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Article

5′-AMP-Activated Protein Kinase (AMPK) Is Induced by Low-Oxygen and Glucose Deprivation Conditions Found in Solid-Tumor Microenvironments

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Pages 5336-5347 | Received 29 Jan 2006, Accepted 26 Apr 2006, Published online: 27 Mar 2023

REFERENCES

  • Airley, R. E., J. Loncaster, J. A. Raleigh, A. L. Harris, S. E. Davidson, R. D. Hunter, C. M. West, and I. J. Stratford. 2003. GLUT-1 and CAIX as intrinsic markers of hypoxia in carcinoma of the cervix: relationship to pimonidazole binding. Int. J. Cancer 104:85–91.
  • Almeida, A., S. Moncada, and J. P. Bolanos. 2004. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat. Cell Biol. 6:45–51.
  • Arcasoy, M. O., K. Amin, S. C. Chou, Z. A. Haroon, M. Varia, and J. A. Raleigh. 2005. Erythropoietin and erythropoietin receptor expression in head and neck cancer: relationship to tumor hypoxia. Clin. Cancer Res. 11:20–27.
  • Barabasi, A. L., and Z. N. Oltvai. 2004. Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5:101–113.
  • Beauloye, C., A. S. Marsin, L. Bertrand, U. Krause, D. G. Hardie, J. L. Vanoverschelde, and L. Hue. 2001. Insulin antagonizes AMP-activated protein kinase activation by ischemia or anoxia in rat hearts, without affecting total adenine nucleotides. FEBS Lett. 505:348–352.
  • Birnbaum, M. J. 2005. Activating AMP-activated protein kinase without AMP. Mol. Cell 19:289–290.
  • Brugarolas, J., and W. G. Kaelin, Jr. 2004. Dysregulation of HIF and VEGF is a unifying feature of the familial hamartoma syndromes. Cancer Cell 6:7–10.
  • Cardenas-Navia, L. I., D. Yu, R. D. Braun, D. M. Brizel, T. W. Secomb, and M. W. Dewhirst. 2004. Tumor-dependent kinetics of partial pressure of oxygen fluctuations during air and oxygen breathing. Cancer Res. 64:6010–6017.
  • Carling, D. 2004. The AMP-activated protein kinase cascade—a unifying system for energy control. Trends Biochem. Sci. 29:18–24.
  • Chou, S. C., Y. Azuma, M. A. Varia, and J. A. Raleigh. 2004. Evidence that involucrin, a marker for differentiation, is oxygen regulated in human squamous cell carcinomas. Br. J. Cancer 90:728–735.
  • 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. 277:32791–32798.
  • Evans, A. M., K. J. W. Mustard, C. N. Wyatt, C. Peers, M. Dipp, P. Kumar, N. P. Kinnear, and D. G. Hardie. 2005. Does AMP-activate protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells? J. Biol. Chem. 280:41504–41511.
  • Frederich, M., L. Zhang, and J. A. Balschi. 2005. Hypoxia and AMP independently regulate AMP-activated protein kinase activity in the heart. Am. J. Physiol. Heart Circ. Physiol. 288:2412–2421.
  • Grunstein, J., W. G. Roberts, O. Mathieu-Costello, D. Hanahan, and R. S. Johnson. 1999. Tumor-derived expression of vascular endothelial growth factor is a critical factor in tumor expansion and vascular function. Cancer Res. 59:1592–1598.
  • Han, S., F. R. Khuri, and J. Roman. 2006. Fibronectin stimulates non-small cell lung carcinoma cell growth through activation of Akt/mammalian target of rapamycin/S6 kinase and inactivation of LKB1/AMP-activated protein kinase signal pathways. Cancer Res. 66:315–323.
  • Han, S., and J. Roman. 2006. Rosiglitazone suppresses human lung carcinoma cell growth through PPARγ-dependent and PPARγ-independent signal pathways. Mol. Cancer Ther. 5:430–437.
  • Hanahan, D., D. Lane, L. Lipsich, M. Wigler, and M. Botchan. 1980. Characteristics of an SV40-plasmid recombinant and its movement into and out of the genome of a murine cell. Cell 21:127–139.
  • Hardie, D. G., and D. A. Pan. 2002. Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem. Soc. Trans. 30:1064–1070.
  • Hardie, D. G., J. W. Scott, D. A. Pan, and E. R. Hudson. 2003. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546:113–120.
  • Horman, S., C. Beauloye, D. Vertommen, J. L. Vanoverschelde, L. Hue, and M. H. Rider. 2003. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J. Biol. Chem. 278:41970–41976.
  • Huang, L. E., and H. F. Bunn. 2003. Hypoxia-inducible factor and its biomedical relevance. J. Biol. Chem. 278:19575–19578.
  • Hue, L., C. Beauloye, L. Bertrand, S. Horman, U. Krause, A. S. Marsin, D. Meisse, D. Vertommen, and M. H. Rider. 2003. New targets of AMP-activated protein kinase. Biochem. Soc. Trans. 31:213–215.
  • Janssen, H. L., K. M. Haustermans, D. Sprong, G. Blommestijn, I. Hofland, F. J. Hoebers, E. Blijweert, J. A. Raleigh, G. L. Semenza, M. A. Varia, A. J. Balm, M. L. van Velthuysen, P. Delaere, R. Sciot, and A. C. Begg. 2002. HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. Int. J. Radiat. Oncol. Biol. Phys. 54:1537–1549.
  • Jiang, B. H., G. L. Semenza, C. Bauer, and H. H. Marti. 1996. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am. J. Physiol. 271:C1172–C1180.
  • Johnson, R., B. Spiegelman, D. Hanahan, and R. Wisdom. 1996. Cellular transformation and malignancy induced by ras require c-jun. Mol. Cell. Biol. 16:4504–4511.
  • Jorgensen, S. B., B. Viollet, F. Andreelli, C. Frosig, J. B. Birk, P. Schjerling, S. Vaulont, E. A. Richter, and J. F. Wojtaszewski. 2004. Knockout of the α2 but not α1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-β-4-ribofuranoside but not contraction-induced glucose uptake in skeletal muscle. J. Biol. Chem. 279:1070–1079.
  • 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.
  • Kim, K. H., M. J. Song, J. Chung, H. Park, and J. B. Kim. 2005. Hypoxia inhibits adipocyte differentiation in a HDAC-independent manner. Biochem. Biophys. Res. Commun. 333:1178–1184.
  • Kusakai, G., A. Suzuki, T. Ogura, M. Kaminishi, and H. Esumi. 2004. Strong association of ARK5 with tumor invasion and metastasis. J. Exp. Clin. Cancer Res. 23:263–268.
  • Laderoute, K. 2005. The interaction between HIF-1 and AP-1 transcription factors in response to low oxygen. Semin. Cell Dev. Biol. 16:502–513.
  • Laderoute, K. R., J. M. Calaoagan, C. Gustafson-Brown, A. M. Knapp, G. C. Li, H. L. Mendonca, H. E. Ryan, Z. Wang, and R. S. Johnson. 2002. The response of c-Jun/AP-1 to chronic hypoxia is hypoxia-inducible factor 1α dependent. Mol. Cell. Biol. 22:2515–2523.
  • Laderoute, K. R., J. M. Calaoagan, M. Knapp, and R. S. Johnson. 2004. Glucose utilization is essential for hypoxia-inducible factor 1α-dependent phosphorylation of c-Jun. Mol. Cell. Biol. 24:4128–4137.
  • Lee, M., J. T. Hwang, H. J. Lee, S. N. Jung, I. Kang, S. G. Chi, S. S. Kim, and J. Ha. 2003. AMP-activated protein kinase activity is critical for hypoxia-inducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells. J. Biol. Chem. 278:39653–39661.
  • Leff, T. 2003. AMP-activated protein kinase regulates gene expression by direct phosphorylation of nuclear proteins. Biochem. Soc. Trans. 31:224–227.
  • Leo, C., A. J. Giaccia, and N. C. Denko. 2004. The hypoxic tumor microenvironment and gene expression. Semin. Radiat. Oncol. 14:207–214.
  • Lizcano, J. M., O. Goransson, R. Toth, M. Deak, N. A. Morrice, J. Boudeau, S. A. Hawley, L. Udd, T. P. Makela, D. G. Hardie, and D. R. Alessi. 2004. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23:833–843.
  • Marignani, P. A. 2005. LKB1, the multitasking tumour suppressor kinase. J. Clin. Pathol. 58:15–19.
  • Marsin, A., C. Bouzin, L. Bertrand, and L. Hue. 2002. The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J. Biol. Chem. 277:30778–30783.
  • Marsin, A. S., L. Bertrand, M. H. Rider, J. Deprez, C. Beauloye, M. F. Vincent, G. Van den Berghe, D. Carling, and L. Hue. 2000. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10:1247–1255.
  • Murphy, B. J., B. Sato, T. P. Dalton, and K. R. Laderoute. 2005. The metal responsive transcription factor 1 (MTF-1) contributes to HIF-1 activation during hypoxic stress. Biochem. Biophys. Res. Commun. 337:860–867.
  • Nagata, D., M. Mogi, and K. Walsh. 2003. AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278:31000–31006.
  • Neurath, K. M., M. P. Keough, T. Mikkelsen, and K. P. Claffey. 2006. AMP-dependent protein kinase α2 isoform promotes hypoxia-induced VEGF expression in human glioblastoma. Glia 53:733–743.
  • Poellinger, L., and R. S. Johnson. 2004. HIF-1 and hypoxic response: the plot thickens. Curr. Opin. Genet. Dev. 14:81–85.
  • Raleigh, J. A., D. P. Calkins-Adams, L. H. Rinker, C. A. Ballenger, M. C. Weissler, W. C. Fowler, Jr., D. B. Novotny, and M. A. Varia. 1998. Hypoxia and vascular endothelial growth factor expression in human squamous cell carcinomas using pimonidazole as a hypoxia marker. Cancer Res. 58:3765–3768.
  • Raleigh, J. A., S. C. Chou, D. P. Calkins-Adams, C. A. Ballenger, D. B. Novotny, and M. A. Varia. 2000. A clinical study of hypoxia and metallothionein protein expression in squamous cell carcinomas. Clin. Cancer Res. 6:855–862.
  • Rattan, R., S. Giri, A. K. Singh, and I. Singh. 2005. 5-Aminoimidazole-4-carboxamide-1-β-d-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase. J. Biol. Chem. 280:39582–39593.
  • Rutter, G. A., G. Da Silva Xavier, and I. Leclerc. 2003. Roles of 5′-AMP-activated protein kinase (AMPK) in mammalian glucose homoeostasis. Biochem. J. 375:1–16.
  • Ryan, H. E., M. Poloni, W. McNulty, D. Elson, M. Gassmann, J. M. Arbeit, and R. S. Johnson. 2000. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res. 60:4010–4015.
  • Schroeder, T., H. Yuan, B. L. Viglianti, C. Peltz, S. Asopa, Z. Vujaskovic, and M. W. Dewhirst. 2005. Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res. 65:5163–5171.
  • Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721–732.
  • Shan, S., A. C. Lockhart, W. Y. Saito, A. M. Knapp, K. R. Laderoute, and M. W. Dewhirst. 2001. The novel tubulin-binding drug BTO-956 inhibits R3230ac mammary carcinoma growth and angiogenesis in Fischer 344 rats. Clin. Cancer Res. 7:2590–2596.
  • Shaw, R. J., M. Kosmatka, N. Bardeesy, R. L. Hurley, L. A. Witters, R. A. DePinho, and L. C. Cantley. 2004. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc. Natl. Acad. Sci. USA 101:3329–3335.
  • 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 the ATM protein. J. Biol. Chem. 278:48–53.
  • Suzuki, A., G. Kusakai, A. Kishimoto, Y. Minegichi, 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.
  • Suzuki, A., G. Kusakai, A. Kishimoto, Y. Shimojo, S. Miyamoto, T. Ogura, A. Ochiai, and H. Esumi. 2004. Regulation of caspase-6 and FLIP by the AMPK family member ARK5. Oncogene 23:7067–7075.
  • Suzuki, A., G. I. Kusakai, Y. Shimojo, J. Chen, T. Ogura, M. Kobayashi, and H. Esumi. 2005. Involvement of TGF-β1 signaling in hypoxia-induced tolerance to glucose starvation. J. Biol. Chem. 280:31557–31563.
  • Suzuki, A., J. Lu, G. Kusakai, A. Kishimoto, T. Ogura, and H. Esumi. 2004. ARK5 is a tumor invasion-associated factor downstream of Akt signaling. Mol. Cell. Biol. 24:3526–3535.
  • Terai, K., Y. Hiramoto, M. Masaki, S. Sugiyama, T. Kuroda, M. Hori, I. Kawase, and H. Hirota. 2005. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell. Biol. 25:9554–9575.
  • Vaupel, P. 2004. Tumor microenvironmental physiology and its implications for radiation oncology. Semin. Radiat. Oncol. 14:198–206.
  • Viollet, B., F. Andreelli, S. B. Jorgensen, C. Perrin, A. Geloen, D. Flamez, J. Mu, C. Lenzner, O. Baud, M. Bennoun, E. Gomas, G. Nicolas, J. F. Wojtaszewski, A. Kahn, D. Carling, F. C. Schuit, M. J. Birnbaum, E. A. Richter, R. Burcelin, and S. Vaulont. 2003. The AMP-activated protein kinase α2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Investig. 111:91–98.
  • Yun, H., M. Lee, S. S. Kim, and J. Ha. 2005. Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J. Biol. Chem. 280:9963–9972.

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