From proliferative to neurological role of an hsp70 stress chaperone, mortalin

Biogerontology

Volumn 9, Issue 6, 2008, Pages 391-403

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

^a UNIVERSITY OF TSUKUBA   (Japan)

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

Author keywords

Adult neurogenesis; Chaperone; CNS; Mitochondrial functions; Mortalin; Neurodegenerative diseases; Oxidative stress

Indexed keywords

BIOLOGICAL MARKER; CALCIUM; CHAPERONE; CYTOKINE; GROWTH FACTOR; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE; MORTALIN; PROTEIN P53; PROTEOME; RAF PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; AGING; ALZHEIMER DISEASE; APOPTOSIS; BIOGENESIS; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL AGING; CELL ORGANELLE; CENTROSOME; CONFERENCE PAPER; CYTOPLASM; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HEART OUTPUT; HOMEOSTASIS; HUMAN; METABOLISM; MITOCHONDRION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN TRANSPORT; PROTEOMICS; REGULATORY MECHANISM; RISK FACTOR;

AGING; BRAIN; CELL DIVISION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MITOCHONDRIA; NEURODEGENERATIVE DISEASES;

EID: 56049114860     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-008-9174-2     Document Type: Conference Paper

References (114)

1. Andersson SG, Karlberg O, Canbäck B, Kurland CG (2003) On the origin of mitochondria: A genomics perspective. Philos Trans R Soc Lond B Biol Sci 358:165-177. doi: 10.1098/rstb.2002.1193
2. 2+ network. J Cell Biol 136:833-844. doi: 10.1083/jcb.136.4.833
3. Bhattacharyya T, Karnezis AN, Murphy SP, Hoang T, Freeman BC, Phillips B et al (1995) Cloning and subcellular localization of human mitochondrial hsp70. J Biol Chem 270:1705-1710. doi: 10.1074/jbc.270.4.1705
4. Bota DA, Davies KJ (2001) Protein degradation in mitochondria: implications for oxidative stress, aging and disease: A novel etiological classification of mitochondrial proteolytic disorders. Mitochondrion 1:33-49. doi: 10.1016/S1567-7249(01)00005-8
5. Bota DA, Davies KJ (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4:674-680. doi: 10.1038/ncb836
6. Bruschi SA, Lindsay JG (1994) Mitochondrial stress protein actions during chemically induced renal proximal tubule cell death. Biochem Cell Biol 72:663-667
7. Bruschi SA, West KA, Crabb JW, Gupta RS, Stevens JL (1993) Mitochondrial HSP60 (P1 protein) and a HSP70-like protein (mortalin) are major targets for modification during S-(1, 1, 2, 2-tetrafluoroethyl)-l-cysteine-induced nephrotoxicity. J Biol Chem 268:23157-23161
8. Bruschi SA, Lindsay JG, Crabb JW (1998) Mitochondrial stress protein recognition of inactivated dehydrogenases during mammalian cell death. Proc Natl Acad Sci USA 95:13413-13418. doi: 10.1073/pnas.95.23.13413
9. Bryant SS, Briggs S, Smithgall TE, Martin GA, McCormick F, Chang JH et al (1995) Two SH2 domains of p120 Ras GTPase-activating protein bind synergistically to tyrosine phosphorylated p190 Rho GTPase-activating protein. J Biol Chem 270:17947-17952. doi: 10.1074/jbc.270.30.17947
10. Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L (2008) In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 56:412-425. doi: 10.1002/glia.20616
11. Cajal RY (1928) Degeneration and regeneration of the nervous system (Translated by RM Day from the 1913 Spanish edition) (Oxford University Press)
12. Chang DT, Reynolds IJ (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 80:241-268. doi: 10.1016/ j.pneurobio.2006.09.003
13. Cheng MY, Hartl FU, Martin J, Pollock RA, Kalousek F, Neupert W et al (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337:620-625. doi: 10.1038/337620a0
14. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M et al (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010-1014. doi: 10.1126/science.1092734
15. Choi J, Forster MJ, McDonald SR, Weintraub ST, Carroll CA, Gracy RW (2004) Proteomic identification of specific oxidized proteins in ApoE-knockout mice: Relevance to Alzheimer's disease. Free Radic Biol Med 36:1155-1162. doi: 10.1016/j.freeradbiomed.2004.02.002
16. Cooper AJ, Wang J, Gartner CA, Bruschi SA (2001) Co-purification of mitochondrial HSP70 and mature protein disulfide isomerase with a functional rat kidney high-M(r) cysteine S-conjugate beta-lyase. Biochem Pharmacol 62:1345-1353. doi: 10.1016/S0006-2952(01)00802-4
17. Cooper AJ, Bruschi SA, Anders MW (2002) Toxic, halogenated cysteine S-conjugates and targeting of mitochondrial enzymes of energy metabolism. Biochem Pharmacol 64:553-564. doi: 10.1016/ S0006-2952(02)01076-6
18. Craig EA, Kramer J, Kosic-Smithers J (1987) SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc Natl Acad Sci USA 84:4156-4160. doi: 10.1073/ pnas.84.12.4156
19. Craig EA, Kramer J, Shilling J, Werner-Washburne M, Holmes S, Kosic-Smithers J et al (1989) SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol Cell Biol 9:3000-3008
20. Davis JE, Voisine C, Craig EA (1999) Intragenic suppressors of Hsp70 mutants: Interplay between the ATPase- and peptide-binding domains. Proc Natl Acad Sci USA 96:9269-9276. doi: 10.1073/pnas.96.16.9269
21. Deocaris CC, Kaul SC, Wadhwa R (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperones 11:116-128. doi: 10.1379/CSC-144R.1
22. Deocaris CC, Widodo N, Shrestha BG, Kaur K, Ohtaka M, Yamasaki K et al (2007) Mortalin sensitizes human cancer cells to MKT-077-induced senescence. Cancer Lett 252:259-269. doi: 10.1016/j.canlet.2006.12.038
23. Deocaris CC, Takano S, Priyandoko D, Kaul Z, Yaguchi T, Kraft DC et al (2008) Glycerol stimulates innate chaperoning, proteasomal and stress-resistance functions: Implications for geronto-manipulation. Biogerontology 9(4):269-282
24. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK (2006) Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 26:9057-9068. doi: 10.1523/ JNEUROSCI.1469-06.2006
25. Domanico SZ, DeNagel DC, Dahlseid JN, Green JM, Pierce SK (1993) 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 13:3598-3610
26. Erecinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 43:37-71. doi: 10.1016/0301-0082(94)90015-9
27. Erecinska M, Nelson D, Yudkoff M, Silver IA (1994) Energetics of the nerve terminal in relation to central nervous system function. Biochem Soc Trans 22:959-965
28. Feng Y, Ariza ME, Goulet AC, Shi J, Nelson MA (2005) Death signal induced relocalization of cyclin dependent kinase 11 to mitochondria. Biochem J 392:65-73. doi: 10.1042/BJ20050195
29. Frazier AE, Chacinska A, Truscott KN, Guiard B, Pfanner N, Rehling P (2003) Mitochondria use different mechanisms for transport of multispanning membrane proteins through the intermembrane space. Mol Cell Biol 23:7818-7828. doi: 10.1128/MCB.23.21.7818-7828.2003
30. Geissler A, Rassow J, Pfanner N, Voos W (2001) Mitochondrial import driving forces: Enhanced trapping by matrix Hsp70 stimulates translocation and reduces the membrane potential dependence of loosely folded preproteins. Mol Cell Biol 21:7097-7104. doi: 10.1128/ MCB.21.20.7097-7104.2001
31. Goering PL, Fisher BR, Noren BT, Papaconstantinou A, Rojko JL, Marler RJ (2000) Mercury induces regional and cell-specific stress protein expression in rat kidney. Toxicol Sci 53:447-457. doi: 10.1093/toxsci/ 53.2.447
32. Hall CL, Collis LA, Bo AJ, Lange L, McNicol A, Gerrard JM et al (2001) Fibroblasts require protein kinase C activation to respond to hyaluronan with increased locomotion. Matrix Biol 20:183-192. doi: 10.1016/ S0945-053X(01)00133-0
33. Horst M, Oppliger W, Rospert S, Schonfeld HJ, Schatz G, Azem A (1997) Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J 16:1842-1849. doi: 10.1093/emboj/16.8.1842
34. Huang S, Ratliff KS, Matouschek A (2002) Protein unfolding by the mitochondrial membrane potential. Nat Struct Biol 9:301-307. doi: 10.1038/nsb772
35. Hunzinger C, Wozny W, Schwall GP, Poznanovic S, Stegmann W, Zengerling H et al (2006) Comparative profiling of the mammalian mitochondrial proteome: Multiple aconitase-2 isoforms including N -formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species. J Proteome Res 5:625-633. doi: 10.1021/pr050377+
36. Jin J, Hulette C, Wang Y, Zhang T, Pan C, Wadhwa R et al (2006) Proteomic identification of a Stress Protein, Mortalin/mthsp70/GRP75: relevance to Parkinson disease. Mol Cell Proteomics 5:1193-1204. doi: 10.1074/mcp.M500382-MCP200
37. Kanai M, Ma Z, Izumi H, Kim SH, Mattison CP, Winey M et al (2007) Physical and functional interaction between mortalin and Mps1 kinase. Genes Cells 12:797-810
38. Kaneko N, Kudo K, Mabuchi T, Takemoto K, Fujimaki K, Wati H et al (2006) Suppression of cell proliferation by interferon-alpha through interleukin-1 production in adult rat dentate gyrus. Neuropsychopharmacology 31:2619-2626. doi: 10.1038/sj.npp.1301137
39. Kann O, Kovacs R (2007) Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292:C641-C657. doi: 10.1152/ajpcell.00222.2006
40. Kaul SC, Aida S, Yaguchi T, Kaur K, Wadhwa R (2005) Activation of wild type p53 function by its mortalin-binding, cytoplasmically localizing carboxyl terminus peptides. J Biol Chem 280:39373-39379. doi: 10.1074/ jbc.M500022200
41. Kaul SC, Deocaris CC, Wadhwa R (2007) Three faces of mortalin: A housekeeper, guardian and killer. Exp Gerontol 42:263-274. doi: 10.1016/ j.exger.2006.10.020
42. Kimura K, Tanaka N, Nakamura N, Takano S, Ohkuma S (2007) Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. J Biol Chem 282:5910-5918. doi: 10.1074/ jbc.M609025200
43. Kuwabara H, Yoneda M, Hayasaki H, Nakamura T, Mori H (2006) Glucose regulated proteins 78 and 75 bind to the receptor for hyaluronan mediated motility in interphase microtubules. Biochem Biophys Res Commun 339:971-976. doi: 10.1016/j.bbrc.2005.11.101
44. Leonhard K, Stiegler A, Neupert W, Langer T (1999) Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature 398:348-351. doi: 10.1038/18704
45. Liu Y, Liu W, Song XD, Zuo J (2005) 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 268:45-51. doi: 10.1007/s11010-005-2996-1
46. Ma Z, Izumi H, Kanai M, Kabuyama Y, Ahn NG, Fukasawa K (2006) Mortalin controls centrosome duplication via modulating centrosomal localization of p53. Oncogene 25:5377-5390. doi: 10.1038/sj.onc.1209543
47. Macario AJ, Conway de Macario E (2007a) Chaperonopathies by defect, excess, or mistake. Ann N Y Acad Sci 1113:178-191. doi: 10.1196/ annals.1391.009
48. Macario AJ, Conway de Macario E (2007b) Chaperonopathies and chaperonotherapy. FEBS Lett 581:3681-3688. doi: 10.1016/ j.febslet.2007.04.030
49. Macario AJ, Conway de Macario E (2007c) Molecular chaperones: Multiple functions, pathologies, and potential applications. Front Biosci 12:2588-2600. doi: 10.2741/2257
50. Mannella CA, Buttle K, Rath BK, Marko M (1998) Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8:225-228
51. Massa SM, Longo FM, Zuo J, Wang S, Chen J, Sharp FR (1995) Cloning of rat grp75, an hsp70-family member, and its expression in normal and ischemic brain. J Neurosci Res 40:807-819. doi: 10.1002/jnr.490400612
52. Matouschek A, Azem A, Ratliff K, Glick BS, Schmid K, Schatz G (1997) Active unfolding of precursor proteins during mitochondrial protein import. EMBO J 16:6727-6736. doi: 10.1093/emboj/16.22.6727
53. Mattson MP (2006) Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders. Antioxid Redox Signal 8:1997-2006. doi: 10.1089/ars.2006.8.1997
54. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6:337-350. doi: 10.1111/j.1474-9726.2007.00275.x
55. Michishita E, Nakabayashi K, Suzuki T, Kaul SC, Ogino H, Fujii M et al (1999) 5-Bromodeoxyuridine induces senescence-like phenomena in mammalian cells regardless of cell type or species. J Biochem 126:1052-1059
56. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577-590. doi: 10.1016/S1097-2765(03)00050-9
57. Mizukoshi E, Suzuki M, Loupatov A, Uruno T, Hayashi H, Misono T et al (1999) Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. Biochem J 343:461-466. doi: 10.1042/ 0264-6021:3430461
58. Mizukoshi E, Suzuki M, Misono T, Loupatov A, Munekata E, Kaul SC et al (2001) Cell-cycle dependent tyrosine phosphorylation on mortalin regulates its interaction with fibroblast growth factor-1. Biochem Biophys Res Commun 280:1203-1209. doi: 10.1006/bbrc.2001.4225
59. Nottebohm F (1981) A brain for all seasons: Cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368-1370. doi: 10.1126/science.7313697
60. O'Donnell MP, Kasiske BL, Kim Y, Atluru D, Keane WF (1993) The mevalonate pathway: Importance in mesangial cell biology and glomerular disease. Miner Electrolyte Metab 19:173-179
61. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D et al (2004) The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem 279:25689-25695. doi: 10.1074/ jbc.M401844200
62. Osorio C, Sullivan PM, He DN, Mace BE, Ervin JF, Strittmatter WJ et al (2007) Mortalin is regulated by APOE in hippocampus of AD patients and by human APOE in TR mice. Neurobiol Aging 28:1853-1862. doi: 10.1016/ j.neurobiolaging.2006.08.011
63. Ostermann J, Voos W, Kang PJ, Craig EA, Neupert W, Pfanner N (1990) Precursor proteins in transit through mitochondrial contact sites interact with hsp70 in the matrix. FEBS Lett 277:281-284. doi: 10.1016/ 0014-5793(90)80865-G
64. Pilzer D, Fishelson Z (2005) Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis. Int Immunol 17:1239-1248. doi: 10.1093/intimm/ dxh300
65. Pilzer D, Gasser O, Moskovich O, Schifferli JA, Fishelson Z (2005) Emission of membrane vesicles: Roles in complement resistance, immunity and cancer. Springer Semin Immunopathol 27:375-387. doi: 10.1007/ s00281-005-0004-1
66. Pimentel B, Sanz C, Varela-Nieto I, Rapp UR, De Pablo F, de La Rosa EJ (2000) c-Raf regulates cell survival and retinal ganglion cell morphogenesis during neurogenesis. J Neurosci 20:3254-3262
67. Poindexter BJ, Pereira-Smith O, Wadhwa R, Buja LM, Bick RJ (2002) 3D reconstruction and localization of mortalin by deconvolution microscopy. Microsc Anal 89:21-23
68. Ran Q, Wadhwa R, Kawai R, Kaul SC, Sifers RN, Bick RJ et al (2000) Extramitochondrial localization of mortalin/mthsp70/PBP74/GRP75. Biochem Biophys Res Commun 275:174-179. doi: 10.1006/bbrc.2000.3237
69. Rivolta MN, Holley MC (2002) Asymmetric segregation of mitochondria and mortalin correlates with the multi-lineage potential of inner ear sensory cell progenitors in vitro. Brain Res Dev Brain Res 133:49-56. doi: 10.1016/S0165-3806(01)00321-2
70. 2+ responses. Science 280:1763-1766. doi: 10.1126/science.280.5370.1763
71. Sacht G, Brigelius-Flohe R, Kiess M, Sztajer H, Flohe L (1999) ATP-sensitive association of mortalin with the IL-1 receptor type I. Biofactors 9:49-60
72. Sanjuan Szklarz LK, Guiard B, Rissler M, Wiedemann N, Kozjak V, van der Laan M et al (2005) Inactivation of the mitochondrial heat shock protein zim17 leads to aggregation of matrix hsp70s followed by pleiotropic effects on morphology and protein biogenesis. J Mol Biol 351:206-218. doi: 10.1016/j.jmb.2005.05.068
73. Savel'ev AS, Novikova LA, Kovaleva IE, Luzikov VN, Neupert W, Langer T (1998) ATP-dependent proteolysis in mitochondria. m-AAA protease and PIM1 protease exert overlapping substrate specificities and cooperate with the mtHsp70 system. J Biol Chem 273:20596-20602. doi: 10.1074/ jbc.273.32.20596
74. Saveliev AS, Kovaleva IE, Novikova LA, Isaeva LV, Luzikov VN (1999) Can foreign proteins imported into yeast mitochondria interfere with PIM1p protease and/or chaperone function? Arch Biochem Biophys 363:373-376. doi: 10.1006/abbi.1998.1092
75. Schneider HC, Berthold J, Bauer MF, Dietmeier K, Guiard B, Brunner M et al (1994) Mitochondrial Hsp70/MIM44 complex facilitates protein import. Nature 371:768-774. doi: 10.1038/371768a0
76. Schwarzer C, Barnikol-Watanabe S, Thinnes FP, Hilschmann N (2002) Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int J Biochem Cell Biol 34:1059-1070. doi: 10.1016/S1357-2725(02)00026-2
77. Sherman MY, Goldberg AL (1993) Heat shock of Escherichia coli increases binding of dnaK (the hsp70 homolog) to polypeptides by promoting its phosphorylation. Proc Natl Acad Sci USA 90:8648-8652. doi: 10.1073/ pnas.90.18.8648
78. Shi M, Jin J, Wang Y, Beyer RP, Kitsou E, Albin RL et al (2008) Mortalin: A protein associated with progression of parkinson disease? J Neuropathol Exp Neurol 67:117-124. doi: 10.1097/nen.0b013e318163354a
79. Shin BK, Wang H, Yim AM, Le Naour F, Brichory F, Jang JH et al (2003) Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J Biol Chem 278:7607-7616. doi: 10.1074/jbc.M210455200
80. Silver I, Erecinska M (1998) Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol 454:7-16
81. Soltys BJ, Gupta RS (1999) Mitochondrial-matrix proteins at unexpected locations: Are they exported? Trends Biochem Sci 24:174-177. doi: 10.1016/S0968-0004(99)01390-0
82. Soltys BJ, Gupta RS (2000) Mitochondrial proteins at unexpected cellular locations: Export of proteins from mitochondria from an evolutionary perspective. Int Rev Cytol 194:133-196. doi: 10.1016/ S0074-7696(08)62396-7
83. Stacchiotti A, Lavazza A, Rezzani R, Borsani E, Rodella L, Bianchi R (2004) Mercuric chloride-induced alterations in stress protein distribution in rat kidney. Histol Histopathol 19:1209-1218
84. Stadtman ER (2006) Protein oxidation and aging. Free Radic Res 40:1250-1258. doi: 10.1080/10715760600918142
85. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321-336. doi: 10.1016/0891-5849(94)00159-H
86. Strub A, Zufall N, Voos W (2003) The putative helical lid of the Hsp70 peptide-binding domain is required for efficient preprotein translocation into mitochondria. J Mol Biol 334:1087-1099
87. Sullivan PG, Dragicevic NB, Deng JH, Bai Y, Dimayuga E, Ding Q et al (2004) Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover. J Biol Chem 279:20699-20707. doi: 10.1074/ jbc.M313579200
88. 2+ channels. J Cell Biol 175:901-911. doi: 10.1083/jcb.200608073
89. Takano S, Wadhwa R, Yoshii Y, Nose T, Kaul SC, Mitsui Y (1997) Elevated levels of mortalin expression in human brain tumors. Exp Cell Res 237:38-45. doi: 10.1006/excr.1997.3754
90. Takano S, Wadhwa R, Mitsui Y, Kaul SC (2001) Identification and characterization of molecular interactions between glucose-regulated proteins (GRPs) mortalin/GRP75/peptide-binding protein 74 (PBP74) and GRP94. Biochem J 357:393-398. doi: 10.1042/0264-6021:3570393
91. Temple S, Qian X (1995) bFGF, neurotrophins, and the control or cortical neurogenesis. Neuron 15:249-252. doi: 10.1016/0896-6273(95)90030-6
92. Tong JJ (2007) Mitochondrial delivery is essential for synaptic potentiation. Biol Bull 212:169-175
93. Truscott KN, Brandner K, Pfanner N (2003) Mechanisms of protein import into mitochondria. Curr Biol 13:R326-R337. doi: 10.1016/ S0960-9822(03)00239-2
94. Uberti D, Piccioni L, Cadei M, Grigolato P, Rotter V, Memo M (2001) p53 is dispensable for apoptosis but controls neurogenesis of mouse dentate gyrus cells following gamma-irradiation. Brain Res Mol Brain Res 93:81-89. doi: 10.1016/S0169-328X(01)00180-2
95. Van Laar VS, Dukes AA, Cascio M, Hastings TG (2008) Proteomic analysis of rat brain mitochondria following exposure to dopamine quinone: implications for Parkinson disease. Neurobiol Dis 29:477-489. doi: 10.1016/j.nbd.2007.11.007
96. Wadhwa R, Kaul SC, Ikawa Y, Sugimoto Y (1993a) Identification of a novel member of mouse hsp70 family. Its association with cellular mortal phenotype. J Biol Chem 268:6615-6621
97. Wadhwa R, Kaul SC, Sugimoto Y, Mitsui Y (1993b) Induction of cellular senescence by transfection of cytosolic mortalin cDNA in NIH 3T3 cells. J Biol Chem 268:22239-22242
98. Wadhwa R, Pereira-Smith OM, Reddel RR, Sugimoto Y, Mitsui Y, Kaul SC (1995) Correlation between complementation group for immortality and the cellular distribution of mortalin. Exp Cell Res 216:101-106. doi: 10.1006/excr.1995.1013
99. Wadhwa R, Takano S, Robert M, Yoshida A, Nomura H, Reddel RR et al (1998) Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J Biol Chem 273:29586-29591. doi: 10.1074/jbc.273.45.29586
100. Wadhwa R, Sugihara T, Yoshida A, Nomura H, Reddel RR, Simpson R et al (2000) Selective toxicity of MKT-077 to cancer cells is mediated by its binding to the hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res 60:6818-6821
101. Wadhwa R, Colgin L, Yaguchi T, Taira K, Reddel RR, Kaul SC (2002) Rhodacyanine dye MKT-077 inhibits in vitro telomerase assay but has no detectable effects on telomerase activity in vivo. Cancer Res 62:4434-4438
102. Wadhwa R, Ando H, Kawasaki H, Taira K, Kaul SC (2003a) Targeting mortalin using conventional and RNA-helicase-coupled hammerhead ribozymes. EMBO Rep 4:595-601. doi: 10.1038/sj.embor.embor855
103. Wadhwa R, Yaguchi T, Hasan MK, Taira K, Kaul SC (2003b) Mortalin-MPD (mevalonate pyrophosphate decarboxylase) interactions and their role in control of cellular proliferation. Biochem Biophys Res Commun 302:735-742. doi: 10.1016/S0006-291X(03)00226-2
104. Wadhwa R, Takano S, Taira K, Kaul SC (2004) Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J Gene Med 6:439-444. doi: 10.1002/jgm.530
105. Wadhwa R, Takano S, Kaur K, Aida S, Yaguchi T, Kaul Z et al (2005) Identification and characterization of molecular interactions between mortalin/mtHsp70 and HSP60. Biochem J 391:185-190. doi: 10.1042/ BJ20050861
106. Wagner I, Arlt H, van Dyck L, Langer T, Neupert W (1994) Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J 13:5135-5145
107. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu Rev Genet 39:359-407. doi: 10.1146/annurev.genet.39.110304.095751
108. Walter L, Hajnoczky G (2005) Mitochondria and endoplasmic reticulum: The lethal interorganelle cross-talk. J Bioenerg Biomembr 37:191-206. doi: 10.1007/s10863-005-6600-x
109. Wang C, Thor AD, Moore DH 2nd, Zhao Y, Kerschmann R, Stern R et al (1998) The overexpression of RHAMM, a hyaluronan-binding protein that regulates ras signaling, correlates with overexpression of mitogen-activated protein kinase and is a significant parameter in breast cancer progression. Clin Cancer Res 4:567-576
110. Widodo N, Deocaris CC, Kaur K, Hasan K, Yaguchi T, Yamasaki K et al (2007) Stress chaperones, mortalin, and pex19p mediate 5-aza-2′ deoxycytidine-induced senescence of cancer cells by DNA methylation-independent pathway. J Gerontol A Biol Sci Med Sci 62:246-255
111. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T et al (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25:778-791. doi: 10.1523/JNEUROSCI.4235-04.2005
112. Zhang S, Chang MC, Zylka D, Turley S, Harrison R, Turley EA (1998) The hyaluronan receptor RHAMM regulates extracellular-regulated kinase. J Biol Chem 273:11342-11348. doi: 10.1074/jbc.273.18.11342
113. Zheng DH, Zuo J, Yang ZJ, Xia BL, Zhang XN (2000) Grp75 protects cells from injuries caused by glucose deprivation. Yi Chuan Xue Bao 27:666-671
114. Zinsmaier KE, Bronk P (2001) Molecular chaperones and the regulation of neurotransmitter exocytosis. Biochem Pharmacol 62:1-11. doi: 10.1016/ S0006-2952(01)00648-7