Targeting heat shock proteins in cancer

Cancer Letters

Volumn 332, Issue 2, 2013, Pages 275-285

  Jego, Gaëtan ^a,b   Hazoumé, Adonis ^a   Seigneuric, Renaud ^a,b,c   Garrido, Carmen ^a  

^a Chu   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c LABORATOIRE INTERDISCIPLINAIRE CARNOT DE BOURGOGNE   (France)

Author keywords

Apoptosis; Cancer cell growth; Cancer cell resistance; Heat shock proteins; Immunogenicity

Indexed keywords

1 ETHYL 2 [[3 ETHYL 5 (3 METHYLBENZOTHIAZOLIN 2 YLIDENE) 4 OXOTHIAZOLIDIN 2 YLIDENE]METHYL]PYRIDINIUM CHLORIDE; 2 PHENYLETHYNESULFONAMIDE; 3 (5 CHLORO 2,4 DIHYDROXYPHENYL) N ETHYL 4 (4 METHOXYPHENYL) 5 PYRAZOLECARBOXAMIDE; 4 [4 (1,4 BENZODIOXAN 6 YL) 5 METHYL 1H PYRAZOL 3 YL] 6 ETHYLRESORCINOL; ALVESPIMYCIN; ANTINEOPLASTIC AGENT; APOPTOSIS INDUCING FACTOR DERIVED DECOY FOR HEAT SHOCK PROTEIN 70; ARSENIC TRIOXIDE; BIIB 021; CNF 2024; GELDANAMYCIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 CLIENT PROTEIN; HEAT SHOCK PROTEIN 90 INHIBITOR; IMATINIB; MAL 3 101; NOVOBIOCIN; OGX 427; ONCOPROTEIN; PU DZ 8; PU H 71; RETASPIMYCIN; SHEPHERIDIN; SNX 5422; TANESPIMYCIN; TRASTUZUMAB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VER 155008;

AMINO TERMINAL ATPASE DOMAIN; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CHRONIC MYELOID LEUKEMIA; COLON CANCER; DRUG BIOAVAILABILITY; DRUG DOSE ESCALATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; GASTROINTESTINAL STROMAL TUMOR; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; INTRACELLULAR SIGNALING; KIDNEY DYSFUNCTION; LEUKEMIA; LUNG NON SMALL CELL CANCER; LYMPHOMA; MALIGNANT NEOPLASTIC DISEASE; MEDULLOBLASTOMA; MELANOMA; METASTASIS; MOLECULARLY TARGETED THERAPY; NONHUMAN; PANCREAS CANCER; PEPTIDE BINDING DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TARGETING; SOLID TUMOR; TRIPLE NEGATIVE BREAST CANCER; UNSPECIFIED SIDE EFFECT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; NEOPLASMS; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84876084273     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.10.014     Document Type: Article

References (103)

1. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 2004, 5:781-791.
2. Bruey J.M., Ducasse C., Bonniaud P., Ravagnan L., Susin S.A., Diaz-Latoud C., Gurbuxani S., Arrigo A.P., Kroemer G., Solary E., Garrido C. Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2000, 2:645-652.
3. Garrido C., Brunet M., Didelot C., Zermati Y., Schmitt E., Kroemer G. Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 2006, 5:2592-2601.
4. Ravagnan L., Gurbuxani S., Susin S.A., Maisse C., Daugas E., Zamzami N., Mak T., Jaattela M., Penninger J.M., Garrido C., Kroemer G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol. 2001, 3:839-843.
5. Lanneau D., de Thonel A., Maurel S., Didelot C., Garrido C. Apoptosis versus cell differentiation: role of heat shock proteins HSP90, HSP70 and HSP27. Prion 2007, 1:53-60.
6. Parcellier A., Brunet M., Schmitt E., Col E., Didelot C., Hammann A., Nakayama K., Nakayama K.I., Khochbin S., Solary E., Garrido C. HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells. Faseb J. 2006, 20:1179-1181.
7. Calderwood S.K., Khaleque M.A., Sawyer D.B., Ciocca D.R. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci. 2006, 31:164-172.
8. Stebbins C.E., Russo A.A., Schneider C., Rosen N., Hartl F.U., Pavletich N.P. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 1997, 89:239-250.
9. Onuoha S.C., Coulstock E.T., Grossmann J.G., Jackson S.E. Structural studies on the co-chaperone Hop and its complexes with Hsp90. J. Mol. Biol. 2008, 379:732-744.
10. Zhang Y., Kwon S., Yamaguchi T., Cubizolles F., Rousseaux S., Kneissel M., Cao C., Li N., Cheng H.L., Chua K., Lombard D., Mizeracki A., Matthias G., Alt F.W., Khochbin S., Matthias P. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol. Cell Biol. 2008, 28:1688-1701.
11. Taherian A., Krone P.H., Ovsenek N. A comparison of Hsp90alpha and Hsp90beta interactions with cochaperones and substrates. Biochem. Cell Biol. 2008, 86:37-45.
12. Chadli A., Felts S.J., Toft D.O. GCUNC45 is the first Hsp90 co-chaperone to show alpha/beta isoform specificity. J. Biol. Chem. 2008, 283:9509-9512.
13. McClellan A.J., Xia Y., Deutschbauer A.M., Davis R.W., Gerstein M., Frydman J. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 2007, 131:121-135.
14. Eustace B.K., Sakurai T., Stewart J.K., Yimlamai D., Unger C., Zehetmeier C., Lain B., Torella C., Henning S.W., Beste G., Scroggins B.T., Neckers L., Ilag L.L., Jay D.G. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat. Cell Biol. 2004, 6:507-514.
15. Whitesell L., Lindquist S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 2005, 5:761-772.
16. Pick E., Kluger Y., Giltnane J.M., Moeder C., Camp R.L., Rimm D.L., Kluger H.M. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res. 2007, 67:2932-2937.
17. Shimamura T., Shapiro G.I. Heat shock protein 90 inhibition in lung cancer. J. Thorac. Oncol. 2008, 3:S152-159.
18. Kamal A., Thao L., Sensintaffar J., Zhang L., Boehm M.F., Fritz L.C., Burrows F.J. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003, 425:407-410.
19. Workman P. Altered states: selectively drugging the Hsp90 cancer chaperone. Trends Mol. Med. 2004, 10:47-51.
20. Delmotte P., Delmotte-Plaque J. A new antifungal substance of fungal origin. Nature 1953, 171:344.
21. Soga S., Shiotsu Y., Akinaga S., Sharma S.V. Development of radicicol analogues. Curr. Cancer Drug Targets 2003, 3:359-369.
22. Shiotsu Y., Neckers L.M., Wortman I., An W.G., Schulte T.W., Soga S., Murakata C., Tamaoki T., Akinaga S. Novel oxime derivatives of radicicol induce erythroid differentiation associated with preferential G(1) phase accumulation against chronic myelogenous leukemia cells through destabilization of Bcr-Abl with Hsp90 complex. Blood 2000, 96:2284-2291.
23. Supko J.G., Hickman R.L., Grever M.R., Malspeis L. Preclinical pharmacologic evaluation of geldanamycin as an antitumor agent. Cancer Chemother. Pharmacol. 1995, 36:305-315.
24. Eiseman J.L., Lan J., Lagattuta T.F., Hamburger D.R., Joseph E., Covey J.M., Egorin M.J. Pharmacokinetics and pharmacodynamics of 17-demethoxy 17-[[(2-dimethylamino)ethyl]amino]geldanamycin (17DMAG, NSC 707545) in C.B-17 SCID mice bearing MDA-MB-231 human breast cancer xenografts. Cancer Chemother. Pharmacol. 2005, 55:21-32.
25. Pacey S., Banerji U., Judson I., Workman P. Hsp90 inhibitors in the clinic. Handbook Exp. Pharmacol. 2006, 331-358.
26. Lancet E., Gojo I., Burton M., Quinn M., Tighe S.M., Kersey K., Zhong Z., Albitar M.X., Bhalla K., Hannah A.L., Baer M.R. Phase I study of the heat shock protein 90 inhibitor alvespimycin (KOS-1022, 17-DMAG) administered intravenously twice weekly to patients with acute myeloid leukemia. Leukemia 2010, 24:699-705.
27. Kummar S., Gutierrez M.E., Gardner E.R., Chen X., Figg W.D., Zajac-Kaye M., Chen M., Steinberg S.M., Muir C.A., Yancey M.A., Horneffer Y.R., Juwara L., Melillo G., Ivy S.P., Merino M., Neckers L., Steeg P.S., Conley B.A., Giaccone G., Doroshow J.H., Murgo A.J. Phase I trial of 17-dimethylaminoethylamino-17-demethoxygeldanamycin (17-DMAG), a heat shock protein inhibitor, administered twice weekly in patients with advanced malignancies. Eur. J. Cancer 2010, 46:340-347.
28. Palacios C., Lopez-Perez A.I., Lopez-Rivas A. Down-regulation of RIP expression by 17-dimethylaminoethylamino-17-demethoxygeldanamycin promotes TRAIL-induced apoptosis in breast tumor cells. Cancer Lett. 2010, 287:207-215.
29. Ayrault O., Godeny M.D., Dillon C., Zindy F., Fitzgerald P., Roussel M.F., Beere H.M. Inhibition of Hsp90 via 17-DMAG induces apoptosis in a p53-dependent manner to prevent medulloblastoma. Proc. Natl. Acad. Sci. USA 2009, 106:17037-17042.
30. Hanson B.E., Vesole D.H. Retaspimycin hydrochloride (IPI-504): a novel heat shock protein inhibitor as an anticancer agent. Expert Opin. Investig. Drugs 2009, 18:1375-1383.
31. Song D., Chaerkady R., Tan A.C., Garcia-Garcia E., Nalli A., Suarez-Gauthier A., Lopez-Rios F., Zhang X.F., Solomon A., Tong J., Read M., Fritz C., Jimeno A., Pandey A., Hidalgo M. Antitumor activity and molecular effects of the novel heat shock protein 90 inhibitor, IPI-504, in pancreatic cancer. Mol. Cancer Ther. 2008, 7:3275-3284.
32. Bedi A., Barber J.P., Bedi G.C., el-Deiry W.S., Sidransky D., Vala M.S., Akhtar A.J., Hilton J., Jones R.J. BCR-ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: a mechanism of resistance to multiple anticancer agents. Blood 1995, 86:1148-1158.
33. Barnes D.J., De S., van Hensbergen P., Moravcsik E., Melo J.V. Different target range and cytotoxic specificity of adaphostin and 17-allylamino-17-demethoxygeldanamycin in imatinib-resistant and sensitive cell lines. Leukemia 2007, 21:421-426.
34. Peng C., Brain J., Hu Y., Goodrich A., Kong L., Grayzel D., Pak R., Read M., Li S. Inhibition of heat shock protein 90 prolongs survival of mice with BCR-ABL-T315I-induced leukemia and suppresses leukemic stem cells. Blood 2007.
35. Erlichman C. Tanespimycin: the opportunities and challenges of targeting heat shock protein 90. Expert Opin. Investig. Drugs 2009, 18:861-868.
36. Wu Y.C., Yen W.Y., Lee T.C., Yih L.H. Heat shock protein inhibitors, 17-DMAG and KNK437, enhance arsenic trioxide-induced mitotic apoptosis. Toxicol. Appl. Pharmacol. 2009, 236:231-238.
37. Robles A.I., Wright M.H., Gandhi B., Feis S.S., Hanigan C.L., Wiestner A., Varticovski L. Schedule-dependent synergy between the heat shock protein 90 inhibitor 17-(dimethylaminoethylamino)-17-demethoxygeldanamycin and doxorubicin restores apoptosis to p53-mutant lymphoma cell lines. Clin. Cancer Res. 2006, 12:6547-6556.
38. Rao R., Fiskus W., Yang Y., Lee P., Joshi R., Fernandez P., Mandawat A., Atadja P., Bradner J.E., Bhalla K. HDAC6 inhibition enhances 17-AAG-mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood 2008, 112:1886-1893.
39. Lin T.Y., Fenger J., Murahari S., Bear M.D., Kulp S.K., Wang D., Chen C.S., Kisseberth W.C., London C.A. AR-42, a novel HDAC inhibitor, exhibits biologic activity against malignant mast cell lines via downregulation of constitutively activated Kit. Blood 2010, 115:4217-4225.
40. Chen L., Meng S., Wang H., Bali P., Bai W., Li B., Atadja P., Bhalla K.N., Wu J. Chemical ablation of androgen receptor in prostate cancer cells by the histone deacetylase inhibitor LAQ824. Mol. Cancer Ther. 2005, 4:1311-1319.
41. Heddle J.G., Barnard F.M., Wentzell L.M., Maxwell A. The interaction of drugs with DNA gyrase: a model for the molecular basis of quinolone action. Nucleos. Nucleot. Nucleic Acids 2000, 19:1249-1264.
42. Allan R.K., Mok D., Ward B.K., Ratajczak T. Modulation of chaperone function and cochaperone interaction by novobiocin in the C-terminal domain of Hsp90: evidence that coumarin antibiotics disrupt Hsp90 dimerization. J. Biol. Chem. 2006, 281:7161-7171.
43. Wu L.X., Xu J.H., Zhang K.Z., Lin Q., Huang X.W., Wen C.X., Chen Y.Z. Disruption of the Bcr-Abl/Hsp90 protein complex: a possible mechanism to inhibit Bcr-Abl-positive human leukemic blasts by novobiocin. Leukemia 2008, 22:1402-1409.
44. Shelton S.N., Shawgo M.E., Matthews S.B., Lu Y., Donnelly A.C., Szabla K., Tanol M., Vielhauer G.A., Rajewski R.A., Matts R.L., Blagg B.S., Robertson J.D. KU135, a novel novobiocin-derived C-terminal inhibitor of the 90-kDa heat shock protein, exerts potent antiproliferative effects in human leukemic cells. Mol. Pharmacol. 2009, 76:1314-1322.
45. Matthews S.B., Vielhauer G.A., Manthe C.A., Chaguturu V.K., Szabla K., Matts R.L., Donnelly A.C., Blagg B.S., Holzbeierlein J.M. Characterization of a novel novobiocin analogue as a putative C-terminal inhibitor of heat shock protein 90 in prostate cancer cells. Prostate 2010, 70:27-36.
46. Chiosis G., Timaul M.N., Lucas B., Munster P.N., Zheng F.F., Sepp-Lorenzino L., Rosen N. A small molecule designed to bind to the adenine nucleotide pocket of Hsp90 causes Her2 degradation and the growth arrest and differentiation of breast cancer cells. Chem. Biol. 2001, 8:289-299.
47. Cerchietti L.C., Lopes E.C., Yang S.N., Hatzi K., Bunting K.L., Tsikitas L.A., Mallik A., Robles A.I., Walling J., Varticovski L., Shaknovich R., Bhalla K.N., Chiosis G., Melnick A. A purine scaffold Hsp90 inhibitor destabilizes BCL-6 and has specific antitumor activity in BCL-6-dependent B cell lymphomas. Nat. Med. 2009, 15:1369-1376.
48. Boll B., Eltaib F., Reiners K.S., von Tresckow B., Tawadros S., Simhadri V.R., Burrows F.J., Lundgren K., Hansen H.P., Engert A., von Strandmann E.P. Heat shock protein 90 inhibitor BIIB021 (CNF2024) depletes NF-kappaB and sensitizes Hodgkin's lymphoma cells for natural killer cell-mediated cytotoxicity. Clin. Cancer Res. 2009, 15:5108-5116.
49. Zhang H., Neely L., Lundgren K., Yang Y.C., Lough R., Timple N., Burrows F. BIIB021, a synthetic Hsp90 inhibitor, has broad application against tumors with acquired multidrug resistance. Int. J. Cancer 2010, 126:1226-1234.
50. Caldas-Lopes E., Cerchietti L., Ahn J.H., Clement C.C., Robles A.I., Rodina A., Moulick K., Taldone T., Gozman A., Guo Y., Wu N., de Stanchina E., White J., Gross S.S., Ma Y., Varticovski L., Melnick A., Chiosis G. Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc. Natl. Acad. Sci. USA 2009, 106:8368-8373.
51. Chandarlapaty S., Scaltriti M., Angelini P., Ye Q., Guzman M., Hudis C.A., Norton L., Solit D.B., Arribas J., Baselga J., Rosen N. Inhibitors of HSP90 block p95-HER2 signaling in Trastuzumab-resistant tumors and suppress their growth. Oncogene 2010, 29:325-334.
52. Rowlands M.G., Newbatt Y.M., Prodromou C., Pearl L.H., Workman P., Aherne W. High-throughput screening assay for inhibitors of heat-shock protein 90 ATPase activity. Anal. Biochem. 2004, 327:176-183.
53. Cheung K.M., Matthews T.P., James K., Rowlands M.G., Boxall K.J., Sharp S.Y., Maloney A., Roe S.M., Prodromou C., Pearl L.H., Aherne G.W., McDonald E., Workman P. The identification, synthesis, protein crystal structure and in vitro biochemical evaluation of a new 3,4-diarylpyrazole class of Hsp90 inhibitors. Bioorg. Med. Chem. Lett. 2005, 15:3338-3343.
54. Sharp S.Y., Prodromou C., Boxall K., Powers M.V., Holmes J.L., Box G., Matthews T.P., Cheung K.M., Kalusa A., James K., Hayes A., Hardcastle A., Dymock B., Brough P.A., Barril X., Cansfield J.E., Wright L., Surgenor A., Foloppe N., Hubbard R.E., Aherne W., Pearl L., Jones K., McDonald E., Raynaud F., Eccles S., Drysdale M., Workman P. Inhibition of the heat shock protein 90 molecular chaperone in vitro and in vivo by novel, synthetic, potent resorcinylic pyrazole/isoxazole amide analogues. Mol. Cancer Ther. 2007, 6:1198-1211.
55. Plescia J., Salz W., Xia F., Pennati M., Zaffaroni N., Daidone M.G., Meli M., Dohi T., Fortugno P., Nefedova Y., Gabrilovich D.I., Colombo G., Altieri D.C. Rational design of shepherdin, a novel anticancer agent. Cancer Cell 2005, 7:457-468.
56. Yi F., Regan L. A novel class of small molecule inhibitors of Hsp90. ACS Chem. Biol. 2008, 3:645-654.
57. Morrow P.K., Zambrana F., Esteva F.J. Recent advances in systemic therapy: advances in systemic therapy for HER2-positive metastatic breast cancer. Breast Cancer Res. 2009, 11:207.
58. Modi S., Stopeck A.T., Gordon M.S., Mendelson D., Solit D.B., Bagatell R., Ma W., Wheler J., Rosen N., Norton L., Cropp G.F., Johnson R.G., Hannah A.L., Hudis C.A. Combination of trastuzumab and tanespimycin (17-AAG, KOS-953) is safe and active in trastuzumab-refractory HER-2 overexpressing breast cancer: a phase I dose-escalation study. J. Clin. Oncol. 2007, 25:5410-5417.
59. Wong C., Chen S. Heat shock protein 90 inhibitors: new mode of therapy to overcome endocrine resistance. Cancer Res. 2009, 69:8670-8677.
60. Didelot C., Lanneau D., Brunet M., Bouchot A., Cartier J., Jacquel A., Ducoroy P., Cathelin S., Decologne N., Chiosis G., Dubrez-Daloz L., Solary E., Garrido C. Interaction of heat-shock protein 90 beta isoform (HSP90 beta) with cellular inhibitor of apoptosis 1 (c-IAP1) is required for cell differentiation. Cell Death Differ. 2008, 15:859-866.
61. Becker B., Multhoff G., Farkas B., Wild P.J., Landthaler M., Stolz W., Vogt T. Induction of Hsp90 protein expression in malignant melanomas and melanoma metastases. Exp. Dermatol. 2004, 13:27-32.
62. Wang X., Song X., Zhuo W., Fu Y., Shi H., Liang Y., Tong M., Chang G., Luo Y. The regulatory mechanism of Hsp90alpha secretion and its function in tumor malignancy. Proc. Natl. Acad. Sci. USA 2009, 106:21288-21293.
63. Jaattela M. Heat shock proteins as cellular lifeguards. Ann. Med. 1999, 31:261-271.
64. Shi Y., Thomas J.O. The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate. Mol. Cell Biol. 1992, 12:2186-2192.
65. Nylandsted J., Brand K., Jaattela M. Heat shock protein 70 is required for the survival of cancer cells. Ann. NY Acad. Sci. 2000, 926:122-125.
66. Gurbuxani S., Schmitt E., Cande C., Parcellier A., Hammann A., Daugas E., Kouranti I., Spahr C., Pance A., Kroemer G., Garrido C. Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene 2003, 22:6669-6678.
67. Schmitt E., Parcellier A., Gurbuxani S., Cande C., Hammann A., Morales M.C., Hunt C.R., Dix D.J., Kroemer R.T., Giordanetto F., Jaattela M., Penninger J.M., Pance A., Kroemer G., Garrido C. Chemosensitization by a non-apoptogenic heat shock protein 70-binding apoptosis-inducing factor mutant. Cancer Res. 2003, 63:8233-8240.
68. Ray S., Lu Y., Kaufmann S.H., Gustafson W.C., Karp J.E., Boldogh I., Fields A.P., Brasier A.R. Genomic mechanisms of p210BCR-ABL signaling: induction of heat shock protein 70 through the GATA response element confers resistance to paclitaxel-induced apoptosis. J. Biol. Chem. 2004, 279:35604-35615.
69. Schmitt E., Maingret L., Puig P.E., Rerole A.L., Ghiringhelli F., Hammann A., Solary E., Kroemer G., Garrido C. Heat shock protein 70 neutralization exerts potent antitumor effects in animal models of colon cancer and melanoma. Cancer Res. 2006, 66:4191-4197.
70. Leu J.I., Pimkina J., Frank A., Murphy M.E., George D.L. A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell. 2009, 36:15-27.
71. Steele A.J., Prentice A.G., Hoffbrand A.V., Yogashangary B.C., Hart S.M., Lowdell M.W., Samuel E.R., North J.M., Nacheva E.P., Chanalaris A., Kottaridis P., Cwynarski K., Wickremasinghe R.G. 2-Phenylacetylenesulfonamide (PAS) induces p53-independent apoptotic killing of B-chronic lymphocytic leukemia (CLL) cells. Blood 2009, 114:1217-1225.
72. Williamson D.S., Borgognoni J., Clay A., Daniels Z., Dokurno P., Drysdale M.J., Foloppe N., Francis G.L., Graham C.J., Howes R., Macias A.T., Murray J.B., Parsons R., Shaw T., Surgenor A.E., Terry L., Wang Y., Wood M., Massey A.J. Novel adenosine-derived inhibitors of 70 kDa heat shock protein, discovered through structure-based design. J. Med. Chem. 2009, 52:1510-1513.
73. Massey A.J., Williamson D.S., Browne H., Murray J.B., Dokurno P., Shaw T., Macias A.T., Daniels Z., Geoffroy S., Dopson M., Lavan P., Matassova N., Francis G.L., Graham C.J., Parsons R., Wang Y., Padfield A., Comer M., Drysdale M.J., Wood M. A novel, small molecule inhibitor of Hsc70/Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother. Pharmacol. 2009.
74. Jinwal U.K., Miyata Y., Koren J., Jones J.R., Trotter J.H., Chang L., O'Leary J., Morgan D., Lee D.C., Shults C.L., Rousaki A., Weeber E.J., Zuiderweg E.R., Gestwicki J.E., Dickey C.A. Chemical manipulation of hsp70 ATPase activity regulates tau stability. J. Neurosci. 2009, 29:12079-12088.
75. Britten C.D., Rowinsky E.K., Baker S.D., Weiss G.R., Smith L., Stephenson J., Rothenberg M., Smetzer L., Cramer J., Collins W., Von Hoff D.D., Eckhardt S.G. A phase I and pharmacokinetic study of the mitochondrial-specific rhodacyanine dye analog MKT 077. Clin. Cancer Res. 2000, 6:42-49.
76. Deocaris C.C., Widodo N., Shrestha B.G., Kaur K., Ohtaka M., Yamasaki K., Kaul S.C., Wadhwa R. Mortalin sensitizes human cancer cells to MKT-077-induced senescence. Cancer Lett. 2007, 252:259-269.
77. Evans C.G., Wisen S., Gestwicki J.E. Heat shock proteins 70 and 90 inhibit early stages of amyloid beta-(1-42) aggregation in vitro. J. Biol. Chem. 2006, 281:33182-33191.
78. Wright C.M., Seguin S.P., Fewell S.W., Zhang H., Ishwad C., Vats A., Lingwood C.A., Wipf P., Fanning E., Pipas J.M., Brodsky J.L. Inhibition of Simian Virus 40 replication by targeting the molecular chaperone function and ATPase activity of T antigen. Virus Res. 2009, 141:71-80.
79. Roodveldt C., Bertoncini C.W., Andersson A., van der Goot A.T., Hsu S.T., Fernandez-Montesinos R., de Jong J., van Ham T.J., Nollen E.A., Pozo D., Christodoulou J., Dobson C.M. Chaperone proteostasis in Parkinson's disease: stabilization of the Hsp70/alpha-synuclein complex by Hip. EMBO J. 2009, 28:3758-3770.
80. Guo F., Rocha K., Bali P., Pranpat M., Fiskus W., Boyapalle S., Kumaraswamy S., Balasis M., Greedy B., Armitage E.S., Lawrence N., Bhalla K. Abrogation of heat shock protein 70 induction as a strategy to increase antileukemia activity of heat shock protein 90 inhibitor 17-allylamino-demethoxy geldanamycin. Cancer Res. 2005, 65:10536-10544.
81. Lanneau D., Brunet M., Frisan E., Solary E., Fontenay M., Garrido C. Heat shock proteins: essential proteins for apoptosis regulation. J. Cell Mol. Med. 2008, 12:743-761.
82. Chang Y.S., Lee L.C., Sun F.C., Chao C.C., Fu H.W., Lai Y.K. Involvement of calcium in the differential induction of heat shock protein 70 by heat shock protein 90 inhibitors, geldanamycin and radicicol, in human non-small cell lung cancer H460 cells. J. Cell Biochem. 2006, 97:156-165.
83. Yun C.H., Yoon S.Y., Nguyen T.T., Cho H.Y., Kim T.H., Kim S.T., Kim B.C., Hong Y.S., Kim S.J., Lee H.J. Geldanamycin inhibits TGF-beta signaling through induction of Hsp70. Arch. Biochem. Biophys. 2010, 495:8-13.
84. Powers M.V., Clarke P.A., Workman P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell. 2008, 14:250-262.
85. Chalmin F., Ladoire S., Mignot G., Vincent J., Bruchard M., Remy-Martin J.P., Boireau W., Rouleau A., Simon B., Lanneau D., De Thonel A., Multhoff G., Hamman A., Martin F., Chauffert B., Solary E., Zitvogel L., Garrido C., Ryffel B., Borg C., Apetoh L., Rebe C., Ghiringhelli F. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 2010, 120:457-471.
86. Kostenko S., Moens U., kinases Heat shock protein 27 phosphorylation:, phosphatases functions and pathology. Cell. Mol. Life Sci. 2009, 66:3289-3307.
87. Mehlen P., Schulze-Osthoff K., Arrigo A.P. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J. Biol. Chem. 1996, 271:16510-16514.
88. Garrido C., Mehlen P., Fromentin A., Hammann A., Assem M., Arrigo A.P., Chauffert B. Inconstant association between 27-kDa heat-shock protein (Hsp27) content and doxorubicin resistance in human colon cancer cells. The doxorubicin-protecting effect of Hsp27. Eur. J. Biochem. 1996, 237:653-659.
89. Garrido C., Fromentin A., Bonnotte B., Favre N., Moutet M., Arrigo A.P., Mehlen P., Solary E. Heat shock protein 27 enhances the tumorigenicity of immunogenic rat colon carcinoma cell clones. Cancer Res. 1998, 58:5495-5499.
90. Zoubeidi A., Zardan A., Wiedmann R.M., Locke J., Beraldi E., Fazli L., Gleave M.E. Hsp27 promotes insulin-like growth factor-I survival signaling in prostate cancer via p90Rsk-dependent phosphorylation and inactivation of BAD. Cancer Res. 2010, 70:2307-2317.
91. Andrieu C., Taieb D., Baylot V., Ettinger S., Soubeyran P., De-Thonel A., Nelson C., Garrido C., So A., Fazli L., Bladou F., Gleave M., Iovanna J.L., Rocchi P. Heat shock protein 27 confers resistance to androgen ablation and chemotherapy in prostate cancer cells through eIF4E. Oncogene 2010, 29:1883-1896.
92. Garcia M.C., Ray D.M., Lackford B., Rubino M., Olden K., Roberts J.D. Arachidonic acid stimulates cell adhesion through a novel p38 MAPK-RhoA signaling pathway that involves heat shock protein 27. J. Biol. Chem. 2009, 284:20936-20945.
93. Sarto C., Valsecchi C., Magni F., Tremolada L., Arizzi C., Cordani N., Casellato S., Doro G., Favini P., Perego R.A., Raimondo F., Ferrero S., Mocarelli P., Galli-Kienle M. Expression of heat shock protein 27 in human renal cell carcinoma. Proteomics 2004, 4:2252-2260.
94. Rocchi P., So A., Kojima S., Signaevsky M., Beraldi E., Fazli L., Hurtado-Coll A., Yamanaka K., Gleave M. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res. 2004, 64:6595-6602.
95. Song T.F., Zhang Z.F., Liu L., Yang T., Jiang J., Li P. Small interfering RNA-mediated silencing of heat shock protein 27 (HSP27) Increases chemosensitivity to paclitaxel by increasing production of reactive oxygen species in human ovarian cancer cells (HO8910). J. Int. Med. Res. 2009, 37:1375-1388.
96. Hadchity E., Aloy M.T., Paulin C., Armandy E., Watkin E., Rousson R., Gleave M., Chapet O., Rodriguez-Lafrasse C. Heat shock protein 27 as a new therapeutic target for radiation sensitization of head and neck squamous cell carcinoma. Mol. Ther. 2009, 17:1387-1394.
97. Hadaschik B.A., Jackson J., Fazli L., Zoubeidi A., Burt H.M., Gleave M.E., So A.I. Intravesically administered antisense oligonucleotides targeting heat-shock protein-27 inhibit the growth of non-muscle-invasive bladder cancer. BJU Int. 2008, 102:610-616.
98. Xia Y., Liu Y., Wan J., Wang M., Rocchi P., Qu F., Iovanna J.L., Peng L. Novel triazole ribonucleoside down-regulates heat shock protein 27 and induces potent anticancer activity on drug-resistant pancreatic cancer. J. Med. Chem. 2009, 52:6083-6096.
99. Oba M., Yano S., Shuto T., Suico M.A., Eguma A., Kai H. IFN-gamma down-regulates Hsp27 and enhances hyperthermia-induced tumor cell death in vitro and tumor suppression in vivo. Int. J. Oncol. 2008, 32:1317-1324.
100. Chauhan D., Li G., Shringarpure R., Podar K., Ohtake Y., Hideshima T., Anderson K.C. Blockade of Hsp27 overcomes Bortezomib/proteasome inhibitor PS-341 resistance in lymphoma cells. Cancer Res. 2003, 63:6174-6177.
101. Tezel G., Wax M.B. The mechanisms of hsp27 antibody-mediated apoptosis in retinal neuronal cells. J. Neurosci. 2000, 20:3552-3562.
102. Collins I., Workman P. New approaches to molecular cancer therapeutics. Nat. Chem. Biol. 2006, 2:689-700.
103. Chalmin F., Ladoire S., Mignot G., Vincent J., Bruchard M., Remy-Martin J.P., Boireau W., Rouleau A., Simon B., Lanneau D., De Thonel A., Multhoff G., Hamman A., Martin F., Chauffert B., Solary E., Zitvogel L., Garrido C., Ryffel B., Borg C., Apetoh L., Rebe C., Ghiringhelli F. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 2010, 120:457-471.