25. Yano A, Tsutsumi S, Soga S et al. Inhibition of Hsp90 activates osteoclast c-Src signaling and promotes growth of prostate carcinoma cells in bone. Proc Natl Acad Sci USA 2008;105:15541-6.
26. Price JT, Quinn JM, Sims NA et al. The heat shock protein 90 inhibitor, 17-allylamino-17-demethoxygeldanamycin, enhances osteoclast formation and potentiates bone metastasis of a human breast cancer cell line. Cancer Res 2005;65:4929-38.
27. Richardson PG, Chanan-Khan AA, Alsina M et al. Tanespimycin monotherapy in relapsed multiple myeloma: results of a phase 1 dose-escalation study. Br J Haematol 2010;150:438-45.
28. Huang QQ, Sobkoviak R, Jockheck-Clark AR et al. Heat shock protein 96 is elevated in rheumatoid arthritis and activates macrophages primarily via TLR2 signaling. J Immunol 2009;182:4965-73.
29. Huang QQ, Koessler RE, Birkett R et al. Gp96 perpetuates the persistent inflammation of rheumatoid arthritis. Arthritis Rheum 2012;64:3638-48.
30. Liu B, Dai J, Zheng H et al. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc Natl Acad Sci USA 2003;100:15824-9.
31. Baker-LePain JC, Sarzotti M, Nicchitta CV. Glucoseregulated protein 94/glycoprotein 96 elicits bystander activation of CD4+ T cell Th1 cytokine production in vivo. J Immunol 2004;172:4195-203.
32. Kampinga HH, Craig EA. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 2010;11:579-92.
33. Borges TJ, Wieten L, van Herwijnen MJ et al. The antiinflammatory mechanisms of Hsp70. Front Immunol 2012; 3:95.
34. Schett G, Redlich K, Xu Q et al. Enhanced expression of heat shock protein 70 (hsp70) and heat shock factor 1 (HSF1) activation in rheumatoid arthritis synovial tissue. Differential regulation of hsp70 expression and HSF1 activation in synovial fibroblasts by proinflammatory cytokines, shear stress, and antiinflammatory drugs. J Clin Invest 1998;102:302-11.
35. Kang EH, Kim DJ, Lee EY et al. Downregulation of heat shock protein 70 protects rheumatoid arthritis fibroblastlike synoviocytes from nitric oxide-induced apoptosis. Arthritis Res Ther 2009;11:R130.
36. Martin CA, Carsons SE, Kowalewski R et al. 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. J Immunol 2003;171:5736-42.
37. Auger I, Escola JM, Gorvel JP et al. HLA-DR4 and HLADR10 motifs that carry susceptibility to rheumatoid arthritis bind 70-kD heat shock proteins. Nat Med 1996;2: 306-10.
38. Asea A, Kraeft SK, Kurt-Jones EA et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000;6:435-42.
39. Wallin RP, Lundqvist A, More SH et al. Heat-shock proteins as activators of the innate immune system. Trends Immunol 2002;23:130-5.
40. Bausinger H, Lipsker D, Ziylan U et al. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur J Immunol 2002;32:3708-13.
41. Detanico T, Rodrigues L, Sabritto AC et al. Mycobacterial heat shock protein 70 induces interleukin-10 production: immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol 2004;135: 336-42.
42. Luo X, Zuo X, Zhou Y et al. Extracellular heat shock protein 70 inhibits tumour necrosis factor-alpha induced proinflammatory mediator production in fibroblast-like synoviocytes. Arthritis Res Ther 2008;10:R41.
43. Luo X, Zuo X, Mo X et al. Treatment with recombinant Hsp72 suppresses collagen-induced arthritis in mice. Inflammation 2011;34:432-9.
44. Delpino A, Castelli M. The 78 kDa glucose-regulated protein (GRP78/BIP) is expressed on the cell membrane, is released into cell culture medium and is also present in human peripheral circulation. Biosci Rep 2002;22:407-20.
45. Blass S, Union A, Raymackers J et al. The stress protein BiP is overexpressed and is a major B and T cell target in rheumatoid arthritis. Arthritis Rheum 2001;44:761-71.
46. Yoo SA, You S, Yoon HJ et al. A novel pathogenic role of the ER chaperone GRP78/BiP in rheumatoid arthritis. J Exp Med 2012;209:871-86.
47. Sato M, Shin-ya K, Lee JI et al. Human telomerase reverse transcriptase and glucose-regulated protein 78 increase the life span of articular chondrocytes and their repair potential. BMC Musculoskelet Disord 2012;13:51.
48. Ravindran S, Gao Q, Ramachandran A et al. Stress chaperone GRP-78 functions in mineralized matrix formation. J Biol Chem 2011;286:8729-39.
49. Albani S, Keystone EC, Nelson JL et al. Positive selection in autoimmunity: abnormal immune responses to a bacterial dnaJ antigenic determinant in patients with early rheumatoid arthritis. Nat Med 1995;1:448-52.
50. Prakken BJ, Samodal R, Le TD et al. Epitope-specific immunotherapy induces immune deviation of proinflammatory T cells in rheumatoid arthritis. Proc Natl Acad Sci USA 2004;101:4228-33.
51. Massa M, Passalia M, Manzoni SM et al. Differential recognition of heat-shock protein dnaJ-derived epitopes by effector and Treg cells leads to modulation of inflammation in juvenile idiopathic arthritis. Arthritis Rheum 2007;56: 1648-57.
52. Koffeman EC, Genovese M, Amox D et al. Epitope-specific immunotherapy of rheumatoid arthritis: clinical responsiveness occurs with immune deviation and relies on the expression of a cluster of molecules associated with T cell tolerance in a double-blind, placebo-controlled, pilot phase II trial. Arthritis Rheum 2009;60:3207-16.
53. Kurzik-Dumke U, Schick C, Rzepka R et al. Overexpression of human homologs of the bacterial DnaJ chaperone in the synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum 1999;42:210-20.
54. Sironen RK, Karjalainen HM, Elo MA et al. cDNA array reveals mechanosensitive genes in chondrocytic cells under hydrostatic pressure. Biochim Biophys Acta 2002; 1591:45-54.
55. Vercoulen Y, van Teijlingen NH, de Kleer IM et al. Heat shock protein 60 reactive T cells in juvenile idiopathic arthritis: what is new? Arthritis Res Ther 2009;11:231.
56. Anderton SM, van der Zee R, Prakken B et al. Activation of T cells recognizing self 60-kD heat shock protein can protect against experimental arthritis. J Exp Med 1995; 181:943-52.
57. Wang FS, Wu RW, Ko JY et al. Heat shock protein 60 protects skeletal tissue against glucocorticoid-induced bone mass loss by regulating osteoblast survival. Bone 2011;49:1080-9.
58. Kim YS, Koh JM, Lee YS et al. Increased circulating heat shock protein 60 induced by menopause, stimulates apoptosis of osteoblast-lineage cells via up-regulation of Toll-like receptors. Bone 2009;45:68-76.
59. Marker T, Sell H, Zillessen P et al. Heat shock protein 60 as a mediator of adipose tissue inflammation and insulin resistance. Diabetes 2012;61:615-25.
60. Boog CJ, de Graeff-Meeder ER, Lucassen MA et al. Two monoclonal antibodies generated against human hsp60 show reactivity with synovial membranes of patients with juvenile chronic arthritis. J Exp Med 1992;175: 1805-10.
61. van den IP, Norman DG, Quinlan RA. Molecular chaperones: small heat shock proteins in the limelight. Curr Biol 1999;9:R103-5.
62. Kriehuber T, Rattei T, Weinmaier T et al. Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 2010;24:3633-42.
63. Mymrikov EV, Seit-Nebi AS, Gusev NB. Large potentials of small heat shock proteins. Physiol Rev 2011;91:1123-59.
64. Haslbeck M, Franzmann T, Weinfurtner D et al. Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 2005;12:842-6.
65. Kato K, Adachi S, Matsushima-Nishiwaki R et al. Regulation by heat shock protein 27 of osteocalcin synthesis in osteoblasts. Endocrinology 2011;152:1872-82.
66. Evgrafov OV, Mersiyanova I, Irobi J et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet 2004;36:602-6.
67. Irobi J, Van Impe K, Seeman P et al. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 2004;36:597-601.
68. Vicart P, Caron A, Guicheney P et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desminrelated myopathy. Nat Genet 1998;20:92-5.
69. Berry V, Francis P, Reddy MA et al. Alpha-B crystallin gene (CRYAB) mutation causes dominant congenital posterior polar cataract in humans. Am J Hum Genet 2001;69:1141-5.
70. Sedlackova L, Sosna A, Vavrincova P et al. Heat shock protein gene expression profile may differentiate between rheumatoid arthritis, osteoarthritis and healthy controls. Scand J Rheumatol 2011;40:354-7.
71. Lambrecht S, Dhaenens M, Almqvist F et al. Proteome characterization of human articular chondrocytes leads to novel insights in the function of small heat-shock proteins in chondrocyte homeostasis. Osteoarthritis Cartilage 2010;18:440-6.
72. Lambrecht S, Verbruggen G, Elewaut D et al. Differential expression of alphaB-crystallin and evidence of its role as a mediator of matrix gene expression in osteoarthritis. Arthritis Rheum 2009;60:179-88.
73. Alford KA, Glennie S, Turrell BR et al. Heat shock protein 27 functions in inflammatory gene expression and transforming growth factor-beta-activated kinase-1 (TAK1)-mediated signaling. J Biol Chem 2007;282:6232-41.
74. Kato K, Tokuda H, Mizutani J et al. Role of HSP27 in tumor necrosis factor-alpha-stimulated interleukin-6 synthesis in osteoblasts. Int J Mol Med 2011;28:887-93.
75. Fan Z, Bau B, Yang H et al. Freshly isolated osteoarthritic chondrocytes are catabolically more active than normal chondrocytes, but less responsive to catabolic stimulation with interleukin-1beta. Arthritis Rheum 2005; 52:136-43.
76. Sreekumar PG, Kannan R, Kitamura M et al. alphaB crystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells. PLoS One 2010;5: e12578.
77. Rothbard JB, Kurnellas MP, Brownell S et al. Therapeutic effects of systemic administration of chaperone alphaBcrystallin associated with binding proinflammatory plasma proteins. J Biol Chem 2012;287:9708-21.
78. Wang Q, Rozelle AL, Lepus CM et al. Identification of a central role for complement in osteoarthritis. Nat Med 2011;17:1674-9.
79. Roelofs MF, Boelens WC, Joosten LA et al. Identification of small heat shock protein B8 (HSP22) as a novel TLR4 ligand and potential involvement in the pathogenesis of rheumatoid arthritis. J Immunol 2006;176:7021-7.
80. Joosten LA, Koenders MI, Smeets RL et al. Toll-like receptor 2 pathway drives streptococcal cell wall-induced joint inflammation: critical role of myeloid differentiation factor 88. J Immunol 2003;171:6145-53.
81. Lee EK, Kang SM, Paik DJ et al. Essential roles of Toll-like receptor-4 signaling in arthritis induced by type II collagen antibody and LPS. Int Immunol 2005;17:325-33.
82. Tasab M, Batten MR, Bulleid NJ. Hsp47: a molecular chaperone that interacts with and stabilizes correctlyfolded procollagen. EMBO J 2000;19:2204-11.
83. Nagai N, Hosokawa M, Itohara S et al. Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J Cell Biol 2000;150:1499-506.
84. Masago Y, Hosoya A, Kawasaki K et al. The molecular chaperone Hsp47 is essential for cartilage and endochondral bone formation. J Cell Sci 2012;125:1118-28.
85. Christiansen HE, Schwarze U, Pyott SM et al. Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am J Hum Genet 2010;86:389-98.
86. Hattori T, Fujisawa T, Sasaki K et al. Isolation and characterization of a rheumatoid arthritis-specific antigen (RA-A47) from a human chondrocytic cell line (HCS-2/8). Biochem Biophys Res Commun 1998;245: 679-83.
87. Hattori T, Kubota S, Yutani Y et al. Change in cellular localization of a rheumatoid arthritis-related antigen (RAA47) with downregulation upon stimulation by inflammatory cytokines in chondrocytes. J Cell Physiol 2001;186: 268-81.
88. Brownlie RJ, Myers LK, Wooley PH et al. Treatment of murine collagen-induced arthritis by the stress protein BiP via interleukin-4-producing regulatory T cells: a novel function for an ancient protein. Arthritis Rheum 2006;54: 854-63.
89. Roord ST, Zonneveld-Huijssoon E, Le T et al. Modulation of T cell function by combination of epitope specific and low dose anticytokine therapy controls autoimmune arthritis. PLoS One 2006;1:e87.
90. Ragno S, Winrow VR, Mascagni P et al. A synthetic 10-kD heat shock protein (hsp10) from Mycobacterium tuberculosis modulates adjuvant arthritis. Clin Exp Immunol 1996; 103:384-90.
91. Vanags D, Williams B, Johnson B et al. Therapeutic efficacy and safety of chaperonin 10 in patients with rheumatoid arthritis: a double-blind randomised trial. Lancet 2006;368:855-63.
92. Weber CK, Haslbeck M, Englbrecht M et al. Antibodies to the endoplasmic reticulum-resident chaperones calnexin, BiP and Grp94 in patients with rheumatoid arthritis and systemic lupus erythematosus. Rheumatology 2010;49: 2255-63.
93. Dominguez-Lopez ML, Ortega-Ortega Y, Manriquez-Raya JC et al. Antibodies against recombinant heat shock proteins of 60 kDa from enterobacteria in the sera and synovial fluid of HLA-B27 positive ankylosing spondylitis patients. Clin Exp Rheumatol 2009; 27:626-32.
94. de Graeff-Meeder ER, Rijkers GT, Voorhorst-Ogink MM et al. Antibodies to human HSP60 in patients with juvenile chronic arthritis, diabetes mellitus, and cystic fibrosis. Pediatr Res 1993;34:424-8.
95. Tsoulfa G, Rook GA, Van-Embden JD et al. Raised serum IgG and IgA antibodies to mycobacterial antigens in rheumatoid arthritis. Ann Rheum Dis 1989;48: 118-23.
96. Panchapakesan J, Daglis M, Gatenby P. Antibodies to 65 kDa and 70 kDa heat shock proteins in rheumatoid arthritis and systemic lupus erythematosus. Immunol Cell Biol 1992;70:295-300.
97. Hayem G, De Bandt M, Palazzo E et al. Anti-heat shock protein 70 kDa and 90 kDa antibodies in serum of patients with rheumatoid arthritis. Ann Rheum Dis 1999; 58:291-6.
98. Tsan MF, Gao B. Heat shock proteins and immune system. J Leukoc Biol 2009;85:905-10.
99. Zanin-Zhorov A, Nussbaum G, Franitza S et al. T cells respond to heat shock protein 60 via TLR2: activation of adhesion and inhibition of chemokine receptors. FASEB J 2003;17:1567-9.
100. de Kleer IM, Kamphuis SM, Rijkers GT et al. The spontaneous remission of juvenile idiopathic arthritis is characterized by CD30+ T cells directed to human heat-shock protein 60 capable of producing the regulatory cytokine interleukin-10. Arthritis Rheum 2003; 48:2001-10.
101. Chen X, Tao Q, Yu H et al. Tumor cell membrane-bound heat shock protein 70 elicits antitumor immunity. Immunol Lett 2002;84:81-7.
102. Zheng H, Dai J, Stoilova D et al. Cell surface targeting of heat shock protein gp96 induces dendritic cell maturation and antitumor immunity. J Immunol 2001; 167:6731-5.
103. Stetler RA, Cao G, Gao Y et al. Hsp27 protects against ischemic brain injury via attenuation of a novel stressresponse cascade upstream of mitochondrial cell death signaling. J Neurosci 2008;28:13038-55.
104. Esser C, Alberti S, Hohfeld J. Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim Biophys Acta 2004;1695:171-88.
105. Dice JF. Chaperone-mediated autophagy. Autophagy 2007;3:295-9.
106. Friedman MJ, Li S, Li XJ. Activation of gene transcription by heat shock protein 27 may contribute to its neuronal protection. J Biol Chem 2009;284:27944-51.
107. Ruiz-Romero C, Calamia V, Rocha B et al. Hypoxia conditions differentially modulate human normal and osteoarthritic chondrocyte proteomes. J Proteome Res 2010;9:3035-45.