Extracellular cell stress proteins as biomarkers of human disease

Biochemical Society Transactions

Volumn 42, Issue 6, 2014, Pages 1744-1751

  Pockley, A Graham ^a   Henderson, Brian ^b   Multhoff, Gabriele ^c,d  

^a NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Biomarker; Cancer; Cell stress protein; Enzyme immunoassay; Heat shock protein; Molecular chaperone

Indexed keywords

CELL SURFACE PROTEIN; HEAT SHOCK PROTEIN 70; BIOLOGICAL MARKER; PLASMA PROTEIN;

ARTICLE; CELL STRESS; CELLULAR STRESS RESPONSE; DISEASE MARKER; HUMAN; NEOPLASM; NONHUMAN; PERIPHERAL CIRCULATION; PROTEIN FUNCTION; PROTEIN SECRETION; BLOOD; EXTRACELLULAR SPACE; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

BIOLOGICAL MARKERS; BLOOD PROTEINS; EXTRACELLULAR SPACE; HUMANS; NEOPLASMS; OXIDATIVE STRESS;

EID: 84911874159     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140205     Document Type: Article

References (79)

1. Ritossa, F.A. (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18, 571-573 CrossRef
2. Tissières, A., Mitchell, H.K. and Tracy, U. (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J. Mol. Biol. 84, 389-398 CrossRef PubMed
3. Ashburner, M. (1970) Patterns of puffing activity in the salivary gland chromosomes of Drosophila. V. Responses to environmental treatments. Chromosoma 31, 356-376 CrossRef PubMed
4. Ananthan, J., Goldberg, A.L. and Voellmy, R. (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232, 522-524 CrossRef PubMed
5. Hemmingsen, S.M., Woolford, C., van der Vies, S.M., Tilly, K., Dennis, D.T., Georgopoulos, C.P., Hendrix, R.W. and Ellis, R.J. (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333, 330-334 CrossRef PubMed
6. Ellis, R.J. (2005) Chaperone function: the orthodox view. In Molecular Chaperones and Cell Signalling (Henderson, B. and Pockley, A.G., eds), pp. 3-21, Cambridge University Press, Cambridge CrossRef
7. Pockley, A.G., Bulmer, J., Hanks, B.M. and Wright, B.H. (1999) Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals. Cell Stress Chaperones 4, 29-35 CrossRef PubMed
8. Pockley, A.G., Shepherd, J. and Corton, J. (1998) Detection of heat shock protein 70 (Hsp70) and anti-Hsp70 antibodies in the serum of normal individuals. Immunol. Invest. 27, 367-377 CrossRef PubMed
9. Chimini, C. and Rubartelli, A. (2005) Novel pathways of protein secretion. In Molecular Chaperones and Cell Signalling (Henderson, B. and Pockley, A.G., eds), pp. 45-60, Cambridge University Press, New York CrossRef
10. Gastpar, R., Gehrmann, M., Bausero, M.A., Asea, A., Gross, C., Schroeder, J.A. and Multhoff, G. (2005) Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 65, 5238-5247 CrossRef PubMed
11. Bausero, M.A., Gastpar, R., Multhoff, G. and Asea, A. (2005) Alternative mechanism by which IFN-γ enhances tumor recognition: active release of heat shock protein 72. J. Immunol. 175, 2900-2912 CrossRef PubMed
12. Broquet, A.H., Thomas, G., Masliah, J., Trugnan, G. and Bachelet, M. (2003) Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J. Biol. Chem. 278, 21601-21606 CrossRef PubMed
13. Mambula, S.S. and Calderwood, S.K. (2006) Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J. Immunol. 177, 7849-7857 CrossRef PubMed
14. Evdonin, A.L., Martynova, M.G., Bystrova, O.A., Guzhova, I.V., Margulis, B.A. and Medvedeva, N.D. (2006) The release of Hsp70 from A431 carcinoma cells is mediated by secretory-like granules. Eur. J. Cell Biol. 85, 443-455 CrossRef PubMed
15. Evdonin, A.L., Guzhova, I.V., Margulis, B.A. and Medvedeva, N.D. (2004) Phospholipase C inhibitor, U73122, stimulates release of hsp-70 stress protein from A431 human carcinoma cells. Cancer Cell Int. 4, 2 CrossRef PubMed
16. Frostegård, J. and Pockley, A.G. (2005) Heat shock protein release and naturally-occurring, exogenous heat shock proteins. In Molecular Chaperones and Cell Signalling (Henderson, B. and Pockley, A.G., eds), pp. 195-219, Cambridge University Press, Cambridge CrossRef
17. Hightower, L.E. and Guidon, P.T. (1989) Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J. Cell. Physiol. 138, 257-266 CrossRef PubMed
18. Tytell, M., Greenberg, S.G. and Lasek, R.J. (1986) Heat shock-like protein is transferred from glia to axon. Brain Res. 363, 161-164 CrossRef PubMed
19. Pockley, A.G. and Multhoff, G. (2008) Cell stress proteins in extracellular fluids: friend or foe? Novartis Found. Symp. 291, 86-95
20. Morton, H., Rolfe, B. and Clunie, G.J. (1977) An early pregnancy factor detected in human serum by the rosette inhibition test. Lancet 1, 394-397 CrossRef PubMed
21. Noonan, F.P., Halliday, W.J., Morton, H. and Clunie, G.J. (1979) Early pregnancy factor is immunosuppressive. Nature 278, 649-651 CrossRef PubMed
22. Cavanagh, A.C. and Morton, H. (1994) The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10. Eur. J. Biochem. 222, 551-560 CrossRef PubMed
23. Multhoff, G. and Hightower, L.E. (2011) Distinguishing integral and receptor-bound heat shock protein 70 (Hsp70) on the cell surface by Hsp70-specific antibodies. Cell Stress Chaperones 16, 251-255 CrossRef PubMed
24. Njemini, R., Demanet, C. and Mets, T. (2005) Comparison of two ELISAs for the determination of Hsp70 in serum. J. Immunol. Methods 306, 176-182 CrossRef PubMed
25. Pockley, A.G., de Faire, U., Kiessling, R., Lemne, C., Thulin, T. and Frostegård, J. (2002) Circulating heat shock protein and heat shock protein antibody levels in established hypertension. J. Hypertension 20, 1815-1820 CrossRef
26. Pockley, A.G. and Frostegård, J. (2005) Heat shock proteins in cardiovascular disease and the prognostic value of heat shock protein-related measurements. Heart 91, 1124-1126 CrossRef PubMed
27. Pockley, A.G., Georgiades, A., Thulin, T., de Faire, U. and Frostegård, J. (2003) Serum heat shock protein 70 levels predict the development of atherosclerosis in subjects with established hypertension. Hypertension 42, 235-238 CrossRef PubMed
28. Pockley, A.G., Wu, R., Lemne, C., Kiessling, R., de Faire, U. and Frostegård, J. (2000) Circulating heat shock protein 60 is associated with early cardiovascular disease. Hypertension 36, 303-307 CrossRef PubMed
29. Shamaei-Tousi, A., Stephens, J.W., Bin, R., Cooper, J.A., Steptoe, A., Coates, A.R., Henderson, B. and Humphries, S.E. (2006) Association between plasma levels of heat shock protein 60 and cardiovascular disease in patients with diabetes mellitus. Eur. Heart J. 27, 1565-1570 CrossRef PubMed
30. Molvarec, A., Rigo, Jr, J., Nagy, B., Walentin, S., Szalay, J., Fust, G., Karadi, I. and Prohászka, Z. (2007) Serum heat shock protein 70 levels are decreased in normal human pregnancy. J. Reprod. Immunol. 74, 163-169 CrossRef PubMed
31. Njemini, R., Lambert, M., Demanet, C. and Mets, T. (2003) Elevated serum heat-shock protein 70 levels in patients with acute infection: use of an optimized enzyme-linked immunosorbent assay. Scand. J. Immunol. 58, 664-669 CrossRef PubMed
32. Bayer, C., Liebhardt, M.E., Schmid, T.E., Trajkovic-Arsic, M., Hube, K., Specht, H.M., Schilling, D., Gehrmann, M., Stangl, S., Siveke, J.T., Wilkens, J.J. and Multhoff, G. (2014) Validation of heat shock protein 70 as a tumor-specific biomarker for monitoring the outcome of radiation therapy in tumor mouse models. Int. J. Radiat. Oncol. Biol. Phys. 88, 694-700 CrossRef PubMed
33. Gehrmann, M., Specht, H.M., Bayer, C., Brandstetter, M., Chizzali, B., Duma, M., Breuninger, S., Hube, K., Lehnerer, S., van Phi, V. et al. (2014) Hsp70: a biomarker for tumor detection and monitoring of outcome of radiation therapy in patients with squamous cell carcinoma of the head and neck. Radiat. Oncol. 9, 131 CrossRef PubMed
34. Gehrmann, M., Cervello, M., Montalto, G., Cappello, F., Gulino, A., Knape, C., Specht, H.M. and Multhoff, G. (2014) Heat shock protein 70 serum levels differ significantly in patients with chronic hepatitis, liver cirrhosis, and hepatocellular carcinoma. Front. Immunol. 5, 307 CrossRef PubMed
35. Dutta, S.K., Girotra, M., Singla, M., Dutta, A., Otis Stephen, F., Nair, P.P. and Merchant, N.B. (2012) Serum HSP70: a novel biomarker for early detection of pancreatic cancer. Pancreas 41, 530-534 CrossRef PubMed
36. Dakappagari, N., Neely, L., Tangri, S., Lundgren, K., Hipolito, L., Estrellado, A., Burrows, F. and Zhang, H. (2010) An investigation into the potential use of serum Hsp70 as a novel tumour biomarker for Hsp90 inhibitors. Biomarkers 15, 31-38 CrossRef PubMed
37. Kampinga, H.H., Hageman, J., Vos, M.J., Kubota, H., Tanguay, R.M., Bruford, E.A., Cheetham, M.E., Chen, B. and Hightower, L.E. (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14, 105-111 CrossRef PubMed
38. Murphy, M.E. (2013) The HSP70 family and cancer. Carcinogenesis 34, 1181-1188 CrossRef PubMed
39. - large granular lymphocytes recognize a heat-inducible immunogenic determinant associated with the 72-kD heat shock protein on human sarcoma cells. Blood 86, 1374-1382 PubMed
40. Multhoff, G., Botzler, C., Wiesnet, M., Muller, E., Meier, T., Wilmanns, W. and Issels, R.D. (1995) A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int. J. Cancer 61, 272-279 CrossRef PubMed
41. Stangl, S., Gehrmann, M., Riegger, J., Kuhs, K., Riederer, I., Sievert, W., Hube, K., Mocikat, R., Dressel, R., Kremmer, E. et al. (2011) Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc. Natl. Acad. Sci. U.S.A. 108, 733-738 CrossRef PubMed
42. Gehrmann, M., Pfister, K., Hutzler, P., Gastpar, R., Margulis, B. and Multhoff, G. (2002) Effects of antineoplastic agents on cytoplasmic and membrane-bound heat shock protein 70 (Hsp70) levels. Biol. Chem. 383, 1715-1725 PubMed
43. Gehrmann, M., Stangl, S., Kirschner, A., Foulds, G.A., Sievert, W., Doss, B.T., Walch, A., Pockley, A.G. and Multhoff, G. (2012) Immunotherapeutic targeting of membrane hsp70-expressing tumors using recombinant human granzyme B. PLoS ONE 7, e41341 CrossRef PubMed
44. Pfister, K., Radons, J., Busch, R., Tidball, J.G., Pfeifer, M., Freitag, L., Feldmann, H.J., Milani, V., Issels, R. and Multhoff, G. (2007) Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer 110, 926-935 CrossRef PubMed
45. Multhoff, G., Botzler, C., Jennen, L., Schmidt, J., Ellwart, J. and Issels, R. (1997) Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J. Immunol. 158, 4341-4350 PubMed
46. Gross, C., Koelch, W., DeMaio, A., Arispe, N. and Multhoff, G. (2003) Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J. Biol. Chem. 278, 41173-41181 CrossRef PubMed
47. Gehrmann, M., Doss, B.T., Wagner, M., Zettlitz, K.A., Kontermann, R.E., Foulds, G., Pockley, A.G. and Multhoff, G. (2011) A novel expression and purification system for the production of enzymatic and biologically active human granzyme B. J. Immunol. Methods 371, 8-17 CrossRef PubMed
48. Pockley, A.G. (2001) Heat shock proteins in health and disease: therapeutic targets or therapeutic agents? Exp. Rev. Mol. Med. 3, 1-21 CrossRef
49. Pockley, A.G. (2003) Heat shock proteins and their role as regulators of the immune response. Lancet 362, 469-476 CrossRef PubMed
50. Shamaei-Tousi, A., D'Aiuto, F., Nibali, L., Steptoe, A., Coates, A.R., Parkar, M., Donos, N. and Henderson, B. (2007) Differential regulation of circulating levels of molecular chaperones in patients undergoing treatment for periodontal disease. PLoS ONE 2, e1198 CrossRef PubMed
51. Lebherz-Eichinger, D., Ankersmit, H.J., Hacker, S., Hetz, H., Kimberger, O., Schmidt, E.M., Reiter, T., Horl, W.H., Haas, M., Krenn, C.G. and Roth, G.A. (2012) HSP27 and HSP70 serum and urine levels in patients suffering from chronic kidney disease. Clin. Chim. Acta 413, 282-286 CrossRef PubMed
52. Gruden, G., Bruno, G., Chaturvedi, N., Burt, D., Schalkwijk, C., Pinach, S., Stehouwer, C.D., Witte, D.R., Fuller, J.H. and Perin, P.C. (2008) Serum heat shock protein 27 and diabetes complications in the EURODIAB prospective complications study: a novel circulating marker for diabetic neuropathy. Diabetes 57, 1966-1970 CrossRef PubMed
53. Lewthwaite, J., Owen, N., Coates, A., Henderson, B. and Steptoe, A. (2002) Circulating human heat shock protein 60 in the plasma of British civil servants. Circulation 106, 196-201 CrossRef PubMed
54. Wright, B.H., Corton, J., El-Nahas, A.M., Wood, R.F.M. and Pockley, A.G. (2000) Elevated levels of circulating heat shock protein 70 (Hsp70) in peripheral and renal vascular disease. Heart Vessels 15, 18-22 CrossRef PubMed
55. Xu, Q., Schett, G., Perschinka, H., Mayr, M., Egger, G., Oberhollenzer, F., Willeit, J., Kiechl, S. and Wick, G. (2000) Serum soluble heat shock protein 60 is elevated in subjects with atherosclerosis in a general population. Circulation 102, 14-20 CrossRef PubMed
56. Schett, G., Metzler, B., Kleindienst, R., Amberger, A., Recheis, H., Xu, Q. and Wick, G. (1999) Myocardial injury leads to a release of heat shock protein (hsp) 60 and a suppression of the anti-hsp65 immune response. Cardiovasc. Res. 42, 685-695 CrossRef PubMed
57. Nahas, E.A., Nahas-Neto, J., Orsatti, C.L., Tardivo, A.P., Uemura, G., Peracoli, M.T. and Witkin, S.S. (2014) The 60-and 70-kDa heat-shock proteins and their correlation with cardiovascular risk factors in postmenopausal women with metabolic syndrome. Cell Stress Chaperones 19, 559-568 CrossRef PubMed
58. Halcox, J.P.J., Deanfield, J., Shamaei-Tousi, A., Henderson, B., Steptoe, A., Coates, A.R.M., Singhal, A. and Lucas, A. (2005) Circulating human heat shock protein 60 in the blood of healthy teenagers: a novel determinant of endothelial dysfunction and early vascular injury. Arterioscler Thromb. Vasc. Biol. 25, e141-e142 CrossRef PubMed
59. Anraku, I., Rajasuriar, R., Dobbin, C., Brown, R., Lewin, S.R. and Suhrbier, A. (2012) Circulating heat shock protein 60 levels are elevated in HIV patients and are reduced by anti-retroviral therapy. PLoS ONE 7, e45291 CrossRef PubMed
60. Rizzo, M., Cappello, F., Marfil, R., Nibali, L., Marino Gammazza, A., Rappa, F., Bonaventura, G., Galindo-Moreno, P., O'Valle, F., Zummo, G. et al. (2012) Heat-shock protein 60 kDa and atherogenic dyslipidemia in patients with untreated mild periodontitis: a pilot study. Cell Stress Chaperones 17, 399-407 CrossRef PubMed
61. Wu, C.T., Ou, L.S., Yeh, K.W., Lee, W.I. and Huang, J.L. (2011) Serum heat shock protein 60 can predict remission of flare-up in juvenile idiopathic arthritis. Clin. Rheumatol. 30, 959-965 CrossRef PubMed
62. Kimura, F., Itoh, H., Ambiru, S., Shimizu, H., Togawa, A., Yoshidome, H., Ohtsuka, M., Shimamura, F., Kato, A., Nukui, Y. and Miyazaki, M. (2004) Circulating heat-shock protein 70 is associated with postoperative infection and organ dysfunction after liver resection. Am. J. Surg. 187, 777-784 CrossRef PubMed
63. Dybdahl, B., Wahba, A., Lien, E., Flo, T.H., Waage, A., Qureshi, N., Sellevold, O.F., Espevik, T. and Sundan, A. (2002) Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through toll-like receptor-4. Circulation 105, 685-690 CrossRef PubMed
64. Zhu, J., Quyyumi, A.A., Wu, H., Csako, G., Rott, D., Zalles-Ganley, A., Ogunmakinwa, J., Halcox, J. and Epstein, S.E. (2003) Increased serum levels of heat shock protein 70 are associated with low risk of coronary artery disease. Arterioscler Thromb. Vasc. Biol. 23, 1055-1059 CrossRef PubMed
65. Kornej, J., Reinhardt, C., Kosiuk, J., Arya, A., Hindricks, G., Adams, V., Husser, D. and Bollmann, A. (2013) Response of circulating heat shock protein 70 and anti-heat shock protein 70 antibodies to catheter ablation of atrial fibrillation. J. Transl. Med. 11, 49 CrossRef PubMed
66. Krepuska, M., Szeberin, Z., Sotonyi, P., Sarkadi, H., Fehervari, M., Apor, A., Rimely, E., Prohászka, Z. and Acsady, G. (2011) Serum level of soluble Hsp70 is associated with vascular calcification. Cell Stress Chaperones 16, 257-265 CrossRef PubMed
67. Njemini, R., Smitz, J., Demanet, C., Sosso, M. and Mets, T. (2011) Circulating heat shock protein 70 (Hsp70) in elderly members of a rural population from Cameroon: association with infection and nutrition. Arch. Gerontol. Geriatr. 53, 359-363 CrossRef PubMed
68. Molvarec, A., Prohászka, Z., Nagy, B., Szalay, J., Fust, G., Karadi, I. and Rigo, Jr, J. (2006) Association of elevated serum heat-shock protein 70 concentration with transient hypertension of pregnancy, preeclampsia and superimposed preeclampsia: a case-control study. J. Hum. Hypertens. 20, 780-786 CrossRef PubMed
69. Molvarec, A., Szarka, A., Walentin, S., Beko, G., Karádi, I., Prohászka, Z. and Rigó, Jr, J. (2011) Serum heat shock protein 70 levels in relation to circulating cytokines, chemokines, adhesion molecules and angiogenic factors in women with preeclampsia. Clin. Chim. Acta 412, 1957-1962 CrossRef PubMed
70. Hou, C., Zhao, H., Li, W., Liang, Z., Zhang, D., Liu, L., Tong, W., Cai, S.X. and Zou, F. (2011) Increased heat shock protein 70 levels in induced sputum and plasma correlate with severity of asthma patients. Cell Stress Chaperones 16, 663-671 CrossRef PubMed
71. Pagetta, A., Folda, A., Brunati, A.M. and Finotti, P. (2003) Identification and purification from the plasma of Type 1 diabetic subjects of a proteolytically active Grp94: evidence that Grp94 is entirely responsible for plasma proteolytic activity. Diabetologia 46, 996-1006 CrossRef PubMed
72. 1-antitrypsin in plasma of Type 1 diabetic subjects. Biochem. Biophys. Res. Commun. 315, 297-305 CrossRef PubMed
73. Zhao, M., Ding, J.X., Zeng, K., Zhao, J., Shen, F., Yin, Y.X. and Chen, Q. (2014) Heat shock protein 27: a potential biomarker of peritoneal metastasis in epithelial ovarian cancer? Tumour Biol. 35, 1051-1056 CrossRef PubMed
74. Liebhardt, S., Ditsch, N., Nieuwland, R., Rank, A., Jeschke, U., Von Koch, F., Friese, K. and Toth, B. (2010) CEA-, Her2/neu-, BCRP-and Hsp27-positive microparticles in breast cancer patients. Anticancer Res. 30, 1707-1712 PubMed
75. Zimmermann, M., Nickl, S., Lambers, C., Hacker, S., Mitterbauer, A., Hoetzenecker, K., Rozsas, A., Ostoros, G., Laszlo, V., Hofbauer, H. et al. (2012) Discrimination of clinical stages in non-small cell lung cancer patients by serum HSP27 and HSP70: a multi-institutional case-control study. Clin. Chim. Acta 413, 1115-1120 CrossRef PubMed
76. Yeh, C.H., Tseng, R., Hannah, A., Estrov, Z., Estey, E., Kantarjian, H. and Albitar, M. (2010) Clinical correlation of circulating heat shock protein 70 in acute leukemia. Leuk. Res. 34, 605-609 CrossRef PubMed
77. Yeh, C.H., Tseng, R., Zhang, Z., Cortes, J., O'Brien, S., Giles, F., Hannah, A., Estrov, Z., Keating, M., Kantarjian, H. and Albitar, M. (2009) Circulating heat shock protein 70 and progression in patients with chronic myeloid leukemia. Leuk. Res. 33, 212-217 CrossRef PubMed
78. Rozenberg, P., Kocsis, J., Saar, M., Prohászka, Z., Fust, G. and Fishelson, Z. (2013) Elevated levels of mitochondrial mortalin and cytosolic HSP70 in blood as risk factors in patients with colorectal cancer. Int. J. Cancer 133, 514-518 CrossRef PubMed
79. Kocsis, J., Madaras, B., Toth, E.K., Fust, G. and Prohászka, Z. (2010) Serum level of soluble 70-kD heat shock protein is associated with high mortality in patients with colorectal cancer without distant metastasis. Cell Stress Chaperones 15, 143-151 CrossRef PubMed