535
Views
69
CrossRef citations to date
0
Altmetric
Review

Exosomal HSP60: a potentially useful biomarker for diagnosis, assessing prognosis, and monitoring response to treatment

ORCID Icon, , , , , & show all
Pages 815-822 | Received 31 May 2017, Accepted 13 Jul 2017, Published online: 25 Jul 2017

References

  • Vlassov AV, Magdaleno S, Setterquist R, et al. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta - Gen Subj. 2012;1820:940–948.
  • Fais S, O’Driscoll L, Borras FE, et al. Evidence-based clinical use of nanoscale extracellular vesicles in nanomedicine. ACS Nano. 2016;10:3886–3899.
  • Cappello F, Logozzi M, Campanella C, et al. Exosome levels in human body fluids: A tumor marker by themselves? Eur J Pharm Sci. 2017;96:93–98.
  • An T, Qin S, Xu Y, et al. Exosomes serve as tumour markers for personalized diagnostics owing to their important role in cancer metastasis. J Extracell Vesicles. 2015;4:27522.
  • Choi DS, Lee JM, Park GW, et al. Proteomic analysis of microvesicles derived from human colorectal cancer cells. J Proteome Res. 2007;6:4646–4655.
  • Rappa F, Farina F, Zummo G, et al. HSP-molecular chaperones in cancer biogenesis and tumor therapy: an overview. Anticancer Res. 2012;32:5139–5150.
  • Khalil AA, Kabapy NF, Deraz SF, et al. Heat shock proteins in oncology: diagnostic biomarkers or therapeutic targets? Biochim Biophys Acta. 2011;1816:89–104.
  • Nakamura H, Minegishi H. HSP60 as a drug target. Curr Pharm Des. 2013;19:441–451.
  • Cappello F, Angileri F, Conway de Macario E, et al. Chaperonopathies and chaperonotherapy. Hsp60 as therapeutic target in cancer: potential benefits and risks. Curr Pharm Des. 2013;19:452–457.
  • Campanella C, Bucchieri F, Merendino AM, et al. The odyssey of Hsp60 from tumor cells to other destinations includes plasma membrane-associated stages and Golgi and exosomal protein-trafficking modalities. PLoS One. 2012;7:e42008. DOI:10.1371/journal.pone.0042008
  • Campanella C, Rappa F, Sciumè C, et al. Heat shock protein 60 levels in tissue and circulating exosomes in human large bowel cancer before and after ablative surgery. Cancer. 2015;121(18):3230–3239.
  • Campanella C, D’Anneo A, Marino Gammazza A, et al. The histone deacetylase inhibitor SAHA induces HSP60 nitration and its extracellular release by exosomal vesicles in human lung-derived carcinoma cells. Oncotarget. 2016;7:28849–28867.
  • Pace A, Barone G, Lauria A, et al. Hsp60, a novel target for antitumor therapy: structure-function features and prospective drugs design. Curr Pharm Des. 2013;19:2757–2764.
  • Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med. 2013;7:769–778.
  • Whiteside TL. The potential of tumor-derived exosomes for noninvasive cancer monitoring. Expert Rev Mol Diagn. 2015;15:1293–1310.
  • Tovar-Camargo OA, Toden S, Goel A. Exosomal microRNA biomarkers: emerging frontiers in colorectal and other human cancers. Expert Rev Mol Diagn. 2016;16:553–567.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373–383.
  • Lo Cicero A, Stahl PD, Raposo G. Extracellular vesicles shuffling intercellular messages: for good or for bad. Curr Opin Cell Biol. 2015;35:69–77.
  • Whiteside TL. Exosomes carrying immunoinhibitory proteins and their role in cancer. Clin Exp Immunol. 2017. DOI:10.1111/cei.12974
  • Mears R, Craven RA, Hanrahan S, et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics. 2004;4:4019–4031.
  • Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–579.
  • Hegmans JPJJ, Gerber PJ, Lambrecht BN. Exosomes. Methods Mol Biol. 2008;484:97–109.
  • Rivoltini L, Chiodoni C, Squarcina P, et al. TNF-related apoptosis-inducing ligand (TRAIL)-armed exosomes deliver proapoptotic signals to tumor site. Clin Cancer Res. 2016;22:3499–3512.
  • Clayton A, Mitchell JP, Court J, et al. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res. 2007;67:7458–7466.
  • Denzer K, Kleijmeer MJ, Heijnen HF, et al. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;113(19):3365–3374.
  • Menay F, Herschlik L, De Toro J, et al. Exosomes isolated from ascites of T-cell lymphoma-bearing mice expressing surface CD24 and HSP90 induce a tumor-specific immune response. Front Immunol. 2017;8:286.
  • Malik ZA, Kott KS, Poe AJ, et al. Cardiac myocyte exosomes: stability, HSP60, and proteomics. Am J Physiol Heart Circ Physiol. 2013;304:954–965.
  • Zheng P, Chen L, Yuan X, et al. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res. 2017;36:53.
  • Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73:1907–1920.
  • Lian Q, Xu J, Yan S, et al. Chemotherapy-induced intestinal inflammatory responses are mediated by exosome secretion of double-strand DNA via AIM2 inflammasome activation. Cell Res. 2017. DOI:10.1038/cr.2017.54
  • Selmaj I, Mycko MP, Raine CS, et al. The role of exosomes in CNS inflammation and their involvement in multiple sclerosis. J Neuroimmunol. 2017;306:1–10.
  • Kapustin AN, Shanahan CM. Emerging roles for vascular smooth muscle cell exosomes in calcification and coagulation. J Physiol. 2016;594:2905–2914.
  • Qu Y, Zhang Q, Cai X, et al. Exosomes derived from miR-181-5p-modified adipose-derived mesenchymal stem cells prevent liver fibrosis via autophagy activation. J Cell Mol Med. 2017. DOI:10.1111/jcmm.13170
  • Tao SC, Yuan T, Rui BY, et al. Exosomes derived from human platelet-rich plasma prevent apoptosis induced by glucocorticoid-associated endoplasmic reticulum stress in rat osteonecrosis of the femoral head via the Akt/Bad/Bcl-2 signal pathway. Theranostics. 2017;7:733–750.
  • Demonbreun AR, McNally EM. Muscle cell communication in development and repair. Curr Opin Pharmacol. 2017;34:7–14.
  • Ludwig S, Floros T, Theodoraki M-N, et al. Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer. Clin Cancer Res. 2017;pii: clincanres.2819. DOI:10.1158/1078-0432.CCR-16-2819
  • Jia S, Zhang R, Li Z, et al. Clinical and biological significance of circulating tumor cells, circulating tumor DNA, and exosomes as biomarkers in colorectal cancer. Oncotarget. 2017. DOI:10.18632/oncotarget.17184
  • Pinet S, Bessette B, Vedrenne N, et al. TrkB-containing exosomes promote the transfer of glioblastoma aggressiveness to YKL-40-inactivated glioblastoma cells. Oncotarget. 2016;7:50349–50364.
  • Sun X, Ma X, Wang J, et al. Glioma stem cells-derived exosomes promote the angiogenic ability of endothelial cells through miR-21/VEGF signal. Oncotarget. 2017. DOI:10.18632/oncotarget.16661
  • Zhang H, Deng T, Liu R, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nat Commun. 2017;8:15016.
  • Herreros-Villanueva M, Bujanda L. Glypican-1 in exosomes as biomarker for early detection of pancreatic cancer. Ann Transl Med. 2016;4:64.
  • Lundholm M, Schröder M, Nagaeva O, et al. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion. PLoS One. 2014;9:e108925.
  • Szajnik M, Derbis M, Lach M, et al. Exosomes in plasma of patients with ovarian carcinoma: potential biomarkers of tumor progression and response to therapy. Gynecol Obstet (Sunnyvale). 2013;Suppl 4:3.
  • Liu T, Mendes DE, Berkman CE. Functional prostate-specific membrane antigen is enriched in exosomes from prostate cancer cells. Int J Oncol. 2014;44:918–922.
  • González E, Falcón-Pérez JM. Cell-derived extracellular vesicles as a platform to identify low-invasive disease biomarkers. Expert Rev Mol Diagn. 2015;15:1–17.
  • Santiago-Dieppa DR, Steinberg J, Gonda D, et al. Extracellular vesicles as a platform for “liquid biopsy” in glioblastoma patients. Expert Rev Mol Diagn. 2014;14:819–825.
  • Caruso Bavisotto C, Nikolic D, Marino Gammazza A, et al. The dissociation of the Hsp60/pro-Caspase-3 complex by bis(pyridyl)oxadiazole copper complex (CubipyOXA) leads to cell death in NCI-H292 cancer cells. J Inorg Biochem. 2017;170:8–16.
  • Czarnecka AM, Campanella C, Zummo G, et al. Mitochondrial chaperones in cancer: from molecular biology to clinical diagnostics. Cancer Biol Ther. 2006;5:714–720.
  • Vilasi S, Carrotta R, Mangione MR, et al. Human Hsp60 with its mitochondrial import signal occurs in solution as heptamers and tetradecamers remarkably stable over a wide range of concentrations. PLoS One. 2014;9:e97657.
  • Zhao Y, Zhang C, Wei X, et al. Heat shock protein 60 stimulates the migration of vascular smooth muscle cells via Toll-like receptor 4 and ERK MAPK activation. Sci Rep. 2015;5:15352.
  • Spierings J, van Eden W. Heat shock proteins and their immunomodulatory role in inflammatory arthritis. Rheumatology (Oxford). 2017;56:198–208.
  • Fagone P, Di Rosa M, Palumbo M, et al. Modulation of heat shock proteins during macrophage differentiation. Inflamm Res. 2012;61:1131–1139.
  • Campanella C, Bucchieri F, Ardizzone NM, et al. Upon oxidative stress, the antiapoptotic Hsp60/procaspase-3 complex persists in mucoepidermoid carcinoma cells. Eur J Histochem. 2008;52:221–228.
  • Allegra A, Sant’antonio E, Penna G, et al. Novel therapeutic strategies in multiple myeloma: role of the heat shock protein inhibitors. Eur J Haematol. 2011;86:93–110.
  • Landriscina M, Amoroso MR, Piscazzi A, et al. Heat shock proteins, cell survival and drug resistance: the mitochondrial chaperone TRAP1, a potential novel target for ovarian cancer therapy. Gynecol Oncol. 2010;117:177–182.
  • Rizzo M, Cappello F, Marfil R, et al. Heat-shock protein 60 kDa and atherogenic dyslipidemia in patients with untreated mild periodontitis: a pilot study. Cell Stress Chaperones. 2012;17:399–407.
  • Bonanad C, Núñez J, Sanchis J, et al. Serum heat shock protein 60 in acute heart failure: a new biomarker? Congest Heart Fail. 2013;19:6–10.
  • Ireland HE, Leoni F, Altaie O, et al. Measuring the secretion of heat shock proteins from cells. Methods. 2007;43:176–183.
  • Graner MW, Cumming RI, Bigner DD. The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J Neurosci. 2007;27:11214–11227.
  • Tanaka T, Kajiwara T, Kutomi G, et al. CpG-A stimulates Hsp72 secretion from plasmacytoid dendritic cells, facilitating cross-presentation. Immunol Lett. 2015;167:34–40.
  • Hightower LE, Guidon PT. Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J Cell Physiol. 1989;138:257–266.
  • Pockley AG, Bulmer J, Hanks BM, et al. Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals. Cell Stress Chaperones. 1999;4:29–35.
  • Pockley AG, Shepherd J, Corton JM. Detection of heat shock protein 70 (Hsp70) and anti-Hsp70 antibodies in the serum of normal individuals. Immunol Invest. 1998;27:367–377.
  • De Maio A, Vazquez D. Extracellular heat shock proteins: a new location, a new function. Shock. 2013;40:239–246.
  • Cappello F, Conway de Macario E, Marino Gammazza A, et al. Hsp60 and human aging: les liaisons dangereuses. Front Biosci Landmark Ed. 2013;18:626–637.
  • Clayton A, Turkes A, Navabi H, et al. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005;118:3631–3638.
  • Multhoff G, Hightower LE. Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones. 1996;1:167–176.
  • Merendino AM, Bucchieri F, Campanella C, et al. Hsp60 is actively secreted by human tumor cells. PLoS One. 2010;5:e9247.
  • Vulpis E, Cecere F, Molfetta R, et al. Genotoxic stress modulates the release of exosomes from multiple myeloma cells capable of activating NK cell cytokine production: role of HSP70/TLR2/NF-kB axis. Oncoimmunology. 2017;6:e1279372.
  • Bausero MA, Gastpar R, Multhoff G, et al. Alternative mechanism by which IFN-gamma enhances tumor recognition: active release of heat shock protein 72. J Immunol. 2005;175:2900–2912.
  • Lv LH, Wan Y-L, Lin Y, et al. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem. 2012;287:15874–15885.
  • Sevin M, Girodon F, Garrido C, et al. HSP90 and HSP70: implication in inflammation processes and therapeutic approaches for myeloproliferative neoplasms. Mediators Inflamm. 2015;2015:970242.
  • Lancaster GI, Febbraio MA. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem. 2005;280:23349–23355.
  • Kumar S, Stokes J, Singh UP, et al. Targeting Hsp70: a possible therapy for cancer. Cancer Lett. 2016;374:156–166.
  • Vega VL, Rodríguez-Silva M, Frey T, et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol. 2008;180:4299–4307.
  • Gastpar R, Gehrmann M, Bausero MA, et al. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 2005;65:5238–5247.
  • Lancaster GI, Febbraio MA. Mechanisms of stress-induced cellular HSP72 release: implications for exercise-induced increases in extracellular HSP72. Exerc Immunol Rev. 2005;11:46–52.
  • McCready J, Sims JD, Chan D, et al. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer. 2010;10:294.
  • Elsner L, Muppala V, Gehrmann M, et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol. 2007;179:5523–5533.
  • Xiao W, Dong W, Zhang C, et al. Effects of the epigenetic drug MS-275 on the release and function of exosome-related immune molecules in hepatocellular carcinoma cells. Eur J Med Res. 2013;18:61.
  • Franzen CA, Simms PE, Van Huis AF, et al. Characterization of uptake and internalization of exosomes by bladder cancer cells. Biomed Res Int. 2014;2014:619829.
  • Czarnecka AM, Campanella C, Zummo G, et al. Heat shock protein 10 and signal transduction: a “capsula eburnea” of carcinogenesis? Cell Stress Chaperones. 2006;11:287–294.
  • Marino Gammazza A, Rizzo M, Citarrella R, et al. Elevated blood Hsp60, its structural similarities and cross-reactivity with thyroid molecules, and its presence on the plasma membrane of oncocytes point to the chaperonin as an immunopathogenic factor in Hashimoto’s thyroiditis. Cell Stress Chaperones. 2014;19:343–353.
  • Huber V, Fais S, Iero M, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology. 2005;128:1796–1804.
  • Cappello F, Caramori G, Campanella C, et al. Convergent sets of data from in vivo and in vitro methods point to an active role of Hsp60 in chronic obstructive pulmonary disease pathogenesis. PLoS One. 2011;6:e28200.
  • Cappello F, Marino Gammazza A, Palumbo Piccionello A, et al. Hsp60 chaperonopathies and chaperonotherapy: targets and agents. Expert Opin Ther Targets. 2014;18:185–208.
  • Nahas EAP, Nahas-Neto J, Orsatti CL, et al. The 60- and 70-kDa heat-shock proteins and their correlation with cardiovascular risk factors in postmenopausal women with metabolic syndrome. Cell Stress Chaperones. 2014;19:559–568.
  • Lin L, Kim SC, Wang Y, et al. HSP60 in heart failure: abnormal distribution and role in cardiac myocyte apoptosis. Am J Physiol Heart Circ Physiol. 2007;293:2238–2247.
  • Gupta S, Knowlton AA. HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am J Physiol Heart Circ Physiol. 2007;292:3052–3056.
  • Hayoun D, Kapp T, Edri-Brami M, et al. HSP60 is transported through the secretory pathway of 3-MCA-induced fibrosarcoma tumour cells and undergoes N-glycosylation. FEBS J. 2012;279:2083–2095.
  • Cappello F, Czarnecka AM, Di Stefano A, et al. Hsp60 and Hsp10 as antitumor molecular agents. Cancer Biol Ther. 2007;6(4):487–489.
  • Nagumo Y, Kakeya H, Shoji M, et al. Epolactaene binds human Hsp60 Cys442 resulting in the inhibition of chaperone activity. Biochem J. 2005;387:835–840.
  • Ghosh JC, Dohi T, Kang BH, et al. Hsp60 regulation of tumor cell apoptosis. J Biol Chem. 2008;283:5188–5194.
  • Marino Gammazza A, Campanella C, Barone R, et al. Doxorubicin anti-tumor mechanisms include Hsp60 post-translational modifications leading to the Hsp60/p53 complex dissociation and instauration of replicative senescence. Cancer Lett. 2017;385:75–86.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.