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Mithochondria signaling in adaptation to hypoxia
Luk'ianova LD
Institute of General Pathology and Pathophysiology, RAMS, Moscow, Russia
DOI: https://doi.org/10.15407/fz59.06.141
Abstract
A bioenergetic mechanism for development of urgent adaptation to hypoxia is considered. Hypoxia induces reprogramming of respiratory chain function and switching from oxidation of NAD-related substrates (complex I) to succinate oxidation (complex II). Transient, reversible, compensatory activation of respiratory chain complex II is a major mechanism of urgent adaptation to hypoxia necessary for 1) succinate- related energy synthesis in conditions of oxygen deficiency and formation of urgent resistance in the body; 2) succinate- related stabilization of HIF-1alpha and initiation of its transcriptional activity related with formation of urgent and long-term adaptation; 3) succinate- related activation of a succinate-specific receptor GPR91. Therefore succinate is a signaling molecule, and its effects are realized at three levels in hypoxia, intramitochondrial, intracellular and intercellular.
Keywords:
hypoxia, adaptation, respiratory chain reprogramming,mitochondrial complexes I and II, HIF-1б, GPR91
References
- Kirova Yu.I., Germanova E.L., Luk'yanova L.D. Fenotipicheskie osobennosti dinamiki soderzhaniya HIF-1α v neortekse kris pri razlichnih rezhimah gipoksii . Byul. eksperim. biologii i meditsini. 2012. 154(12). P. 681-686.
- Luk'yanova L.D. Bioenergeticheskaya gipoksiya. ponyatie, mehanizmi, korrektsiya . Tam zhe. 1997. 124 (9). P. 244-254.
- Luk'yanova L.D. Mitohondrial'naya disfunktsiya tipovoi patologicheskii protsess, molekulyarnii mehanizm gipoksii. V kn.: Problemi gipoksii. molekulyarnie, fiziologicheskie i klinicheskie aspekti . Pod red. Luk'yanovoi L.D, Ushakova I.B. M., 2004. P. 5-31.
- Luk'yanova L.D. Cignal'naya funktsiya mitohondrii pri gipoksii i adaptatsii . Patogenez. 2008, N 3. P. 4-12.
- Luk'yanova L.D. Sovremennie problemi adaptatsii k gipoksii. Signal'nie mehanizmi i ih rol' v sistemnoi regulyatsii . Patol. fiziologiya i eksperim.. terapiya. 2011, N 1. P. 3-19.
- Luk'yanova L.D., Germanova E.L., Tsibina T.A., Chernobaeva G.N. Energotropnoe deistvie suktsinatsoderzhashchih proizvodnih 3-oksipiridina . Byul. eksperim. biologii i meditsini. 2009. 148(10). P. 388-392.
- Luk'yanova L.D, Germanova E.L., Kopaladze R.A.. Zakonomernosti formirovaniya rezistentnosti organizma pri raznih rezhimah gipoksicheskogo prekonditsionirovaniya. rol' gipoksicheskogo perioda i reoksigenatsii . Tam zhe. 2009. 147(4). P. 380-384.
- Luk'yanova L.D., Dudchenko A.M., Tsibina T.A., Germanova E.L., Tkachuk E.N., Erenburg I.V. Deistvie interval'noi normobaricheskoi gipoksii na kineticheskie svoistva mitohondrial'nih fermentov . Tam zhe. 2007, N 12. P.644-651.
- Luk'yanova L.D., Kirova Yu.I. Vliyanie gipoksicheskogo prekonditsionirovaniya na svobodnoradikal'nie protsessi v tkanyah kris s razlichnoi tolerantnost'yu k gipoksii . Tam zhe. 2011. 151(3). P. 263-267.
- Luk'yanova L.D., Kirova Yu.I., Sukoyan G.V. Signal'nie mehanizmi adaptatsii k gipoksii i ih rol' v sistemnoi regulyatsii . Biol. membrani. 2012, N 4. P. 238-252.
- Luk'yanova L.D., Sukoyan G.V, Kirova Yu. I. O roli provospalitel'nih faktorov, NO i nekotorih pokazatelei lipidnogo obmena v formirovanii srochnoi adaptatsii k gipoksii i akkumulyatsii HIF-1α . Byul. eksperim. biologii i meditsini. 2012. 11. P. 510-514.
- Maevskii E.I., Rozenfel'd A.S., Grishina E.V., Kondrashova M.N. Korrektsiya metabolicheskogo atsidoza putem podderzhaniya funktsii mitohondrii. Pushchino, 2001.
PubMed
- Agani F. H., Pichiule P., Chavez J.C., La Manna J.C. The role of Mitochondria in the regulation of Hypoxia-inducible Factor 1 Expression during Hypoxia . JBC. 2000. 275(46). p. 35863-35867.
CrossRef
PubMed
- Agani F. H., Puchowicz M., Chavez J.C., Pichiule P., LaManna J. Inhibitors of mitochondrial complex I attenuate the accumulation of hypoxia-inducible factor-1 during hypoxia in Hep3B cells . Compar. Biochem. and Physiol. 2000. 132(1). p. 107-109.
CrossRef
- Agani F.H., Pichule P., Chavez C., LaManna J.C. Inhibitors of mitochondrial complex I attenuate the accumulation of hypoxia-inducible factor-1 during hypoxia in Hep3B cells . Compar. Biochem. Physiol. Part A. 2002. 132(1). p. 107-109.
CrossRef
- Aithal H.N, Ramasarma T. Activation of liver succinate dehydrogenase in rats exposed to hypobaric conditions . Biochem J. 1969. 115(1). p. 77-83.
CrossRef
PubMed PubMedCentral
- Baumbach L., Leyssac P.P., Skinner S.L. Studies on rennin release from isolated superfused glomeruli. effects of temperature, urea, oubain and ethacrynic acid . J. Physiol. 1976. 258. p. 243-256.
CrossRef
PubMed PubMedCentral
- Baysal B.E. On the assotiation of succinate dehydrogenese mutations with hereditary paraganglion . Trends Endocrinil. Metab. 2003. 14. p. 453-459.
CrossRef
PubMed
- Brandt U. Proton translocation by membrane-bound NADH-ubiquinone oxidoreductaise (complex I) through redox-gated ligand conduction . Biochem. Biophys. Acta. 1997. 1318. p. 79-91.
CrossRef
- Briere J-J., Chretien D., Benit P., Rustin P. Respiratory chain defects. what do we know for sure about their consequences in vivo . BBA. 2004. 1659. p. 172-177.
CrossRef
- Brunk U.T., Terman A. The mitochondrial-lysosomal axis theory of aging . Eur. J. Biochem. 2002. 269. p. 1996-2002.
CrossRef
PubMed
- Butow R.A., Avadhani N.G. Mitochondria signaling . The retrograde response. Molecular Cell. 2004. 14(1). p. 1-15.
CrossRef
- Cascarano J., Ades I.Z., O'Conner J.D. Hypoxia. a succinate-fumerate electron shuttle between peripheral cells and lung . J Exp Zool. 1976. 198(2). p. 149-153.
CrossRef
PubMed
- Chandel N.S., Schumacker P.T. Cell depleted of mitochondrial DNA (ρº) yield insight into physiological mechanisms . FEBS Lett. 1999. 454. p. 173-176.
CrossRef
- Chandel N.S., Schumacker P.T. Cellular oxygen sensing by mitochondria. old questions, new insight . J. Amer. Physiol. 2000. 88. p. 1880-1889.
CrossRef
- Chavez J.C., Agani F., Pichule P., LaManna J.C. Expression of hypoxia-inducible factor-1α in the brain of rats during chronic hypoxia . Ibid. 2000. 89(5). p. 1937- 1942.
CrossRef
- Correa P.R., Kruglov E.A, Thompson M., Leite M.F., Dranoff J.A., Nathanson M.H. Succinate is a paracrine signal for liver damage . J. Hepatology. 2007. 47. p. 262-269.
CrossRef
PubMed PubMedCentral
- Das J. The role of mitochondrial respiration in physiological and evolutionary adaptation . Bioessays. 2006. 28(9). p. 890-901.
CrossRef
PubMed
- Da Silva M.M., Sartori A., Belisle E., Kowaltowsky A.J. Ischemic preconditioning inhibits mitochondrial respiration, increase H2O2 release, and enhances K+ transport . Amer. J. Physiol. Heart Circ. Physiol. 2003. 285. P. 154-162.
CrossRef
PubMed
- Devin A., Rigoulet M. Mechanisms of mitochondrial response to variations in energy demand in eukaryotic cells . Amer. J. Physiol. Cell Physiol. 2007. 292(1). p. 52-58.
CrossRef
PubMed
- Di Lisa F., Ziegler M. Pathophysiological revelance of mitochondria in NAD+ metabolism . FEBS Lett. 2001. 492. p. 4-8.
CrossRef
- Duchen M.R. Roles of Mitochondria in Health and Disease. Diabetes. 2004. 53. p. 96-102.
CrossRef
- Feldkamp T., Kribben A., Roeser N.F., Senter R.A., Kemner S., Venkatachalam M.A., Nissim I., Weinberg J.M. Preservation of complex I function during hypoxiareoxygenation-induced mitochondrial injury in proximal tubules . Amer. J. Renal. Physiol. 2004. 286(4). p. 749-759.
- Fiermonte G. Organization and sequence of the gene for the human mitochondrial dicarboxylate carrier. evolution of the carrier family . Bioch. J. 1999. 344. p. 953-960.
CrossRef
- Felty Q., Roy D. Estrogen, mitochondrea, and growth of cancer non cancer cells . J. Carcinogenesis. 2005. 4, N 1. p. 1-34.
CrossRef
PubMed PubMedCentral
- Genova M.I., C. Casteluccio, R. Fato, G. Parenti-Castelli, M. Merlo-Pich, G. Formiggini, C. Bovina, M. Marchetti, G. Lenaz. Major changes in Complex I activity in mitochondrian from aged rats may not be detected by direct assay of NADH-coenzymeQ reductase . Biochem. J. 1995. 311. p. 105-109.
CrossRef
PubMed PubMedCentral
- Gnaiger E. Mitochondrial Physiology. The many Faces and functions of on organelle. MiP . Austria, 2005.
PubMed
- Goldberg N. D., Passonneau J. V., Lowry O.H. Effects of Changes in Brain Acid Cycle Intermediates . J. Biol. Chem. 1966. 241. p. 3997-4003.
PubMed
- Grai M.W., Burger G., Lang B.F. Mitochondrion evolution . Science. 1999. 283. P. 1467- 1481.
- Gullans, S. R., Kone, B. C., Avison, M. J., Giebisch, G. Succinate alters respiration, membrane potential, and intracellular K+ in proximal tubule . Amer. J. Physiol. 1988. 55. p. F1170-F1177.
- Gutman M. Modulation of mitochondrial succinate dehydrogenese activity, mechanism and function. Mol . Cell Biochem. 1978. 20. p. 41-60.
CrossRef
PubMed
- Hakak Y., Lehmann-Bruinsma K., Phillips Sh., Le Th., Llaw Ch., Connolly DT., Behan D.P.The role of the GPR91 ligand succinate in hematopoiesis . J. Leukoc. Boil. 2009. 85. p. 229-243.
CrossRef
PubMed
- He W., Miao F.J., Lin D.C. Citric acid cycle intermediates as ligands for orphan-G-protein-coupled receptors . Nature. 2004. 429. p. 188-193.
CrossRef
PubMed
- Hems, D. A., Brosnan, J. T. Effects of ischaemia on content of metabolites in rat liver and kidney in vivo . Biochem. J. 1970. 120. p. 105-111.
CrossRef
PubMed PubMedCentral
- Hewitson K. S., Lienard B. M., McDonough M. A., Clifton I. J., Butler D., Soares A. S., Oldham N.J., McNeill L.A., Schofield C.J. Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarbonic acid cycle intermediates . J. Biol Chem. 2007. 282(5). p. 3293-3230.
CrossRef
PubMed
- Hochachka P. W., Dressendorfer R. H. Succinate accumulation in man during exercise . Eur. J. Appl. Physiol. Occup. Physiol. 1976. 35. p. 235-242.
CrossRef
PubMed
- Hochachka P.W., Somero G.N. Biochemical Adaptation Mechanism and Process in Physiological Evolution . New York. Oxford University Press, 2001.
- Hohl C., Oestreich R., Rösen P., Wiesner R., Grieshaber M. Evidence for succinate production by reduction of fumarate during hypoxia inisolat adult rat heart cells . Arch Biochem, and Biophys. 1987. 59(2). P. 527-535.
CrossRef
- Kermorvant-Duchemin E., Sapieha P., Sirinyan M., Beauchamp M., Checchin D., Hardy P., Sennlaub F., Lachapelle P., Chemtob S. Understanding ischemic retinopathies. emerging concepts from oxygen-induced retinopathy . Doc Ophthalmol. 2010. 120. P. 51-60.
CrossRef
PubMed
- Kim J-W., Tchernyshyov I., Semenza G. L., Dang C. V. HIF-1-mediated expression of pyruvate dehydrogenase kinase. A metabolic switch required for cellular adaptation to hypoxia . Cell Metabolism. 2006. 3(3). P. 150-151.
CrossRef
PubMed
- King A., Selak M. A., Gottlieb E. Succinate dehydrogenase and fumarate hydratase. linking mitochondrial dysfunction and cancer . Oncogene. 2006. 25(34). P. 4675-4682.
CrossRef
PubMed
- Kolvunen P., Hirsila M., Remes A.M., Hassinen I.E., Kivirikko K.I., Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydrolases by citric acid cycle intermediates. possible links between cell metabolism and stabilization of HIF. J Biol Chem. 2007. 82(7). P. 4524-4532.
CrossRef
PubMed
- Komaromy-Hiller G., Sundquist P.D., Jacobsen L.J., Nuttall K.L. Serum succinate by capillary zone electrophoresis. marker candidate for hypoxia . Ann Clin Lab Sci. 1997. 27(2). P. 163-168.
PubMed
- Kondrashova M. N. The formation and utilization of succinate in mitochondria as a control mechanism of energization and energy state of tissue. In: Chance B. (Ed.). Biological and Biochemical Oscillators . New York: Acad. Press. 1993. P. 373-397.
- Kondrashova M.N., Doliba N.M. Polarografiphic observation of substrate-level phosphorylation and its stimulation by acetylcholine . FEBS Lett. 1989. 243. P. 153-155.
CrossRef
- Kunz W.S. Kudin A.P., Vielhaber S., Blumke I. Mitochondrial complex I deficiency in epileptic focus of patients with temporal lode epilepsy . Ann. Neurol. 2000. 48. P. 766-773.
CrossRef
- Kushnir, M. M., Komaromy-Hiller, G., Shushan, B., Urry, F. M., Roberts, W. L. Analysis of dicarboxylic acids by tandem mass spectrometry.High-throughput quantitative measurement of methylmalonic acid in serum, plasma, and urine . Clin. Chem. 2001. . P. 1993-2002.
PubMed
- Kusnetsov A.V., Schneeberger S., Seiler R., Brandacher G., Mark W., Steurer W., Sacs V., Usson Y, Margreiter R, Gnaiger E. Mitochondria. defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion . Amer. J. Heart. Circ. Physiol. 2004. 286. P. H1633-H1641.
CrossRef
PubMed
- Lukyanova L.D. Limiting steps of energy metabolism in brain in hypoxia . Neurochem. Intern. 1988. 13(I). P. 146-147.
- Lukyanova L.D. Molecular, metabolic and functional mechanisms of individual resistance to hypoxia. In. Sharma B.K., Takeda N., et al. (eds), Adaptation Biology and Medicine, Narosa Publishing House New Dehli, India. 1997. I. P. 261-272.
PubMed
- Lukyanova L. D. Cellular mechanism responsible for beneficial effects of hypoxic therapy. In. Adaptation Biology and Medicine. Moraveč, et al. (eds), Narosa Publishing House New Dehli, India. 2002. 3. P. 290-303.
- Lukyanova L.D. Novel approaches to the understanding of molecular mechanisms of adaptation. In. Adaptation Biology and Medicine. Hargens A., Takeda N., Singal P.K. (eds). 2004.4. P. 11-22.
PubMed
- Lukyanova L. D., A. M. Dudchenko. Regulatory role of the adenylate pool in the formation of hepatocyte resistance to hypoxia. In. K.B. Pandolf, N. Takeda, P.K. Singal (eds.), Adaptation Biology and Medicine. Narosa Publishing House New Dehli, India. 1999. 2. P. 139-150.
PubMedCentral
- Lukyanova L.D., Dudchenko A.V., Tsybina T.A., Germanova E.L., Tkatchuk E.N. Mitochondrial signaling in adaptation to hypoxia. In. Adaptation Biology and Medicine. Eds Lukyanova L., Singal P., Takeda N. New Dehli, India. Narosa Publ. House. 2008. 5. P. 5-15.
- Lukyanova L.D., Dudchenko A.M., Germanova E.L.,Tsybina T.A.,Kapaladse R.A., Ehrenbourg I.V., Tkatchouk E.N. Mitochondria signaling in formation of body resistance to hypoxia. Intermitten Hypoxia. from molecular mechanisms to clinical applications . Eds. Lei Xi, Serebrovskaya T. Nova Science Publishers, USA Chapter. 2009. 20. P. 423-450.
- Lukyanova L. D., Germanova E. L, Kirova Yu. I. The Signal Function of Succinate and Free Radicals in Mechanisms of Preconditioning and Long-termAdaptation to Hypoxia. In. Adaptation Biology and Medicine. Cell Adaptations and Challenges. Wang P., Kuo C.-H., Takeda N. and Singal P.K. (eds). 2011. 6. P. 251-277.
PubMedCentral
- MacDonald M.J., Fahien L.A., Brown L.J., Hasan N.M., Buss J.D., Kendrick M. A. Perspective. emerging evidence for signaling roles of mitochondrial anaplerotic products insulin secretion . Amer. J. Physiol. Endocrinol. Metab. 2005. 288. P. E1-E15.
CrossRef
PubMed
- Maklashinas E., Sher E., Zhou H-Z, Gray M. Effect of anoxia. reperfusion on the reversible active. de-active transition of complex I in rat hear . BBA, Bioenergetics. 2002. 1556(1). P. 6-12.
CrossRef
- Mela L., Goodwin C.W., Miller L.D. In vivo control of mitochondrial enzyme concentrations and activity by oxygen . Amer. J. Physiol. 1976. 231. P. 1811-1816.
CrossRef
PubMed
- Michiels K. Physiological and pathological responses to hypoxia . Amer. J. Pathology. 2004. 164. P. 1875-1882.
CrossRef
- Murphy E. Primary and Secondary Signaling Pathways in Early Preconditioning That Converge on the Mitochondria to Produce Cardioprotection . Circulat. Res. 2004. 94. P. 7-16.
CrossRef
PubMed
- Napolitano M., Centoze D., Gubellini P., Rossi S., Spiezia S., Bernardi G., Gulino F., Calabresi P. Inhibition of mitochondrial complex II alters strial expression of genes involved in glutamatergi signaling. possible implications for Huginton's diease . Neurobiol. Dis. 2004. 15(2). P. 407-414.
CrossRef
PubMed
- Nichols D.G., Samantha L.B. Mitochondria and Neuronal Survival . Physiol Rev. 2000. 80(1). P. 315-360.
CrossRef
PubMed
- Nishimura G, Proske RJm Doyama H, Higuchi M. Regulation of apoptosis by respiratory substrates . FEBS Letters. 2001. 505, N 3. P. 399-404.
CrossRef
- Nowak G., Clifton G. L, Bakajsova D. Succinate ameliorates energy deficits and prevents dysfunction of complex I in injured renal proximal tubular cells . J. Pharmacol. Exp Therap. 2008. 324(3). P. 1155-1162.
CrossRef
PubMed PubMedCentral
- Paddenberg R., Ishak B., Goldenberg A., Faulhammer P., Rose F., Weissmann N., Braun Dullaeus R., Kummer W. Essential role of complex II of the respiraitory chain in hypoxia-induced ROS generation in pulmonary vasculature . Amer. J. Physiol. Lung. Cell Mol. Physiol. 2003. 284. P. 1710-1719.
CrossRef
PubMed
- Peers Ch., Kemp P.J. Acute oxygen sensing. diverse but convergent mechanisms in airway and arterial chemoreceptors . Respirat. Res. 2001. 2(3). P. 145-149.
CrossRef
PubMed PubMedCentral
- Peter M.T. Deen and Joris H. Robben Succinate Receptors in the Kidney . J. Amer. Soc Nephrol. 2011. 22. P. 1416-1422,
CrossRef
PubMed
- Pitkänen S., B.H. Robinson. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase . J. Clin. Invest. 1996. 98. P. 345-351.
CrossRef
PubMed PubMedCentral
- Porwol T., Eheleben W., Brand V., Acker H. Tissue oxygen sensor function of NADPH oxidase isoforms, an unusiual cytochrome aa3 and reactive oxygen species . Respirat. Physiol. 2001. 128(3). P. 331-348.
CrossRef
- Regard J.B., Sato I.T., Coughlin S.R. Anatomical profiling of G protein-coupled receptor expression . Cell. 2008. 135. P. 561-571.
CrossRef
PubMed PubMedCentral
- Robinson B.H. Human Comlex I deficiency. Clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect . Biochem. Biophys. Acta. 1998. 1364. P. 271-286.
CrossRef
- Rouslin W., Millard R.W. Canine myocardial ischemia. defect in mitochondrial electron transfer complex I. J. Mol. Cell Cardiol. 1980. 12. P. 639-645.
CrossRef
- Rubic T., Lametschwandtner G., Hinteregger S., Kund J. (Triggering the succinate receptor GPR91 on dendritic cells enhances immunity . Nat Immunol. 2008. 9. P. 1261-1269.
CrossRef
PubMed
- Sadek H.A., Sweda P.A., Sweda.L.I. Modulation of mitochondrial complex I activity by reversible Ca2+ and NADH mediated superoxide anion dependent inhibition . Biochemistry. 2004. 43. P. 8494-8502.
CrossRef
PubMed
- Sadagopan N., Roberds S.L., Major T., Preston G.M., YuY., Tones M.A. Circulating succinate is elevated in rodent models of hypertension and metabolic disease . Amer. J. Hypertens. 2007. 20. P. 1209-1215.
PubMed
- Sanborn T., Gavin,W., Berkowitz S., Perille T., Lesch M. Augmented conversion of aspartate and glutamate to succinate during anoxia in rabbit heart . Amer. J. Physiol. 1979. 237. P. H535-H541.
PubMed
- Sapieha P., Sirinyan M., Hamel D., Zaniolo K, Joya J.-S., Cho J.-H., Honoré J.-C., Kermorvant-Duchemin E., Varma D. R., Tremblay S., Leduc M., Rihakova L., Hardy P., Klein W. H., Mu X., Mamer O., Lachapelle P., Di Polo A., Beauséjour C., Andelfinger G., Mitchell G., Sennlaub F., Chemtob S., The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis . Nat. Med. 2008. 14. P. 1067-1076.
CrossRef
PubMed
- Sardanelli A.M., Papa S. Phosphorylationof an 18 kDa subunit of bovine Heart complex I by camp dependent kinase . FEBS Lett. 1996. 379. P. 299-301.
CrossRef
- Sekine T., Miyazaki H., Endou H. Molekular physiology of renal organic anion transporters . Amer. J. Renal Physiol. 2006. 290. P. F251-F261.
CrossRef
PubMed
- Selak M.A, Armour S.M., McKenzie E. D. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-prolyl hydroxylase . Cancer Cell. 2005. 7. P. 77-85.
CrossRef
PubMed
- Semenza G.L. Signal transduction to hypoxia-inducible factor 1 . Bioch. Pharmacol. 2002. 64. P. 993-998.
CrossRef
- Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1 . Biochem J. 2007. 405(1). P. 1-9.
CrossRef
PubMed
- Semenza G.L. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis . Blood. 2009. 114(10). P. 2015-2019.
CrossRef
PubMed
- Semenza G.L., Wang G. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation . Mol.Cell Biol. 1992. 12. P. 5447-5454.
CrossRef
PubMed PubMedCentral
- Stroka D.M., Burkhardt T., Desballerts I. HIF-1 is expressed in normoxia tissue and displays an organ-specific regulation under systemic hypoxia . FASEB J. 2001. 15. P. 2445-2453.
CrossRef
- Taegmeyer H. Metabolic responses to cardiac hypoxia. increased production of succinate by rabbit papillary muscles . Circ Res. 1978. 43. P. 808-815.
CrossRef
- Toma I., Kang J.J., Sipos A., Vargas S., Bansal E., Hanner F., Meer E., Peti-Peterdi J. Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney . J. Clin. Invest. 2008. 118. P. 2526-2534.
CrossRef
- Wang G., Semenza G.L. Characterization of hypoxia-inducible factor I and regulation of DNA binding activity by hypoxia . J. Biol Chem; 1993. 268. P. 21513-21518.
PubMed
- Weinberg J.M., Venkatachalm M.A, Nancy F. Anaerobic and aerobic pathways for salvage of proximal tubules from hypoxia-induced mitochondrial injury . Amer. J. Renal. Physiol. 2000. 279. P. F927-F943.
- Weinberg J.M.,Venkatachalm M.A., Nancy F. Mitochondrial disfunction during hypoxia. reoxigenation and its correction by anaerobic metabolism of citric acid cycle intermediates . PNAS. 2000. 97(3). P. 2826-2831.
CrossRef
PubMed
- Vargas S.L., Toma I., Kang J.J., Meer E.J., Peti-Peterdi J. Activation of the succinate receptor GPR91 in macula densa cells causes renin release . J. Amer. Soc. Nephrol. 2009. 20. P. 1002-1011.
CrossRef
PubMed PubMedCentral
- Vaux E.C., Metzen E., Yeates K.M., Ratcliffe P.J. Regulation of hypoxia-inducible factor is reserved in the absence of a functioning respiratory chain . Blood. 2001. 98. P. 296-302.
CrossRef
PubMed
- Voos W., Rotgers K. Molecular chaperones as essential mediators of mitochondrial biogenesis . BBA. 2002. 1592. P. 51-62.
CrossRef
- Zoccarato F., Cavallini L., Bortolami S., Alexandre A. Succinate modulation of H2O2 release at NADH.ubiquinone oxidoreductase (Complex I) in brain mitochondria . Biochem J. 2007. 406(1). P.125-129.
CrossRef
PubMed PubMedCentral
- Zhu H., Bunn F. Oxygen sensing and signaling. impact on regulation of physiologically important genes . Respir Physiol. 1999. 2. P. 239-247.
CrossRef
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