The versatile stress protein mortalin as a chaperone therapeutic agent

Protein and Peptide Letters

Volumn 16, Issue 5, 2009, Pages 517-529

  Deocaris, Custer C ^a,b   Kaul, Sunil C ^b   Wadhwa, Renu ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Aging; Cancer; Chaperono therapeutic agent; Mortalin; Stress chaperone; Upregulation

Indexed keywords

HEAT SHOCK PROTEIN 70; MORTALIN;

AGING; ANIMAL; ARTICLE; DRUG ANTAGONISM; GENETICS; HUMAN; METABOLISM; THERAPY;

AGING; ANIMALS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; THERAPEUTICS;

EID: 67649306594     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986609788167770     Document Type: Article

References (136)

1. Wadhwa, R.; Kaul, S. C.; Ikawa, Y.; Sugimoto, Y. Identification of a novel member of mouse hsp70 family: its association with cellular mortal phenotype. J. Biol. Chem., 1993, 268(9), 6615-6621.
2. Wadhwa, R.; Kaul, S. C.; Mitsui, Y.; Sugimoto, Y. Differential subcellular distribution of mortalin in mortal and immortal mouse, and human fibroblasts. Exp. Cell Res., 1993, 207(2), 442-448.
3. Wadhwa, R.; Kaul, S. C.; Sugimoto, Y.; Mitsui, Y. Spontaneous immortalization of mouse fibroblasts involves structural changes in senescence inducing protein, mortalin. Biochem. Biophys. Res. Commun., 1993, 797(1), 202-206.
4. Kaul, S. C.; Deocaris, C. C.; Wadhwa, R. Three faces of mortalin: A housekeeper, guardian and killer. Exp. Gerontol., 2007, 42(4), 263-274.
5. Kaul, S. C.; Wadhwa, R.; Matsuda, Y.; Hensler, P. J.; Pereira- Smith, O. M.; Komatsu, Y.; Mitsui, Y. Mouse and human chromosomal assignments of mortalin, a novel member of murine hsp70 family of proteins. FEBSLett., 1995, 361(2-3), 269-272.
6. Kaul, S. C.; Duncan, E.; Sugihara, T.; Reddel, R. R.; Mitsui, Y.; Wadhwa, R. Structurally and functionally distinct mouse hsp70 family members mot-1 and mot-2 proteins are encoded by two al leles. DNA Res., 2000, 7(3), 229-231.
7. Deocaris, C. C.; Kaul, S. C.; Wadhwa, R. On the brotherhood of the mitochondrial chaperones mortalin and Hsp60. Cell Stress Chaperones, 2006, 11(2), 116-128.
8. Michikawa, Y.; Baba, T.; Arai, Y.; Sakakura, T.; Kusakabe, M. Structure and organization of the gene encoding a mouse mito- chondrial stress-70 protein. FEBS Lett., 1993, 336(1), 27-33.
9. Michikawa, Y.; Baba, T.; Arai, Y.; Sakakura, T.; Tanaka, M.; Ku-sakabe, M. Antigenic protein specific for C3H strain mouse is a mi- tochondrial stress-70 protein. Biochem. Biophys. Res. Commun., 1993, 196(1), 223-232.
10. Wadhwa, R.; Akiyama, S.; Sugihara, T.; Reddel, R. R.; Mitsui, Y.; Kaul, S. C. Genetic differences between the pancytosolic and per- inuclear forms of murine mortalin. Exp. Cell Res. 1996, 226(2),381-386.
11. Wadhwa, R.; Kaul, S. C.; Sugimoto, Y.; Mitsui, Y. Induction of cellular senescence by transfection of cytosolic mortalin cDNA in NIH 3T3 cells.J. Biol. Chem., 1993, 268(30), 22239-22242.
12. 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(6), 3598-3610.
13. Pilzer, D.; Fishelson, Z. Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis. Int. Immunol., 2005, 17(9), 1239-1248.
14. Pilzer, D.; Gasser, O.; Moskovich, O.; Schifferli, J. A.; Fishelson, Z. Emission of membrane vesicles: roles in complement resistance, immunity and cancer. Springer Semin. Immunopathol., 2005, 27(3),375-387.
15. Massa, S. M.; Longo, F. M.; Zuo, J.; Wang, S.; Chen, J.; Sharp, F. R. Cloning of rat grp75, an hsp70-family member, and its expression in normal and ischemic brain. J. Neurosci. Res., 1995, 40(6),807-819.
16. Merrick, B. A.; Walker, V. R.; He, C.; Patterson, R. M.; Selkirk, J. K. Induction of novel Grp75 isoforms by 2-deoxyglucose in human and murine fibroblasts. Cancer Lett., 1997, 119(2), 185-190.
17. Ornatsky, O. I.; Connor, M. K.; Hood, D. A. Expression of stress proteins and mitochondrial chaperonins in chronically stimulated skeletal muscle. Biochem. J., 1995, 311(1), 119-123.
18. O'Neill, D. E.; Noble, E. G. Constitutive expression of inducible Hsp70 is linked to natural shifts in skeletal muscle phenotype. Acta Physiol. Scand., 2004, 181(1), 35-41.
19. Orsini, F.; Migliaccio, E.; Moroni, M.; Contursi, C.; Raker, V. A.; Piccini, D.; Martin-Padura, I.; Pelliccia, G.; Trinei, M.; Bono, M.; Puri, C.; Tacchetti, C.; Ferrini, M.; Mannucci, R.; Nicoletti, I.; Lan- francone, L.; Giorgio, M.; Pelicci, P. G. The life span determinant p66Shc localizes to mitochondria where it associates with mito- chondrial heat shock protein 70 and regulates trans-membrane potential. J. Biol. Chem., 2004, 279(24), 25689-25695.
20. Saretzki, G.; Armstrong, L.; Leake, A.; Lako, M.; von Zglinicki, T.Stress defense in murine embryonic stem cells is superior to that of various differentiated murine cells. Stem Cells, 2004, 22(6), 962-971.
21. Sadekova, S.; Lehnert, S.; Chow, T. Y. Induction of PBP74/ mor- talin/Grp75, a member of the hsp70 family, by low doses of ionizing radiation: a possible role in induced radioresistance. Int. J. Radiat. Biol., 1997, 72(6), 653-660.
22. Um, J. H.; Kang, C. D.; Hwang, B. W.; Ha, M. Y.; Hur, J. G.; Kim, D. W.; Chung, B. S.; Kim, S. H. Involvement of DNA-dependent protein kinase in regulation of the mitochondrial heat shock proteins. Leuk. Res., 2003, 27(6), 509-516.
23. Dahlseid, J. N.; Lill, R.; Green, J. M.; Xu, X.; Qiu, Y.; Pierce, S. K. PBP74, a new member of the mammalian 70-kDa heat shock protein family, is amitochondrial protein. Mol. Biol. Cell, 1994, 5(11), 1265-1275.
24. Bhattacharyya, T.; Karnezis, A. N.; Murphy, S. P.; Hoang, T.; Freeman, B. C.; Phillips, B.; Morimoto, R. I. Cloning and subcellu- lar localization of human mitochondrial hsp70. J. Biol. Chem. 1995, 270(4), 1705-1710.
25. Voloboueva, L. A.; Duan, M.; Ouyang, Y.; Emery, J. F.; Stoy, C.; Giffard, R. G. J. Cereb. Blood Flow Metab., 2008, 28(5), 1009-1016.
26. Montesano Gesualdi, N.; Chirico, G.; Pirozzi, G.; Costantino, E.; Landriscina, M.; Esposito, F. Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress, 2007, 10(4), 342-350.
27. Cechetto, J. D.; Gupta, R. S. Immunoelectron microscopy provides evidence that tumor necrosis factor receptor-associated protein 1 (TRAP-1) is a mitochondrial protein which also localizes at specific extramitochondrial sites. Exp. Cell Res., 2000, 260(1), 30-39.
28. Naylor, D. J.; Hoogenraad, N. J.; Hoj, P. B. Isolation and characterisation of a cDNA encoding rat mitochondrial GrpE, a stress- inducible nucleotide-exchange factor of ubiquitous appearance in mammalian organs. FEBS Lett., 1996, 396(2-3), 181-188.
29. Jensen, R. E.; Dunn, C. D.; Youngman, M. J.; Sesaki, H. Mitochondrial building blocks. Trends Cell Biol., 2004, 14(5), 215-218.
30. Schneider, H. C.; Berthold, J.; Bauer, M. F.; Dietmeier, K.; Guiard, B.; Brunner, M.; Neupert, W. Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature, 1994, 371(6500), 768-774.
31. Brunner, M.; Schneider, H. C.; Lill, R.; Neupert, W. Dissection of protein translocation across the mitochondrial outer and inner membranes. Cold Spring Harb. Symp. Quant. Biol., 1995, 60, 619-627.
32. Rehling, P.; Brandner, K.; Pfanner, N. Mitochondrial import and the twin-pore translocase. Nat. Rev. Mol. Cell. Biol., 2004, 5(7),519-530.
33. Geissler, A.; Rassow, J.; Pfanner, N.; Voos, W. Mitochondrial import driving forces: enhanced trapping by matrix Hsp70 stimulates translocation and reduces the membrane potential dependence of loosely folded preproteins. Mol. Cell Biol., 2001, 21(20), 7097-7104.
34. Strub, A.; Lim, J. H.; Pfanner, N.; Voos, W. The mitochondrial protein import motor. Biol. Chem., 2000, 381(9-10), 943-949.
35. Voos, W.; von Ahsen, O.; Muller, H.; Guiard, B.; Rassow, J.;Pfanner, N. Differential requirement for the mitochondrial Hsp70- Tim44 complex in unfolding and translocation of preproteins. EMBO J., 1996, 15(11), 2668-2677.
36. Glick, B. S. Can Hsp70 proteins act as force-generating motors? Cell 1995, 80(1), 11-14.
37. Glick, B. S. Pathways and energetics of mitochondrial protein import in Saccharomyces cerevisiae. Methods Enzymol., 1995, 260, 224-231.
38. Horst, M.; Oppliger, W.; Rospert, S.; Schonfeld, H. J.; Schatz, G.; Azem, A. Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J., 1997, 16(8), 1842-1849.
39. Pockley, A. G. Heat shock proteins in health and disease: therapeutic targets or therapeutic agents? Expert. Rev. Mol. Med., 2001, 3(23), 1-21.
40. Hartl, F. U.; Martin, J.; Neupert, W. Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu. Rev. Biophys. Biomol. Struct., 1992, 21, 293-322.
41. Cheng, M. Y.; Hartl, F. U.; Martin, J.; Pollock, R. A.; Kalousek, F.; Neupert, W.; Hallberg, E. M.; Hallberg, R. L.; Horwich, A. L. Mi- tochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature, 1989, 337(6208), 620-625.
42. Liu, Y.; Liu, W.; Song, X. D.; Zuo, J. Effect of GRP75/mthsp70/PBP74/ mortalin overexpression on intracellular ATP level, mitochondrial membrane potential and ROS accumulation following glucose deprivation in PC12 cells. Mol. Cell Biochem., 2005, 268(1-2), 45-51.
43. Yoneda, T.; Benedetti, C.; Urano, F.; Clark, S. G.; Harding, H. P.; Ron, D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci., 2004, 117(18), 4055-4066.
44. Zhao, Q.; Wang, J.; Levichkin, I. V.; Stasinopoulos, S.; Ryan, M. T.; Hoogenraad, N. J. A mitochondrial specific stress response in mammalian cells. EMBO J., 2002, 27(17), 4411-4419.
45. Ran, Q.; Wadhwa, R.; Kawai, R.; Kaul, S. C.; Sifers, R. N.; Bick, R. J.; Smith, J. R.; Pereira-Smith, O. M. Extra-mitochondrial localization of mortalin/mthsp70/PBP74/GRP75. Biochem. Biophys. Res. Commun., 2000, 275(1), 174-179.
46. Passarella, S.; Marra, E.; Atlante, A.; Barile, M.; Doonan, S.; Qua- gliariello, E. Uptake of aspartate aminotransferase into mitochondria in vitro causes efflux of malate dehydrogenase and vice versa. Biochim. Biophys. Acta, 1990, 7022(3), 273-282.
47. Zhou, S. L.; Gordon, R. E.; Bradbury, M.; Stump, D.; Kiang, C. L.; Berk, P. D. Ethanol up-regulates fatty acid uptake and plasma membrane expression and export of mitochondrial aspartate aminotransferase in HepG2 cells. Hepatology, 1998, 27(4), 1064-1074.
48. Venner, T. J.; Singh, B.; Gupta, R. S. Nucleotide sequences and novel structural features of human and Chinese hamster hsp60 (chaperonin) gene families. DNA Cell Biol., 1990, 9(8), 545-552.
49. Singh, B.; Soltys, B. J.; Wu, Z. C.; Patel, H. V.; Freeman, K. B.; Gupta, R. S. Cloning and some novel characteristics of mitochondrial Hsp70 from Chinese hamster cells. Exp. Cell Res., 1997, 234(2), 205-216.
50. Gupta, R. S. Resistance to the microtubule inhibitor podophyllotoxin: selection and partial characterization of mutants in CHO cells. Somatic Cell Genet., 1981, 7(1), 59-71.
51. Soltys, B. J.; Gupta, R. S. Mitochondrial proteins at unexpected cellular locations: export of proteins from mitochondria from an evolutionary perspective. Int. Rev. Cytol., 2000, 794, 133-196.
52. Jones, M.; Gupta, R. S.; Englesberg, E. Enhancement in amount of P1 (hsp60) in mutants of Chinese hamster ovary (CHO-K1) cells exhibiting increases in the A system of amino acid transport. Proc. Natl. Acad. Sci. USA, 1994, 97(3), 858-862.
53. Brudzynski, K.; Martinez, V.; Gupta, R. S. Immunocytochemical localization of heat-shock protein 60-related protein in beta-cell secretory granules and its altered distribution in non-obese diabetic mice. Diabetologia, 1992, 35(4), 316-324.
54. Khan, I. U.; Wallin, R.; Gupta, R. S.; Kammer, G. M. Protein kinase A-catalyzed phosphorylation of heat shock protein 60 chap- erone regulates its attachment to histone 2B in the T lymphocyte plasma membrane. Proc. Natl. Acad. Sci. USA, 1998, 95(18), 10425-10430.
55. Ikawa, S.; Weinberg, R. A. An interaction between p21ras and heat shock protein hsp60, a chaperonin. Proc. Natl. Acad. Sci. USA, 1992, 89(6), 2012-2016.
56. Brocchieri, L.; Conway de Macario, E.; Macario, A. J. Chaper- onomics, a new tool to study ageing and associated diseases. Mech. Ageing Dev., 2007, 728(1), 125-136.
57. Yokoyama, K.; Fukumoto, K.; Murakami, T.; Harada, S.; Hosono, R.; Wadhwa, R.; Mitsui, Y.; Ohkuma, S. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett., 2002, 576(1-3), 53-57.
58. Kimura, K.; Tanaka, N.; Nakamura, N.; Takano, S.; Ohkuma, S. Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in caenorhabditis elegans. J. Biol. Chem., 2007, 282(8), 5910-5918.
59. Macario, A. J.; Conway de Macario, E. Sick chaperones and ageing: a perspective. Ageing Res. Rev., 2002, 7(2), 295-311.
60. Choi, J.; Forster, M. J.; McDonald, S. R.; Weintraub, S. T.; Carroll, C. A.; Gracy, R. W. Proteomic identification of specific oxidized proteins in ApoE-knockout mice: relevance to Alzheimer's disease. FreeRadic. Biol. Med., 2004, 36(9), 1155-1162.
61. Berner, Y. N.; Stern, F. Energy restriction controls aging through neuroendocrine signal transduction. Ageing Res. Rev., 2004, 3(2),189-198.
62. Boxenbaum, H. Commentary: does caloric restriction induce hor-mesis? Hum. Exp. Toxicol., 2000, 79(6), 330-331.
63. Kirkwood, T. B.; Shanley, D. P. Caloric restriction, hormesis and life history plasticity. Hum. Exp. Toxicol., 2000, 79(6), 338-339.
64. Um, J. H.; Kim, S. J.; Kim, D. W.; Ha, M. Y.; Jang, J. H.; Chung, B. S.; Kang, C. D.; Kim, S. H. Tissue-specific changes of DNA repair protein Ku and mtHSP70 in aging rats and their retardation by caloric restriction. Mech. Ageing Dev., 2003, 724(8-9), 967-975.
65. Polyak, K.; Li, Y.; Zhu, H.; Lengauer, C.; Willson, J. K.; Markow- itz, S. D.; Trush, M. A.; Kinzler, K. W.; Vogelstein, B. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat. Genet., 1998, 20(3), 291-293.
66. Soti, C.; Csermely, P. Chaperones and aging: role in neurodegen- eration and in other civilizational diseases. Neurochem. Int., 2002, 47(6), 383-389.
67. Soti, C.; Nardai, G.; Csermely, P. [Stress proteins in medicine]. Orv. Hetil., 2003, 744(13), 605-611.
68. Wadhwa, R.; Takano, S.; Kaur, K.; Deocaris, C. C.; Pereira-Smith, O. M.; Reddel, R. R.; Kaul, S. C. Up-regulation of mor-talin/mthsp70/Grp75 contributes to human carcinogenesis. Int. J. Cancer, 2006, 778(12), 2973-2980.
69. Takano, S.; Wadhwa, R.; Yoshii, Y.; Nose, T.; Kaul, S. C.; Mitsui, Y. Elevated levels of mortalin expression in human brain tumors. Exp. Cell Res., 1997, 237(1), 38-45.
70. 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(1), 74-81.
71. Yi, X.; Luk, J. M.; Lee, N. P.; Peng, J.; Leng, X.; Guan, X. Y.; Lau, G. K.; Beretta, L.; Fan, S. T. Association of mortalin (HSPA9) with liver cancer metastasis and prediction for early tumor recurrence. Mol. Cell Proteomics, 2008, 7(2), 315-325.
72. Smith, D. L.; Evans, C. A.; Pierce, A.; Gaskell, S. J.; Whetton, A. D. Changes in the proteome associated with the action of Bcr-Abl tyrosine kinase are not related to transcriptional regulation. Mol. Cell Proteomics, 2002, 7(11), 876-884.
73. Pizzatti, L.; Sa, L. A.; de Souza, J. M.; Bisch, P. M.; Abdelhay, E. Altered protein profile in chronic myeloid leukemia chronic phase identified by a comparative proteomic study. Biochim. Biophys. Acta, 2006, 7764(5), 929-942.
74. Craven, S. E.; French, D.; Ye, W.; de Sauvage, F.; Rosenthal, A. Loss of Hspa9b in zebrafish recapitulates the ineffective hema- topoiesis of the myelodysplastic syndrome. Blood, 2005, 705(9), 3528-3534.
75. Burkholder, W. F.; Zhao, X.; Zhu, X.; Hendrickson, W. A.; Gragerov, A.; Gottesman, M. E. Mutations in the C-terminal fragment of DnaK affecting peptide binding. Proc. Natl. Acad. Sci. USA, 1996, 93(20), 10632-10637.
76. Wadhwa, R.; Takano, S.; Robert, M.; Yoshida, A.; Nomura, H.; Reddel, R. R.; Mitsui, Y.; Kaul, S. C. Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J. Biol. Chem., 1998, 273(5), 29586-29591.
77. Wadhwa, R.; Sugihara, T.; Yoshida, A.; Nomura, H.; Reddel, R. R.; Simpson, R.; Maruta, H.; Kaul, S. C. Selective toxicity of MKT-077 to cancer cells is mediated by its binding to hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res., 2000, 60(24), 6818-6821.
78. Wadhwa, R.; Kaul, S. C.; Mitsui, Y. Cellular mortality and immortalization: a complex interplay of multiple gene functions. Prog. Mol. Subcell. Biol., 2000, 24, 191-204.
79. Kaul, S. C.; Reddel, R. R.; Mitsui, Y.; Wadhwa, R. An N-terminal region of t-2 binds to p53 in vitro. Neoplasia, 2001, 3(2), 11
80. Taurin, S.; Seyrantepe, V.; Orlov, S. N.; Tremblay, T. L.; Thibault, P.; Bennett, M. R.; Hamet, P. Proteome analysis and functional exression identify mortalin as an antiapoptotic gene induced by elevation of [Na+]i/[K+]i ratio in cultured vascular smooth muscle cells. Circ. Res., 2002, 97(10), 915-922.
81. Mihara, M.; Erster, S.; Zaika, A.; Petrenko, O.; Chittenden, T.; Pancoska, P.; Moll, U. M. p53 has a direct apoptogenic role at the
82. mitochondria. Mol. Cell, 2003, 77(3), 577-590.
83. Wadhwa, R.; Colgin, L.; Yaguchi, T.; Taira, K.; Reddel, R. R.; Kaul, S. C. Rhodacyanine dye MKT-077 inhibits in vitro telom- erase assay but has no detectable effects on telomerase activity in vivo. Cancer Res., 2002, 62(15), 4434-4438.
84. Walker, C.; Bottger, S.; Low, B. Mortalin-based cytoplasmic sequestration of p53 in a nonmammalian cancer model. Am. J. Pathol., 2006, 768(5), 1526-1530.
85. Bottger, S.; Jerszyk, E.; Low, B.; Walker, C. Genotoxic stress- induced expression of p53 and apoptosis in leukemic clam hemo- cytes with cytoplasmically sequestered p53. Cancer Res., 2008,68(3), 777-782.
86. Ma, Z.; Izumi, H.; Kanai, M.; Kabuyama, Y.; Ahn, N. G.; Fuka-sawa, K. Mortalin controls centrosome duplication via modulating centrosomal localization of p53. Oncogene, 2006, 25(39), 5377-5390.
87. Kanai, M.; Ma, Z.; Izumi, H.; Kim, S. H.; Mattison, C. P.; Winey, M.; Fukasawa, K. Physical and functional interaction between mortalin and Mps1 kinase. Genes Cells, 2007, 72(6), 797-810.
88. Massa, S. M.; Longo, F. M.; Zuo, J.; Wang, S.; Chen, J.; Sharp, F. R. Cloning of rat grp75, an hsp70-family member, and its expression in normal and ischemic brain. J. Neurosci. Res., 1995, 40(6), 807-819.
89. Kirmanoglou, K.; Hannekum, A.; Schafler, A. E. Expression of mortalin in patients with chronic atrial fibrillation. Basic Res. Cardiol., 2004, 99(6), 404-408.
90. Dai, Q.; Escobar, G. P.; Hakala, K. W.; Lambert, J. M.; Weintraub, S. T.; Lindsey, M. L. The left ventricle proteome differentiates middle-aged and old left ventricles in mice. J. Proteome Res., 2008, 7(2), 756-765.
91. Yamagishi, N.; Nakayama, K.; Wakatsuki, T.; Hatayama, T. Characteristic changes of stress protein expression in streptozotocin- induced diabetic rats. Life Sci., 2001, 69(22), 2603-2609
92. Zhang, Y.; Wada, J.; Hashimoto, I.; Eguchi, J.; Yasuhara, A.; Kanwar, Y. S.; Shikata, K.; Makino, H. Therapeutic approach for diabetic nephropathy using gene delivery of translocase of inner mitochondrial membrane 44 by reducing mitochondrial superoxide production. J. Am. Soc. Nephrol., 2006, 7 7(4), 1090-1101.
93. Matsuoka, T.; Wada, J.; Hashimoto, I.; Zhang, Y.; Eguchi, J.; Ogawa, N.; Shikata, K.; Kanwar, Y. S.; Makino, H. Gene delivery of Tim44 reduces mitochondrial superoxide production and ameliorates neointimal proliferation of injured carotid artery in diabetic rats. Diabetes, 2005, 54(10), 2882-2890.
94. Vaishnav, R. A.; Getchell, M. L.; Huang, L.; Hersh, M. A.; Strom- berg, A. J.; Getchell, T. V. Cellular and molecular characterization of oxidative stress in olfactory epithelium of Harlequin mutant mouse. J. Neurosci. Res., 2008, 86(1), 165-182.
95. Osorio, C.; Sullivan, P. M.; He, D. N.; Mace, B. E.; Ervin, J. F.; Strittmatter, W. J.; Alzate, O. Mortalin is regulated by APOE in hippocampus of AD patients and by human APOE in TR mice. Neurobiol. Aging. 2007, 28(12), 1853-1862.
96. Calabrese, V.; Scapagnini, G.; Colombrita, C.; Ravagna, A.; Pen- nisi, G.; Giuffrida Stella, A. M.; Galli, F.; Butterfield, D. A. Redox regulation of heat shock protein expression in aging and neurode- generative disorders associated with oxidative stress: a nutritional approach. Amino Acids, 2003, 25(3-4), 437-444.
97. Seyb, K. I.; Ansar, S.; Bean, J.; Michaelis, M. L. beta-Amyloid and endoplasmic reticulum stress responses in primary neurons: effects of drugs that interact with the cytoskeleton. J. Mol. Neurosci., 2006, 28(2), 111-123.
98. Sirk, D.; Zhu, Z.; Wadia, J. S.; Shulyakova, N.; Phan, N.; Fong, J.; Mills, L. R. Chronic exposure to sub-lethal beta-amyloid (Abeta) inhibits the import of nuclear-encoded proteins to mitochondria in differentiated PC12 cells. J. Neurochem., 2007, 705(5), 1989-2003.
99. Jin, J.; Hulette, C.; Wang, Y.; Zhang, T.; Pan, C.; Wadhwa, R.; Zhang, J. Proteomic identification of a stress protein, mor- talin/mthsp70/GRP75: relevance to Parkinson disease. Mol. Cell Proteomics, 2006, 5(7), 1193-1204.
100. Shi, M.; Jin, J.; Wang, Y.; Beyer, R. P.; Kitsou, E.; Albin, R. L.; Gearing, M.; Pan, C.; Zhang, J. Mortalin: a protein associated with progression of Parkinson disease? J. Neuropathol. Exp. Neurol. 2008, 67(2), 117-124.
101. Jin, J.; Li, G. J.; Davis, J.; Zhu, D.; Wang, Y.; Pan, C.; Zhang, J. Identification of novel proteins associated with both alpha-synuclein and DJ-1. Mol. Cell Proteomics, 2007, 6(5), 845-859.
102. Li, H. M.; Niki, T.; Taira, T.; Iguchi-Ariga, S. M.; Ariga, H. Association of DJ-1 with chaperones and enhanced association and colocalization with mitochondrial Hsp70 by oxidative stress. Free Radic. Res., 2005, 59(10), 1091-1099.
103. Van Laar, V. S.; Dukes, A. A.; Cascio, M.; Hastings, T. G. Proteomic analysis of rat brain mitochondria following exposure to dopamine quinone: implications for Parkinson disease. Neurobiol. Dis., 2008, 29(3), 477-489.
104. Houenou, L. J.; Li, L.; Lei, M.; Kent, C. R.; Tytell, M. Exogenous heat shock cognate protein Hsc 70 prevents axotomy-induced death of spinal sensory neurons. Cell Stress Chaperones, 1996, 7(3), 161166.
105. Gifondorwa, D. J.; Robinson, M. B.; Hayes, C. D.; Taylor, A. R.; Prevette, D. M.; Oppenheim, R. W.; Caress, J.; Milligan, C. E. Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis. J. Neurosci., 2007, 27(48), 13173-13180.
106. Johnson, A. D.; Tytell, M. Exogenous HSP70 becomes cell associated, but not internalized, by stressed arterial smooth muscle cells. In Vitro Cell. Dev. Biol. Anim., 1993, 29A, (10) 807-812.
107. Wang, R.; Kovalchin, J. T.; Muhlenkamp, P.; Chandawarkar, R. Y. Exogenous heat shock protein 70 binds macrophage lipid raft mi- crodomain and stimulates phagocytosis, processing, and MHC-II presentation of antigens. Blood, 2006, 707(4), 1636-1642.
108. Wang, R.; Town, T.; Gokarn, V.; Flavell, R. A.; Chandawarkar, R. Y. HSP70 enhances macrophage phagocytosis by interaction with lipid raft-associated TLR-7 and upregulating p38 MAPK and PI3K pathways. J. Surg. Res., 2006, 756(1), 58-69.
109. Kustanova, G. A.; Murashev, A. N.; Karpov, V. L.; Margulis, B. A.; Guzhova, I. V.; Prokhorenko, I. R.; Grachev, S. V.; Evgen'ev, M. B. Exogenous heat shock protein 70 mediates sepsis manifestations and decreases the mortality rate in rats. Cell Stress Chaperones, 2006, 77(3), 276-286.
110. Nishikawa, M.; Takemoto, S.; Takakura, Y. Heat shock protein derivatives for delivery of antigens to antigen presenting cells. Int. J. Pharm., 2008, 554(1-2), 23-27.
111. Kaul, S. C.; Aida, S.; Yaguchi, T.; Kaur, K.; Wadhwa, R. Activation of wild type p53 function by its mortalin-binding cytoplasmi- cally localizing carboxy-terminus peptides. J. Biol. Chem., 2005,280(47), 39373-39379.
112. Pereira-Smith, O. M.; Smith, J. R. Genetic analysis of indefinite division in human cells: identification of four complementation groups. Proc. Natl. Acad. Sci. USA, 1988, 85(16), 6042-6046.
113. Pereira-Smith, O. M.; Ning, Y. Molecular genetic studies of cellular senescence. Exp. Gerontol., 1992, 27(5-6), 519-522.
114. Macario, A. J. Heat-shock proteins and molecular chaperones: implications for pathogenesis, diagnostics, and therapeutics. Int. J. Clin. Lab. Res., 1995, 25(2), 59-70.
115. Hargitai, J.; Lewis, H.; Boros, I.; Racz, T.; Fiser, A.; Kurucz, I.; Benjamin, I.; Vigh, L.; Penzes, Z.; Csermely, P.; Latchman, D. S. Bimoclomol, a heat shock protein co-inducer, acts by the prolonged activation of heat shock factor-1. Biochem. Biophys. Res. Commun., 2003, 507(3), 689-695.
116. Deocaris, C. C.; Shrestha, B. G.; Kraft, D. C.; Yamasaki, K.; Kaul, S. C.; Rattan, S. I.; Wadhwa, R. Geroprotection by glycerol: insights to its mechanisms and clinical potentials. Ann. N. Y. Acad.Sci., 2006, 7067, 488-492.
117. 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(2), 259-269.
118. Campisi, J. Fragile fugue: p53 in aging, cancer and IGF signaling. 2004, Nat. Med., 70(3), 231-232.
119. Campisi, J. Aging, tumor suppression and cancer: high wire-act! Mech. Ageing Dev., 2005, 726(1), 51-58.
120. Michishita, E.; Nakabayashi, K.; Suzuki, T.; Kaul, S. C.; Ogino, H.; Fujii, M.; Mitsui, Y.; Ayusawa, D. 5-Bromodeoxyuridine induces senescence-like phenomena in mammalian cells regardless of cell type or species. J. Biochem., 1999, 726(6), 1052-1059.
121. Widodo, N.; Deocaris, C. C.; Kaur, K.; Hasan, K.; Yaguchi, T.; Yamasaki, K.; Sugihara, T.; Ishii, T.; Wadhwa, R.; Kaul, S. C. Stress chaperones, mortalin, and pex19p mediate 5-aza-2' deoxy- cytidine-induced senescence of cancer cells by DNA methylation- independent pathway. J. Gerontol. A Biol. Sci. Med. Sci., 2007, 62(3), 246-255.
122. Wadhwa, R.; Ando, H.; Kawasaki, H.; Taira, K.; Kaul, S. C. Conventional and RNA helicase coupled hammerhead ribozymes for mortalin. EMBO Rep., 2003, 4(6), 595-601.
123. Deocaris, C. C.; Kaul, S. C.; Wadhwa, R. Use of ribozymes in cellular aging research. Methods Mol. Biol., 2007, 577, 209-226.
124. Wadhwa, R.; Takano, S.; Taira, K.; Kaul, S. C. Reduction in mor- talin level by its antisense expression causes senescence like growth arrest in human immortalized cells. J. Gene Med., 2004, 6(4), 439-444.
125. Lopatin, D. E.; Shelburne, C. E.; Van Poperin, N.; Kowalski, C. J.; Bagramian, R. A. Humoral immunity to stress proteins and perio- dontal disease. 1999, J. Periodontal., 70(10), 1185-1193.
126. Kaul, Z.; Yaguchi, T.; Harada, J. I.; Ikeda, Y.; Hirano, T.; Chiura, H. X.; Kaul, S. C.; Wadhwa, R. An antibody-conjugated internalizing quantum dot suitable for long-term live imaging of cells. Bio- chem. Cell Biol., 2007, 85(1), 133-140.
127. Shiota, M.; Ikeda, Y.; Kaul, Z.; Itadani, J.; Kaul, S. C.; Wadhwa, R. Internalizing antibody-based targeted gene delivery for human cancer cells. Hum. Gene Ther., 2007, 18(11), 1153-1160.
128. Deocaris, C. C.; Taira, K.; Kaul, S. C.; Wadhwa, R. Mimotope- hormesis and mortalin/grp75/mthsp70: a new hypothesis on how infectious disease-associated epitope mimicry may explain low cancer burden in developing nations. FEBS Lett., 2005, 579(3), 586-590.
129. Zhao, T.; Murphy, R. F. Automated learning of generative models for subcellular location: building blocks for systems biology. Cy- tometry A, 2007, 71(12), 978-990.
130. Mizukoshi, E.; Suzuki, M.; Loupatov, A.; Uruno, T.; Hayashi, H.; Misono, T.; Kaul, S. C.; Wadhwa, R.; Imamura, T. Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. Biochem. J., 1999, 343 (2), 461-466.
131. Mizukoshi, E.; Suzuki, M.; Misono, T.; Loupatov, A.; Munekata, E.; Kaul., S. C.; Wadhwa, R.; Imamura, T. Cell-cycle dependent ty- rosine phosphorylation on mortalin regulates its interaction with internalized fibroblast growth factor-1. Biochem. Biophys. Res. Commun., 2001, 280(4), 1203-1209.
132. Sacht, G.; Brigelius-Flohe, R.; Kiess, M.; Sztajer, H.; Flohe, L. ATP-sensitive association of mortalin with the IL-1 receptor type I. 1999, Biofactors, 9(1), 49-60.
133. Wadhwa, R.; Yaguchi, T.; Hasan, M. K.; Taira, K.; Kaul, S. C. Mortalin-MPD (mevalonate pyrophosphate decarboxylase) interactions and their role in control of cellular proliferaction. Biochem. Biophys. Res. Commun., 2003, 302(4), 735-742.
134. Wang, R.; Town, T.; Gokarn, V.; Flavell, R. A.; Chandawarkar, R. Y. HSP70 enhances macrophage phagocytosis by interaction with lipid raft-associated TLR-7 and upregulating p38 MAPK and PI3K pathways. J. Surg. Res., 2006, 136(1), 58-69.
135. Kim, K. B.; Lee, J. W.; Lee, C. S.; Kim, B. W.; Choo, H. J.; Jung, S. Y.; Chi,S. G.; Yoon, Y. S.; Yoon, G.; Ko, Y. G. Oxidation- reduction respiratory chains and ATP synthase complex are localized in detergent-resistant lipid rafts. Proteomics, 2006, 6(8), 24442453.
136. Kuwabara, H.; Yoneda, M.; Hayasaki, H.; Nakamura, T.; Mori, H. Glucose regulated proteins 78 and 75 bind to the receptor for hyaluronan mediated motility in interphase microtubules. Biochem. Biophys. Res. Commun., 2006, 339(3), 971-976.