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Mediators of Inflammation
Volume 2012, Article ID 436203, 7 pages
http://dx.doi.org/10.1155/2012/436203
Review Article

Heat Shock Proteins in Tendinopathy: Novel Molecular Regulators

1Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8TA, UK
2Department of Orthopaedic Surgery, Orthopaedic Research Institute, University of New South Wales, St. George Hospital Campus, Kogarah, Sydney, NSW 2217, Australia

Received 30 July 2012; Accepted 25 September 2012

Academic Editor: Chiara De Luca

Copyright © 2012 Neal L. Millar and George A. C. Murrell. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. V. Gulotta, S. Chaudhury, and D. Wiznia, “Stem cells for augmenting tendon repair,” Stem Cells International, vol. 2012, Article ID 291431, 7 pages, 2012. View at Publisher · View at Google Scholar
  2. D. A. Hart, C. B. Frank, A. Kjdd, T. Ivie, P. Sciore, and C. Reno, “Neurogenic, mast cell and gender variables in tendon biology: potential role in chronic tendinopathy,” in Tendon Injuries, pp. 40–48, Springer, London, UK, 2005. View at Google Scholar
  3. S. M. Perry, S. E. McIlhenny, M. C. Hoffman, and L. J. Soslowsky, “Inflammatory and angiogenic mRNA levels are altered in a supraspinatus tendon overuse animal model,” Journal of Shoulder and Elbow Surgery, vol. 14, no. 1, supplement, pp. 79S–83S, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Yoshioka, W. A. Chutkow, S. Lee, J. B. Kim, J. Yan, and R. Tian, “Deletion of thioredoxin-interacting protein in mice impairs mitochondrial function but protects the myocardium from ischemia-reperfusion injury,” Journal of Clinical Investigation, vol. 122, no. 1, pp. 267–279, 2012. View at Google Scholar
  5. J. M. Bruey, C. Ducasse, P. Bonniaud et al., “Hsp27 negatively regulates cell death by interacting with cytochrome c,” Nature Cell Biology, vol. 2, no. 9, pp. 645–652, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Srivastava, “Roles of heat-shock proteins in innate and adaptive immunity,” Nature Reviews Immunology, vol. 2, no. 3, pp. 185–194, 2002. View at Google Scholar · View at Scopus
  7. F. J. Quintana and I. R. Cohen, “Heat shock proteins as endogenous adjuvants in sterile and septic inflammation,” Journal of Immunology, vol. 175, no. 5, pp. 2777–2782, 2005. View at Google Scholar · View at Scopus
  8. C. V. Nicchitta, “Re-evaluating the role of heat-shock protein-peptide interactions in tumour immunity,” Nature Reviews Immunology, vol. 3, no. 5, pp. 427–432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Gao and M. F. Tsan, “Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor α release by murine macrophages,” Journal of Biological Chemistry, vol. 278, no. 1, pp. 174–179, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Locke, “The cellular stress response to exercise: role of stress proteins,” Exercise and Sport Sciences Reviews, vol. 25, pp. 105–136, 1997. View at Google Scholar · View at Scopus
  11. M. Jäättelä, “Heat shock proteins as cellular lifeguards,” Annals of Medicine, vol. 31, no. 4, pp. 261–271, 1999. View at Google Scholar · View at Scopus
  12. S. Basu, R. J. Binder, R. Suto, K. M. Anderson, and P. K. Srivastava, “Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway,” International Immunology, vol. 12, no. 11, pp. 1539–1546, 2000. View at Google Scholar · View at Scopus
  13. A. Barreto, J. M. Gonzalez, E. Kabingu, A. Asea, and S. Fiorentino, “Stress-induced release of HSC70 from human tumors,” Cellular Immunology, vol. 222, no. 2, pp. 97–104, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. B. V. Edington, S. A. Whelan, and L. E. Hightower, “Inhibition of heat shock (stress) protein induction by deuterium oxide and glycerol: additional support for the abnormal protein hypothesis of induction,” Journal of Cellular Physiology, vol. 139, no. 2, pp. 219–228, 1989. View at Google Scholar · View at Scopus
  15. A. G. Pockley, J. Bulmer, B. M. Hanks, and B. H. Wright, “Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals,” Cell Stress and Chaperones, vol. 4, no. 1, pp. 29–35, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. I. M. Rea, S. McNerlan, and A. G. Pockley, “Serum heat shock protein and anti-heat shock protein antibody levels in aging,” Experimental Gerontology, vol. 36, no. 2, pp. 341–352, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. A. G. Pockley, R. Wu, C. Lemne, R. Kiessling, U. De Faire, and J. Frostegård, “Circulating heat shock protein 60 is associated with early cardiovascular disease,” Hypertension, vol. 36, no. 2, pp. 303–307, 2000. View at Google Scholar · View at Scopus
  18. M. Mayr, S. Kiechl, J. Willeit, G. Wick, and Q. Xu, “Infections, immunity, and atherosclerosis: associations of antibodies to Chlamydia pneumoniae, Helicobacter pylori, and cytomegalovirus with immune reactions to heat-shock protein 60 and carotid or femoral atherosclerosis,” Circulation, vol. 102, no. 8, pp. 833–839, 2000. View at Google Scholar · View at Scopus
  19. Q. Q. Huang, R. Sobkoviak, A. R. Jockheck-Clark et al., “Heat shock protein 96 is elevated in rheumatoid arthritis and activates macrophages primarily via TLR2 signaling,” Journal of Immunology, vol. 182, no. 8, pp. 4965–4973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. L. E. Hightower, “Heat shock, stress proteins, chaperones, and proteotoxicity,” Cell, vol. 66, no. 2, pp. 191–197, 1991. View at Google Scholar · View at Scopus
  21. M. J. Schlesinger, “Heat shock proteins,” Journal of Biological Chemistry, vol. 265, no. 21, pp. 12111–12114, 1990. View at Google Scholar · View at Scopus
  22. A. L. Fink, “Chaperone-mediated protein folding,” Physiological Reviews, vol. 79, no. 2, pp. 425–449, 1999. View at Google Scholar · View at Scopus
  23. S. Lindquist and E. A. Craig, “The heat-shock proteins,” Annual Review of Genetics, vol. 22, pp. 631–677, 1988. View at Google Scholar · View at Scopus
  24. P. Antal-Szalmas, “Evaluation of CD14 in host defence,” European Journal of Clinical Investigation, vol. 30, no. 2, pp. 167–179, 2000. View at Google Scholar
  25. W. Chen, U. Syldath, K. Bellmann, V. Burkart, and H. Kolb, “Human 60-kDa heat-shock protein: a danger signal to the innate immune system,” Journal of Immunology, vol. 162, no. 6, pp. 3212–3219, 1999. View at Google Scholar · View at Scopus
  26. S. B. Flohé, J. Brüggemann, S. Lendemans et al., “Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype,” Journal of Immunology, vol. 170, no. 5, pp. 2340–2348, 2003. View at Google Scholar · View at Scopus
  27. L. E. Hightower and P. T. Guidon Jr., “Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins,” Journal of Cellular Physiology, vol. 138, no. 2, pp. 257–266, 1989. View at Google Scholar · View at Scopus
  28. Y. Xu and G. A. C. Murrell, “The basic science of tendinopathy,” Clinical Orthopaedics and Related Research, vol. 466, no. 7, pp. 1528–1538, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Yuan, G. A. C. Murrell, A. Q. Wei, and M. X. Wang, “Apoptosis in rotator cuff tendonopathy,” Journal of Orthopaedic Research, vol. 20, no. 6, pp. 1372–1379, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. F. Tsan and B. Gao, “Heat shock proteins and immune system,” Journal of Leukocyte Biology, vol. 85, no. 6, pp. 905–910, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. P. K. Srivastava, H. Udono, N. E. Blachere, and Z. Li, “Heat shock proteins transfer peptides during antigen processing and CTL priming,” Immunogenetics, vol. 39, no. 2, pp. 93–98, 1994. View at Google Scholar · View at Scopus
  32. Y. M. Snyder, L. Guthrie, G. F. Evans, and S. H. Zuckerman, “Transcriptional inhibition of endotoxin-induced monokine synthesis following heat shock in murine peritoneal macrophages,” Journal of Leukocyte Biology, vol. 51, no. 2, pp. 181–187, 1992. View at Google Scholar · View at Scopus
  33. M. J. Kluger, K. Rudolph, D. Soszynski et al., “Effect of heat stress on LPS-induced fever and tumor necrosis factor,” American Journal of Physiology, vol. 273, no. 3, pp. R858–R863, 1997. View at Google Scholar · View at Scopus
  34. W. V. Eden, J. E. R. Tholet, R. V. D. Zee et al., “Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis,” Nature, vol. 331, no. 6152, pp. 171–173, 1988. View at Google Scholar · View at Scopus
  35. S. R. Brand, D. P. McIntosh, and R. M. Berstein, “Antibody to a 63kDa protein in ankylosing spondylitis,” British Journal of Rheumatology, vol. 28, supplement, article 5, 1989. View at Google Scholar
  36. S. Minota, S. Koyasu, I. Yahara, and J. Winfield, “Autoantibodies to the heat-stock protein hsp90 in systemic lupus erythematosus,” Journal of Clinical Investigation, vol. 81, no. 1, pp. 106–109, 1988. View at Google Scholar · View at Scopus
  37. S. Minota, B. Cameron, W. J. Welch, and J. B. Winfield, “Autoantibodies to the constitutive 73-kD member of the hsp70 family of heat shock proteins in systemic lupus erythematosus,” Journal of Experimental Medicine, vol. 168, no. 4, pp. 1475–1480, 1988. View at Google Scholar · View at Scopus
  38. E. H. Kang, D. J. Kim, E. Y. Lee, Y. J. Lee, E. B. Lee, and Y. W. Song, “Downregulation of heat shock protein 70 protects rheumatoid arthritis fibroblast-like synoviocytes from nitric oxide-induced apoptosis,” Arthritis Research & Therapy, vol. 11, no. 4, article R130, 2009. View at Google Scholar · View at Scopus
  39. M. M. Newkirk, S. Mitchell, M. Procino, Z. Li, M. Cosio, and W. Mazur, “Chronic smoke exposure induces rheumatoid factor and anti-heat shock protein 70 autoantibodies in susceptible mice and humans with lung disease,” European Journal of Immunology, vol. 42, no. 4, pp. 1051–1061, 2012. View at Google Scholar
  40. A. Hashiramoto, M. Murata, T. Kawazoe 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, vol. 50, no. 5, Article ID keq385, pp. 852–861, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. G. L. Puga Yung, T. D. Le, S. Roord, B. Prakken, and S. Albani, “Heat shock proteins (HSP) for immunotherapy of rheumatoid arthritis (RA),” Inflammation Research, vol. 52, no. 11, pp. 443–451, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. G. A. C. Murrell, C. Szabo, J. A. Hannafin et al., “Modulation of tendon healing by nitric oxide,” Inflammation Research, vol. 46, no. 1, pp. 19–27, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Scott and M. C. Ashe, “Common tendinopathies in the upper and lower extremities,” Current Sports Medicine Reports, vol. 5, no. 5, pp. 233–241, 2006. View at Google Scholar · View at Scopus
  44. B. M. Andres and G. A. Murrell, “Molecular and clinical developments in tendinopathy: editorial comment,” Clinical Orthopaedics and Related Research, vol. 466, no. 7, pp. 1519–1520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. G. P. Riley, H. Harrall, C. R. Constant, M. D. Chard, T. E. Cawston, and B. L. Hazleman, “Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis,” Annals of the Rheumatic Diseases, vol. 53, no. 6, pp. 359–366, 1994. View at Google Scholar · View at Scopus
  46. T. Hashimoto, K. Nobuhara, and T. Hamada, “Pathologic evidence of degeneration as a primary cause of rotator cuff tear,” Clinical Orthopaedics and Related Research, no. 415, pp. 111–120, 2003. View at Google Scholar · View at Scopus
  47. D. Kader, A. Saxena, T. Movin, and N. Maffulli, “Achilles tendinopathy: some aspects of basic science and clinical management,” British Journal of Sports Medicine, vol. 36, no. 4, pp. 239–249, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Öhberg, R. Lorentzon, and H. Alfredson, “Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 9, no. 4, pp. 233–238, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Gisslén and H. Alfredson, “Neovascularisation and pain in jumper's knee: a prospective clinical and sonographic study in elite junior volleyball players,” British Journal of Sports Medicine, vol. 39, no. 7, pp. 423–427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Sharma and N. Maffulli, “Tendon injury and tendinopathy: healing and repair,” Journal of Bone and Joint Surgery Series A, vol. 87, no. 1, pp. 187–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. N. L. Millar, A. Q. Wei, T. J. Molloy, F. Bonar, and G. A. C. Murrell, “Cytokines and apoptosis in supraspinatus tendinopathy,” Journal of Bone and Joint Surgery Series B, vol. 91, no. 3, pp. 417–424, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Lundgreen, O. B. Lian, L. Engebretsen, and A. Scott, “Tenocyte apoptosis in the torn rotator cuff: a primary or secondary pathological event?” British Journal of Sports Medicine, vol. 45, no. 13, pp. 1035–1039, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. N. L. Millar, J. H. Reilly, S. C. Kerr, A. L. Campbell, K. J. Little, and W. J. Leach, “Hypoxia: a critical regulator of early human tendinopathy,” Annals of the rheumatic diseases, vol. 71, no. 2, pp. 302–310, 2012. View at Google Scholar
  54. H. Pan and J. Halper, “Regulation of heat shock protein 47 and type I procollagen expression in avian tendon cells,” Cell and Tissue Research, vol. 311, no. 3, pp. 373–382, 2003. View at Google Scholar · View at Scopus
  55. M. Jagodzinski, S. Hankemeier, M. van Griensven, U. Bosch, C. Krettek, and J. Zeichen, “Influence of cyclic mechanical strain and heat of human tendon fibroblasts on HSP-72,” European Journal of Applied Physiology, vol. 96, no. 3, pp. 249–256, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Barkhausen, M. Van Griensven, J. Zeichen, and U. Bosch, “Modulation of cell functions of human tendon fibroblasts by different repetitive cyclic mechanical stress patterns,” Experimental and Toxicologic Pathology, vol. 55, no. 2-3, pp. 153–158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. T. J. Molloy, M. W. Kemp, Y. Wang, and G. A. C. Murrell, “Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration,” Journal of Applied Physiology, vol. 101, no. 6, pp. 1702–1709, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. N. L. Millar, A. Q. Wei, T. J. Molloy, F. Bonar, and G. A. C. Murrell, “Heat shock protein and apoptosis in supraspinatus tendinopathy,” Clinical Orthopaedics and Related Research, vol. 466, no. 7, pp. 1569–1576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. J. L. Martin-Ventura, V. Nicolas, X. Houard et al., “Biological significance of decreased HSP27 in human atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 6, pp. 1337–1343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Leeuwenburgh, J. Hollander, S. Leichtweis, M. Griffiths, M. Gore, and L. L. Ji, “Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific,” American Journal of Physiology, vol. 272, no. 1, pp. R363–R369, 1997. View at Google Scholar · View at Scopus
  61. D. D. Mosser, A. W. Caron, L. Bourget, C. Denis-Larose, and B. Massie, “Role of the human heat shock protein hsp70 in protection against stress- induced apoptosis,” Molecular and Cellular Biology, vol. 17, no. 9, pp. 5317–5327, 1997. View at Google Scholar · View at Scopus
  62. M. Jaattela, D. Wissing, P. A. Bauer, and G. C. Li, “Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity,” EMBO Journal, vol. 11, no. 10, pp. 3507–3512, 1992. View at Google Scholar · View at Scopus
  63. K. Bellmann, M. Jäättelä, D. Wissing, V. Burkart, and H. Kolb, “Heat shock protein hsp70 overexpression confers resistance against nitric oxide,” FEBS Letters, vol. 391, no. 1-2, pp. 185–188, 1996. View at Publisher · View at Google Scholar · View at Scopus