Advanced search
Publication Cover
International Journal of Hyperthermia Volume 18, 2002 - Issue 6: Hyperthermia and the Immune System
Submit an article Journal homepage
192
Views
18
CrossRef citations to date
0
Altmetric
Research Article

The heat shock protein Gp96 links innate and specific immunity

N. Hilf Department of Immunology, University of Tübingen, Auf der Morgenstelle 15, 72076 Tübingen, Germany
,
H. Singh-Jasuja Department of Immunology, University of Tübingen, Auf der Morgenstelle 15, 72076 Tübingen, Germany; Immatics Biotechnologies GmbH, Tübingen, Germany
&
H. Schild Department of Immunology, University of Tübingen, Auf der Morgenstelle 15, 72076 Tübingen, Germany
Pages 521-533 | Published online: 09 Jul 2009

  • Lindquist S. The heat-shock response. Amu Rev Biochem 1986; 55: 1151-91.
  • Bukau B, Deuerling E, Pfund C, Craig EA. Getting newly synthesized proteins into shape. Cell 2000; 101: 119-22.
  • Gupta RS. Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. MoI Biol Evol 1995; 12: 1063-73.
  • Larreta R, So to M, Alonso C, Requena JM. Leishmania infantum: gene cloning of the GRP94 homologue, its expression as recombinant protein, and analysis of antigenicity. Exp Parasitai 2000; 96: 108-15.
  • Stebbins CE, Russo AA, Schneider C, Rosen N, Haiti FU, Pavletich NP. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumour agent. Cell 1997; 89: 239-50.
  • Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997; 90: 65-75.
  • Nemoto T, Ohara-Nemoto Y, Ota M, Takagi T, Yokoyama K. Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur J Biochem 1995; 233: 1-8.
  • Wearsch PA, Nicchitta CV. Endoplasmic reticulum chaperone GRP94 subunit assembly is regulated through a defined oligomerization domain. Biochemistry 1996; 35: 16760-9.
  • Chadli A, Ladjimi MM, Baulieu EE, Catelli MG. Heat-induced oligomerization of the molecular chaperone Hsp90. Inhibition by ATP and geldanamycin and activation by transition metal oxyanions. J Biol Chem 1999; 274: 4133-9.
  • Wearsch PA, Voglino L, Nicchitta CV. Structural transitions accompanying the activation of peptide binding to the endoplasmic reticulum Hsp90 chaperone GRP94. Biochemistry 1998; 37: 5709-19.
  • Jakob U, Lilie H, Meyer I, Buchner J. Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo. J Biol Chem 1995; 270: 7288-94.
  • Melnick J, Aviel S, Argon Y. The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J Biol Chem 1992; 267: 21303-6.
  • Schaiff WT, Hruska KA, Jr., McCourt DW, Green M, Schwarte BD. HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells. J Exp Med 1992; 176: 657-66.
  • Chavany C, Mimnaugh E, Miller P, Bitton R, Nguyen P, Trepel J, Whitesell L, Schnur R, Moyer J, Neckers L. p185erbB2 binds to GRP94 in vivo. Dissociation of the p185erbB2/ GRP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185erbB2. J Biol Chem 1996; 271: 4974-7.
  • Melnick J, DuI JL, Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 1994; 370: 373-5.
  • Randow F, Seed B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nature Cell Biology 2001; 3: 891-6.
  • Stoilova D, Dai J, de Crom R, van Harperen R, Li Z. Haplosufficiency or functional redundancy of a heat shock protein gp96 gene in the adoptive immune response [abstract]. Cell Stress Chaperones 2000; 5: 395.
  • Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci USA 1994; 91: 8324-8.
  • Obermann WM, Sondermann H, Russo AA, Pavletich NP, Haiti FU. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 1998; 143: 901-10.
  • Prodromou C, Panaretou B, Chohan S, Siligardi G, O'Brien R, Ladbury JE, et al. The ATPase cycle of hsp90 drives a molecular 'clamp' via transient dimerization of the Nterminal domains. EMBO J 2000; 19: 4383-92.
  • Blachere NE, Li Z, Chandawarkar RY, Suto R, Jaikaria NS, Basu S, et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumour immunity. J Exp Med 1997; 186: 1315-22.
  • Wassenberg JJ, Reed RC, Nicchitta CV. Ligand interactions in the adenosine nucleotidebinding domain of the Hsp90 chaperone, GRP94. II. Ligand-mediated activation of GRP94 molecular chaperone and peptide binding activity. / Biol Chem 2000; 275: 22806-14.
  • Rosser MF, Nicchitta CV. Ligand interactions in the adenosine nucleotide-binding domain of the Hsp90 chaperone, GRP94. I. Evidence for allosteric regulation of ligand binding. J Biol Chem 2000; 275: 22798-805.
  • Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996; 272: 1606-14.
  • Nieland TJ, Tan MC, Monne-van MM, Koning F, Kruisbeek AM, van Bleek GM. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc Natl AcadSci USA 1996; 93: 6135-9.
  • Breloer M, Marti T, Fleischer B, von Bonin A. Isolation of processed, H-2Kb-binding ovalbumin-derived peptides associated with the stress proteins HSP70 and gp96. Eur J Immunol 1998; 28: 1016-21.
  • Ishii T, Udono H, Yamano T, Ohta H, Uenaka A, Ono T, Hituta A, Tanaka N, Srivastava PK, Nakagama E. Isolation of MHC class !-restricted tumour antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J Immunol 1999; 162: 1303-9.
  • Spee P, Neefjes J. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur J Immunol 1997; 27: 2441-9.
  • Linderoth NA, Popowicz A, Sastry S. Identification of the peptide-binding site in the heat shock chaperone/tumour rejection antigen gp96 (Grp94). J Biol Chem 2000; 275: 5472-7.
  • Scheibel T, Weikl T, Buchner J. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc Natl Acad Sd USA 1998; 95: 1495-9.
  • Arnold D, Wahl C, Faath S, Rammensee HG, Schild H. Influences of transporter associated with antigen processing (TAP) on the repertoire of peptides associated with the endoplasmic reticulum-resident stress protein gp96. J Exp Med 1997; 186: 461-6.
  • Lammert E, Arnold D, Nijenhuis M, Momburg F, Hammerling GJ, Brunner J, Stevanovic S, Rammensee HG, Schild H. The endoplasmic reticulum-resident stress protein gp96 binds peptides translocated by TAP. Eur J Immunol 1997; 27: 923-7.
  • Spee P, Subjeck J, Neefjes J. Identification of novel peptide binding proteins in the endoplasmic reticulum: ERp72, calnexin, and grp170. Biochemistry 1999; 38: 10559-66.
  • Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 1994; 39: 93-8.
  • Binder RJ, Blachere NE, Srivastava PK. Heat shock protein-chaperoned peptides but not free peptides introduced into the cytosol are presented efficiently by major histocompatibility complex I molecules. / Biol Chem 2001; 276: 17163-71.
  • Menoret A, Li Z, Niswonger ML, Altmeyer A, Srivastava PK. An endoplasmic reticulum protein implicated in chaperoning peptides to major histocompatibility of class I is an aminopeptidase. J Biol Chem 2001; 276: 33313-8.
  • Srivastava PK, Menoret A, Basu S, Binder RJ, McQuade KL. Heat shock proteins come of age: primitive functions acquire new roles in an adaptive world. Immunity 1998; 8: 65765.
  • Tamura Y, Peng P, Liu K, Daou M, Srivastava PK. Immunotherapy of tumours with au to logo us tumour-derived heat shock protein preparations. Science 1997; 278: 117-20.
  • Udono H, Srivastava PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med 1993; 178: 1391-6.
  • Udono H, Srivastava PK. Comparison of tumour-specific immunogenicities of stressinduced proteins gp96, hsp90, and hsp70. J Immunol 1994; 152: 5398-403.
  • Basu S, Srivastava PK. Calreticulin, a peptide-binding chaperone of the endoplasmic reticulum, elicits tumour- and peptide-specific immunity. / Exp Med 1999; 189: 797802.
  • Nair S, Wearsch PA, Mitchell DA, Wassenberg JJ, Gilboa E, Nicchitta CV. Calreticulin displays in vivo peptide-binding activity and can elicit CTL responses against bound peptides. / Immunol 1999; 162: 6426-32.
  • Wang XY, Kazim L, Repasky EA, Subjeck JR. Characterization of heat shock protein 110 and glucose-regulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine activity. J Immunol 2001; 166: 490-7.
  • Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Palendran B, Palucka K, Ricciardi-Castagnoli P, Neefjes J, Rammensee HG, Arnold-Schild D, Schild H. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767-811.
  • Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 1995; 269: 1585-8.
  • Singh-Jasuja H, Toes RE, Spee P, Munz C, Hilf N, Schoenberger SP, Germain RN. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. / Exp Med 2000; 191: 1965-74.
  • Castellino F, Boucher PE, Eichelberg K, Mayhew M, Rothman JE, Houghton AN, Germain, RN. Receptor-mediated uptake of Antigen/Heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J Exp Med 2000; 191: 1957-64.
  • Nicchitta CV. Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96. Curr Opin Immunol 1998; 10: 103-9.
  • Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med 1995; 182: 885-9.
  • Sevan MJ. Minor H antigens introduced on H-2 different stimulating cells cross-react at the cytotoxic T cell level during in vivo priming. / Immunol 1976; 117: 2233-8.
  • Sigal LJ, Crotty S, Andino R, Rock KL. Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 1999; 398: 77-80.
  • Lammert E, Stevanovic S, Brunner J, Rammensee HG, Schild H. Protein disulfide isomerase is the dominant acceptor for peptides translocated into the endoplasmic reticulum. Eur J Immunol 1997; 27: 1685-90.
  • Spee P, Neefjes J. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Ew J Immunol 1997; 27: 2441-9.
  • Singh-Jasuja H, HiIf N, Scherer HU, Arnold-Schild D, Rammensee HG, Toes RE, Schild H. The heat shock protein gp96: a receptor-targeted cross-priming carrier and activator of dendritic cells. Cell Stress Chaperones 2000; 5: 462-70.
  • Arnold-Schild D, Hanau D, Spehner D, Schmid C, Rammensee HG, de la Salle H, Schild H. Cutting edge: receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J Immunol 1999; 162: 3757-60.
  • Wassenberg JJ, Dezfulian C, Nicchitta CV. Receptor mediated and fluid phase pathways for internalization of the ER Hsp90 chaperone GRP94 in murine macrophages. / Cell Sd 1999; 112:2167-75.
  • Binder RJ, Han DK, Srivastava PK. CD91: a receptor for heat shock protein gp96. Nature Immunology 2000; 1: 151-5.
  • Basu S, Binder RJ, Ramalingam T, Srivastava PK. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 2001; 14: 303-13.
  • Strickland DK, Kounnas MZ, Argraves WS. LDL receptor-related protein: a multiligand receptor for lipoprotein and proteinase catabolism. FASEB J 1995; 9: 890-8.
  • Binder RJ, Karimeddirri D, Srivastava PK. Adjuvanticity of alpha 2-macroglobulin, an independent ligand for the heat shock protein receptor CD91. J Immunol 2001; 166: 4968-72.
  • Rodriguez A, Regnault A, Kleijmeer M, Ricciardi-Castagnnoli P, Amigorena S. Selective transport of internalized aantigens to the cytosol for MHC class I presentation in dendritic cells. Nature Cell Biology 1999; 1: 362-8.
  • Watts TH, DeBenedette MA. T cell co-stimulatory molecules other than CD28. Curr Opin Immunol 1999; 11:286-93.
  • Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumour cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. JExp Med 2000; 191: 423-34.
  • KoI A, Lichtman AH, Finberg RW, Libby P, Kurt-Jones EA. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD 14 is an essential receptor for HSP60 activation of mononuclear cells. J Immunol 2000; 164: 13-7.
  • Ohashi K, Burkart V, Flohe S, KoIb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 2000; 164: 558-61.
  • Singh-Jasuja H, Scherer HU, HiIfN, Arnold-Schild D, Rammensee HG, Toes RE, Schild H. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur J Immunol 2000; 30: 2211-5.
  • Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappaB pathway. Int Immunol 2000; 12: 1539-46.
  • Braedel S, Vabulas RM, Hilf N, Singh-Jasuja H, Herter S, Ahmad-Nejad P, Kirschning CJ, da Costa CP, Rammensee HG, Wagner H, Schild H. The endoplasmic reticulumresident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 2002; 277: 20847-53.
  • Vabulas RM, Ahmad-Nejad P, da Costa C, Miethke T, Kirschning CJ, Hacker H, Wagner H. Endocytosed HSPoOs use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 2001; 276: 31332-9.
  • Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfore A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002; 195: 559-70.
  • Hilf N, Singh-Jasuja H, Schwarzmaier P, Gouttefangeas C, Rammensee H, Schild H. Human platelets express heat shock protein receptors and regulate dendritic cell maturation. Blood 2002; 99: 3676-82.
  • Pouyssegur J, Yamada KM. Isolation and immunological characterization of a glucoseregulated nbroblast cell surface glycoprotein and its nonglycosylated precursor. Cell 1978; 13: 139-40.
  • Berwin B, Reed RC, Nicchitta CV. Vitally induced lytic cell death elicits the release of immunogenic GRP94/gp96. J Biol Chem 2001; 276: 21083-8.
  • Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000; 405: 85-90.
  • Albert ML, Pearce SF, Francisco LM, Sauter B, Roy P, Silverstein RL, Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 1998; 188: 1359-68.
  • Devitt A, Moffatt OD, Raykundalia C, Capra JD, Simmons DL, Gregory CD. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 1998; 392: 505-9.
  • Schild H, Rammensee HG. gp96-the immune system's Swiss army knife. Nat Immunol 2000; 1: 100-1.

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.