The role of secreted heat shock protein-90 (Hsp90) in wound healing - how could it shape future therapeutics?

References

• Singer A, Clark R. Cutaneous wound healing. N Engl J Med. 1999;341:738–746.
   PubMed Web of Science ®Google Scholar
• Martin P. Wound healing–aiming for perfect skin regeneration. Science. 1997;276:75–81.
   PubMed Web of Science ®Google Scholar
• Choi S, Lee S, Kim Y, et al. Role of heat shock proteins in gastric inflammation and ulcer healing. J Physiol Pharmacol. 2009;60:5–17.
   PubMed Web of Science ®Google Scholar
• Atalay M, Oksala N, Lappalainen J, et al. Heat shock proteins in diabetes and wound healing. Curr Protein Pept Sci. 2009;10:85–95.
   PubMed Web of Science ®Google Scholar
• Magalhães W, Nogueira M, Kaneko T. Heat shock proteins (HSP): dermatological implications and perspectives. Eur J Dermatol. 2012;22:8–13.
   PubMed Web of Science ®Google Scholar
• Bellaye P, Burgy O, Causse S, et al. Heat shock proteins in fibrosis and wound healing: good or evil? Pharmacol Ther. 2014;143:119–132.
   PubMed Web of Science ®Google Scholar
• Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83:835–870.
   PubMed Web of Science ®Google Scholar
• Grose R, Werner S. Wound-healing studies in transgenic and knockout mice. Mol Biotechnol. 2004;28:147–166.
   PubMed Web of Science ®Google Scholar
• LeGrand E. Preclinical promise of becaplermin (rhPDGF-BB) in wound healing. Am J Surg. 1998;176:48–54.
   PubMed Web of Science ®Google Scholar
• Brown G, Nanney LB,Griffen J, et al. Enhancement of wound healing by topical treatment with epidermal growth factor. N Engl J Med. 1989;321:76–79.
   PubMed Web of Science ®Google Scholar
• Pastor J, Calonge M. Epidermal growth factor and corneal wound healing. A Multicenter Study Cornea. 1992;11:311–314.
   PubMed Web of Science ®Google Scholar
• Ramsay H, Heikkonen E, Laurila P. Effect of epidermal growth factor on tympanic membranes with chronic perforations: a clinical trial. Otolaryngol Head Neck Surg. 1995;113:375–379.
   PubMed Web of Science ®Google Scholar
• Fernandez-Montequin J. Intralesional injections of Citoprot-P (recombinant human epidermal growth factor) in advanced diabetic foot ulcers with risk of amputation. Int Wound J. 2007;4:333–343.
   PubMedGoogle Scholar
• Mohan V. Recombinant human epidermal growth factor (REGEN-D 150): effect on healing of diabetic foot ulcers. Diabetes Res Clin Pract. 2007;78:405–411.
   PubMed Web of Science ®Google Scholar
• Greenhalgh D, Rieman M. Effects of basic fibroblast growth factor on the healing of partial-thickness donor sites. A prospective, randomized, double-blind trial. Wound Repair Regen. 1994;2:113–121.
   PubMedGoogle Scholar
• Fu X, Shen Z, Chen Y, et al. Randomised placebo-controlled trial of use of topical recombinant bovine basic fibroblast growth factor for second-degree burns. Lancet. 1998;352:1661–1664.
   PubMed Web of Science ®Google Scholar
• Uchi H, Igarashi A, Urabe K, et al. Clinical efficacy of basic fibroblast growth factor (bFGF) for diabetic ulcer. Eur J Dermatol. 2009;19:461–468.
   PubMed Web of Science ®Google Scholar
• Ma B, Cheng D-S, Xia Z-F, et al. Randomized, multicenter, double-blind, and placebo-controlled trial using topical recombinant human acidic fibroblast growth factor for deep partial-thickness burns and skin graft donor site. Wound Repair Regen. 2007;15:795–799.
   PubMed Web of Science ®Google Scholar
• Robson M, Hill DP, Smith PD, et al. Sequential cytokine therapy for pressure ulcers: clinical and mechanistic response. Ann Surg. 2000;31:600–611.
   Web of Science ®Google Scholar
• Robson M, Phillips L, Thomason A, et al. Platelet-derived growth factor BB for the treatment of chronic pressure ulcers. Lancet. 1992;339:23–25.
   PubMed Web of Science ®Google Scholar
• Pierce G, Tarpley J, Yanagihara D, et al. Platelet-derived growth factor (BB homodimer), transforming growth factor-beta 1, and basic fibroblast growth factor in dermal wound healing. Neovessel and matrix formation and cessation of repair. Am J Pathol. 1992;140:1375–1388.
   PubMed Web of Science ®Google Scholar
• Steed D. Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity diabetic ulcers. diabetic ulcer study group. J Vasc Surg. 1995;21:71–78.
   PubMed Web of Science ®Google Scholar
• Smiell J, Wieman T, Steed D, et al. Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with nonhealing, lower extremity diabetic ulcers: a combined analysis of four randomized studies. Wound Repair Regen. 1999;7:335–346.
   PubMed Web of Science ®Google Scholar
• Wieman T, Smiell J, Su Y. Efficacy and safety of a topical gel formulation of recombinant human platelet-derived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers. A phase III randomized placebo-controlled double-blind study. Diabetes Care. 1998;21:822–827.
   PubMed Web of Science ®Google Scholar
• Nagai M, Embil J. Becaplermin: recombinant platelet derived growth factor, a new treatment for healing diabetic foot ulcers. Expert Opin Biol Ther. 2002;2:211–218.
   PubMed Web of Science ®Google Scholar
• Mandracchia V, Sanders S, Frerichs J. The use of becaplermin (rhPDGF-BB) gel for chronic nonhealing ulcers. A retrospective analysis. Clin Podiatr Med Surg. 2001;18:189–209.
   PubMedGoogle Scholar
• Bejcek B. The v-sis oncogene product but not platelet-derived growth factor (PDGF) A homodimers activate PDGF alpha and beta receptors intracellularly and initiate cellular transformation. J Biol Chem. 1992;267:3289–3293.
   PubMed Web of Science ®Google Scholar
• van den Dolder J, Mooren R, Vloon A, et al. Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng. 2006;12:3067–3073.
   PubMedGoogle Scholar
• Cheng C, Sahu D, Tsen F, et al. A fragment of secreted Hsp90α carries properties that enable it to accelerate effectively both acute and diabetic wound healing in mice. J Clin Invest. 2011;121:4348–4361.
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay B, Fan J, Guan S, et al. A “traffic control” role for TGFbeta3: orchestrating dermal and epidermal cell motility during wound healing. J Cell Biol. 2006;172:1093–1105.
   PubMed Web of Science ®Google Scholar
• O’Brien K, Bhatia A, Tsen F, et al. Identification of the critical therapeutic entity in secreted Hsp90α that promotes wound healing in newly re-standardized healthy and diabetic pig models. PLoS One. 2014;9:e113956.
   PubMed Web of Science ®Google Scholar
• Li W. Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. Embo J. 2007;26:1221–1233.
   PubMed Web of Science ®Google Scholar
• Cheng C. Transforming growth factor alpha (TGFα)-stimulated secretion of Hsp90α: using the receptor LRP-1/CD91 to promote human skin cell migration against a TGFbeta-rich environment during wound healing. Mol Cell Biol. 2008;28:3344–3358.
   PubMed Web of Science ®Google Scholar
• Bhatia A, O’Brien K, Guo J et al., Requirement for Injury-Induced Deposition and Function of Secreted Heat Shock Protein-90alpha (Hsp90α) during Normal Wound Healing. 2017 under submission
   Google Scholar
• Imai T, Kato Y, Kajiwara C, et al. Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proc Natl Acad Sci. 2011;108:16363–16368.
   PubMed Web of Science ®Google Scholar
• Li W, Sahu D, Tsen F. Secreted heat shock protein-90 (Hsp90) in wound healing and cancer. Biochim Biophys Acta. 2012;1823:730–741.
   PubMed Web of Science ®Google Scholar
• Jayaprakash P, Dong H, Zou M, et al. Hsp90α and Hsp90β together operate a hypoxia and nutrient paucity stress-response mechanism during wound healing. J Cell Sci. 2015;128:1475–1480.
   PubMed Web of Science ®Google Scholar
• Sullivan T, Eaglstein W, Davis S, et al. The pig as a model for human wound healing. Wound Repair Regen. 2001;9:66–76.
   PubMed Web of Science ®Google Scholar
• Brahmatewari J, Serafini A, Serralta V, et al. The effects of topical transforming growth factor-beta2 and anti-transforming growth factor-beta2,3 on scarring in pigs. J Cutan Med Surg. 2000;4:126–131.
   PubMedGoogle Scholar
• Davis C, Cazzaniga A, Eaglstein W, et al. Over-the-counter topical antimicrobials: effective treatments? Arch Dermatol Res. 2005;297:190–195.
   PubMed Web of Science ®Google Scholar
• Lindblad W. Considerations for selecting the correct animal model for dermal wound-healing studies. J Biomater Sci Polym Ed. 2008;19:1087–1096.
   PubMed Web of Science ®Google Scholar
• Bhatia A, O’Brien K, Chen M, et al. Dual therapeutic functions of F-5 fragment in burn wounds: preventing wound progression and promoting wound healing in pigs. Mol Ther Methods Clin Dev. 2016;3:16041.
   PubMedGoogle Scholar
• Dong H, Zou M, Bhatia A, et al. Breast cancer MDA-MB-231 cells use secreted heat shock protein-90alpha (Hsp90α) to survive a hostile hypoxic environment. Sci Rep. 2016;6:20605.
   PubMed Web of Science ®Google Scholar
• Young J, Moarefi I, Hartl F. Hsp90: a specialized but essential protein-folding tool. J Cell Biol. 2001;154:267–273.
   PubMed Web of Science ®Google Scholar
• Woodley D, Fan J, Cheng C, et al. Participation of the lipoprotein receptor LRP1 in hypoxia-HSP90alpha autocrine signaling to promote keratinocyte migration. J Cell Sci. 2009;122:1495–1498.
   PubMed Web of Science ®Google Scholar
• Tsen F, O’Brien K, Cheng C, et al. eHsp90 (extracellular heat shock protein 90) signals through subdomain II and NPVY Motif of LRP-1 receptor to Akt1 and Akt2: a circuit essential for promoting skin cell migration in vitro and wound healing in vivo. Mol Cell Biol. 2013;33:4947–4953.
   PubMed Web of Science ®Google Scholar
• Lillis A, Van Duyn L, Murphy-Ullrich J, et al. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev. 2008;88:887–918.
   PubMed Web of Science ®Google Scholar
• Clayton A, Turkes A, Navabi H, et al. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005;118:3631–3638.
   PubMed Web of Science ®Google Scholar
• Yu X, Harris S, Levine A. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006;66:4795–4801.
   PubMed Web of Science ®Google Scholar
• Denzer K, Kleijmeer M, Heijnen H, et al. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;113:3365–3374.
   PubMed Web of Science ®Google Scholar
• Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–579.
   PubMed Web of Science ®Google Scholar
• Lancaster G, Febbraio M. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem. 2005;280:23349–23355.
   PubMed Web of Science ®Google Scholar
• Savina A, Furlan M, Vidal M, et al. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem. 2003;278:20083–20090.
   PubMed Web of Science ®Google Scholar
• Hegmans J, Bard M, Hemmes A, et al. Proteomic analysis of exosomes secreted by human mesothelioma cells. Am J Pathol. 2004;164:1807–1815.
   PubMed Web of Science ®Google Scholar
• Guo J, Jayaprakash P, Dan J, et al. PRAS40 Connects microenvironmental stress signaling to exosome-mediated secretion. Mol Cell Biol. 2017 Epub ahead of print
   Google Scholar
• Sahu D, Zhao Z, Tsen F, et al. Identification of a novel tumor epitope in secreted Hsp90α for HIF-1α-overexpressing breast cancer. Mol Biol Cell. 2011;23:602–613.
   PubMed Web of Science ®Google Scholar
• Csermely P, Schnaider T, Soti C, et al. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A Comprehensive Review. Pharmacol Ther. 1998;79:129–168.
   PubMed Web of Science ®Google Scholar
• Multhoff G, Hightower L. Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones. 1996;1:167–176.
   PubMed Web of Science ®Google Scholar
• Hightower L, Guidon P. Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol. 1989;138:257–266.
   PubMed Web of Science ®Google Scholar
• Liao D, Jin Z, Baas A, et al. Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells. J Biol Chem. 2000;275:189–196.
   PubMed Web of Science ®Google Scholar
• Ito J, Nagayasu Y, Hoshikawa M, et al. Enhancement of FGF-1 release along with cytosolic proteins from rat astrocytes by hydrogen peroxide. Brain Res. 2013;1522:12–21.
   PubMed Web of Science ®Google Scholar
• Kuroita T, Tachibana H, Ohashi H. Growth stimulating activity of heat shock protein 90 alpha to lymphoid cell lines in serum-free medium. Cytotechnology. 1992;8:109–117.
   PubMed Web of Science ®Google Scholar
• Eustace B, Sakurai T, Stewart J, et al. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat Cell Biol. 2004;6:507–514.
   PubMed Web of Science ®Google Scholar
• Wang X, Song X, Zhuo W, et al. The regulatory mechanism of Hsp90alpha secretion and its function in tumor malignancy. Proc Natl Acad Sci U S A. 2009;106:21288–21293.
   PubMed Web of Science ®Google Scholar
• Suzuki S, Kulkarni A. Extracellular heat shock protein HSP90beta secreted by MG63 osteosarcoma cells inhibits activation of latent TGF-beta1. Biochem Biophys Res Commun. 2010;398:525–5331.
   PubMed Web of Science ®Google Scholar
• Chen J, Hsu Y, Chen C, et al. Secreted heat shock protein 90alpha induces colorectal cancer cell invasion through CD91/LRP-1 and NF-kappaB-mediated integrin alphaV expression. J Biol Chem. 2010;285:25458–25466.
   PubMed Web of Science ®Google Scholar
• Tsutsumi S, Scroggins B, Koga F, et al. A small molecule cell-impermeant Hsp90 antagonist inhibits tumor cell motility and invasion. Oncogene. 2008;27:2478–2487.
   PubMed Web of Science ®Google Scholar
• Aubert C, Michel P, Gillery P, et al. Association of peripheral neuropathy with circulating advanced glycation end products, soluble receptor for advanced glycation end products and other risk factors in patients with type 2 diabetes. Diabetes Metab Res Rev. 2014;30:679–685.
   PubMed Web of Science ®Google Scholar
• Bos D, de Ranitz-Greven W, de Valk H. Advanced glycation end products, measured as skin autofluorescence and diabetes complications: a systematic review. Diabetes Technol Ther. 2011;13:773–779.
   PubMed Web of Science ®Google Scholar
• Dvorack H. Tumors: wounds that do not heal. New Eng J Med. 1986;315:1650–1659.
   PubMed Web of Science ®Google Scholar
• Zou M, Bhatia A, Dong H, et al. Evolutionarily conserved dual lysine motif determines the non-chaperone function of secreted Hsp90alpha in tumor progression. Oncogene. 2017;36:2160–2171.
   PubMed Web of Science ®Google Scholar