Upregulation of mortalin/mthsp70/Grp75 contributes to human carcinogenesis

International Journal of Cancer

Volumn 118, Issue 12, 2006, Pages 2973-2980

  Wadhwa, Renu ^a,b   Takano, Syuichi ^c   Kaur, Kamaljit ^a   Deocaris, Custer C ^a,b   Pereira Smith, Olivia M ^d   Reddel, Roger R ^e   Kaul, Sunil C ^a  

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

^b UNIVERSITY OF TOKYO   (Japan)

^c KANAZAWA UNIVERSITY   (Japan)

^d Barshop Institute for Longevity and Aging Studies   (United States)

^e CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Chemotaxis; E6; E7; Expression; GRP75; Human papillomavirus; Metastasis; Mortalin; mot 2; mthsp70; Nude mice assay; TERT; Tumors

Indexed keywords

COMPLEMENTARY DNA; GENOMIC DNA; HEAT SHOCK PROTEIN 70; MORTALIN; PROTEIN P53; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CARCINOGENESIS; CELL IMMORTALIZATION; CHEMOTAXIS; CONTROLLED STUDY; DNA FINGERPRINTING; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALIGNANT TRANSFORMATION; METASTASIS; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; UPREGULATION; WART VIRUS; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHEMOTAXIS; DNA FINGERPRINTING; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HSP70 HEAT-SHOCK PROTEINS; HUMAN PAPILLOMAVIRUS 6; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; TELOMERASE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 33646409045     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21773     Document Type: Article

References (46)

1. Wadhwa R, Kaul SC, Ikawa Y, Sugimoto Y. Identification of a novel member of mouse hspVO family. Its association with cellular mortal phenotype. J Biol Chem 1993;268:6615-21.
2. Craig EA, Kramer J, Shilling J, Werner-Washburne M, Holmes S, Kosic-Smithers J, Nicolet CM. SSCI, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol Cell Biol 1989;9:3000-8.
3. Kaul SC, Taira K, Pereira-Smith OM, Wadhwa R. Mortalin: present and prospective. Exp Gerontol 2002;37:1157-64.
4. Merrick BA, Walker VR, He C, Patterson RM, Selkirk JK. Induction of novel Grp75 isoforms by 2-deoxyglucose in human and murine fibroblasts. Cancer Lett 1997;119:185-90.
5. Wadhwa R, Taira K, Kaul SC. Mortalin: a potential candidate for biotechnology and biomedicine. Histol Histopathol 2002;17:1173-7.
6. Wadhwa R, Taira K, Kaul SC. An hsp70 family chaperone, mortalin/ mthsp70/PBP74/Grp75: what, when and where? Cell Stress Chaperones 2002;7:309-16.
7. Ran Q, Wadhwa R, Kawai R, Kaul SC, Sifers RN, Bick RJ, Smith JR, Pereira-Smith OM. Extramitochondrial localization of mortalin/ mthsp70/PBP74/GRP75. Biochem Biophys Res Commun 2000;275: 174-9.
8. Wadhwa R, Kaul SC, Mitsui Y, Sugimoto Y. Differential subcellular distribution of mortalin in mortal and immortal mouse and human fibroblasts. Exp Cell Res 1993;207:442-8.
9. Wadhwa R, Takano S, Robert M, Yoshida A, Nomura H, Reddel RR, Mitsui Y, Kaul SC. Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J Biol Chem 1998;273:29586-91.
10. Mizukoshi E, Suzuki M, Loupatov A, Uruno T, Hayashi H, Misono T, Kaul SC, Wadhwa R, Imamura T. Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. Biochem J 1999;343:461-6.
11. Sacht G, Brigelius-Flohe R, Kiess M, Sztajer H, Flohe L. ATP-sensitive association of mortalin with the IL-1 receptor type I. Biofactors 1999;9:49-60.
12. Takano S, Wadhwa R, Mitsui Y, Kaul SC. Identification and characterization of molecular interactions between glucose-regulated proteins (GRPs) mortalin/GRP75/peptide-binding protein 74 (PBP74) and GRP94. Biochem J 2001;357:393-8.
13. Schwarzer C, Barnikol-Watanabe S, Thinnes FP, Hilschmann N. Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int J Biochem Cell Biol 2002;34:1059-70.
14. Wadhwa R, Yaguchi T, Hasan MK, Taira K, Kaul SC. Mortalin-MPD (mevalonate pyrophosphate decarboxylase) interactions and their role in control of cellular proliferation. Biochem Biophys Res Commun 2003;302:735-42.
15. Wadhwa R, Yaguchi T, Hasan MK, Mitsui Y, Reddel RR, Kaul SC. Hsp70 family member, mot-2/mthsp70/grp75, binds to the cytoplasmic sequestration domain of the p53 protein. Exp Cell Res 2002; 274:246-53.
16. Kaul SC, Reddel RR, Mitsui Y, Wadhwa R. An N-terminal region of mot-2 binds to p53 in vitro. Neoplasia 20013:110-14.
17. Kaul SC, Reddel RR, Sugihara T, Mitsui Y, Wadhwa R. Inactivation of p53 and life span extension of human diploid fibroblasts by mot-2. FEBS Lett 2000;474:159-64.
18. Kaul SC, Yaguchi T, Taira K, Reddel RR Wadhwa R. Overexpressed mortalin (mot-2)/mthsp70/GRP75 and hTERT cooperate to extend the in vitro lifespan of human fibroblasts. Exp Cell Res 2003;286:96-101.
19. Kaul SC, Duncan EL, Englezou A, Takano S, Reddel RR, Mitsui Y, Wadhwa R. Malignant transformation of NIH3T3 cells by overexpression of mot-2 protein. Oncogene 1998;17:907-11.
20. Xu J, Xiao HH, Sartorelli AC. Attenuation of the induced differentia-tion of HL-60 leukemia cells by mitochondrial chaperone HSP70. Oncol Res 1999;11:429-35.
21. 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;516:53-7.
22. Webster TJ, Naylor DJ, Hartman DJ, Hoj PB, Hoogenraad NJ. cDNA cloning and efficient mitochondrial import of pre-mtHSP70 from rat liver. DNA Cell Biol 1994;13:1213-20.
23. Truscott KN, Brandner K, Pfanner N. Mechanisms of protein import into mitochondria. CurrBiol 2003;13:R326-37.
24. Krimmer T, Rassow J, Kunau WH, Voos W, Pfanner N. Mitochondrial protein import motor: the ATPase domain of matrix Hsp70 is crucial for binding to Tim44, while the peptide binding domain and the carboxy-terminal segment play a stimulatory role. Mol Cell Biol 2000;20:5879-87.
25. Wadhwa R, Ando H, Kawasaki H, Taira K, Kaul SC. Targeting mortalin using conventional and RNA-helicase-coupled hammerhead ribozymes. EMBO Rep 2003;4:595-601.
26. Wadhwa R, Takano S, Taira K, Kaul SC. Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J Gene Med 2004;6:439-44.
27. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE. Extension of lifespan by introduction of telomerase into normal human cells. Science 1998;279:349-52.
28. Jiang XR, Jimenez G, Chang E, Frolkis M, Kusler B, Sage M, Beeche M, Bodnar AG, Wahl GM, Tlsty TD, Chiu CP. Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat Genet 1999;21:111-14.
29. Yang J, Chang E, Cherry AM, Bangs CD, Oei Y, Bodnar A, Bronstein A, Chiu CP, Herron GS. Human endothelial cell life extension by telomerase expression. J Biol Chem 1999;274:26141-8.
30. Alvero AB, Fishman DA, Qumsiyeh MB, Garg M, Kacinski BM, Sapi E. Telomerase prolongs the lifespan of normal human ovarian surface epithelial cells without inducing neoplastic phenotype. J Soc Gynecol Investig 2004;11:553-61.
31. Milyavsky M, Shats I, Erez N, Tang X, Senderovich S, Meerson A, Tabach Y, Goldfinger N, Ginsberg D, Harris CC, Rotter V. Prolonged culture of telomerase-immortalized human fibroblasts leads to a premalignant phenotype. Cancer Res 2003;63:7147-57.
32. Noble JR, Zhong ZH, Neumann AA, Melki JR, Clark SJ, Reddel RR. Alterations in the p16(INK4a) and p53 tumor suppressor genes of hTERT-immortalized human fibroblasts. Oncogene 2004;23: 3116-21.
33. Di Felice V, Ardizzone N, Marciano V, Bartolotta T, Cappello F, Farina F, Zummo G. Senescence-associated HSP60 expression in normal human skin fibroblasts. Anat Rec A Discov Mol Cell Evol Biol 2005;284:446-53.
34. Di Felice V, David S, Cappello F, Farina F, Zummo G. Is chlamydial heat shock protein 60 a risk factor for oncogenesis? Cell Mol Life Sci 2005;62:4-9.
35. Cappello F, Bellafiore M, Palma A, Marciano V, Martorana G, Belfiore P, Martorana A, Farina F, Zummo G, Bucchieri F. Expression of 60-kD heat shock protein increases during carcinogenesis in the uterine exocervix. Pathobiology 2002;70:83-8.
36. Cappello F, Bellafiore M, Palma A, David S, Marciano V, Bartolotta T, Sciume C, Modica G, Farina F, Zummo G, Bucchieri F. 60KDa chaperonin (HSP60) is over-expressed during colorectal carcinogenesis. Eur J Histochem 2003;47:105-10.
37. Lebret T, Watson RW, Molinie V, O'Neill A, Gabriel C, Fitzpatrick JM, Botto H. Heat shock proteins HSP27, HSP60, HSP70, and HSP90: expression in bladder carcinoma. Cancer 2003;98:970-7.
38. Sreedhar AS, Csermely P. Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy. A comprehensive review. Pharmacol Ther 2004;101:227-57.
39. Ciocca DR, Calderwood SK. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 2005;10:86-103.
40. 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;21:7097-104.
41. Lim JH, Martin F, Guiard B, Pfanner N, Voos W. The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J 2001;20:941-50.
42. Voos W, Martin H, Krimmer T, Pfanner N. Mechanisms of protein translocation into mitochondria. Biochim Biophys Acta 1999;16: 235-54.
43. Mizukoshi E, Suzuki M, Misono T, Loupatov A, Munekata E, Kaul SC, Wadhwa R, Imamura T. Cell-cycle dependent tyrosine phosphorylation on mortalin regulates its interaction with fibroblast growth factor-1. Biochem Biophys Res Commun 2001;280:1203-9.
44. Dundas SR, Lawrie LC, Rooney PH, Murray GI. Mortalin is overexpressed by colorectal adenocarcinomas and correlates with poor survival. J Pathol 2005;205:74-81.
45. VanBuskirk AM, DeNagel DC, Guagliardi LE, Brodsky FM, Pierce SK. Cellular and subcellular distribution of PBP72/74, a peptide-binding protein that plays a role in antigen processing. J Immunol 1991;146: 500-6.
46. Shin BK, Wang H, Yim AM, Le Naour F, Brichory F, Jang JH, Zhao R, Puravs E, Tra J, Michael CW, Misek DE, Hanash SM. Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J Biol Chem 2003; 278:7607-16.