Differential contribution of key metabolic substrates and cellular oxygen in HIF signalling

Experimental Cell Research

Volumn 330, Issue 1, 2015, Pages 13-28

  Zhdanov, Alexander V ^a   Waters, Alicia H C ^a   Golubeva, Anna V ^b   Papkovsky, Dmitri B ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Cancer cell; Cellular oxygen; Glutaminolysis; Glycolysis; HIF signalling; Metabolic substrates

Indexed keywords

ADENOSINE TRIPHOSPHATE; DORSOMORPHIN; GLUCOSE; GLUTAMINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OXYGEN; PROTEIN KINASE B; UNCLASSIFIED DRUG; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL HYPOXIA; CELL METABOLISM; CONTROLLED STUDY; DEOXYGENATION; GLYCOLYSIS; HYPOXIC CELL; INTRACELLULAR SIGNALING; NONHUMAN; OXYGEN CONSUMPTION; PC12 CELL LINE; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; METABOLISM; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; GLUCOSE; GLUTAMINE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; OXYGEN; PC12 CELLS; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZOLES; PYRIMIDINES; RATS;

EID: 84916898065     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.10.005     Document Type: Article

References (85)

1. Mole D.R., Blancher C., Copley R.R., Pollard P.J., Gleadle J.M., Ragoussis J., Ratcliffe P.J. Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts. J. Biol. Chem. 2009, 284:16767-16775.
2. Ratcliffe P.J. Oxygen sensing and hypoxia signalling pathways in animals: the implications of physiology for cancer. J. Physiol. 2013, 591:2027-2042.
3. Loboda A., Jozkowicz A., Dulak J. HIF-1 and HIF-2 transcription factors-similar but not identical. Mol. Cells 2010, 29:435-442.
4. Semenza G.L. Hypoxia-inducible factors in physiology and medicine. Cell 2012, 148:399-408.
5. van Uden P., Kenneth N.S., Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem. J. 2008, 412:477-484.
6. Nguyen M.P., Lee S., Lee Y.M. Epigenetic regulation of hypoxia inducible factor in diseases and therapeutics. Arch. Pharm. Res. 2013, 36:252-263.
7. Bruning U., Cerone L., Neufeld Z., Fitzpatrick S.F., Cheong A., Scholz C.C., Simpson D.A., Leonard M.O., Tambuwala M.M., Cummins E.P., Taylor C.T. MicroRNA-155 promotes resolution of hypoxia-inducible factor 1alpha activity during prolonged hypoxia. Mol. Cell Biol. 2011, 31:4087-4096.
8. Rane S., He M., Sayed D., Vashistha H., Malhotra A., Sadoshima J., Vatner D.E., Vatner S.F., Abdellatif M. Downregulation of MiR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circul. Res. 2009, 104:879-886.
9. Mathew L.K., Lee S.S., Skuli N., Rao S., Keith B., Nathanson K.L., Lal P., Simon M.C. Restricted expression of miR-30c-2-3p and miR-30a-3p in clear cell renal cell carcinomas enhances HIF2α activity. Cancer Disc. 2014, 4:53-60.
10. Koh M.Y., Spivak-Kroizman T.R., Powis G. HIF-1 regulation: not so easy come, easy go. Trends Biochem. Sci. 2008, 33:526-534.
11. Davis M.R., Shawron K.M., Rendina E., Peterson S.K., Lucas E.A., Smith B.J., Clarke S.L. Hypoxia inducible factor-2 alpha is translationally repressed in response to dietary iron deficiency in Sprague-Dawley rats. J. Nutr. 2011, 141:1590-1596.
12. Sanchez M., Galy B., Muckenthaler M.U., Hentze M.W. Iron-regulatory proteins limit hypoxia-inducible factor-2alpha expression in iron deficiency. Nat. Struct. Mol. Biol. 2007, 14:420-426.
13. Zimmer M., Lamb J., Ebert B.L., Lynch M., Neil C., Schmidt E., Golub T.R., Iliopoulos O. The connectivity map links iron regulatory protein-1-mediated inhibition of hypoxia-inducible factor-2a translation to the anti-inflammatory 15-deoxy-delta12,14-prostaglandin J2. Cancer Res. 2010, 70:3071-3079.
14. Liu L., Cash T.P., Jones R.G., Keith B., Thompson C.B., Simon M.C. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 2006, 21:521-531.
15. Papandreou I., Lim A.L., Laderoute K., Denko N.C. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ. 2008, 15:1572-1581.
16. Laderoute K.R., Amin K., Calaoagan J.M., Knapp M., Le T., Orduna J., Foretz M., Viollet B. 5[U+05F3]-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol. Cell Biol. 2006, 26:5336-5347.
17. Laplante M., Sabatini David M. mTOR signalling in growth control and disease. Cell 2012, 149:274-293.
18. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
19. Nguyen L.K., Cavadas M.A., Scholz C.C., Fitzpatrick S.F., Bruning U., Cummins E.P., Tambuwala M.M., Manresa M.C., Kholodenko B.N., Taylor C.T. A dynamic model of the hypoxia-inducible factor 1α (HIF-1α) network. J. Cell Sci. 2013, 126:1454-1463.
20. Zhdanov A.V., Ogurtsov V.I., Taylor C.T., Papkovsky D.B. Monitoring of cell oxygenation and responses to metabolic stimulation by intracellular oxygen sensing technique. Integr. Biol. 2010, 2:443-451.
21. Zhdanov A.V., Dmitriev R.I., Papkovsky D.B. Bafilomycin A1 activates HIF-dependent signalling in human colon cancer cells via mitochondrial uncoupling. Biosci. Rep. 2012, 32:587-595.
22. Brown S.T., Nurse C.A. Induction of HIF-2alpha is dependent on mitochondrial O2 consumption in an O2-sensitive adrenomedullary chromaffin cell line. Am. J. Physiol. Cell. Physiol. 2008, 294:C1305-C1312.
23. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008, 7:11-20.
24. Anastasiou D., Cantley L.C. Breathless cancer cells get fat on glutamine. Cell Res. 2012.
25. Zhao Y., Butler E., Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013, 4:e532.
26. Cheong H., Lu C., Lindsten T., Thompson C.B. Therapeutic targets in cancer cell metabolism and autophagy. Nat. Biotechnol. 2012, 30:671-678.
27. Hamanaka R.B., Chandel N.S. Targeting glucose metabolism for cancer therapy. J. Exp. Med. 2012, 209:211-215.
28. Daye D., Wellen K.E. Metabolic reprogramming in cancer: unraveling the role of glutamine in tumorigenesis. in: Zachary T. Schafer, Leta K. Nutt, Mark E. Fortini (Eds.), Seminars in Cell & Developmental Biology 2012, 23:362-369. Elsevier.
29. Wilson W.R., Hay M.P. Targeting hypoxia in cancer therapy. Nat. Rev. Cancer 2011, 11:393-410.
30. Semenza G.L. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol. Sci. 2012, 33:207-214.
31. Staab A., Löffler J., Said H.M., Katzer A., Beyer M., Polat B., Einsele H., Flentje M., Vordermark D. Modulation of glucose metabolism inhibits hypoxic accumulation of hypoxia-inducible factor-1α (HIF-1α). Strahlenther. Onkol. 2007, 183:366-373.
32. Vordermark D., Kraft P., Katzer A., Bölling T., Willner J., Flentje M. Glucose requirement for hypoxic accumulation of hypoxia-inducible factor-1α (HIF-1α). Cancer Lett. 2005, 230:122-133.
33. Kwon S.J., Lee Y.J. Effect of low glutamine/glucose on hypoxia-induced elevation of hypoxia-inducible factor-1α in human pancreatic cancer MiaPaCa-2 and human prostatic cancer DU-145 cells. Clin. Cancer Res. 2005, 11:4694-4700.
34. Drogat B., Bouchecareilh M., North S., Petibois C., Déléris G., Chevet E., Bikfalvi A., Moenner M. Acute L-glutamine deprivation compromises VEGF-a upregulation in A549/8 human carcinoma cells. J. Cell. Physiol. 2007, 212:463-472.
35. Brahimi-Horn M.C., Chiche J., Pouysségur J. Hypoxia signalling controls metabolic demand. Curr. Opin. Cell Biol. 2007, 19:223-229.
36. Dehne N., Kerkweg U., Otto T., Fandrey J. The HIF-1 response to simulated ischemia in mouse skeletal muscle cells neither enhances glycolysis nor prevents myotube cell death. Am. J. Physiol.-Regul., Integr. Compar. Physiol. 2007, 293:R1693-R1701.
37. Deschepper M., Oudina K., David B., Myrtil V., Collet C., Bensidhoum M., Logeart-Avramoglou D., Petite H. Survival and function of mesenchymal stem cells (MSCs) depend on glucose to overcome exposure to long-term, severe and continuous hypoxia. J. Cell. Mol. Med. 2011, 15:1505-1514.
38. Karuppagounder S.S., Basso M., Sleiman S.F., Ma T.C., Speer R.E., Smirnova N.A., Gazaryan I.G., Ratan R.R. In vitro ischemia suppresses hypoxic induction of hypoxia-inducible factor-1alpha by inhibition of synthesis and not enhanced degradation. J. Neurosci. Res. 2013, 91:1066-1075.
39. Zhdanov A.V., Dmitriev R.I., Golubeva A.V., Gavrilova S.A., Papkovsky D.B. Chronic hypoxia leads to a glycolytic phenotype and suppressed HIF-2 signalling in PC12 cells. Biochim. Biophys. Acta 1830, 2013:3553-3569.
40. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 1976, 73:2424-2428.
41. Hynes J., Floyd S., Soini A.E., O'Connor R., Papkovsky D.B. Fluorescence-based cell viability screening assays using water-soluble oxygen probes. J. Biomol. Screen 2003, 8:264-272.
42. Fercher A., Borisov S.M., Zhdanov A.V., Klimant I., Papkovsky D.B. Intracellular O2 sensing probe based on cell-penetrating phosphorescent nanoparticles. ACS Nano 2011, 5:5499-5508.
43. Hynes J., O'Riordan T.C., Zhdanov A.V., Uray G., Will Y., Papkovsky D.B. In vitro analysis of cell metabolism using a long-decay pH-sensitive lanthanide probe and extracellular acidification assay. Anal. Biochem. 2009, 390:21-28.
44. Robinson M.M., McBryant S.J., Tsukamoto T., Rojas C., Ferraris D.V., Hamilton S.K., Hansen J.C., Curthoys N.P. Novel mechanism of inhibition of rat kidney-type glutaminase by bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulphide (BPTES). Biochem. J. 2007, 406:407-414.
45. Alvarez-Tejado M., Naranjo-Suárez S., Jiménez C., Carrera A.C., Landázuri M.O., del Peso L. Hypoxia induces the activation of the phosphatidylinositol 3-Kinase/Akt cell survival pathway in PC12 cells protective role in apoptosis. J. Biol. Chem. 2001, 276:22368-22374.
46. O'Driscoll C.M., Gorman A.M. Hypoxia induces neurite outgrowth in PC12 cells that is mediated through adenosine A2A receptors. Neuroscience 2005, 131:321-329.
47. Torii S., Okamura N., Suzuki Y., Ishizawa T., Yasumoto K., Sogawa K. Cyclic AMP represses the hypoxic induction of hypoxia-inducible factors in PC12 cells. J. Biochem. 2009, 146:839-844.
48. Zhdanov A.V., Dmitriev R.I., Papkovsky D.B. Bafilomycin A1 activates respiration of neuronal cells via uncoupling associated with flickering depolarization of mitochondria. Cell Mol. Life Sci. 2011, 68:903-917.
49. Zhdanov A.V., Waters A.H., Golubeva A.V., Dmitriev R.I., Papkovsky D.B. Availability of the key metabolic substrates dictates the respiratory response of cancer cells to the mitochondrial uncoupling. Biochim. Biophys. Acta (BBA)-Bioener. 2014, 1837:51-62.
50. O'Riordan T.C., Zhdanov A.V., Ponomarev G.V., Papkovsky D.B. Analysis of intracellular oxygen and metabolic responses of mammalian cells by time-resolved fluorometry. Anal. Chem. 2007, 79:9414-9419.
51. Zhdanov A.V., Favre C., O'Flaherty L., Adam J., O'Connor R., Pollard P.J., Papkovsky D.B. Comparative bioenergetic assessment of transformed cells using a cell energy budget platform. Integr. Biol. 2011, 3:1135-1142.
52. Brand M. The efficiency and plasticity of mitochondrial energy transduction. Biochem. Soc. Trans. 2005, 33:897-904.
53. Jochmanová I., Zelinka T., Widimský J., Pacak K. HIF signaling pathway in pheochromocytoma and other neuroendocrine tumors. Physiol. Res. 2014, 63:S251-S262.
54. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyk-Melody J., Wu M., Ventre J., Doebber T., Fujii N. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 2001, 108:1167-1174.
55. Zhdanov A.V., Ward M.W., Prehn J.H., Papkovsky D.B. Dynamics of intracellular oxygen in PC12 Cells upon stimulation of neurotransmission. J. Biol. Chem. 2008, 283:5650-5661.
56. Elvidge G.P., Glenny L., Appelhoff R.J., Ratcliffe P.J., Ragoussis J., Gleadle J.M. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J. Biol. Chem. 2006, 281:15215-15226.
57. Le A., Lane A.N., Hamaker M., Bose S., Gouw A., Barbi J., Tsukamoto T., Rojas C.J., Slusher B.S., Zhang H. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab. 2012, 15:110-121.
58. Jiang B.H., Semenza G.L., Bauer C., Marti H.H. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am. J. Physiol. 1996, 271:C1172-C1180.
59. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Sci. Signall. 2009, 324:1029.
60. Hawley S.A., Davison M., Woods A., Davies S.P., Beri R.K., Carling D., Hardie D.G. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 1996, 271:27879-27887.
61. Wu S.-B., Wei Y.-H. AMPK-mediated increase of glycolysis as an adaptive response to oxidative stress in human cells: implication of the cell survival in mitochondrial diseases. Biochim. Biophys. Acta (BBA)-Mol. Basis Dis. 2011.
62. Mihaylova M.M., Shaw R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 2011, 13:1016-1023.
63. Faubert B., Boily G., Izreig S., Griss T., Samborska B., Dong Z., Dupuy F., Chambers C., Fuerth Benjamin J., Viollet B., Mamer Orval A., Avizonis D., DeBerardinis Ralph J., Siegel Peter M., Jones Russell G. AMPK is a negative regulator of the warburg effect and suppresses tumor growth in vivo. Cell Metab. 2013, 17:113-124.
64. Tan C.Y., Hagen T. Post-translational regulation of mTOR complex 1 in hypoxia and reoxygenation. Cell. Signall. 2013.
65. Inoki K., Zhu T., Guan K.-L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
66. Rathmell J.C., Fox C.J., Plas D.R., Hammerman P.S., Cinalli R.M., Thompson C.B. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol. Cell. Biol. 2003, 23:7315-7328.
67. Elstrom R.L., Bauer D.E., Buzzai M., Karnauskas R., Harris M.H., Plas D.R., Zhuang H., Cinalli R.M., Alavi A., Rudin C.M., Thompson C.B. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 2004, 64:3892-3899.
68. Beitner-Johnson D., Rust R.T., Hsieh T.C., Millhorn D.E. Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell. Signall. 2001, 13:23-27.
69. Elorza A., Soro-Arnáiz I., Meléndez-Rodríguez F., Rodríguez-Vaello V., Marsboom G., Cárcer G.de, Acosta-Iborra B., Albacete-Albacete L., Ordóñez A., Serrano-Oviedo L. HIF2α acts as an mTORC1 activator through the amino acid carrier SLC7A5. Mol. Cell 2012.
70. Seltzer M.J., Bennett B.D., Joshi A.D., Gao P., Thomas A.G., Ferraris D.V., Tsukamoto T., Rojas C.J., Slusher B.S., Rabinowitz J.D. Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1. Cancer Res. 2010, 70:8981-8987.
71. Lu H., Dalgard C.L., Mohyeldin A., McFate T., Tait A.S., Verma A. Reversible inactivation of HIF-1 prolyl hydroxylases allows cell metabolism to control basal HIF-1. J. Biol. Chem. 2005, 280:41928-41939.
72. Cantó C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 2009, 20:98.
73. Lu J., Wu D.-M., Hu B., Cheng W., Zheng Y.-l., Zhang Z.-f., Ye Q., Fan S.-h., Shan Q., Wang Y.-j. Chronic administration of troxerutin protects mouse brain against d-galactose-induced impairment of cholinergic system. Neurobiol. Learn. Mem. 2010, 93:157-164.
74. Aguer C., Gambarotta D., Mailloux R.J., Moffat C., Dent R., McPherson R., Harper M.-E. Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells. PloS one 2011, 6:e28536.
75. Emerling B.M., Viollet B., Tormos K.V., Chandel N.S. Compound C inhibits hypoxic activation of HIF-1 independent of AMPK. FEBS Lett. 2007, 581:5727-5731.
76. Vucicevic L., Misirkic M., Janjetovic K., Vilimanovich U., Sudar E., Isenovic E., Prica M., Harhaji-Trajkovic L., Kravic-Stevovic T., Bumbasirevic V., Trajkovic V. Compound C induces protective autophagy in cancer cells through AMPK inhibition-independent blockade of Akt/mTOR pathway. Autophagy 2011, 7:40-50.
77. Carreau A., El Hafny-Rahbi B., Matejuk A., Grillon C., Kieda C. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J. Cell. Mol. Med. 2011, 15:1239-1253.
78. Wise D.R., Thompson C.B. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem. Sci. 2010, 35:427-433.
79. Taylor S.C., Peers C. Hypoxia evokes catecholamine secretion from rat pheochromocytoma PC-12 cells. Biochem. Biophys. Res. Commun. 1998, 248:13-17.
80. Bracken C.P., Fedele A.O., Linke S., Balrak W., Lisy K., Whitelaw M.L., Peet D.J. Cell-specific regulation of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha stabilization and transactivation in a graded oxygen environment. J. Biol. Chem. 2006, 281:22575-22585.
81. Sims N.R., Muyderman H. Mitochondria, oxidative metabolism and cell death in stroke. Biochim. Biophys. Acta 1802, 2010:80-91.
82. Cryer P.E., Davis S.N., Shamoon H. Hypoglycemia in diabetes. Diab. Care 2003, 26:1902-1912.
83. El-Serag H.B., Marrero J.A., Rudolph L., Reddy K.R. Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology 2008, 134:1752-1763.
84. Steele M.L., Robinson S.R. Reactive astrocytes give neurons less support: implications for Alzheimer[U+05F3]s disease. Neurobiol. Aging 2012, 33(423):e421-e423. e413.
85. He Y., Hakvoort T., Vermeulen J.L., Labruyère W.T., De Waart D.R., Van Der Hel W.S., Ruijter J.M., Uylings H., Lamers W.H. Glutamine synthetase deficiency in murine astrocytes results in neonatal death. Glia 2010, 58:741-754.