Identification and functional characterization of nuclear mortalin in human carcinogenesis

Journal of Biological Chemistry

Volumn 289, Issue 36, 2014, Pages 24832-24844

  Ryu, Jihoon ^a,b   Kaul, Zeenia ^a,c   Yoon, A Rum ^a   Liu, Ye ^a   Yaguchi, Tomoko ^a   Na, Youjin ^b   Ahn, Hyo Min ^a,b   Gao, Ran ^a   Choi, Il Kyu ^b   Yun, Chae Ok ^b   Kaul, Sunil C ^a   Wadhwa, Renu ^a  

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

^b Hanyang University   (South Korea)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; DISEASES; PATHOLOGY; PROTEINS; TUMORS;

ENDOPLASMIC RETICULUM; FUNCTIONAL ACTIVATION; FUNCTIONAL CHARACTERIZATION; HUMAN CARCINOGENESIS; MOLECULAR MECHANISM; RIBONUCLEOPROTEINS; SUBCELLULAR LOCALIZATIONS; TUMOR SUPPRESSOR PROTEINS;

CYTOLOGY;

HEAT SHOCK PROTEIN 70; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; NUCLEAR MORTALIN; NUCLEAR PROTEIN; PROTEIN P53; TELOMERASE; UNCLASSIFIED DRUG; MORTALIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL FRACTIONATION; CELL MOTILITY; CELL NUCLEUS; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; FEMALE; GENE INACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MITOCHONDRIAL TARGETING SIGNAL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TUMOR PROMOTION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CELL TRANSFORMATION; GENETICS; HCT116 CELL LINE; HELA CELL LINE; IMMUNOHISTOCHEMISTRY; MCF 7 CELL LINE; METABOLISM; MUTATION; NEOPLASM; NUDE MOUSE; PATHOLOGY; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; HCT116 CELLS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN K; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MCF-7 CELLS; MICE, INBRED BALB C; MICE, NUDE; MUTATION; NEOPLASM METASTASIS; NEOPLASMS; OXIDATIVE STRESS; TELOMERASE; TRANSPLANTATION, HETEROLOGOUS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84906980711     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.565929     Document Type: Article

References (51)

1. Wadhwa, R., Kaul, S. C., Ikawa, Y., and Sugimoto, Y. (1993) Identification of a novel member of mouse hsp70 family: its association with cellular mortal phenotype. J. Biol. Chem. 268, 6615-6621
2. Lu, W. J., Lee, N. P., Kaul, S. C., Lan, F., Poon, R. T., Wadhwa, R., and Luk, J. M. (2011) Induction of mutant p53-dependent apoptosis in human hepatocellular carcinoma by targeting stress protein mortalin. Int. J. Cancer 129, 1806-1814
3. Park, S. J., Shin, J. H., Jeong, J. I., Song, J. H., Jo, Y. K., Kim, E. S., Lee, E. H., Hwang, J. J., Lee, E. K., Chung, S. J., Koh, J. Y., Jo, D. G., and Cho, D. H. (2014) Down-regulation of mortalin exacerbates aβ-mediated mitochondrial fragmentation and dysfunction. J. Biol. Chem. 289, 2195-2204
4. Kaul, S. C., Aida, S., Yaguchi, T., Kaur, K., and Wadhwa, R. (2005) Activation of wild type p53 function by its mortalin-binding cytoplasmically localizing carboxy-terminus peptides. J. Biol. Chem. 280, 39373-39379
5. Pilzer, D., Saar, M., Koya, K., and Fishelson, Z. (2010) Mortalin inhibitors sensitize K562 leukemia cells to complement-dependent cytotoxicity. Int. J. Cancer 126, 1428-1435
6. Ma, Z., Izumi, H., Kanai, M., Kabuyama, Y., Ahn, N. G., and Fukasawa, K. (2006) Mortalin controls centrosome duplication via modulating centrosomal localization of p53. Oncogene 25, 5377-5390
7. Gestl, E. E., and Anne Böttger, S. (2012) Cytoplasmic sequestration of the tumor suppressor p53 by a heat shock protein 70 family member, mortalin, in human colorectal adenocarcinoma cell lines. Biochem. Biophys. Res. Commun. 423, 411-416
8. Voloboueva, L. A., Emery, J. F., Sun, X., and Giffard, R. G. (2013) Inflammatory response of microglial BV-2 cells includes a glycolytic shift and is modulated by mitochondrial glucose-regulated protein 75/mortalin. FEBS Lett. 587, 756-762
9. Wadhwa, R., Takano, S., Robert, M., Yoshida, A., Nomura, H., Reddel, R. R., Mitsui, Y., and Kaul, S. C. (1998) Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J. Biol. Chem. 273, 29586-29591
10. Lu, W. J., Lee, N. P., Kaul, S. C., Lan, F., Poon, R. T., Wadhwa, R., and Luk, J. M. (2011) Mortalin-p53 interaction in cancer cells is stress dependent and constitutes a selective target for cancer therapy. Cell Death Differ. 18, 1046-1056
11. Walker, C., Böttger, S., and Low, B. (2006) Mortalin-based cytoplasmic sequestration of p53 in a nonmammalian cancer model. Am. J. Pathol. 168, 1526-1530
12. Kaul, S. C., Duncan, E. L., Englezou, A., Takano, S., Reddel, R. R., Mitsui, Y., and Wadhwa, R. (1998) Malignant transformation of NIH3T3 cells by overexpression of mot-2 protein. Oncogene 17, 907-911
13. Kaul, S. C., Yaguchi, T., Taira, K., Reddel, R. R., and Wadhwa, R. (2003) Overexpressed mortalin (mot-2)/mthsp70/GRP75 and hTERT cooperate to extend the in vitro lifespan of human fibroblasts. Exp. Cell Res. 286, 96-101
14. Xu, J., Xiao, H. H., and Sartorelli, A. C. (1999) Attenuation of the induced differentiation of HL-60 leukemia cells by mitochondrial chaperone HSP70. Oncol. Res. 11, 429-435
15. Kanai, M., Ma, Z., Izumi, H., Kim, S. H., Mattison, C. P., Winey, M., and Fukasawa, K. (2007) Physical and functional interaction between mortalin and Mps1 kinase. Genes Cells 12, 797-810
16. Wadhwa, R., Colgin, L., Yaguchi, T., Taira, K., Reddel, R. R., and Kaul, S. C. (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
17. Wadhwa, R., Sugihara, T., Yoshida, A., Nomura, H., Reddel, R. R., Simpson, R., Maruta, H., and Kaul, S. C. (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
18. Wadhwa, R., Takano, S., Kaur, K., Deocaris, C. C., Pereira-Smith, O. M., Reddel, R. R., and Kaul, S. C. (2006) Upregulation of mortalin/mthsp70/Grp75 contributes to human carcinogenesis. Int. J. Cancer 118, 2973-2980
19. Ando, K., Oki, E., Zhao, Y., Ikawa-Yoshida, A., Kitao, H., Saeki, H., Kimura, Y., Ida, S., Morita, M., Kusumoto, T., and Maehara, Y. (2014) Mortalin is a prognostic factor of gastric cancer with normal p53 function. Gastric Cancer 17, 255-262
20. Chen, J., Liu, W. B., Jia, W. D., Xu, G. L., Ma, J. L., Huang, M., Deng, Y. R., and Li, J. S. (2014) Overexpression of Mortalin in hepatocellular carcinoma and its relationship with angiogenesis and epithelial to mesenchymal transition. Int. J. Oncol. 44, 247-255
21. Dundas, S. R., Lawrie, L. C., Rooney, P. H., and Murray, G. I. (2005) Mortalin is over-expressed by colorectal adenocarcinomas and correlates with poor survival. J. Pathol. 205, 74-81
22. Rozenberg, P., Kocsis, J., Saar, M., Prohászka, Z., Füst, G., and Fishelson, Z. (2013) Elevated levels of mitochondrial mortalin and cytosolic HSP70 in blood as risk factors in patients with colorectal cancer. Int. J. Cancer 133, 514-518
23. Mizukoshi, E., Suzuki, M., Misono, T., Loupatov, A., Munekata, E., Kaul, S. C., Wadhwa, R., and Imamura, T. (2001) Cell-cycle dependent tyrosine phosphorylation on mortalin regulates its interaction with fibroblast growth factor-1. Biochem. Biophys. Res. Commun. 280, 1203-1209
24. Qu, M., Zhou, Z., Xu, S., Chen, C., Yu, Z., and Wang, D. (2011) Mortalin overexpression attenuates beta-amyloid-induced neurotoxicity in SHSY5Y cells. Brain Res. 1368, 336-345
25. Burbulla, L. F., Schelling, C., Kato, H., Rapaport, D., Woitalla, D., Schiesling, C., Schulte, C., Sharma, M., Illig, T., Bauer, P., Jung, S., Nordheim, A., Schöls, L., Riess, O., and Krüger, R. (2010) Dissecting the role of the mitochondrial chaperone mortalin in Parkinson's disease: functional impact of disease-related variants on mitochondrial homeostasis. Hum. Mol. Genet. 19, 4437-4452
26. Chiasserini, D., Tozzi, A., de Iure, A., Tantucci, M., Susta, F., Orvietani, P. L., Koya, K., Binaglia, L., and Calabresi, P. (2011) Mortalin inhibition in experimental Parkinson's disease. Mov. Disord. 26, 1639-1647
27. Flachbartová, Z., and Kovacech, B. (2013) Mortalin: a multipotent chaperone regulating cellular processes ranging from viral infection to neurodegeneration. Acta Virol. 57, 3-15
28. Li, H. Y., Yang, L., Liu, W., and Zuo, J. (2011) GRP75 overexpression inhibits apoptosis induced by glucose deprivation via Raf/Mek/Erk1/2 signaling pathway. Sheng Li Xue Bao 63, 69-74
29. Yang, L., Guo, W., Zhang, Q., Li, H., Liu, X., Yang, Y., Zuo, J., and Liu, W. (2011) Crosstalk between Raf/MEK/ERK and PI3K/AKT in suppression of Bax conformational change by Grp75 under glucose deprivation conditions. J. Mol. Biol. 414, 654-666
30. Wadhwa, R., Takano, S., Taira, K., and Kaul, S. C. (2004) Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J. Gene Med. 6, 439-444
31. Yoo, J. Y., Ryu, J., Gao, R., Yaguchi, T., Kaul, S. C., Wadhwa, R., and Yun C. O. (2010) Tumor suppression by apoptotic and anti-angiogenic effects of mortalin-targeting adeno-oncolytic virus. J. Gene Med. 12, 586-595
32. Yi, X., Luk, J. M., Lee, N. P., Peng, J., Leng, X., Guan, X. Y., Lau, G. K., Beretta, L., and Fan, S. T. (2008) Association of mortalin (HSPA9) with liver cancer metastasis and prediction for early tumor recurrence. Mol. Cell Proteomics 7, 315-325
33. Ran, Q., Wadhwa, R., Kawai, R., Kaul, S. C., Sifers, R. N., Bick, R. J., Smith, J. R., and Pereira-Smith, O. M. (2000) Extramitochondrial localization of mortalin/mthsp70/PBP74/GRP75. Biochem. Biophys. Res. Commun. 275, 174-179
34. Kaul, S. C., Deocaris, C. C., and Wadhwa, R. (2007) Three faces of mortalin: a housekeeper, guardian and killer. Exp. Gerontol. 42, 263-274
35. Shih, Y. Y., Lee, H., Nakagawara, A., Juan, H. F., Jeng, Y. M., Tsay, Y. G., Lin, D. T., Hsieh, F. J., Pan, C. Y., Hsu, W. M., and Liao, Y. F. (2011) Nuclear GRP75 binds retinoic acid receptors to promote neuronal differentiation of neuroblastoma. PLoS ONE 6, e26236
36. Inoue, A., Sawata, S. Y., Taira, K., and Wadhwa, R. (2007) Loss-of-function screening by randomized intracellular antibodies: identification of hn- RNP-K as a potential target for metastasis. Proc. Natl. Acad. Sci. U.S.A. 104, 8983-8988
37. Li, L. P., Lu, C. H., Chen, Z. P., Ge, F., Wang, T., Wang, W., Xiao, C. L., Yin, X. F., Liu, L., He, J. X., and He, Q. Y. (2011) Subcellular proteomics revealed the epithelial-mesenchymal transition phenotype in lung cancer. Proteomics 11, 429-439
38. He, Z. Y., Wen, H., Shi, C. B., and Wang, J. (2010) Up-regulation of hnRNP A1, Ezrin, tubulin β-2C and Annexin A1 in sentinel lymph nodes of colorectal cancer. World J. Gastroenterol. 16, 4670-4676
39. Gao, R., Yu, Y., Inoue, A., Widodo, N., Kaul, S. C., and Wadhwa, R. (2013) Heterogeneous nuclear ribonucleoprotein K (hnRNP-K) promotes tumor metastasis by induction of genes involved in extracellular matrix, cell movement, and angiogenesis. J. Biol. Chem. 288, 15046-15056
40. Moumen, A., Masterson, P., O'Connor, M. J., and Jackson, S. P. (2005) hnRNP K: an HDM2 target and transcriptional coactivator of p53 in response to DNA damage. Cell 123, 1065-1078
41. Shay, J. W., and Keith, W. N. (2008) Targeting telomerase for cancer therapeutics. Br. J. Cancer 98, 677-683
42. Fujiki, T., Miura, T., Maura, M., Shiraishi, H., Nishimura, S., Imada, Y., Uehara, N., Tashiro, K., Shirahata, S., and Katakura, Y. (2007) TAK1 represses transcription of the human telomerase reverse transcriptase gene. Oncogene 26, 5258-5266
43. Papanikolaou, V., Iliopoulos, D., Dimou, I., Dubos, S., Tsougos, I., Theodorou, K., Kitsiou-Tzeli, S., and Tsezou, A. (2009) The involvement of HER2 and p53 status in the regulation of telomerase in irradiated breast cancer cells. Int. J. Oncol. 35, 1141-1149
44. Kang, X., Chen, W., Kim, R. H., Kang, M. K., and Park, N. H. (2009) Regulation of the hTERT promoter activity by MSH2, the hnRNPs K and D, and GRHL2 in human oral squamous cell carcinoma cells. Oncogene 28, 565-574
45. Ostareck-Lederer, A., and Ostareck, D. H. (2004) Control ofmRNAtranslation and stability in haematopoietic cells: the function of hnRNPs K and E1/E2. Biol. Cell 96, 407-411
46. Habelhah, H., Shah, K., Huang, L., Ostareck-Lederer, A., Burlingame, A. L., Shokat, K. M., Hentze, M. W., and Ronai, Z. (2001) ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat. Cell Biol. 3, 325-330
47. Hope, N. R., and Murray, G. I. (2011) The expression profile of RNAbinding proteins in primary and metastatic colorectal cancer: relationship of heterogeneous nuclear ribonucleoproteins with prognosis. Hum. Pathol. 42, 393-402
48. Ostrowski, J., Kawata, Y., Schullery, D. S., Denisenko, O. N., and Bomsztyk, K. (2003) Transient recruitment of the hnRNP K protein to inducibly transcribed gene loci. Nucleic Acids Res. 31, 3954-3962
49. Ostrowski, J., and Bomsztyk, K. (2003) Nuclear shift of hnRNPKprotein in neoplasms and other states of enhanced cell proliferation. Br. J. Cancer 89, 1493-1501
50. Sataranatarajan, K., Lee, M. J., Mariappan, M. M., and Feliers, D. (2008) PKCδ regulates the stimulation of vascular endothelial factor mRNA translation by angiotensin II through hnRNP K. Cell Signal. 20, 969-977
51. Wu, P. K., Hong, S. K., Veeranki, S., Karkhanis, M., Starenki, D., Plaza, J. A., and Park, J. I. (2013) A mortalin/HSPA9-mediated switch in tumor suppressive signaling of Raf/MEK/extracellular signal-regulated kinase. Mol. Cell. Biol. 33, 4051-4067