Peptides modulating conformational changes in secreted chaperones: From in silico design to preclinical proof of concept

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 33, 2009, Pages 13797-13801

  Kliger, Yossef ^a   Levy, Ofer ^a   Oren, Anat ^a   Ashkenazy, Haim ^a,b   Tiran, Zohar ^a   Novik, Amit ^a   Rosenberg, Avi ^a   Amir, Anat ^a   Wool, Assaf ^a   Toporik, Amir ^a   Schreiber, Ehud ^a   Eshel, Dani ^a   Levine, Zurit ^a   Cohen, Yossi ^a   Nold Petry, Claudia ^a,c   Dinarello, Charles A ^c   Borukhov, Itamar ^a  

^a Compugen Ltd ^*  (Israel)

^b BAR ILAN UNIVERSITY   (Israel)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Cancer; Contact map prediction; Cytokines; Helix; Inflammation

Indexed keywords

CHAPERONE; CLUSTERIN; GLYCOPROTEIN GP 96; PEPTIDE;

ARTICLE; COMPUTER MODEL; FOURIER TRANSFORMATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; CLUSTERIN; COMPUTATIONAL BIOLOGY; FEMALE; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTES, MONONUCLEAR; MEMBRANE GLYCOPROTEINS; MICE; MICE, NUDE; MOLECULAR CHAPERONES; NEOPLASM TRANSPLANTATION; PEPTIDES; PROTEIN CONFORMATION; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 69549131215     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906514106     Document Type: Article

References (60)

1. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118.
2. Hayouka Z, et al. (2007) Inhibiting HIV-1 integrase by shifting its oligomerization equilibrium. Proc Natl Acad Sci USA 104:8316-8321. (Pubitemid 47175485)
3. Yin H, et al. (2007) Computational design of peptides that target transmembrane helices. Science 315:1817-1822. (Pubitemid 46580135)
4. Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823-832. (Pubitemid 23159019)
5. Jones PL, Korte T, Blumenthal R (1998) Conformational changes in cell surface HIV-1 envelope glycoproteins are triggered by cooperation between cell surface CD4 and co-receptors. J Biol Chem 273:404-409. (Pubitemid 28042225)
6. Lambert DM, et al. (1996) Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc Natl Acad Sci USA 93:2186-2191.
7. Rapaport D, Ovadia M, Shai Y (1995) A synthetic peptide corresponding to a conserved heptad repeat domain is a potent inhibitor of Sendai virus-cell fusion: An emerging similarity with functional domains of other viruses. EMBO J 14:5524-5531.
8. Wild CT, Shugars DC, Greenwell TK, McDanal CB, Matthews TJ (1994) Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc Natl Acad Sci USA 91:9770-9774.
9. Lalezari JP, et al. (2003) Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in North and South America. N Engl J Med 348:2175-2185.
10. Lazzarin A, et al. (2003) Efficacy of enfuvirtide in patients infected with drug-resistant HIV-1 in Europe and Australia. N Engl J Med 348:2186-2195. (Pubitemid 36618129)
11. Calderwood SK, Mambula SS, Gray PJ, Jr (2007) Extracellular heat shock proteins in cell signaling and immunity. Ann NY Acad Sci 1113:28-39.
12. Ni M, Lee AS (2007) ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641-3651. (Pubitemid 47082516)
13. Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C (2007) Intracellular and extracellular functions of heat shock proteins: Repercussions in cancer therapy. J Leukoc Biol 81:15-27. (Pubitemid 46021247)
14. So A, Hadaschik B, Sowery R, Gleave M (2007) The role of stress proteins in prostate cancer. Curr Genomics 8:252-261. (Pubitemid 47240702)
15. Yang Y, et al. (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26:215-226. (Pubitemid 46329432)
16. Lakins JN, et al. (2002) Evidence that clusterin has discrete chaperone and ligand binding sites. Biochemistry 41:282-291.
17. Yang CR, et al. (1999) Isolation of Ku70-binding proteins (KUBs). Nucleic Acids Res 27:2165-2174.
18. Ashkenazy H, Unger R, Kliger Y (2009) Optimal data collection for correlated mutation analysis. Proteins 74:545-555.
19. Cheng J, Baldi P (2007) Improved residue contact prediction using support vector machines and a large feature set. BMC Bioinformatics 8:113. (Pubitemid 46605894)
20. Gobel U, Sander C, Schneider R, Valencia A (1994) Correlated mutations and residue contacts in proteins. Proteins 18:309-317. (Pubitemid 24111530)
21. Pazos F, Olmea O, Valencia A (1997) A graphical interface for correlated mutations and other protein structure prediction methods. Comput Appl Biosci 13:319-321. (Pubitemid 27249940)
22. Shackelford G, Karplus K (2007) Contact prediction using mutual information and neural nets. Proteins 69:159-164. (Pubitemid 350210123)
23. Eisenberg D, Weiss RM, Terwilliger TC (1984) The hydrophobic moment detects periodicity in protein hydrophobicity. Proc Natl Acad Sci USA 81:140-144. (Pubitemid 14180843)
24. Bailey RW, Dunker AK, Brown CJ, Garner EC, Griswold MD (2001) Clusterin, a binding protein with a molten globule-like region. Biochemistry 40:11828-11840.
25. Sastry S, Linderoth N (1999) Molecular mechanisms of peptide loading by the tumor rejection antigen/heat shock chaperone gp96 (GRP94). J Biol Chem 274:12023-12035. (Pubitemid 129518464)
26. Liu B, et al. (2006) TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J Immunol 177:6880-6888. (Pubitemid 44715053)
27. Biroccio A, D'Angelo C, Jansen B, Gleave ME, Zupi G (2005) Antisense clusterin oligodeoxynucleotides increase the response of HER-2 gene amplified breast cancer cells to Trastuzumab. J Cell Physiol 204:463-469. (Pubitemid 40934641)
28. Miyake H, et al. (2004) Synergistic antitumor activity by combined treatment with gemcitabine and antisense oligodeoxynucleotide targeting clusterin gene in an intravesical administration model against human bladder cancer kotcc-1 cells. J Urol 171:2477-2481. (Pubitemid 38625518)
29. Miyake H, Yamanaka K, Muramaki M, Hara I, Gleave ME (2005) Therapeutic efficacy of adenoviral-mediated p53 gene transfer is synergistically enhanced by combined use of antisense oligodeoxynucleotide targeting clusterin gene in a human bladder cancer model. Neoplasia 7:171-179. (Pubitemid 40315994)
30. So A, Sinnemann S, Huntsman D, Fazli L, Gleave M (2005) Knockdown of the cytoprotective chaperone, clusterin, chemosensitizes human breast cancer cells both in vitro and in vivo. Mol Cancer Ther 4:1837-1849. (Pubitemid 43056967)
31. Yamanaka K, Gleave M, Muramaki M, Hara I, Miyake H (2005) Enhanced radiosensitivity by inhibition of the anti-apoptotic gene clusterin using antisense oligodeoxynucleotide in a human bladder cancer model. Oncol Rep 13:885-890.
32. Cheng J, Sweredoski MJ, Baldi P (2005) Accurate prediction of protein disordered regions by mining protein structure data. Data Min Knowl Disc 11:213-222.
33. Lu M, Blacklow SC, Kim PS (1995) A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat Struct Biol 2:1075-1082.
34. Toshchakov VU, Basu S, Fenton MJ, Vogel SN (2005) Differential involvement of BB loops of toll-IL-1 resistance (TIR) domain-containing adapter proteins in TLR4-versus TLR2-mediated signal transduction. J Immunol 175:494-500. (Pubitemid 40884354)
35. Toshchakov VY, Fenton MJ, Vogel SN (2007) Cutting Edge: Differential inhibition of TLR signaling pathways by cell-permeable peptides representing BB loops of TLRs. J Immunol 178:2655-2660.
36. Toshchakov VY, Vogel SN (2007) Cell-penetrating TIR BB loop decoy peptides a novel class of TLR signaling inhibitors and a tool to study topology of TIR-TIR interactions. Expert Opin Biol Ther 7:1035-1050.
37. Liu B, et al. (2003) Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc Natl Acad Sci USA 100:15824-15829. (Pubitemid 38021074)
38. Binder RJ, Srivastava PK (2004) Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci USA 101:6128-6133.
39. De Filippo A, et al. (2008) Human plasmacytoid dendritic cells interact with gp96 via CD91 and regulate inflammatory responses. J Immunol 181:6525-6535.
40. Binder RJ, Kelly JB, III, Vatner RE, Srivastava PK (2007) Specific immunogenicity of heat shock protein gp96 derives from chaperoned antigenic peptides and not from contaminating proteins. J Immunol 179:7254-7261.
41. Bolhassani A, Rafati S (2008) Heat-shock proteins as powerful weapons in vaccine development. Expert Rev Vaccines 7:1185-1199.
42. Li Z, Dai J, Zheng H, Liu B, Caudill M (2002) An integrated view of the roles and mechanisms of heat shock protein gp96-peptide complex in eliciting immune response. Front Biosci 7:d731-751.
43. Murshid A, Gong J, Calderwood SK (2008) Heat-shock proteins in cancer vaccines: Agents of antigen cross-presentation. Expert Rev Vaccines 7:1019-1030.
44. Pilla L, et al. (2006) A phase II trial of vaccination with autologous, tumor-derived heat-shock protein peptide complexes Gp96, in combination with GM-CSF andinterferon-alpha in metastatic melanoma patients. Cancer Immunol Immunother 55:958-968. (Pubitemid 43673585)
45. Zhang H, et al. (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7:909-915. (Pubitemid 41486292)
46. Miyake H, et al. (2005) Enhanced expression of the secreted form of clusterin following neoadjuvant hormonal therapy as a prognostic predictor in patients undergoing radical prostatectomy for prostate cancer. Oncol Rep 14:1371-1375.
47. Andersen CL, et al. (2007) Clusterin expression in normal mucosa and colorectal cancer. Mol Cell Proteomics 6:1039-1048. (Pubitemid 47019405)
48. July LV, et al. (2004) Nucleotide-based therapies targeting clusterin chemosensitize humanlung adenocarcinoma cells both in vitro and in vivo. Mol Cancer Ther 3:223-232.
49. Gleave M, Miyake H (2005) Use of antisense oligonucleotides targeting the cytoprotective gene, clusterin, to enhance androgen- and chemo-sensitivity in prostate cancer. World J Urol 23:38-46. (Pubitemid 40430679)
50. Chi KN, et al. (2005) A phase I pharmacokinetic and pharmacodynamic study of OGX-011, a 2′-methoxyethyl antisense oligonucleotide to clusterin, in patients with localized prostate cancer. J Natl Cancer Inst 97:1287-1296.
51. Chi KN, et al. (2008) A phase I study of OGX-011, a 2′-methoxyethyl phosphorothioate antisense to clusterin, in combination with docetaxel in patients with advanced cancer. Clin Cancer Res 14:833-839. (Pubitemid 351231167)
52. Blumenthal R, Sarkar DP, Durell S, Howard DE, Morris SJ (1996) Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J Cell Biol 135:63-71. (Pubitemid 26337737)
53. Gallo SA, et al. (2006) Kinetic studies of HIV-1 and HIV-2 envelope glycoprotein-mediated fusion. Retrovirology 3:90.
54. Fan H, Kashi RS, Middaugh CR (2006) Conformational lability oftwomolecular chaperones Hsc70 and gp96: Effects of pH and temperature. Arch Biochem Biophys 447:34-45. (Pubitemid 43319264)
55. Hochgrebe T, Pankhurst GJ, Wilce J, Easterbrook-Smith SB (2000) pH-dependent changes in the in vitro ligand-binding properties and structure of human clusterin. Biochemistry 39:1411-1419. (Pubitemid 30090710)
56. Lawless MK, et al. (1996) HIV-1 membrane fusion mechanism: Structural studies of the interactions between biologically-active peptides from gp41. Biochemistry 35:13697-13708.
57. Liu S, et al. (2007) HIV gp41 C-terminal heptad repeat contains multifunctional domains. Relation to mechanisms of action of anti-HIV peptides. J Biol Chem 282:9612-9620.
58. Lee JE, et al. (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177-182.
59. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109-113.
60. Sobolev V, Sorokine A, Prilusky J, Abola EE, Edelman M (1999) Automated analysis of interatomic contacts in proteins. Bioinformatics 15:327-332. (Pubitemid 29213759)