Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages

Journal of Immunology

Volumn 180, Issue 6, 2008, Pages 4299-4307

  Vega, Virginia L ^a   Rodríguez Silva, Monica ^a   Frey, Tiffany ^b   Gehrmann, Mathias ^c   Diaz, Juan Carlos ^d   Steinem, Claudia ^e   Multhoff, Gabriele ^c   Arispe, Nelson ^d   De Maio, Antonio ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; ION CHANNEL; TUMOR NECROSIS FACTOR ALPHA; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; MEMBRANE PROTEIN; OCTOXINOL; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ARTICLE; CELL MEMBRANE; CELL STRESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNE SYSTEM; ION CONDUCTANCE; LIPID BILAYER; MACROPHAGE ACTIVATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; CELL LINE; DRUG ANTAGONISM; EXTRACELLULAR SPACE; IMMUNOLOGY; MACROPHAGE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PROTEIN TRANSPORT; SECRETION; SOLUBILITY; TUMOR CELL LINE;

BACTERIAL PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; EXTRACELLULAR SPACE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; ION CHANNELS; LIPID BILAYERS; LUMINESCENT PROTEINS; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE PROTEINS; OCTOXYNOL; OXIDATIVE STRESS; PROTEIN TRANSPORT; SOLUBILITY;

EID: 44849084963     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.6.4299     Document Type: Article

References (49)

1. De Maio, A. 1999. Heat shock proteins: facts, thoughts, and dreams. Shock 11: 1-12.
2. Campisi, J., T. H. Leem, and M. Fleshner. 2003. Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 8: 272-286.
3. Singh-Jasuja, H., N. Hilf, D. Arnold-Schild, and H. Schild. 2001. The role of heat shock proteins and their receptors in the activation of the immune system. Biol. Chem. 382: 629-636.
4. Srivastava, P. 2002. Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2: 185-194.
5. Asea, A., S. K. Kraeft, E. A. Kurt-Jones, M. A. Stevenson, L. B. Chen, R. W. Finberg, G. C. Koo, and S. K. Calderwood. 2000. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6: 435-442.
6. Basu, S., R. J. Binder, T. Ramalingam, and P. K. Srivastava. 2001. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14: 303-313.
7. Becker, T., F. U. Hartl, and F. Wieland. 2002. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell Biol. 158: 1277-1285.
8. Theriault, J. R., H. Adachi, and S. K. Calderwood. 2006. Role of scavenger receptors in the binding and internalization of heat shock protein 70. J. Immunol. 177: 8604-8611.
9. Wang, Y., C. G. Kelly, J. T. Karttunen, T. Whittall, P. J. Lehner, L. Duncan, P. MacAry, J. S. Younson, M. Singh, W. Oehlmann, et al. 2001. CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15: 971-983.
10. Gastpar, R., C. Gross, L. Rossbacher, J. Ellwart, J. Riegger, and G. Multhoff. 2004. The cell surface-localized heat shock protein 70 epitope TKD induces migration and cytolytic activity selectively in human NK cells. J. Immunol. 172: 972-980.
11. Basu, S., R. J. Binder, R. Suto, K. M. Anderson, and P. K. Srivastava. 2000. 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. Int. Immunol. 12: 1539-1546.
12. Hunter-Lavin, C., E. L. Davies, M. M. Bacelar, M. J. Marshall, S. M. Andrew, and J. H. Williams. 2004. Hsp70 release from peripheral blood mononuclear cells. Biochem. Biophys. Res. Comm. 324: 511-517.
13. Arispe, N., M. Doh, and A. De Maio. 2002. Lipid interaction differentiates the constitutve and stress-induced heat shock proteins Hsc70 and Hsp70. Cell Stress Chaperones 7: 330-338.
14. Arispe, N., M. Doh, O. Simakova, B. Kurganov, and A. De Maio. 2004. Hsc70 and Hsp70 interact with phosphatidylserine on the surface of PC12 cells resulting in a decrease of viability. FASEB J. 18: 1636-1645.
15. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. 1: 31-41.
16. Clayton, A., A. Turkes, H. Navabi, M. D. Mason, and Z. Tabi. 2005. Induction of heat shock proteins in B-cell exosomes. J. Cell Sci. 118: 3631-3638.
17. Gastpar, R., M. Gehrmann, M. A. Bausero, A. Asea, C. Gross, J. A. Schroeder, and G. Multhoff. 2005. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 65: 5238-5247.
18. Altin, J. G., and E. B. Pagler. 1995. A one-step procedure for biotinylation and chemical cross-linking of lymphocyte surface and intracellular membrane-associated molecules. Anal. Biochem. 224: 382-389.
19. Arispe, N., and A. De Maio. 2000. ATP and ADP modulate a cation channel formed by Hsc70 in acidic phospholipid membranes. J. Biol. Chem. 275: 30839-30843.
20. Zou, J., Y. Guo, T. Guettouche, D. F. Smith, and R. Voellmy. 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94: 471-480.
21. Vega, V. L., and A. De Maio. 2005. Increase in phagocytosis after geldanamycin treatment or heat shock: role of heat shock proteins. J. Immunol. 175: 5280-5287.
22. Tytell, M. 2005. Release of heat shock proteins (Hsps) and the effects of extracellular Hsps on neural cells and tissues. Int. J. Hyperthermia 21: 445-455.
23. Hightower, L. E., and P. T. Guidon. 1989. Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J. Cell. Physiol. 138: 257-266.
24. Lancaster, G. I., and M. A. Febbraio. 2005. Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J. Biol. Chem. 280: 23349-23355.
25. Mambula, S. S., and S. K. Calderwood. 2006. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J. Immunol. 177: 7849-7857.
26. Welch, W. J., and J. P. Suhan. 1985. Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J. Cell Biol. 101: 1198-1211.
27. Kurucz, I., B. Tombor, J. Prechl, F. Erdo, E. Hegedus, Z. Nagy, M. Vitai, L. Koranyi, and L. Laszlo. 1999. Ultrastructural localization of Hsp-72 examined with a new polyclonal antibody raised against the truncated variable domain of the heat shock protein. Cell Stress Chaperones 4: 139-152.
28. Multhoff, G., C. Botzler, M. Wiesnet, E. Muller, T. Meier, W. Wilmanns, and R. D. Issels. 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.
29. Arispe, N., E. Rojas, B. R. Genge, L. N. Y. Wu, and R. E. Wuthier. 1996. Similarity in calcium chennel activity of annexin V and matrix vesicles in planar lipid bilayers. Biophys. J. 71: 1764-1775.
30. Rojas, E., N. Arispe, H. T. Haigler, A. L. Burns, and H. B. Pollard. 1992. Identification of annexins as calcium channels in biological membranes. Bone Miner. 17: 214-218.
31. Arispe, N., E. Rojas, and H. B. Pollard. 1993. Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. USA 90: 567-571.
32. Schlossman, D. M., S. L. Schmid, W. A. Brael, and J. E. Rothman. 1984. An enzyme that removes clathrin coats: purification of an uncoating ATPase. J. Cell Biol. 99: 723-733.
33. Gao, B., E. Eisenberg, and L. Greene. 1996. Effect of constitutive 70-kDa heat shock protein polymerization on its interaction with protein substrate. J. Biol. Chem. 271: 16792-16797.
34. Fang, Y., N. Wu, X. Gan, W. Yan, J. C. Morrell, and S. J. Gould. 2007. Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol. 5: 158.
35. Broquet, A. H., G. Thomas, J. Masliah, G. Trugnan, and M. Bachele. 2003. Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J. Biol. Chem. 278: 21601-21606.
36. Triantafilou, M., K. Miyake, D. T. Golenbock, and K. Triantafilou. 2002. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115: 2603-2611.
37. Chen, S., D. Bawa, S. Besshoh, J. W. Gurd, and I. R. Brown. 2005. Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain. J. Neurosci. Res. 81: 522-529.
38. Wang, R., J. T. Kovalchin, P. Muhlenkamp, and R. Y. Chandawarkar. 2006. Exogenous heat shock protein 70 binds macrophage lipid raft microdomain and stimulates phagocytosis, processing, and MHC-II presentation of antigens. Blood 107: 1636-1642.
39. Radons, J., and G. Multhoff. 2005. Immunostimulatory functions of membrane-bound and exported heat shock protein 70. Exerc. Immunol. Rev. 11: 17-33.
40. Azuma, K., S. Shichijo, H. Takedatsu, N. Komatsu, H. Sawamizu, and K. Itoh. 2003. Heat shock cognate protein 70 encodes antigenic epitopes recognised by HLA-B4601-restricted cytotoxic T lymphocytes from cancer patients. Br. J. Cancer 89: 1079-1085.
41. Faure, O., S. Graff-Dubois, L. Bretaudeau, L. Derre, D. A. Gross, P. M. Alves, S. Cornet, M. T. Duffour, S. Chouaib, I. Miconnet, et al. 2004. Inducible Hsp70 as target of anticancer immunotherapy: identification of HLA-A*0201-restricted epitopes. Int. J. Cancer 108: 863-870.
42. Oglesbee, M. J., A. V. Herdman, G. G. Passmore, and W. H. Hoffman. 2005. Diabetic ketoacidosis increases extracellular levels of the major inducible 70-kDa heat shock protein. Clin. Biochem. 38: 900-904.
43. Zhu, J., A. A. Quyyumi, H. Wu, G. Csako, D. Rott, A. Zalles-Ganley, J. Ogunmakinwa, J. Halcox, and S. E. Epstein. 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.
44. Genth-Zotz, S., A. P. Bolger, P. R. Kalra, S. von Haehling, W. Doehner, A. J. Coats, H. D. Volk, and S. D. Anker. 2004. Heat shock protein 70 in patients with chronic heart failure: relation to disease severity and survival. Int. J. Cardiol. 96: 397-401.
45. Dybdahl, B., S. A. Slordahl, A. Waage, P. Kierulf, T. Espevik, and A. Sundan. 2005. Myocardial ischaemia and the inflammatory response: release of heat shock protein 70 after myocardial infarction. Heart 91: 299-304.
46. Pittet, J. F., H. Lee, D. Morabito, M. B. Howard, W. J. Welch, and R. C. Mackersie. 2002. Serum levels of Hsp 72 measured early after trauma correlate with survival. J. Trauma 52: 611-617.
47. Feder, J. H., J. M. Rossi, J. Solomon, N. Solomon, and S. Lindquist. 1992. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 6: 1402-1413.
48. Shi, Y., D. D. Mosser, and R. I. Morimoto. 1998. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12: 654-666.
49. Theodorakis, N. G., D. Drujan, and A. De Maio. 1999. Thermotolerant cells show an attenuated expression of Hsp70 after heat shock. J. Biol. Chem. 274: 12081-12086.