ARK5 Is a Tumor Invasion-Associated Factor Downstream of Akt Signaling

Molecular and Cellular Biology

Volumn 24, Issue 8, 2004, Pages 3526-3535

  Suzuki, Atsushi ^a   Lu, Jie ^a   Kusakai, Gen Ichi ^a   Kishimoto, Atsuhiro ^a   Ogura, Tsutomu ^a   Esumi, Hiroyasu ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; GELATINASE A; GELATINASE B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERSTITIAL COLLAGENASE; MATRIGEL; PROTEIN ARK5; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CANCER INVASION; CATALYSIS; CELL ENERGY; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; METASTASIS; NONHUMAN; NUDE MOUSE; NUTRIENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SIGNAL TRANSDUCTION; STARVATION; TUMOR GROWTH; TUMOR NECROSIS;

ANIMALS; CELL LINE, TUMOR; ENZYME ACTIVATION; HUMANS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROTEIN KINASES; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALIA; MUS MUSCULUS;

EID: 1842505299     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.8.3526-3535.2004     Document Type: Article

References (63)

1. Arboleda, M. J., J. F. Lyons, F. F. Kabbinavar, M. R. Bray, B. E. Snow, R. Ayala, M. Danino, B. Y. Karlan, and D. J. Slamon. 2003. Overexpression of AKT2/protein kinase Bβ leads to up-regulation of β1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res. 63:196-206.
2. Besson, A., S. M. Robbins, and V. M. Yong. 1999. PTEN/MMAC1/TEP1 in signal transduction and tumorigenesis. Eur. J. Biochem. 263:605-611.
3. Boyd, D. 1996. Invasion and metastasis. Cancer Metastasis Rev. 15:77-89.
4. Brazil, D. P., J. Park, and B. A. Hemmings. 2002. PKB binding proteins. Getting in on the Ak1. Cell 111:293-303.
5. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcriptional factor. Cell 96:857-868.
6. Carling, D., K. Aguan, A. Woods, A. J. Verhoeven, R. K. Beri, C. H. Brennan, C. Sidebottom, M. D. Davidson, and J. Scott. 1994. Mammalian AMP-activated protein kinase is homologous to yeast and plant protein kinases involved in the regulation of carbon metabolism. J. Biol. Chem. 269:11442-11448.
7. Carmeliet, P., Y. Dor, J. M. Herbert, D. Fukumura, K. BrusseImans, M. Dewerchln, M. Neeman, F. Bono, R. Abramovitch, P. MaxweII, C. J. Koch, P. Ratcliffe, L. Moons, R. K. Jaln, D. Collen, and E. Keschert. 1998. Role of H1F-1α in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 394:485-490.
8. Cooper, C. R., C. H. Chay, and K. J. Pienta. 2002. The role of αvβ3 in prostate cancer progression. Neoplasia 4:191-194.
9. Cross, D. A., D. R. Alessi, P. Cohen, M. Andleikovich, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
10. Dang, C. V., and G. L. Semenza. 1999. Oncogenic alteration of metabolism. Trends Biochem. Sci. 24:68-71.
11. Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905-2927.
12. Delcommenne, M., C. Tan, V. Gray, L. Rue, J. Woodgett, and S. Dedhar. 1998. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA 95:11211-11216.
13. Denko, N. C., and A. J. Giaccia. 2001. Tumor hypoxia, the physiological link between Trousseau's syndrome (carcinoma-induced coagulopathy) and metastasis. Cancer Res. 61:795-798.
14. Esumi, H., K. Izuishi, K. Kato, K. Hashimoto, Y. Kurashima, A. Kishimoto, T. Ogura, and T. Ozawa. 2002. Hypoxia and nitric oxide treatment confer tolerance to glucose starvation in a 5′-AMP-activated protein kinase-dependent manner. J. Biol. Chem. 277:32791-92798.
15. Folkman, J. 2001. Can mosaic tumor vessels facilitate molecular diagnosis of cancer? Proc. Natl. Acad. Sci. USA 98:398-400.
16. Folkman, J. 1974. Tumor angiogenesis. Adv. Cancer Res. 19:331-358.
17. Franke, T. F., S. I. Yang. T. O. Chan, K. Dalta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
18. Frisch, S. M., and R. A. Screton. 2001. Anoikis mechanisms. Curr. Opin. Cell Biol. 13:555-562.
19. Gelinas, D. S., P. N. Bernatchez, S. Rollin, N. G. Bazan, and M. G. Sirois. 2002. Immediate delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K, PKC and PLC pathways. Br. J. Pharmacol. 137:1021-1030.
20. Grille, S. J., A. Bellacosa, J. Upson, A. J. Klein-Szanto, F. van Roy, W. Lee-Kwon, M. Donovitz, P. N. Tsichlis, and L. Larue. 2003. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 63:2172-2178.
21. Hannigan, G. E., C. Leung-Hagesteijin, L. Fitz-Gibbon, M. G. Coppolino, G. Radeva, J. Filmus, J. C. Bell, and S. Dedhar. 1996. Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase. Nature 379:91-96.
22. Hardie, D. G., and D. Carling. 1997. The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur. J. Biochem. 246:259-273.
23. Harris, A. L. 2002. Hypoxia-a key regulatory factor in tumor growth. Nat. Rev. Cancer 2:38-47.
24. Hashimoto, K., K. Kato, K. Imamura, A. Kishimolo, H. Yoshikawa, Y. Taketani, and H. Esumi. 2002. 5-Amino-4-imidazolecarboxamide ribose (AICAR) confers strong tolerance to glucose starvation in a 5′-AMP-activated protein kinase-dependent fashion. Biochem. Biophys. Res. Commun. 290:263-267.
25. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med. 3:177-182.
26. Heyer, B. S., J. Warsowe, D. Solter, B. B. Knowles, and S. L. Ackerman. 1997. New member of the Snf1/AMPK kinase family, Melk, is expressed in the mouse egg and preimplantation embryo. Mol. Reprod. Dev. 47:148-156.
27. Higuchi, M., N. Masuyama, Y. Fukui, A. Suzuki, and Y. Gotoh. 2001. Akt mediates Rac/Cdc42-regulated cell motility in growth factor-stimutated cells and invasive PTEN knockout cells. Curr. Biol. 11:1958-1962.
28. Hockel, M., and P. Vaupel. 2001. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 93:266-276.
29. Itoh, N., S. Semba, M. Ilo, H. Takeda, S. Kawata, and M. Yamakawa. 2002. Phosphorylation of Akt/PKB is required for suppression of cancer cell apoptosis and tumor progression in human colorectal carcinoma. Cancer 94:3127-3134.
30. Izuishi, K., K. Kato, T. Ogura, T. Kinoshita, and H. Esumi. 2000. Remarkable tolerance of tumor cells to nutrient deprivation: possible new biochemical target for cancer therapy. Cancer Res. 60:6201-6207.
31. Kato, K., T. Ogura, A. Kishimoto, Y. Minegishi, N. Nakajima, M. Miyazaki, and H. Esumi. 2002. Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 21:6082-6090.
32. Kim, D., S. Kim, H. Koh, S.-O. Yoon, A.-S. Chung, K. S. Cho, and J. Chung. 2001. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J. 15:1953-1962.
33. Kimura, H., A. Weisz, Y. Kurashima, K. Hashimoto, T. Ogura, F. D'Acquisto, R. Addeo, M. Makuuchi, and H. Esumi. 2000. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 95:189-197.
34. Kumar, C. C. 1998. Signaling by integrin receptors. Oncogene 17:1365-1373.
35. Lawlor, M. A., and D. R. Alessi. 2001. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114:2903-2910.
36. Lefebvre, D. L., Y. Bai, N. Shahmolky, R. Poon, D. J. Drucker, and C. F. Rosen. 2001. Identification and characterization of a novel sucrose-non-fermenting protein kinase/AMP-activated protein kinase-related protein kinase, SNARK. Biochem. J. 355:297-305.
37. Liotta, L. A. 1986. Tumor invasion and metastases-role of the extracellular matrix: Rhoads Memorial Awards lecture. Cancer Res. 46:1-7.
38. Maeda, N., Y. Inoshima, D. A. Fruman, S. M. Brachmann, and H. Fan. 2003. Transformation of mouse fibroblasts by Jaagsiekte sheep retrovirus envelope does not require phosphatidylinositol 3-kinase. J. Virol. 77:9951-9959.
39. Matsumoto, J., M. Kaneda, M. Tada, J. Hamada, S. Okushiba, S. Kondo, H. Katoh, and T. Moriuchi. 2002. Differential mechanisms of constitutive Akt/PKB activation and its influence on gene expression in pancreatic cancer cells. Jpn. J. Cancer Res. 93:1317-1326.
40. Mitchelhill, K. I., D. Stapleton, G. Gao, C. House, B. Michell, F. Katsis, L. A. Witters, and B. E. Kemp. 1994. Mammalian AMP-activated protein kinase shares structural and functional bomology with the catalytic domain of yeast Snf1 protien kinase. J. Biol. Chem. 269:2361-2364.
41. Muraoka, R. S., N. Dumont, C. A. Ritter, T. C. Dugger, D. M. Brantley, J. Chen, E. Easterly, L. R. Roebuck, S. Ryan, P. J. Gotwais, V. Koteliansky, and C. L. Arteaga. 2002. Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J. Clin. Investig. 109:1551-1559.
42. Nicholson, K. M., and N. G. Anderson. 2002. The protein kinase B/Akt signaling pathway in human malignancy. Cell. Signal. 14:381-395.
43. Park, B. K., X. Zeng, and R. I. Glazer. 2001. Akt1 induces extracellular matrix invasion and matrix metalloproteinase-2 activity in mouse mammary epithelial cells. Cancer Res. 61:7647-7653.
44. Persad, S., S. Attwell, V. Gray, M. Delcommenne, A. Troussard, J. Sanghera, and S. Dedhar. 2000. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoplosis of PTEN-mutant prostate cancer cells. Proc. Natl. Acad. Sci. USA 97:3207-3212.
45. Persad, S., and S. Dedhar. 2003. The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metastasis Rev. 22:375-384.
46. Peterson, R. T., P. A. Beal, M. J. Comb, and S. L. Schreiber. 2000. FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J. Biol. Chem. 275:7416-7423.
47. Ruggeri, B. A., L. Huang, M. Wood, J. Q. Cheng, and J. R. Testa. 1998. Amplification and overexpression of the AKT2 oncogene in a subset of human pancreatic ductal adenocarcinomas. Mol. Carcinog. 21:81-86.
48. Sato, H., T. Takino Y. Okada, J. Cao, A. Shinagawa, E. Yamamoto, and M. Selkl. 1994. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370:61-75.
49. Shamji, A. F., P. Hghiem, and S. L. Schreiber. 2003. Integration of growth factor and nutrient signaling: implications for cancer biology. Mol. Cell 12:271-280.
50. Shinkaruk, S., M. Bayler, G. Lain, and G. Deleris. 2003. Vascular endothelial cell growth factor (VEGF), an emerging target for cancer therapy. Curr. Med. Chem. Anti-Cancer Agents 3:95-117.
51. Southerland, R. M. 1988. Cell and environment interactions in tumor microregions; the multicell spheroid model. Science 240:178-184.
52. Stapleton, D., K. I. Mitchelhill, G. Gao, J. Widmer, B. J. Michell, T. Teh, C. M. House, C. S. Fernandez, T. Cox, L. A. Witters, and B. E. Kemp. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611-614.
53. Streit, M., and M. Detmar. 2003. Angiogenesis, lymphangiogenesis, and melanoma metastasis. Oncogene 22:3172-3179.
54. Sun, H., R. Lesche, D. M. Li, J. Liliental, H. Zhang, J. Gao, N. Gavrilova, B. Mueller, X. Liu, and H. Wu. 1999. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-triphoshate and Akt/protein kinase B signaling pathway. Proc. Natl. Acad. Sci. USA 96:6199-6204.
55. Suzuki, A., G. Kusakai, A. Kishimoto, J. Lu, T. Ogura, and H. Esumi. 2003. ARK5 suppresses the cell death induced by nutrient starvation and death receptors via inhibition of caspase 8 activation, but not by chemotherapeutic agents or UV irradiation. Oncogene 22:6177-6182.
56. Suzuki, A., G. Kusakai, A. Kishimoto, J. Lu, T. Ogura, M. F. Lavin, and H. Esumi. 2003. Identification of a novel protein kinase mediating Akt survival signaling to ATM. J. Biol. Chem. 278:48-53.
57. Suzuki, A., G. Kusakai, A. Kishimoto, Y. Minegishi, T. Ogura, and H. Esumi. 2003. Induction of cell-cell detachment during glucose starvation through F-actin conversion by SNARK, the fourth member of the AMP-activated protein kinase catalytic subunit family. Biochem. Biophys. Res. Commun. 311:156-161.
58. Tanno, S., S. Tanno, Y. Mitsuuchi, D. A. Altomare, G. H. Xiao, and J. R. Testa. 2001. AKT-activation up-regulates insulin-like growth factor 1 receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res. 61:589-593.
59. Teraoko, H., T. Sawada, T. Nishihara, M. Yashiro, M. Ohira, T. Ishikawa, H. Nishino, and K. Hirakawa. 2001. Enhanced VEGF production and decreased immunogenicity induced by TGF-beta 1 promote liver metastasis of pancreatic cancer. Br. J. Cancer 85:612-617.
60. Vaupel, P., D. K. Kelleher, and M. Hockel. 2001. Oxygen status of malignant tumors: pathogenesis of hypoxia and significant for tumor therapy. Semin. Oncol. 28:29-35.
61. Vlahos, C. J., W. F. Matter, K. Y. Hui, and R. F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-41I-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241-5248.
62. Zaman, K., H. Ryu, D. Hall, K. O'Donovan, K. I. Lin, M. P. Miller, J. C. Marquis, J. M. Baraban, G. L. Semenza, and R. R. Ratan. 1999. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J. Neurosci. 19:9821-9830.
63. Zhang, D., and P. Brodt. 2003. Type 1 insulin-like growth factor regulates MT1-MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling. Oncogene 22:974-982.