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

REFERENCES

• Arboleda, M. J., Lyons J. F., Kabbinavar F. F., Bray M. R., Snow B. E., Ayala R., Danino M., Karlan B. Y., and Slamon D. J.. 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.
   PubMed Web of Science ®Google Scholar
• Besson, A., Robbins S. M., and Yong V. M.. 1999. PTEN/MMAC1/TEP1 in signal transduction and tumorigenesis. Eur. J. Biochem. 263:605–611.
   PubMedGoogle Scholar
• Boyd, D. 1996. Invasion and metastasis. Cancer Metastasis Rev. 15:77–89.
   PubMed Web of Science ®Google Scholar
• Brazil, D. P., Park J., and Hemmings B. A.. 2002. PKB binding proteins. Getting in on the Akt. Cell 111:293–303.
   PubMed Web of Science ®Google Scholar
• Brunet, A., Bonni A., Zigmond M. J., Lin M. Z., Juo P., Hu L. S., Anderson M. J., Arden K. C., Blenis J., and Greenberg M. E.. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcriptional factor. Cell 96:857–868.
   PubMed Web of Science ®Google Scholar
• Carling, D., Aguan K., Woods A., Verhoeven A. J., Beri R. K., Brennan C. H., Sidebottom C., Davidson M. D., and Scott J.. 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.
   PubMed Web of Science ®Google Scholar
• Carmeliet, P., Dor Y., Herbert J. M., Fukumura D., Brusselmans K., Dewerchin M., Neeman M., Bono F., Abramovitch R., Maxwell P., Koch C. J., Ratcliffe P., Moons L., Jain R. K., Collen D., and Keschert E.. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 394:485–490.
   PubMed Web of Science ®Google Scholar
• Cooper, C. R., Chay C. H., and Pienta K. J.. 2002. The role of αvβ3 in prostate cancer progression. Neoplasia 4:191–194.
   PubMed Web of Science ®Google Scholar
• Cross, D. A., Alessi D. R., Cohen P., Andleikovich M., and Hemmings B. A.. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785–789.
   PubMed Web of Science ®Google Scholar
• Dang, C. V., and Semenza G. L.. 1999. Oncogenic alteration of metabolism. Trends Biochem. Sci. 24:68–71.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., Brunet A., and Greenberg M. E.. 1999. Cellular survival: a play in three Akts. Genes Dev. 13:2905–2927.
   PubMed Web of Science ®Google Scholar
• Delcommenne, M., Tan C., Gray V., Rue L., Woodgett J., and Dedhar S.. 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.
   PubMed Web of Science ®Google Scholar
• Denko, N. C., and Giaccia A. J.. 2001. Tumor hypoxia, the physiological link between Trousseau's syndrome (carcinoma-induced coagulopathy) and metastasis. Cancer Res. 61:795–798.
   PubMed Web of Science ®Google Scholar
• Esumi, H., Izuishi K., Kato K., Hashimoto K., Kurashima Y., Kishimoto A., Ogura T., and Ozawa T.. 2002. Hypoxia and nitric oxide treatment confer tolerance to glucose starvation in a 5′-AMP-activated protein kinase-dependent manner. J. Biol. Chem. 277:32791–32798.
   PubMedGoogle Scholar
• Folkman, J. 2001. Can mosaic tumor vessels facilitate molecular diagnosis of cancer? Proc. Natl. Acad. Sci. USA 98:398–400.
   PubMed Web of Science ®Google Scholar
• Folkman, J. 1974. Tumor angiogenesis. Adv. Cancer Res. 19:331–358.
   PubMedGoogle Scholar
• Franke, T. F., Yang S. I., Chan T. O., Datta K., Kazlauskas A., Morrison D. K., Kaplan D. R., and Tsichlis P. N.. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727–736.
   PubMed Web of Science ®Google Scholar
• Frisch, S. M., and Screton R. A.. 2001. Anoikis mechanisms. Curr. Opin. Cell Biol. 13:555–562.
   PubMed Web of Science ®Google Scholar
• Gelinas, D. S., Bernatchez P. N., Rollin S., Bazan N. G., and Sirois M. G.. 2002. Immediate delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K, PKC and PLC pathways. Br. J. Pharmacol. 137:1021–1030.
   PubMed Web of Science ®Google Scholar
• Grille, S. J., Bellacosa A., Upson J., Klein-Szanto A. J., van Roy F., Lee-Kwon W., Donovitz M., Tsichlis P. N., and Larue L.. 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.
   PubMed Web of Science ®Google Scholar
• Hannigan, G. E., Leung-Hagesteijin C., Fitz-Gibbon L., Coppolino M. G., Radeva G., Filmus J., Bell J. C., and Dedhar S.. 1996. Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase. Nature 379:91–96.
   PubMed Web of Science ®Google Scholar
• Hardie, D. G., and Carling D.. 1997. The AMP-activated protein kinase—fuel gauge of the mammalian cell? Eur. J. Biochem. 246:259–273.
   PubMedGoogle Scholar
• Harris, A. L. 2002. Hypoxia—a key regulatory factor in tumor growth. Nat. Rev. Cancer 2:38–47.
   PubMed Web of Science ®Google Scholar
• Hashimoto, K., Kato K., Imamura K., Kishimoto A., Yoshikawa H., Taketani Y., and Esumi H.. 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.
   PubMedGoogle Scholar
• Helmlinger, G., Yuan F., Dellian M., and Jain R. K.. 1997. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med. 3:177–182.
   PubMed Web of Science ®Google Scholar
• Heyer, B. S., Warsowe J., Solter D., Knowles B. B., and Ackerman S. L.. 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.
   PubMed Web of Science ®Google Scholar
• Higuchi, M., Masuyama N., Fukui Y., Suzuki A., and Gotoh Y.. 2001. Akt mediates Rac/Cdc42-regulated cell motility in growth factor-stimulated cells and invasive PTEN knockout cells. Curr. Biol. 11:1958–1962.
   PubMed Web of Science ®Google Scholar
• Hockel, M., and Vaupel P.. 2001. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 93:266–276.
   PubMed Web of Science ®Google Scholar
• Itoh, N., Semba S., Ito M., Takeda H., Kawata S., and Yamakawa M.. 2002. Phosphorylation of Akt/PKB is required for suppression of cancer cell apoptosis and tumor progression in human colorectal carcinoma. Cancer 94:3127–3134.
   PubMed Web of Science ®Google Scholar
• Izuishi, K., Kato K., Ogura T., Kinoshita T., and Esumi H.. 2000. Remarkable tolerance of tumor cells to nutrient deprivation: possible new biochemical target for cancer therapy. Cancer Res. 60:6201–6207.
   PubMed Web of Science ®Google Scholar
• Kato, K., Ogura T., Kishimoto A., Minegishi Y., Nakajima N., Miyazaki M., and Esumi H.. 2002. Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 21:6082–6090.
   PubMedGoogle Scholar
• Kim, D., Kim S., Koh H., Yoon S.-O., Chung A.-S., Cho K. S., and Chung J.. 2001. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J. 15:1953–1962.
   PubMed Web of Science ®Google Scholar
• Kimura, H., Weisz A., Kurashima Y., Hashimoto K., Ogura T., D'Acquisto F., Addeo R., Makuuchi M., and Esumi H.. 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.
   PubMed Web of Science ®Google Scholar
• Kumar, C. C. 1998. Signaling by integrin receptors. Oncogene 17:1365–1373.
   PubMed Web of Science ®Google Scholar
• Lawlor, M. A., and Alessi D. R.. 2001. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114:2903–2910.
   PubMed Web of Science ®Google Scholar
• Lefebvre, D. L., Bai Y., Shahmolky N., Poon R., Drucker D. J., and Rosen C. F.. 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.
   PubMedGoogle Scholar
• Liotta, L. A. 1986. Tumor invasion and metastases—role of the extracellular matrix: Rhoads Memorial Awards lecture. Cancer Res. 46:1–7.
   PubMed Web of Science ®Google Scholar
• Maeda, N., Inoshima Y., Fruman D. A., Brachmann S. M., and Fan H.. 2003. Transformation of mouse fibroblasts by Jaagsiekte sheep retrovirus envelope does not require phosphatidylinositol 3-kinase. J. Virol. 77:9951–9959.
   PubMedGoogle Scholar
• Matsumoto, J., Kaneda M., Tada M., Hamada J., Okushiba S., Kondo S., Katoh H., and Moriuchi T.. 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.
   PubMedGoogle Scholar
• Mitchelhill, K. I., Stapleton D., Gao G., House C., Michell B., Katsis F., Witters L. A., and Kemp B. E.. 1994. Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase. J. Biol. Chem. 269:2361–2364.
   PubMed Web of Science ®Google Scholar
• Muraoka, R. S., Dumont N., Ritter C. A., Dugger T. C., Brantley D. M., Chen J., Easterly E., Roebuck L. R., Ryan S., Gotwais P. J., Koteliansky V., and Arteaga C. L.. 2002. Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J. Clin. Investig. 109:1551–1559.
   PubMed Web of Science ®Google Scholar
• Nicholson, K. M., and Anderson N. G.. 2002. The protein kinase B/Akt signaling pathway in human malignancy. Cell. Signal. 14:381–395.
   PubMed Web of Science ®Google Scholar
• Park, B. K., Zeng X., and Glazer R. I.. 2001. Akt1 induces extracellular matrix invasion and matrix metalloproteinase-2 activity in mouse mammary epithelial cells. Cancer Res. 61:7647–7653.
   PubMedGoogle Scholar
• Persad, S., Attwell S., Gray V., Delcommenne M., Troussard A., Sanghera J., and Dedhar S.. 2000. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoptosis of PTEN-mutant prostate cancer cells. Proc. Natl. Acad. Sci. USA 97:3207–3212.
   PubMed Web of Science ®Google Scholar
• Persad, S., and Dedhar S.. 2003. The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metastasis Rev. 22:375–384.
   PubMed Web of Science ®Google Scholar
• Peterson, R. T., Beal P. A., Comb M. J., and Schreiber S. L.. 2000. FKBP12-rapamycin-associated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J. Biol. Chem. 275:7416–7423.
   PubMed Web of Science ®Google Scholar
• Ruggeri, B. A., Huang L., Wood M., Cheng J. Q., and Testa J. R.. 1998. Amplification and overexpression of the AKT2 oncogene in a subset of human pancreatic ductal adenocarcinomas. Mol. Carcinog. 21:81–86.
   PubMed Web of Science ®Google Scholar
• Sato, H., Takino T., Okada Y., Cao J., Shinagawa A., Yamamoto E., and Seiki M.. 1994. A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370:61–65.
   PubMed Web of Science ®Google Scholar
• Shamji, A. F., Hghiem P., and Schreiber S. L.. 2003. Integration of growth factor and nutrient signaling: implications for cancer biology. Mol. Cell 12:271–280.
   PubMed Web of Science ®Google Scholar
• Shinkaruk, S., Bayler M., Lain G., and Deleris G.. 2003. Vascular endothelial cell growth factor (VEGF), an emerging target for cancer therapy. Curr. Med. Chem. Anti-Cancer Agents 3:95–117.
   PubMedGoogle Scholar
• Southerland, R. M. 1988. Cell and environment interactions in tumor microregions; the multicell spheroid model. Science 240:178–184.
   Google Scholar
• Stapleton, D., Mitchelhill K. I., Gao G., Widmer J., Michell B. J., Teh T., House C. M., Fernandez C. S., Cox T., Witters L. A., and Kemp B. E.. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611–614.
   PubMed Web of Science ®Google Scholar
• Streit, M., and Detmar M.. 2003. Angiogenesis, lymphangiogenesis, and melanoma metastasis. Oncogene 22:3172–3179.
   PubMed Web of Science ®Google Scholar
• Sun, H., Lesche R., Li D. M., Liliental J., Zhang H., Gao J., Gavrilova N., Mueller B., Liu X., and Wu H.. 1999. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-triphosphate and Akt/protein kinase B signaling pathway. Proc. Natl. Acad. Sci. USA 96:6199–6204.
   PubMed Web of Science ®Google Scholar
• Suzuki, A., Kusakai G., Kishimoto A., Lu J., Ogura T., and Esumi H.. 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.
   PubMed Web of Science ®Google Scholar
• Suzuki, A., Kusakai G., Kishimoto A., Lu J., Ogura T., Lavin M. F., and Esumi H.. 2003. Identification of a novel protein kinase mediating Akt survival signaling to ATM. J. Biol. Chem. 278:48–53.
   PubMed Web of Science ®Google Scholar
• Suzuki, A., Kusakai G., Kishimoto A., Minegishi Y., Ogura T., and Esumi H.. 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.
   PubMed Web of Science ®Google Scholar
• Tanno, S., Tanno S., Mitsuuchi Y., Altomare D. A., Xiao G. H., and Testa J. R.. 2001. AKT-activation up-regulates insulin-like growth factor I receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res. 61:589–593.
   PubMed Web of Science ®Google Scholar
• Teraoka, H., Sawada T., Nishihara T., Yashiro M., Ohira M., Ishikawa T., Nishino H., and Hirakawa K.. 2001. Enhanced VEGF production and decreased immunogenicity induced by TGF-beta 1 promote liver metastasis of pancreatic cancer. Br. J. Cancer 85:612–617.
   PubMedGoogle Scholar
• Vaupel, P., Kelleher D. K., and Hockel M.. 2001. Oxygen status of malignant tumors: pathogenesis of hypoxia and significant for tumor therapy. Semin. Oncol. 28:29–35.
   PubMed Web of Science ®Google Scholar
• Vlahos, C. J., Matter W. F., Hui K. Y., and Brown R. F.. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241–5248.
   PubMed Web of Science ®Google Scholar
• Zaman, K., Ryu H., Hall D., O'Donovan K., Lin K. I., Miller M. P., Marquis J. C., Baraban J. M., Semenza G. L., and Ratan R. R.. 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.
   PubMed Web of Science ®Google Scholar
• Zhang, D., and Brodt P.. 2003. Type 1 insulin-like growth factor regulates MT1-MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling. Oncogene 22:974–982.
   PubMed Web of Science ®Google Scholar