Role of hsp70 in cancer growth and survival

Protein and Peptide Letters

Volumn 19, Issue 6, 2012, Pages 616-624

  Hatfield, Marcus P D ^a   Lovas, Sándor ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Heat shock protein; Hsp70; Inhibition; Structure

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70-1; HEAT SHOCK PROTEIN 70-2; HEAT SHOCK PROTEIN 70-5; HEAT SHOCK PROTEIN 70-6; HEAT SHOCK PROTEIN 70-8; HEAT SHOCK PROTEIN 70-9; ISOPROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CELL ACTIVITY; CELL STRESS; HUMAN; LEUKEMIA CELL; NONHUMAN; NUCLEOTIDE BINDING DOMAIN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN REFOLDING; PROTEIN STRUCTURE; REVIEW; SUBSTRATE BINDING DOMAIN;

EID: 84861942110     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986612800493968     Document Type: Review

References (164)

1. Flaherty, K.M.; DeLuca-Flaherty, C.; McKay, D.B. Three-dimensional structure of the atpase fragment of a 70k heat-shock cognate protein. Nature, 1990, 346, 623-628.
2. Woo, H.; Jiang, J.; Lafer, E.M.; Sousa, R. Atp-induced conformational changes in hsp70: molecular dynamics and experimental validation of an in silico predicted conformation. Biochemistry, 2009, 48, 11470-11477.
3. Mayer, M.P.; Bukau, B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci., 2005, 62, 670-684.
4. Swain, J.F.; Schulz, E.G.; Gierasch, L.M. Direct comparison of a stable isolated hsp70 substrate-binding domain in the empty and substrate-bound states. J. Biol. Chem., 2006, 281, 1605-1611.
5. Liebscher, M.; Roujeinikova, A. Allosteric coupling between the lid and interdomain linker in dnak revealed by inhibitor binding studies. J. Bacteriol., 2009, 191, 1456-1462.
6. Mayer, M.P.; Schröder, H.; Rüdiger, S.; Paal, K.; Laufen, T.; Bukau, B. Multistep mechanism of substrate binding determines chaperone activity of hsp70. Nat. Struct. Biol., 2000, 7, 586-593. (Pubitemid 30445917)
7. Fernández-Sáiz, V.; Moro, F.; Arizmendi, J.M.; Acebrón, S.P.; Muga, A. Ionic contacts at dnak substrate binding domain involved in the allosteric regulation of lid dynamics. J. Biol. Chem., 2006, 281, 7479-7488. (Pubitemid 43853009)
8. Slepenkov, S.V.; Patchen, B.; Peterson, K.M.; Witt, S.N. Importance of the d and e helices of the molecular chaperone dnak for atp binding and substrate release. Biochemistry, 2003, 42, 5867-5876. (Pubitemid 36582879)
9. Palleros, D.R.; Reid, K.L.; Shi, L.; Fink, A.L. Dnak atpase activity revisited. FEBS Lett., 1993, 336, 124-128. (Pubitemid 23362018)
10. Zhu, X.; Zhao, X.; Burkholder, W.F.; Gragerov, A.; Ogata, C.M.; Gottesman, M.E.; Hendrickson, W.A. Structural analysis of substrate binding by the molecular chaperone dnak. Science, 1996, 272, 1606-1614. (Pubitemid 26200017)
11. Wang, H.; Kurochkin, A.V.; Pang, Y.; Hu, W.; Flynn, G.C.; Zuiderweg, E.R. Nmr solution structure of the 21 kda chaperone protein dnak substrate binding domain: a preview of chaperoneprotein interaction. Biochemistry, 1998, 37, 7929-7940. (Pubitemid 28307053)
12. Morshauser, R.C.; Hu, W.; Wang, H.; Pang, Y.; Flynn, G.C.; Zuiderweg, E.R. High-resolution solution structure of the 18 kda substrate-binding domain of the mammalian chaperone protein hsc70. J. Mol. Biol., 1999, 289, 1387-1403. (Pubitemid 29296712)
13. Bertelsen, E.B.; Chang, L.; Gestwicki, J.E.; Zuiderweg, E.R.P. Solution conformation of wild-type e.coli hsp70 (dnak) chaperone complexed with adp and substrate. Proc. Natl. Acad. Sci. USA, 2009, 106, 8471-8476.
14. Wu, B.; Hunt, C.; Morimoto, R. Structure and expression of the human gene encoding major heat shock protein hsp70. Mol. Cell. Biol., 1985, 5, 330-341. (Pubitemid 15166301)
15. Milner, C.; Campbell, R. Structure and expression of three mhclinked hsp70 genes. Immunogenetics, 1990, 32, 242-251. (Pubitemid 20370377)
16. Anckar, J.; Sistonen, L. Heat shock factor 1 as a coordinator of stress and developmental pathways. Adv. Exp. Med. Biol., 2007, 594, 78-88.
17. Milarski, K.L.; Morimoto, R.I. Expression of human hsp70 during the synthetic phase of the cell cycle. Proc. Natl. Acad. Sci. USA, 1986, 83, 9517-9521. (Pubitemid 17223391)
18. Taira, T.; Narita, T.; Iguchi-Ariga, S.M.; Ariga, H. A novel g1-specific enhancer identified in the human heat shock protein 70 gene. Nucleic Acids Res., 1997, 25, 1975-1983. (Pubitemid 27303393)
19. Li, G.; Li, L.; Liu, Y.; Mak, J.; Chen, L.; Lee, W. Thermal response of rat fibroblasts stably transfected with human 70-kda heat shock protein-encoding gene. Proc. Natl. Acad. Sci. USA, 1991, 88, 1681-1685. (Pubitemid 21916289)
20. Jäättelä, M.; Wissing, D. Heat-shock proteins protect cells from monocyte cytotoxicity: possible mechanism of self-protection. J. Exp. Med., 1993, 177, 231-236. (Pubitemid 23008106)
21. Mestril, R.; Chi, S.H.; Sayen, M.R.; O'Reilly, K.; Dillmann, W.H. Expression of inducible stress protein 70 in rat heart myogenic cells confers protection against simulated ischemia-induced injury. J. Clin. Invest., 1994, 93, 759-767. (Pubitemid 24072819)
22. Marber, M.S.; Mestril, R.; Chi, S.H.; Sayen, M.R.; Yellon, D.M.; Dillmann, W.H. Overexpression of the rat inducible 70-kd heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J. Clin. Invest., 1995, 95, 1446-1456.
23. Wissing, D.; Jäättelä, M. Hsp27 and hsp70 increase the survival of wehi-s cells exposed to hyperthermia. Int. J. Hyperthermia, 1996, 12, 125-138. (Pubitemid 26096971)
24. Bellmann, K.; Jäättelä, M.; Wissing, D.; Burkart, V.; Kolb, H. Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett., 1996, 391, 185-188. (Pubitemid 26325740)
25. Amin, V.; Cumming, D.V.; Latchman, D.S. Over-expression of heat shock protein 70 protects neuronal cells against both thermal and ischaemic stress but with different efficiencies. Neurosci. Lett., 1996, 206, 45-48. (Pubitemid 26084725)
26. Chong, K.; Lai, C.; Lille, S.; Chang, C.; Su, C. Stable overexpression of the constitutive form of heat shock protein 70 confers oxidative protection. J. Mol. Cell. Cardiol., 1998, 30, 599-608. (Pubitemid 28132737)
27. Kwak, H. The role of inducible 70-kda heat shock protein in cell cycle control, differentiation and apoptotic cell death of the human myeloid leukemic hl-60 cells. Cell. Immunol., 1998, 187, 1-12. (Pubitemid 28359688)
28. Jäättelä, M.; Wissing, D.; Bauer, P.A.; Li, G.C. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J., 1992, 11, 3507-3512.
29. Buzzard, K.A.; Giaccia, A.J.; Killender, M.; Anderson, R.L. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J. Biol. Chem., 1998, 273, 17147-17153. (Pubitemid 28311751)
30. Williams, R.; Thomas, J.; Fina, M.; German, Z.; Benjamin, I. Human heat shock protein 70 (hsp70) protects murine cells from injury during metabolic stress. J. Clin. Invest., 1993, 92, 503-508. (Pubitemid 23209035)
31. Karlseder, J.; Wissing, D.; Holzer, G.; Orel, L.; Sliutz, G.; Auer, H.; Jäättelä, M.; Simon, M.M. Hsp70 overexpression mediates the escape of a doxorubicin-induced g2 cell cycle arrest. Biochem. Biophys. Res. Commun., 1996, 220, 153-159. (Pubitemid 26106815)
32. Simon, M.M.; Reikerstorfer, A.; Schwarz, A.; Krone, C.; Luger, T.A.; Jäättelä, M.; Schwarz, T. Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts. evidence for increased cell viability and suppression of cytokine release. J. Clin. Invest., 1995, 95, 926-933.
33. Nylandsted, J.; Rohde, M.; Brand, K.; Bastholm, L.; Elling, F.; Jäättelä, M. Selective depletion of heat shock protein 70 (hsp70) activates a tumor-specific death program that is independent of caspases and bypasses bcl-2. Proc. Natl. Acad. Sci. USA, 2000, 97, 7871-7876. (Pubitemid 30460740)
34. Nylandsted, J.; Wick, W.; Hirt, U.A.; Brand, K.; Rohde, M.; Leist, M.; Weller, M.; Jäättelä, M. Eradication of glioblastoma, and breast and colon carcinoma xenografts by hsp70 depletion. Cancer Res., 2002, 62, 7139-7142. (Pubitemid 36025225)
35. Nylandsted, J.; Gyrd-Hansen, M.; Danielewicz, A.; Fehrenbacher, N.; Lademann, U.; Høyer-Hansen, M.; Weber, E.; Multhoff, G.; Rohde, M.; Jäättelä, M. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med., 2004, 200, 425-435. (Pubitemid 39121900)
36. Rohde, M.; Daugaard, M.; Jensen, M.H.; Helin, K.; Nylandsted, J.; Jäättelä, M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev., 2005, 19, 570-582. (Pubitemid 40314989)
37. Plumier, J.C.; Krueger, A.M.; Currie, R.W.; Kontoyiannis, D.; Kollias, G.; Pagoulatos, G.N. Transgenic mice expressing the human inducible hsp70 have hippocampal neurons resistant to ischemic injury. Cell Stress Chaperones, 1997, 2, 162-167. (Pubitemid 27445576)
38. Lee, S.; Kim, M.; Yoon, B.; Kim, Y.; Ma, S.; Roh, J.; Lee, J.; Seo, J. Targeted hsp70.1 disruption increases infarction volume after local cerebral ischemia in mice. Stroke, 2001, 32, 2905-2912. (Pubitemid 33134488)
39. Van Molle, W.; Wielockx, B.; Mahieu, T.; Takada, M.; Taniguchi, T.; Sekikawa, K.; Libert, C. Hsp70 protects against tnf-induced lethal inflammatory shock. Immunity, 2002, 16, 685-695. (Pubitemid 34626689)
40. Shim, E. Targeted disruption of hsp70.1 sensitizes to osmotic stress. EMBO Rep., 2002, 3, 857-861. (Pubitemid 35154111)
41. Kwon, S. Impaired repair ability of hsp70.1 ko mouse after uvb irradiation. J. Dermatol. Sci., 2002, 28, 144-151. (Pubitemid 34155343)
42. Hwang, J. Spontaneous activation of pancreas trypsinogen in heat shock protein 70.1 knock-out mice. Pancreas, 2005, 31, 332-336. (Pubitemid 41566881)
43. Nollen, E.A.; Brunsting, J.F.; Roelofsen, H.; Weber, L.A.; Kampinga, H.H.In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol. Cell. Biol., 1999, 19, 2069-2079. (Pubitemid 29098265)
44. Mosser, D.D.; Caron, A.W.; Bourget, L.; Meriin, A.B.; Sherman, M.Y.; Morimoto, R.I.; Massie, B. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol. Cell. Biol., 2000, 20, 7146-7159.
45. Patury, S.; Miyata, Y.; Gestwicki, J.E. Pharmacological targeting of the hsp70 chaperone. Curr. Top. Med. Chem., 2009, 9, 1337-1351.
46. Gyrd-Hansen, M.; Nylandsted, J.; Jäättelä, M. Heat shock protein 70 promotes cancer cell viability by safeguarding lysosomal integrity. Cell Cycle, 2004, 3, 1484-1485. (Pubitemid 40521395)
47. Bivik, C.A.; Larsson, P.K.; Kågedal, K.M.; Rosdahl, I.K.; Ollinger, K.M. Uva/b-induced apoptosis in human melanocytes involves translocation of cathepsins and bcl-2 family members. J. Invest. Dermatol. , 2006, 126, 1119-1127.
48. Mambula, S.S.; Calderwood, S.K.Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J. Immunol., 2006, 177, 7849-7857. (Pubitemid 44848243)
49. Doulias, P.; Kotoglou, P.; Tenopoulou, M.; Keramisanou, D.; Tzavaras, T.; Brunk, U.; Galaris, D.; Angelidis, C. Involvement of heat shock protein-70 in the mechanism of hydrogen peroxideinduced dna damage: the role of lysosomes and iron. Free Radic. Biol. Med., 2007, 42, 567-577. (Pubitemid 46162124)
50. Goate, A.M.; Cooper, D.N.; Hall, C.; Leung, T.K.; Solomon, E.; Lim, L. Localization of a human heat-shock hsp 70 gene sequence to chromosome 6 and detection of two other loci by somatic-cell hybrid and restriction fragment length polymorphism analysis. Hum. Genet., 1987, 75, 123-128. (Pubitemid 17017704)
51. Daugaard, M.; Rohde, M.; Jäättelä, M. The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett., 2007, 581, 3702-3710. (Pubitemid 47081009)
52. Bonnycastle, L.L.; Yu, C.E.; Hunt, C.R.; Trask, B.J.; Clancy, K.P.; Weber, J.L.; Patterson, D.; Schellenberg, G.D. Cloning, sequencing, and mapping of the human chromosome 14 heat shock protein gene (hspa2). Genomics, 1994, 23, 85-93. (Pubitemid 24296938)
53. Son, W.; Han, C.; Hwang, S.; Lee, J.; Kim, S.; Kim, Y.Repression of hspa2 messenger rna in human testies with abnormal spermatogenesis. Fertil. Steril., 2000, 73, 1138-1144.
54. Allen, J.W.; Dix, D.J.; Collins, B.W.; Merrick, B.A.; He, C.; Selkirk, J.K.; Poorman-Allen, P.; Dresser, M.E.; Eddy, E.M. Hsp70-2 is part of the synaptonemal complex in mouse and hamster spermatocytes. Chromosoma, 1996, 104, 414-421. (Pubitemid 26103990)
55. Dix, D.J.; Allen, J.W.; Collins, B.W.; Mori, C.; Nakamura, N.; Poorman-Allen, P.; Goulding, E.H.; Eddy, E.M. Targeted gene disruption of hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. USA, 1996, 93, 3264-3268. (Pubitemid 26125606)
56. Munro, S.; Pelham, H.R. An hsp70-like protein in the er: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell, 1986, 46, 291-300.
57. Hendershot, L.M.; Valentine, V.A.; Lee, A.S.; Morris, S.W.; Shapiro, D.N. Localization of the gene encoding human bip/grp78, the endoplasmic reticulum cognate of the hsp70 family, to chromosome 9q34. Genomics, 1994, 20, 281-284. (Pubitemid 24108409)
58. Gething, M. Role and regulation of the er chaperone bip. Semin. Cell Dev. Biol., 1999, 10, 465-472. (Pubitemid 129513234)
59. Su, A. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA, 2004, 101, 6062-6067. (Pubitemid 38520528)
60. Luo, S.; Mao, C.; Lee, B.; Lee, A. Grp78/bip is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol., 2006, 26, 5688-5697. (Pubitemid 44134326)
61. Parsian, A.J.; Sheren, J.E.; Tao, T.Y.; Goswami, P.C.; Malyapa, R.; Van Rheeden, R.; Watson, M.S.; Hunt, C.R. The human hsp70b gene at the hspa7 locus of chromosome 1 is transcribed but nonfunctional. Biochim. Biophys. Acta, 2000, 1494, 201-205.
62. Bonnycastle, L.L.; Yu, C.E.; Hunt, C.R.; Trask, B.J.; Clancy, K.P.; Weber, J.L.; Patterson, D.; Schellenberg, G.D. Cloning, sequencing, and mapping of the human chromosome 14 heat shock protein gene (hspa2). Genomics, 1994, 23, 85-93. (Pubitemid 24296938)
63. Dworniczak, B.; Mirault, M.E. Structure and expression of a human gene coding for a 71 kd heat shock 'cognate' protein. Nucleic Acids Res., 1987, 15, 5181-5197.
64. Lindquist, S.; Craig, E.A. The heat-shock proteins. Annu. Rev. Genet., 1988, 22, 631-677. (Pubitemid 19156675)
65. Bukau, B.; Weissman, J.; Horwich, A. Molecular chaperones and protein quality control. Cell, 2006, 125, 443-451.
66. Rohde, M.; Daugaard, M.; Jensen, M.H.; Helin, K.; Nylandsted, J.; Jäättelä, M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev., 2005, 19, 570-582. (Pubitemid 40314989)
67. Domanico, S.Z.; DeNagel, D.C.; Dahlseid, J.N.; Green, J.M.; Pierce, S.K. Cloning of the gene encoding peptide-binding protein 74 shows that it is a new member of the heat shock protein 70 family. Mol. Cell. Biol., 1993, 13, 3598-3610. (Pubitemid 23157297)
68. Bhattacharyya, T.; Karnezis, A.N.; Murphy, S.P.; Hoang, T.; Freeman, B.C.; Phillips, B.; Morimoto, R.I.Cloning and subcellular localization of human mitochondrial hsp70. J. Biol. Chem., 1995, 270, 1705-1710.
69. Deocaris, C.C.; Kaul, S.C.; Wadhwa, R. On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperones, 2006, 11, 116-128. (Pubitemid 43948351)
70. Mizzen, L.A.; Chang, C.; Garrels, J.I.; Welch, W.J. Identification, characterization, and purification of two mammalian stress proteins present in mitochondria, grp 75, a member of the hsp 70 family and hsp 58, a homolog of the bacterial groel protein. J. Biol. Chem., 1989, 264, 20664-20675. (Pubitemid 20009264)
71. Volloch, V.Z.; Sherman, M.Y. Oncogenic potential of hsp72. Oncogene, 1999, 18, 3648-3651. (Pubitemid 29322390)
72. Morano, K. New tickets for an old dog: the evolving world of Hsp70. Ann. N Y Acad. Sci., 2007, 1113, 1-14. (Pubitemid 350015016)
73. Daugaard, M.; Jäättelä, M.; Rohde, M.Hsp70-2 is required for tumor cell growth and survival. Cell Cycle, 2005, 4, 877-880. (Pubitemid 41359749)
74. Nanbu, K.; Konishi, I.; Komatsu, T.; Mandai, M.; Yamamoto, S.; Kuroda, H.; Koshiyama, M.; Mori, T. Expression of heat shock proteins hsp70 and hsp90 in endometrial carcinomas. correlation with clinicopathology, sex steroid receptor status, and p53 protein expression. Cancer, 1996, 77, 330-338. (Pubitemid 26023352)
75. Rüdiger, S.; Germeroth, L.; Schneider-Mergener, J.; Bukau, B. Substrate specificity of the dnak chaperone determined by screening cellulose-bound peptide libraries. EMBO J., 1997, 16, 1501-1507. (Pubitemid 27151945)
76. Kim, K.; Jang, T.; Kim, J. Hsp70 and er expression in cervical intraepithelial neoplasia and cervical cancer. J. Korean Med. Sci., 1998, 13, 383-388. (Pubitemid 128686417)
77. Kaur, J.; Das, S.; Srivastava, A.; Ralhan, R. Cell surface expression of 70 kda heat shock protein in human oral dysplasia and squamous cell carcinoma: correlation with clinicopathological features. Oral Oncol., 1998, 34, 93-98. (Pubitemid 28207007)
78. Chuma, M.; Sakamoto, M.; Yamazaki, K.; Ohta, T.; Ohki, M.; Asaka, M.; Hirohashi, S. Expression profiling in multistage hepatocarcinogenesis: identification of hsp70 as a molecular marker of early hepatocellular carcinoma. Hepatology, 2003, 37, 198-207. (Pubitemid 36042161)
79. Efferth, T.; Schulten, H.G.; Thelen, P.; Bode, M.E.; Beniers, A.J.; Granzen, B.; Ringert, R.H.; Mertens, R.; Gefeller, O.; Jakse, G.; Fuzesi, L. Differential expression of the heat shock protein 70 in the histological compartments of nephroblastomas. Anticancer Res. , 2001, 21, 2915-2920. (Pubitemid 33051151)
80. Nylandsted, J.; Rohde, M.; Brand, K.; Bastholm, L.; Elling, F.; Jäättelä, M. Selective depletion of heat shock protein 70 (hsp70) activates a tumor-specific death program that is independent of caspases and bypasses bcl-2. Proc. Natl. Acad. Sci. USA, 2000, 97, 7871-7876. (Pubitemid 30460740)
81. Lin, K.; Rockliffe, N.; Johnson, G.G.; Sherrington, P.D.; Pettitt, A.R. Hsp90 inhibition has opposing effects on wild-type and mutant p53 and induces p21 expression and cytotoxicity irrespective of p53/atm status in chronic lymphocytic leukaemia cells. Oncogene, 2008, 27, 2445-2455. (Pubitemid 351521099)
82. Aloy, M.; Hadchity, E.; Bionda, C.; Diaz-Latoud, C.; Claude, L.; Rousson, R.; Arrigo, A.; Rodriguez-Lafrasse, C. Protective role of hsp27 protein against gamma radiation-induced apoptosis and radiosensitization effects of hsp27 gene silencing in different human tumor cells. Int. J. Radiat. Oncol. Biol. Phys., 2008, 70, 543-553.
83. Wei, Y.Q.; Zhao, X.; Kariya, Y.; Teshigawara, K.; Uchida, A. Inhibition of proliferation and induction of apoptosis by abrogation of heat-shock protein (hsp) 70 expression in tumor cells. Cancer Immunol. Immunother., 1995, 40, 73-78.
84. Creagh, E.M.; Sheehan, D.; Cotter, T.G. Heat shock proteins-modulators of apoptosis in tumour cells. Leukemia, 2000, 14, 1161-1173. (Pubitemid 30445021)
85. Takayama, S.; Reed, J.C.; Homma, S. Heat-shock proteins as regulators of apoptosis. Oncogene, 2003, 22, 9041-9047. (Pubitemid 38121704)
86. Saleh, A.; Srinivasula, S.M.; Balkir, L.; Robbins, P.D.; Alnemri, E.S. Negative regulation of the apaf-1 apoptosome by hsp70. Nat. Cell Biol., 2000, 2, 476-483.
87. Galluzzi, L.; Giordanetto, F.; Kroemer, G. Targeting hsp70 for cancer therapy. Mol. Cell, 2009, 36, 176-177.
88. Kroemer, G.; Galluzzi, L.; Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev., 2007, 87, 99-163. (Pubitemid 46209992)
89. Gabai, V.L.; Mabuchi, K.; Mosser, D.D.; Sherman, M.Y.Hsp72 and stress kinase c-jun n-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol. Cell. Biol., 2002, 22, 3415-3424. (Pubitemid 34453981)
90. Saleh, A.; Srinivasula, S.M.; Balkir, L.; Robbins, P.D.; Alnemri, E.S. Negative regulation of the apaf-1 apoptosome by hsp70. Nat. Cell Biol., 2000, 2, 476-483.
91. Beere, H.M.; Wolf, B.B.; Cain, K.; Mosser, D.D.; Mahboubi, A.; Kuwana, T.; Tailor, P.; Morimoto, R.I.; Cohen, G.M.; Green, D.R. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the apaf-1 apoptosome. Nat. Cell Biol., 2000, 2, 469-475.
92. Jäättelä, M.; Wissing, D.; Kokholm, K.; Kallunki, T.; Egeblad, M.Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J., 1998, 17, 6124-6134. (Pubitemid 28497786)
93. Yaglom, J.A.; Gabai, V.L.; Sherman, M.Y. High levels of heat shock protein hsp72 in cancer cells suppress default senescence pathways. Cancer Res., 2007, 67, 2373-2381. (Pubitemid 46424259)
94. Braig, M.; Schmitt, C.A. Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res., 2006, 66, 2881-2884.
95. Ferbevre, G. Oncogenic ras and p53 cooperate to induce cellular senescence. Mol. Cell. Biol., 2002, 22, 3497-3508.
96. Trost, T.M.; Lausch, E.U.; Fees, S.A.; Schmitt, S.; Enklaar, T.; Reutzel, D.; Brixel, L.R.; Schmidtke, P.; Maringer, M.; Schiffer, I.B.; Heimerdinger, C.K.; Hengstler, J.G.; Fritz, G.; Bockamp, E.O.; Prawitt, D.; Zabel, B.U.; Spangenberg, C. Premature senescence is a primary fail-safe mechanism of erbb2-driven tumorigenesis in breast carcinoma cells. Cancer Res., 2005, 65, 840-849. (Pubitemid 40216443)
97. Chen, Z. Crucial role of p53-dependent cellular senescence in suppression of pten-deficient tumorigenesis. Nature, 2005, 436, 725-730. (Pubitemid 41117277)
98. Pelengaris, S.; Rudolph, B.; Littlewood, T. Action of myc in vivo-proliferation and apoptosis. Curr. Opin. Genet. Dev., 2000, 10, 100-105.
99. Prendergast, G.C. Mechanisms of apoptosis by c-myc. Oncogene, 1999, 18, 2967-2987. (Pubitemid 29276537)
100. Pérez-Sala, D.; Rebollo, A. Novel aspects of ras proteins biology: regulation and implications. Cell Death Differ., 1999, 6, 722-728. (Pubitemid 29425382)
101. White, E. Regulation of apoptosis by adenovirus e1a and e1b oncogenes. Semin. Virol., 1998, 8, 505-513. (Pubitemid 28438489)
102. Blyth, K.; Stewart, M.; Bell, M.; James, C.; Evan, G.; Neil, J.C.; Cameron, E.R. Sensitivity to myc-induced apoptosis is retained in spontaneous and transplanted lymphomas of cd2-mycer mice. Oncogene, 2000, 19, 773-782. (Pubitemid 30107708)
103. Nilsson, J.A.; Cleveland, J.L. Myc pathways provoking cell suicide and cancer. Oncogene, 2003, 22, 9007-9021. (Pubitemid 38121701)
104. Eischen, C. Disruption of the arf-mdm2-p53 tumor suppressor pathway in myc-induced lymphomagenesis. Genes Dev., 1999, 13, 2658-2669. (Pubitemid 29508553)
105. Fourie, A.M.; Hupp, T.R.; Lane, D.P.; Sang, B.C.; Barbosa, M.S.; Sambrook, J.F.; Gething, M.J. Hsp70 binding sites in the tumor suppressor protein p53. J. Biol. Chem., 1997, 272, 19471-19479. (Pubitemid 27337746)
106. Liberek, K.; Lewandowska, A.; Zietkiewicz, S. Chaperones in control of protein disaggregation. EMBO J., 2008, 27, 328-335. (Pubitemid 351161659)
107. Pratt, W. Chaperoning of glucocorticoid receptors. Handb. Exp. Pharmacol., 2006, 172, 111-138.
108. Eisenberg, E.; Greene, L.E. Multiple roles of auxilin and hsc70 in clathrin-mediated endocytosis. Traffic, 2007, 8, 640-646. (Pubitemid 46785147)
109. Nollen, E.A.A.; Morimoto, R.I. Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. J. Cell Sci., 2002, 115, 2809-2816.
110. Ravagnan, L.; Gurbuxani, S.; Susin, S.A.; Maisse, C.; Daugas, E.; Zamzami, N.; Mak, T.; Jäättelä, M.; Penninger, J.M.; Garrido, C.; Kroemer, G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol., 2001, 3, 839-843. (Pubitemid 32842690)
111. 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. (Pubitemid 37372207)
112. Gehrmann, M.; Liebisch, G.; Schmitz, G.; Anderson, R.; Steinem, C.; De Maio, A.; Pockley, G.; Multhoff, G. Tumor-specific hsp70 plasma membrane localization is enabled by the glycosphingolipid gb3. PLoS One, 2008, 3, 1925.
113. Schilling, D.; Gehrmann, M.; Steinem, C.; De Maio, A.; Pockley, A.G.; Abend, M.; Molls, M.; Multhoff, G. Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J., 2009, 23, 2467-2477.
114. Gehrmann, M.; Schmetzer, H.; Eissner, G.; Haferlach, T.; Hiddemann, W.; Multhoff, G. Membrane-bound heat shock protein 70 (hsp70) in acute myeloid leukemia: a tumor specific recognition structure for the cytolytic activity of autologous nk cells. Haematologica, 2003, 88, 474-476. (Pubitemid 36547137)
115. Lasunskaia, E.B.; Fridlianskaia, I.; Arnholdt, A.V.; Kanashiro, M.; Guzhova, I.; Margulis, B. Sub-lethal heat shock induces plasma membrane translocation of 70-kda heat shock protein in viable, but not in apoptotic, u-937 leukaemia cells. APMIS, 2010, 118, 179-187.
116. Anand, P.K.; Anand, E.; Bleck, C.K.E.; Anes, E.; Griffiths, G. Exosomal hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS One, 2010, 5, 10136.
117. Asea, A. Hsp72 release: mechanisms and methodologies. Methods, 2007, 43, 194-198. (Pubitemid 47499074)
118. Johnson, J.D.; Fleshner, M. Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J. Leukoc. Biol., 2006, 79, 425-434. (Pubitemid 44831219)
119. Lancaster, G.I.; Febbraio, M.A. Exosome-dependent trafficking of hsp70: a novel secretory pathway for cellular stress proteins. J. Biol. Chem., 2005, 280, 23349-23355. (Pubitemid 40853248)
120. Calderwood, S.K.; Mambula, S.S.; Gray, P.J.J. Extracellular heat shock proteins in cell signaling and immunity. Ann. N Y Acad. Sci., 2007, 1113, 28-39.
121. Calderwood, S.K.; Mambula, S.S.; Gray, P.J.J.; Theriault, J.R. Extracellular heat shock proteins in cell signaling. FEBS Lett., 2007, 581, 3689-3694. (Pubitemid 47081004)
122. Multhoff, G.; Botzler, C. Heat-shock proteins and the immune response. Ann. N Y Acad. Sci., 1998, 851, 86-93. (Pubitemid 28370367)
123. Tauchi, K.; Tsutsumi, Y.; Hori, S.; Yoshimura, S.; Osamura, R.Y.; Watanabe, K. Expression of heat shock protein 70 and c-myc protein in human breast cancer: an immunohistochemical study. Jpn. J. Clin. Oncol., 1991, 21, 256-263.
124. Takahashi, S.; Mikami, T.; Watanabe, Y. Correlation of heat shock protein 70 expression with estrogen receptor levels in invasive human breast cancer. Am. J. Clin. Pathol., 1994, 101, 519-525. (Pubitemid 24123248)
125. Ciocca, D.R.; Clark, G.M.; Tandon, A.K.; Fuqua, S.A.; Welch, W.J.; McGuire, W.L. Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications. J. Natl. Cancer Inst., 1993, 85, 570-574. (Pubitemid 23110932)
126. Lazaris, A.C.; Chatzigianni, E.B.; Panoussopoulos, D.; Tzimas, G.N.; Davaris, P.S.; Golematis, B.C. Proliferating cell nuclear antigen and heat shock protein 70 immunolocalization in invasive ductal breast cancer not otherwise specified. Breast Cancer Res. Treat., 1997, 43, 43-51. (Pubitemid 27090866)
127. Vargas-Roig, L.M.; Fanelli, M.A.; López, L.A.; Gago, F.E.; Tello, O.; Aznar, J.C.; Ciocca, D.R. Heat shock proteins and cell proliferation in human breast cancer biopsy samples. Cancer Detect. Prev., 1997, 21, 441-451. (Pubitemid 27413987)
128. Pavithra, L.; Sreenath, K.; Singh, S.; Chattopadhyay, S. Heat-shock protein 70 binds to a novel sequence in 5' utr of tumor suppressor smar1 and regulates its mrna stability upon prostaglandin a2 treatment. FEBS Lett., 2010, 584, 1187-1192.
129. Townsend, P.A.; Dublin, E.; Hart, I.R.; Kao, R.H.; Hanby, A.M.; Cutress, R.I.; Poulsom, R.; Ryder, K.; Barnes, D.M.; Packham, G.Bag-i expression in human breast cancer: interrelationship between bag-1 rna, protein, hsc70 expression and clinico-pathological data. J. Pathol., 2002, 197, 51-59. (Pubitemid 34450164)
130. Nimmanapalli, R.; O'Bryan, E.; Huang, M.; Bali, P.; Burnette, P.K.; Loughran, T.; Tepperberg, J.; Jove, R.; Bhalla, K. Molecular characterization and sensitivity of sti-571 (imatinib mesylate, gleevec)-resistant, bcr-abl-positive, human acute leukemia cells to src kinase inhibitor pd180970 and 17-allylamino-17-demethoxygeldanamycin. Cancer Res., 2002, 62, 5761-5769. (Pubitemid 35204733)
131. Thijsen, S.; Schuurhuis, G.; van Oostveen, J.; Ossenkoppele, G. Chronic myeloid leukemia from basics to bedside. Leukemia, 1999, 13, 1646-1674. (Pubitemid 29535247)
132. Guo, F.; Sigua, C.; Bali, P.; George, P.; Fiskus, W.; Scuto, A.; Annavarapu, S.; Mouttaki, A.; Sondarva, G.; Wei, S.; Wu, J.; Djeu, J.; Bhalla, K. Mechanistic role of heat shock protein 70 in bcr-ablmediated resistance to apoptosis in human acute leukemia cells. Blood, 2005, 105, 1246-1255. (Pubitemid 40170900)
133. Bases, R. Heat shock protein 70 enhanced deoxyribonucleic acid base excision repair in human leukemic cells after ionizing radiation. Cell Stress Chaperones, 2006, 11, 240-249. (Pubitemid 44343761)
134. Feng, H.; Zeng, Y.; Graner, M.W.; Katsanis, E. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic t cells. Blood, 2002, 100, 4108-4115. (Pubitemid 35396879)
135. Sapozhnikov, A.M.; Ponomarev, E.D.; Tarasenko, T.N.; Telford, W.G. Spontaneous apoptosis and expression of cell surface heatshock proteins in cultured el-4 lymphoma cells. Cell Prolif., 1999, 32, 363-378. (Pubitemid 30050405)
136. Thomas, X.; Campos, L.; Mounier, C.; Cornillon, J.; Flandrin, P.; Le, Q.; Piselli, S.; Guyotat, D. Expression of heat-shock proteins is associated with major adverse prognostic factors in acute myeloid leukemia. Leuk. Res., 2005, 29, 1049-1058. (Pubitemid 40982599)
137. Duval, A.; Olaru, D.; Campos, L.; Flandrin, P.; Nadal, N.; Guyotat, D. Expression and prognostic significance of heat-shock proteins in myelodysplastic syndromes. Haematologica, 2006, 91, 713-714. (Pubitemid 43799480)
138. Steiner, K.; Graf, M.; Hecht, K.; Reif, S.; Rossbacher, L.; Pfister, K.; Kolb, H.; Schmetzer, H.M.; Multhoff, G. High hsp70-membrane expression on leukemic cells from patients with acute myeloid leukemia is associated with a worse prognosis. Leukemia, 2006, 20, 2076-2079. (Pubitemid 44614913)
139. Pocaly, M.; Lagarde, V.; Etienne, G.; Ribeil, J.; Claverol, S.; Bonneu, M.; Moreau-Gaudry, F.; Guyonnet-Duperat, V.; Hermine, O.; Melo, J.V.; Dupouy, M.; Turcq, B.; Mahon, F.; Pasquet, J. Overexpression of the heat-shock protein 70 is associated to imatinib resistance in chronic myeloid leukemia. Leukemia, 2007, 21, 93-101. (Pubitemid 44921840)
140. Yeh, C.; Tseng, R.; Zhang, Z.; Cortes, J.; O'Brien, S.; Giles, F.; Hannah, A.; Estrov, Z.; Keating, M.; Kantarjian, H.; Albitar, M.Circulating heat shock protein 70 and progression in patients with chronic myeloid leukemia. Leuk. Res., 2009, 33, 212-217.
141. Yeh, C.; Tseng, R.; Hannah, A.; Estrov, Z.; Estey, E.; Kantarjian, H.; Albitar, M. Clinical correlation of circulating heat shock protein 70 in acute leukemia. Leuk. Res., 2010, 34, 605-609.
142. Teiten, M.; Reuter, S.; Schmucker, S.; Dicato, M.; Diederich, M. Induction of heat shock response by curcumin in human leukemia cells. Cancer Lett., 2009, 279, 145-154.
143. Daugaard, M.; Jäättelä, M.; Rohde, M. Hsp70-2 is required for tumor cell growth and survival. Cell Cycle, 2005, 4, 877-880. (Pubitemid 41359749)
144. Tauchi, K.; Tsutsumi, Y.; Hori, S.; Yoshimura, S.; Osamura, R.Y.; Watanabe, K. Expression of heat shock protein 70 and c-myc protein in human breast cancer: an immunohistochemical study. Jpn. J. Clin. Oncol., 1991, 21, 256-263.
145. Shotar, A.M. P53 and heat shock protein 70 expressions in colorectal adenocarcinoma. Saudi Med. J., 2005, 26, 1602-1606. (Pubitemid 41794102)
146. Milievi, Z.T.; Petkovi, M.Z.; Drndarevi, N.C.; Pavlovi, M.D.; Todorovi, V.N.Expression of heat shock protein 70 (hsp70) in patients with colorectal adenocarcinoma-immunohistochemistry and western blot analysis. Neoplasma, 2007, 54, 37-45.
147. Ramp, U.; Mahotka, C.; Heikaus, S.; Shibata, T.; Grimm, M.O.; Willers, R.; Gabbert, H.E. Expression of heat shock protein 70 in renal cell carcinoma and its relation to tumor progression and prognosis. Histol. Histopathol., 2007, 22, 1099-1107. (Pubitemid 47470304)
148. Chant, I.D.; Rose, P.E.; Morris, A.G. Analysis of heat-shock protein expression in myeloid leukaemia cells by flow cytometry. Br. J. Haematol., 1995, 90, 163-168.
149. Pfister, K.; Radons, J.; Busch, R.; Tidball, J.G.; Pfeifer, M.; Freitag, L.; Feldmann, H.; Milani, V.; Issels, R.; Multhoff, G. Patient survival by hsp70 membrane phenotype: association with different routes of metastasis. Cancer, 2007, 110, 926-935. (Pubitemid 47257673)
150. Jalbout, M.; Bouaouina, N.; Gargouri, J.; Corbex, M.; Ben Ahmed, S.; Chouchane, L. Polymorphism of the stress protein hsp70-2 gene is associated with the susceptibility to the nasopharyngeal carcinoma. Cancer Lett., 2003, 193, 75-81. (Pubitemid 36412080)
151. Garg, M.; Kanojia, D.; Seth, A.; Kumar, R.; Gupta, A.; Surolia, A.; Suri, A. Heat-shock protein 70-2 (hsp70-2) expression in bladder urothelial carcinoma is associated with tumour progression and promotes migration and invasion. Eur. J. Cancer, 2010, 46, 207-215.
152. Garg, M.; Kanojia, D.; Saini, S.; Suri, S.; Gupta, A.; Surolia, A.; Suri, A. Germ cell-specific heat shock protein 70-2 is expressed in cervical carcinoma and is involved in the growth, migration, and invasion of cervical cells. Cancer, 2010, 116, 3785-3796.
153. Zhu, D.; Dix, D.J.; Eddy, E.M. Hsp70-2 is required for cdc2 kinase activity in meiosis i of mouse spermatocytes. Development, 1997, 124, 3007-3014. (Pubitemid 27370915)
154. Dix, D.J.; Allen, J.W.; Collins, B.W.; Poorman-Allen, P.; Mori, C.; Blizard, D.R.; Brown, P.R.; Goulding, E.H.; Strong, B.D.; Eddy, E.M. Hsp70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development, 1997, 124, 4595-4603. (Pubitemid 27519254)
155. Govin, J.; Caron, C.; Escoffier, E.; Ferro, M.; Kuhn, L.; Rousseaux, S.; Eddy, E.M.; Garin, J.; Khochbin, S. Post-meiotic shifts in hspa2/hsp70.2 chaperone activity during mouse spermatogenesis. J. Biol. Chem., 2006, 281, 37888-37892. (Pubitemid 46042092)
156. Kastan, M.B.; Bartek, J. Cell-cycle checkpoints and cancer. Nature, 2004, 432, 316-323. (Pubitemid 39551659)
157. Lee, A. Grp78 induction in cancer: therapeutic and prognostic implications. Cancer Res., 2007, 67, 3496-3499. (Pubitemid 46762126)
158. Lee, H. Grp78 is overexpressed in glioblastomas and regulates glioma cell growth and apoptosis. NeuroOncol., 2008, 10, 236-243.
159. Dong, D.; Ni, M.; Li, J.; Xiong, S.; Ye, W.; Virrey, J.J.; Mao, C.; Ye, R.; Wang, M.; Pen, L.; Dubeau, L.; Groshen, S.; Hofman, F.M.; Lee, A.S. Critical role of the stress chaperone grp78/bip in tumor proliferation, survival, and tumor angiogenesis in transgeneinduced mammary tumor development. Cancer Res., 2008, 68, 498-505. (Pubitemid 351380077)
160. Nirdé, P.; Derocq, D.; Maynadier, M.; Chambon, M.; Basile, I.; Gary-Bobo, M.; Garcia, M. Heat shock cognate 70 protein secretion as a new growth arrest signal for cancer cells. Oncogene, 2010, 29, 117-127.
161. Dundas, S.R.; Lawrie, L.C.; Rooney, P.H.; Murray, G.I. Mortalin is over-expressed by colorectal adenocarcinomas and correlates with poor survival. J. Pathol., 2005, 205, 74-81. (Pubitemid 40029095)
162. Wadhwa, R.; Takano, S.; Kaur, K.; Deocaris, C.C.; Pereira-Smith, O.M.; Reddel, R.R.; Kaul, S.C. Upregulation of mortalin/ mthsp70/grp75 contributes to human carcinogenesis. Int. J. Cancer, 2006, 118, 2973-2980.
163. Wadhwa, R.; Takano, S.; Taira, K.; Kaul, S.C. Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J. Gene Med., 2004, 6, 439-444. (Pubitemid 40228060)
164. 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.