Mechanisms and triggers of adaptation to hypoxia
Andrey V. Lyubimov , Dmitriy V. Cherkashin , Semen V. Efimov , Andrey E. Alanichev , Valeriy S. Ivanov , Gennadiy G. Kutelev
Reviews on Clinical Pharmacology and Drug Therapy ›› 2021, Vol. 19 ›› Issue (3) : 269 -280.
Mechanisms and triggers of adaptation to hypoxia
It is believed that hypoxia-induced factor (HIF1) is the key mediator of oxygen metabolism. It was first identified as a transcription factor activated in cells and tissues by lowering the partial pressure of oxygen (O2). The HIF1 activator spectrum includes both external factors – hypoxia, psycho-emotional stress and in ternal factors and varies from hormones to iron chelators. This review is dedicated to the molecular mechanisms of HIF1 activation, some of its natural activators HIF1, the potential for which is due to the low level of toxicity and the reduced likelihood of undesirable side effects. In turn, this opens up new options to treat diseases associated with local and general ischemia and hypoxia, the possibilities of their prophylactic use for researchers and clinicians in order to reduce the degree of damage in the event of an unforeseen condition of acute injurious to organs and tissues by hypoxia and reperfusion after it.
hypoxia / preconditioning / activation / ischemia / hypoxia-induced factor
| [1] |
Huang LE, Bunn HF. Hypoxia-inducible factor and its biomedical relevance. J Biol Chem. 2003;278(22):19575–19578. DOI: 10.1074/jbc.R200030200 |
| [2] |
Huang L.E., Bunn H.F. Hypoxia-inducible factor and its biomedical relevance//J Biol Chem. 2003. Vol. 278. No. 22. P. 19575–19578. DOI: 10.1074/jbc.R200030200 |
| [3] |
Poellinger L, Johnson RS. HIF1 and hypoxic response: the plot thickens. Curr Opin Genet Dev. 2004;14(1):81–85. DOI: 10.1016/j.gde.2003.12.006 |
| [4] |
Poellinger L., Johnson R.S. HIF1 and hypoxic response: the plot thickens//Curr Opin Genet Dev. 2004. Vol. 14. No. 1. P. 81–85. DOI: 10.1016/j.gde.2003.12.006 |
| [5] |
Semenza GL. Targeting HIF1 for cancer therapy. Nat Rev Cancer. 2003;3:721–732. DOI: 10.1038/nrc1187 |
| [6] |
Semenza G.L. Targeting HIF1 for cancer therapy//Nat Rev Cancer. 2003. Vol. 3. P. 721–732. DOI: 10.1038/nrc1187 |
| [7] |
Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA. 1995;92(12):5510–5514. DOI: 10.1073/pnas.92.12.5510 |
| [8] |
Wang G.L., Jiang B.H., Rue E.A., Semenza G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension//Proc Natl Acad Sci USA. 1995. Vol. 92. No. 12. P. 5510–5514. DOI: 10.1073/pnas.92.12.5510 |
| [9] |
Dames SA, Martinez-Yamout M, De Guzman RN, et al. Structural basis for HIF1α/CBP recognition in the cellular hypoxic response. Proc Natl Acad Sci USA. 2002;99(8):5271–5276. DOI: 10.1073/pnas.082121399 |
| [10] |
Dames S.A., Martinez-Yamout M., De Guzman R.N., et al. Structural basis for HIF1α/CBP recognition in the cellular hypoxic response//Proc Natl Acad Sci USA. 2002. Vol. 99. No. 8. P. 5271–5276. DOI: 10.1073/pnas.082121399 |
| [11] |
Freedman SJ, Sun ZY, Poy F, et al. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1α. Proc Natl Acad Sci USA. 2002;99(8):5367–5372. DOI: 10.1073/pnas.082117899 |
| [12] |
Freedman S.J., Sun Z.Y., Poy F., et al. Structural basis for recruitment of CBP / p300 by hypoxia-inducible factor-1α//Proc Natl Acad Sci USA. 2002. Vol. 99. No. 8. P. 5367–5372. DOI: 10.1073/pnas.082117899 |
| [13] |
Hewitson KS, McNeill LA, Riordan MV, et al. Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J Biol Chem. 2002;277(29):26351–26355. DOI: 10.1074/jbc.C200273200 |
| [14] |
Hewitson K.S., McNeill L.A., Riordan M.V., et al. Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family//J Biol Chem. 2002. Vol. 277. No. 29. P. 26351–26355. DOI: 10.1074/jbc.C200273200 |
| [15] |
Lando D, Peet DJ, Gorman JJ, et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002;16:1466–1471. DOI: 10.1101/gad.991402 |
| [16] |
Lando D., Peet D.J., Gorman J.J., et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor//Genes Dev. 2002. Vol. 16. P. 1466–1471. DOI: 10.1101/gad.991402 |
| [17] |
Lando D, Peet DJ, Whelan DA, et al. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science. 2002;295(5556):858–861. DOI: 10.1126/science.1068592 |
| [18] |
Lando D., Peet D.J., Whelan D.A., et al. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch//Science. 2002. Vol. 295. No. 5556. P. 858–861. DOI: 10.1126/science.1068592 |
| [19] |
Lin SC, Liao WL, Lee JC, Tsai SJ. Hypoxia-regulated gene network in drug resistance and cancer progression. Exp Biol Med (Maywood). 2014;239(7):779–792. DOI: 10.1177/1535370214532755 |
| [20] |
Lin S.C., Liao W.L., Lee J.C., Tsai S.J. Hypoxia-regulated gene network in drug resistance and cancer progression//Exp Biol Med (Maywood). 2014. Vol. 239. No. 7. P. 779–792. DOI: 10.1177/1535370214532755 |
| [21] |
Mahon PC, Hirota K, Semenza GL. FIH-1: a novel protein that interacts with HIF1α and VHL to mediate repression of HIF1 transcriptional activity. Genes Dev. 2001;15:2675–2686. DOI: 10.1101/gad.924501 |
| [22] |
Mahon P.C., Hirota K., Semenza G.L. FIH-1: a novel protein that interacts with HIF1α and VHL to mediate repression of HIF1 transcriptional activity//Genes Dev. 2001. Vol. 15. P. 2675–2686. DOI: 10.1101/gad.924501 |
| [23] |
McNeill LA, Hewitson KS, Claridge TD, et al. Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the beta-carbon of asparagine-803. Biochem J. 2002;367(3):571–575. DOI: 10.1042/BJ20021162 |
| [24] |
McNeill L.A., Hewitson K.S., Claridge T.D., et al. Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the beta-carbon of asparagine-803//Biochem J. 2002. Vol. 367. No. 3. P. 571–575. DOI: 10.1042/BJ20021162 |
| [25] |
Singh D, Arora R, Kaur P, et al. Overexpression of hypoxia-inducible factor and metabolic pathways: possible targets of cancer. Cell Biosci. 2017;7:62. DOI: 10.1186/s13578-017-0190-2 |
| [26] |
Singh D., Arora R., Kaur P., et al. Overexpression of hypoxia-inducible factor and metabolic pathways: possible targets of cancer//Cell Biosci. 2017. Vol. 7. P. 62. DOI: 10.1186/s13578-017-0190-2 |
| [27] |
Jin P, Kang J, Lee MK, Park JW. Ferritin heavy chain controls the HIF-driven hypoxic response by activating the asparaginylhydroxylase FIH. Biochem Biophys Res Commun. 2018;499(3):475–481. DOI: 10.1016/j.bbrc.2018.03.173 |
| [28] |
Jin P., Kang J., Lee M.K., Park J.W. Ferritin heavy chain controls the HIF-driven hypoxic response by activating the asparaginylhydroxylase FIH//Biochem Biophys Res Commun. 2018. Vol. 499. No. 3. P. 475–481. DOI: 10.1016/j.bbrc.2018.03.173 |
| [29] |
Pugh CW. Modulation of the Hypoxic Response. Adv Exp Med Biol. 2016;903:259–271. DOI: 10.1007/978-1-4899-7678-9_18 |
| [30] |
Pugh C.W. Modulation of the Hypoxic Response//Adv Exp Med Biol. 2016. Vol. 903. P. 259–271. DOI: 10.1007/978-1-4899-7678-9_18 |
| [31] |
Wang V, Davis DA, Yarchoan R. Identification of functional hypoxia inducible factor response elements in the human lysyl oxidase gene promoter. Biochem Biophys Res Commun. 2017;490(2):480–485. DOI: 10.1016/j.bbrc.2017.06.066 |
| [32] |
Wang V., Davis D.A., Yarchoan R. Identification of functional hypoxia inducible factor response elements in the human lysyl oxidase gene promoter//Biochem Biophys Res Commun. 2017. Vol. 490. No. 2. P. 480–485. DOI: 10.1016/j.bbrc.2017.06.066 |
| [33] |
Brahimi-Horn C, Mazure N, Pouyssegur J. Signalling via the hypoxia-inducible factor-1α requires multiple posttranslational modifications. Cell Signal. 2005;17(1):1–9. DOI: 10.1016/j.cellsig.2004.04.010 |
| [34] |
Brahimi-Horn C., Mazure N., Pouyssegur J. Signalling via the hypoxia-inducible factor-1α requires multiple posttranslational modifications//Cell Signal. 2005. Vol. 17. No. 1. P. 1–9. DOI: 10.1016/j.cellsig.2004.04.010 |
| [35] |
Wang GL, Semenza GL. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood. 1993;82(12):3610–3615. DOI: 10.1182/blood.V82.12.3610.3610 |
| [36] |
Wang G.L., Semenza G.L. Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor-1 DNA-binding activity: implications for models of hypoxia signal transduction//Blood. 1993. Vol. 82. No. 12. P. 3610–3615. DOI: 10.1182/blood.V82.12.3610.3610 |
| [37] |
Li L, Yin X, Ma N, et al. Desferrioxamin regulates HIF1 alpha expression in neonatal rat brain after hypoxia-ischemia. Am J Transl Res. 2014;6(4):377–383. |
| [38] |
Li L., Yin X., Ma N., et al. Desferrioxamin regulates HIF1 alpha expression in neonatal rat brain after hypoxia-ischemia//Am J Transl Res. 2014. Vol. 6. No. 4. P. 377–383. |
| [39] |
AHFS Drug Information 2004. McEvoy, GK., editor. Bethesda: American Society of Health-System Pharmacists, Inc. American Hospital Formulary Service; 2004. P. 2870–2873. |
| [40] |
AHFS Drug Information 2004. McEvoy G.K., editor. Bethesda: American Society of Health-System Pharmacists. Inc. American Hospital Formulary Service, 2004. P. 2870–2873. |
| [41] |
Gobin J, Moore CH, Reeve JR Jr, et al. Iron acquisition by Mycobacterium tuberculosis: isolation and characterization of a family of iron-binding exochelins. Proc Natl Acad Sci USA. 1995;92(11):5189–5193. DOI: 10.1073/pnas.92.11.5189 |
| [42] |
Gobin J., Moore C.H., Reeve J.R. Jr., et al. Iron acquisition by Mycobacterium tuberculosis: isolation and characterization of a family of iron-binding exochelins//Proc Natl Acad Sci USA. 1995. Vol. 92. No. 11. P. 5189–5193. DOI: 10.1073/pnas.92.11.5189 |
| [43] |
Chong TW, Horwitz LD, Moore JW, et al. A mycobacterial iron chelator, desferri-exochelin, induces hypoxia-inducible factors 1 and 2, NIP3, and vascular endothelial growth factor in cancer cell lines. Cancer Res. 2002;62:6924–6927. |
| [44] |
Chong T.W., Horwitz L.D., Moore J.W., et al. A mycobacterial iron chelator, desferri-exochelin, induces hypoxia-inducible factors 1 and 2, NIP3, and vascular endothelial growth factor in cancer cell lines//Cancer Res. 2002. Vol. 62. P. 6924–6927. |
| [45] |
Shen T, Huang S. Repositioning the Old Fungicide Ciclopirox for New Medical Uses. Curr Pharm Des. 2016;22(28):4443–4450. DOI: 10.2174/1381612822666160530151209 |
| [46] |
Shen T., Huang S. Repositioning the Old Fungicide Ciclopirox for New Medical Uses//Curr Pharm Des. 2016. Vol. 22. No. 28. P. 4443–4450. DOI: 10.2174/1381612822666160530151209 |
| [47] |
Wanner RM, Spielmann P, Stroka DM, et al. Epolones induce erythropoietin expression via hypoxia-inducible factor-1α activation. Blood. 2000;96(4):1558–1565. DOI: 10.1182/blood.V96.4.1558 |
| [48] |
Wanner R.M., Spielmann P., Stroka D.M., et al. Epolones induce erythropoietin expression via hypoxia-inducible factor-1α activation//Blood. 2000. Vol. 96. No. 4. P. 1558–1565. DOI: 10.1182/blood.V96.4.1558 |
| [49] |
Linden T, Katschinski DM, Eckhardt K, et al. The antimycotic ciclopirox olamine induces HIF1α stability, VEGF expression, and angiogenesis. FASEB J. 2003;17(6):761–763. DOI: 10.1096/fj.02-0586fje |
| [50] |
Linden T., Katschinski D.M., Eckhardt K., et al. The antimycotic ciclopirox olamine induces HIF1α stability, VEGF expression, and angiogenesis//FASEB J. 2003. Vol. 17. No. 6. P. 761–763. DOI: 10.1096/fj.02-0586fje |
| [51] |
Schnitzer SE, Schmid T, Zhou J, et al. Inhibition of GSK3beta by indirubins restores HIF1alpha accumulation under prolonged periods of hypoxia / anoxia. FEBS Lett. 2005;579(2):529–533. DOI: 10.1016/j.febslet.2004.12.023 |
| [52] |
Schnitzer S.E., Schmid T., Zhou J., et al. Inhibition of GSK3beta by indirubins restores HIF1alpha accumulation under prolonged periods of hypoxia / anoxia//FEBS Lett. 2005. Vol. 579. No. 2. P. 529–533. DOI: 10.1016/j.febslet.2004.12.023 |
| [53] |
Cheng YC, Liou JP, Kuo CC, et al. MPT0B098, a novel microtubule inhibitor that destabilizes the hypoxia-inducible factor-1α mRNA through decreasing nuclear-cytoplasmic translocation of RNA-binding protein HuR. Mol Cancer Ther. 2013;12(7):1202–1212. DOI: 10.1158/1535-7163.MCT-12-0778 |
| [54] |
Cheng Y.C., Liou J.P., Kuo C.C., et al. MPT0B098, a novel microtubule inhibitor that destabilizes the hypoxia-inducible factor-1α mRNA through decreasing nuclear-cytoplasmic translocation of RNA-binding protein HuR//Mol Cancer Ther. 2013. Vol. 12. No. 7. P. 1202–1212. DOI: 10.1158/1535-7163.MCT-12-0778 |
| [55] |
Jung YJ, Isaacs JS, Lee S, et al. Microtubule disruption utilizes an NFκB-dependent pathway to stabilize HIF1α protein. J Biol Chem 2003;278(9):7445–7452. DOI: 10.1074/jbc.M209804200 |
| [56] |
Jung Y.J., Isaacs J.S., Lee S., et al. Microtubule disruption utilizes an NFκB-dependent pathway to stabilize HIF1α protei//J Biol Chem. 2003. Vol. 278. No. 9. P. 7445–7452. DOI: 10.1074/jbc.M209804200 |
| [57] |
Shen J, Zhang JH, Xiao H, et al. Mitochondria are transported along microtubules in membrane nanotubes to rescue distressed cardiomyocytes from apoptosis. Cell Death Dis. 2018;9(2):81. DOI: 10.1038/s41419-017-0145-x |
| [58] |
Shen J., Zhang J.H., Xiao H., et al. Mitochondria are transported along microtubules in membrane nanotubes to rescue distressed cardiomyocytes from apoptosis//Cell Death Dis. 2018. Vol. 9. No. 2. P. 81. DOI: 10.1038/s41419-017-0145-x |
| [59] |
Zhou X, Xu Z, Li A, et al. Double-sides sticking mechanism of vinblastine interacting with α, β-tubulin to get activity against cancer cells. J Biomol Struct Dyn. 2019;37(15):4080–4091. DOI: 10.1080/07391102.2018.1539412 |
| [60] |
Zhou X., Xu Z., Li A., et al. Double-sides sticking mechanism of vinblastine interacting with α, β-tubulin to get activity against cancer cells//J Biomol Struct Dyn. 2019. Vol. 37. No. 15. P. 4080–4091. DOI: 10.1080/07391102.2018.1539412 |
| [61] |
Guo C, Wang L, Jiang B, Shi D. Bromophenol curcumin analog BCA-5 exerts an antiangiogenic effect through the HIF1α/VEGF/Akt signaling pathway in human umbilical vein endothelial cells. Anticancer Drugs. 2018;29(10):965–974. DOI: 10.1097/CAD.0000000000000671 |
| [62] |
Guo C., Wang L., Jiang B., Shi D. Bromophenol curcumin analog BCA-5 exerts an antiangiogenic effect through the HIF1α/VEGF/Akt signaling pathway in human umbilical vein endothelial cells//Anticancer Drugs. 2018. Vol. 29. No. 10. P. 965–974. DOI: 10.1097/CAD.0000000000000671 |
| [63] |
Mabjeesh NJ, Willard MT, Harris WB, et al. Dibenzoylmethane, a natural dietary compound, induces HIF1α and increases expression of VEGF. Biochem Biophys Res Commun. 2003;303(1):279–286. DOI: 10.1016/s0006-291x(03)00336-x |
| [64] |
Mabjeesh N.J., Willard M.T., Harris W.B., et al. Dibenzoylmethane, a natural dietary compound, induces HIF1α and increases expression of VEGF//Biochem Biophys Res Commun. 2003. Vol. 303. No. 1. P. 279–286. DOI: 10.1016/s0006-291x(03)00336-x |
| [65] |
Wilson WJ, Poellinger L. The dietary flavonoid quercetin modulates HIF1α activity in endothelial cells. Biochem Biophys Res Commun. 2002;293(1):446–450. DOI: 10.1016/S0006-291X(02)00244-9 |
| [66] |
Wilson W.J., Poellinger L. The dietary flavonoid quercetin modulates HIF1α activity in endothelial cells//Biochem Biophys Res Commun. 2002. Vol. 293. No. 1. P. 446–450. DOI: 10.1016/S0006-291X(02)00244-9 |
| [67] |
Welford RW, Schlemminger I, McNeill LA, et al. The selectivity and inhibition of AlkB. J Biol Chem. 2003;278(12):10157–10161. DOI: 10.1074/jbc.M211058200 |
| [68] |
Welford R.W., Schlemminger I., McNeill L.A., et al. The selectivity and inhibition of AlkB//J Biol Chem. 2003. Vol. 278. No. 12. P. 10157–10161. DOI:10.1074/jbc.M211058200 |
| [69] |
Zhou YD, Kim YP, Li XC, et al Hypoxia-inducible factor-1 activation by (–)-epicatechin gallate: potential adverse effects of cancer chemoprevention with high-dose green tea extracts. J Nat Prod. 2004;67:2063–2069. DOI: 10.1021/np040140c |
| [70] |
Zhou Y.D., Kim Y.P., Li X.C., et al Hypoxia-inducible factor-1 activation by (–)-epicatechin gallate: potential adverse effects of cancer chemoprevention with high-dose green tea extracts//J Nat Prod. 2004. Vol. 67. P. 2063–2069. DOI: 10.1021/np040140c |
| [71] |
Hong J, Lu H, Meng X, et al. Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (–)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells. Cancer Res. 2002;62:7241–7246. |
| [72] |
Hong J., Lu H., Meng X., et al. Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (–)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells//Cancer Res. 2002. Vol. 62. P. 7241–7246. |
| [73] |
Demeule M, Michaud-Levesque J, Annabi B, et al. Green tea catechins as novel antitumor and antiangiogenic compounds. Curr Med Chem Anti-Canc Agents. 2002;2(4):441–463. DOI: 10.2174/1568011023353930 |
| [74] |
Demeule M., Michaud-Levesque J., Annabi B., et al. Green tea catechins as novel antitumor and antiangiogenic compounds//Curr Med Chem Anti-Canc Agents. 2002. Vol. 2. No. 4. P. 441–463. DOI: 10.2174/1568011023353930 |
| [75] |
Burnley-Hall N, Willis G, Davis J, et al. Nitrite-derived nitric oxide reduces hypoxia-inducible factor 1α-mediated extracellular vesicle production by endothelial cells. Nitric Oxide. 2017;63:1–12. DOI: 10.1016/j.niox.2016.12.005 |
| [76] |
Burnley-Hall N., Willis G., Davis J., et al. Nitrite-derived nitric oxide reduces hypoxia-inducible factor 1α-mediated extracellular vesicle production by endothelial cells//Nitric Oxide. 2017. Vol. 63. P. 1–12. DOI: 10.1016/j.niox.2016.12.005 |
| [77] |
Huang LE, Willmore WG, Gu J, et al. Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J Biol Chem. 1999;274(13):9038–9044. DOI: 10.1074/jbc.274.13.9038 |
| [78] |
Huang L.E., Willmore W.G., Gu J., et al. Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling//J Biol Chem. 1999. Vol. 274. No. 13. P. 9038–9044. DOI: 10.1074/jbc.274.13.9038 |
| [79] |
La Padula PH, Etchegoyen M, Czerniczyniec A, et al. Cardioprotection after acute exposure to simulated high altitude in rats. Role of nitric oxide. Nitric Oxide. 2018;73:52–59. DOI: 10.1016/j.niox.2017.12.007 |
| [80] |
La Padula P.H., Etchegoyen M., Czerniczyniec A., et al. Cardioprotection after acute exposure to simulated high altitude in rats. Role of nitric oxide//Nitric Oxide. 2018. Vol. 73. P. 52–59. DOI: 10.1016/j.niox.2017.12.007 |
| [81] |
Liu Y, Christou H, Morita T, et al. Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5’ enhancer. J Biol Chem. 1998;273(24):15257–15262. DOI: 10.1074/jbc.273.24.15257 |
| [82] |
Liu Y., Christou H., Morita T., et al. Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5’ enhancer//J Biol Chem. 1998. Vol. 273. No. 24. P. 15257–15262. DOI: 10.1074/jbc.273.24.15257 |
| [83] |
Sogawa K, Numayama-Tsuruta K, Ema M, et al. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci USA. 1998;95(13):7368–7373. DOI: 10.1073/pnas.95.13.7368 |
| [84] |
Sogawa K., Numayama-Tsuruta K., Ema M., et al. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia//Proc Natl Acad Sci USA. 1998. Vol. 95. No. 13. P. 7368–7373. DOI: 10.1073/pnas.95.13.7368 |
| [85] |
Vetrovoy O, Sarieva K, Galkina O, et al. Neuroprotective Mechanism of Hypoxic Post-conditioning Involves HIF1-Associated Regulation of the Pentose Phosphate Pathway in Rat Brain. Neurochem Res. 2019;44:1425–1436. DOI: 10.1007/s11064-018-2681-x |
| [86] |
Vetrovoy O., Sarieva K., Galkina O., et al. Neuroprotective Mechanism of Hypoxic Post-conditioning Involves HIF1-Associated Regulation of the Pentose Phosphate Pathway in Rat Brain//Neurochem Res. 2019. Vol. 44. P. 1425–1436. DOI: 10.1007/s11064-018-2681-x |
| [87] |
Kimura H, Weisz A, Kurashima Y, et al. 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. 2000;95(1):189–197. DOI: 10.1182/blood.V95.1.189 |
| [88] |
Kimura H., Weisz A., Kurashima Y., et al. 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. 2000. Vol. 95. No. 1. P. 189–97. DOI: 10.1182/blood.V95.1.189 |
| [89] |
Arandarcikaite O, Jokubka R, Borutaite V. Neuroprotective effects of nitric oxide donor NOC-18 against brain ischemia-induced mitochondrial damages: role of PKG and PKC. Neurosci Lett. 2015;586:65–70. DOI: 10.1016/j.neulet.2014.09.012 |
| [90] |
Arandarcikaite O., Jokubka R., Borutaite V. Neuroprotective effects of nitric oxide donor NOC-18 against brain ischemia-induced mitochondrial damages: role of PKG and PKC//Neurosci Lett. 2015. Vol. 586. P. 65–70. DOI: 10.1016/j.neulet.2014.09.012 |
| [91] |
Palmer LA, Gaston B, Johns RA. Normoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxides. Mol Pharmacol. 2000;58(6):1197–1203. DOI: 10.1124/mol.58.6.1197 |
| [92] |
Palmer L.A., Gaston B., Johns R.A. Normoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxides//Mol Pharmacol. 2000. Vol. 58. No. 6. P. 1197–203. DOI: 10.1124/mol.58.6.1197 |
| [93] |
Yang C, Hwang HH, Jeong S, et al. Inducing angiogenesis with the controlled release of nitric oxide from biodegradable and biocompatible copolymeric nanoparticles. Int J Nanomedicine. 2018;13:6517–6530. DOI: 10.2147/IJN.S174989 |
| [94] |
Yang C., Hwang H.H., Jeong S., et al. Inducing angiogenesis with the controlled release of nitric oxide from biodegradable and biocompatible copolymeric nanoparticles//Int J Nanomedicine. 2018. Vol. 13. P. 6517–6530. DOI: 10.2147/IJN.S174989 |
| [95] |
Sumbayev VV, Budde A, Zhou J, Brune B. HIF1α protein as a target for S-nitrosation. FEBS Lett. 2003;535(1–3):106–112. DOI: 10.1016/s0014-5793(02)03887-5 |
| [96] |
Sumbayev V.V., Budde A., Zhou J., Brune B. HIF1α protein as a target for S-nitrosation//FEBS Lett. 2003. Vol. 535. No. 1–3. P. 106–112. DOI: 10.1016/s0014-5793(02)03887-5 |
| [97] |
Yasinska IM, Sumbayev VV. S-nitrosation of Cys-800 of HIF1α protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett. 2003;549(1–3):105–109. DOI: 10.1016/s0014-5793(03)00807-x |
| [98] |
Yasinska I.M., Sumbayev V.V. S-nitrosation of Cys-800 of HIF1α protein activates its interaction with p300 and stimulates its transcriptional activity//FEBS Lett. 2003. Vol. 549. No. 1–3. P. 105–109. DOI: 10.1016/s0014-5793(03)00807-x |
| [99] |
Frise MC, Cheng HY, Nickol AH, et al. Clinical iron deficiency disturbs normal human responses to hypoxia. J Clin Invest. 2016;126(6):2139–2150. DOI: 10.1172/JCI85715 |
| [100] |
Frise M.C., Cheng H.Y., Nickol A.H., et al. Clinical iron deficiency disturbs normal human responses to hypoxia//J Clin Invest. 2016. Vol. 126. No. 6. P. 2139–2150. DOI: 10.1172/JCI85715 |
| [101] |
Shah YM, Xie L. Hypoxia-inducible factors link iron homeostasis and erythropoiesis. Gastroenterology. 2014;146(3):630–642. DOI: 10.1053/j.gastro.2013.12.031 |
| [102] |
Shah Y.M., Xie L. Hypoxia-inducible factors link iron homeostasis and erythropoiesis//Gastroenterology. 2014. Vol. 146. No. 3. P. 630–642. DOI: 10.1053/j.gastro.2013.12.031 |
| [103] |
Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol. 2004;5:343–354. DOI: 10.1038/nrm1366 |
| [104] |
Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases//Nat Rev Mol Cell Biol. 2004. Vol. 5. P. 343–354. DOI: 10.1038/nrm1366 |
| [105] |
Thomas DD, Espey MG, Ridnour LA, et al. Hypoxic inducible factor 1α, extracellular signal-regulated kinase, and p53 are regulated by distinct threshold concentrations of nitric oxide. Proc Natl Acad Sci USA. 2004;101(24):8894–8899. DOI: 10.1073/pnas.0400453101 |
| [106] |
Thomas D.D., Espey M.G., Ridnour L.A., et al. Hypoxic inducible factor 1α, extracellular signal-regulated kinase, and p53 are regulated by distinct threshold concentrations of nitric oxide//Proc Natl Acad Sci USA. 2004. Vol. 101. No. 24. P. 8894–8899. DOI: 10.1073/pnas.0400453101 |
| [107] |
Mukundan H, Kanagy NL, Resta TC. 17-β estradiol attenuates hypoxic induction of HIF1α and erythropoietin in Hep3B cells. J Cardiovasc Pharmacol. 2004;44(1):93–100. DOI: 10.1097/00005344-200407000-00013 |
| [108] |
Mukundan H., Kanagy N.L., Resta T.C. 17-β estradiol attenuates hypoxic induction of HIF1α and erythropoietin in Hep3B cells//J Cardiovasc Pharmacol. 2004. Vol. 44. No. 1. P. 93–100. DOI: 10.1097/00005344-200407000-00013 |
| [109] |
Lu H, Forbes RA, Verma A. Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem. 2002;277(26):23111–23115. DOI: 10.1074/jbc.M202487200 |
| [110] |
Lu H., Forbes R.A., Verma A. Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis//J Biol Chem. 2002. Vol. 277. No. 26. P. 23111–23115. DOI: 10.1074/jbc.M202487200 |
| [111] |
Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA. 1993;90(9):4304–4308. DOI: 10.1073/pnas.90.9.4304 |
| [112] |
Wang G.L., Semenza G.L. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia//Proc Natl Acad Sci USA. 1993. Vol. 90. No. 9. P. 4304–4308. DOI: 10.1073/pnas.90.9.4304 |
| [113] |
Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270(3):1230–1237. DOI: 10.1074/jbc.270.3.1230 |
| [114] |
Wang G.L., Semenza G.L. Purification and characterization of hypoxia-inducible factor 1//J Biol Chem. 1995. Vol. 270. No. 3. P. 1230–1237. DOI: 10.1074/jbc.270.3.1230 |
| [115] |
Muñoz-Sánchez J, Chánez-Cárdenas ME. The use of cobalt chloride as a chemical hypoxia model. J Appl Toxicol. 2018;39(4):556–570. DOI: 10.1002/jat.3749 |
| [116] |
Muñoz-Sánchez J., Chánez-Cárdenas M.E. The use of cobalt chloride as a chemical hypoxia model//J Appl Toxicol. 2018. Vol. 39. No. 4. P. 556–570. DOI: 10.1002/jat.3749 |
| [117] |
Luczak MW, Zhitkovich A. Nickel-induced HIF1α promotes growth arrest and senescence in normal human cells but lacks toxic effects in transformed cells. Toxicol Appl Pharmacol. 2017;331:94–100. DOI: 10.1016/j.taap.2017.05.029 |
| [118] |
Luczak M.W., Zhitkovich A. Nickel-induced HIF1α promotes growth arrest and senescence in normal human cells but lacks toxic effects in transformed cells//Toxicol Appl Pharmacol. 2017. Vol. 331. P. 94–100. DOI: 10.1016/j.taap.2017.05.029 |
| [119] |
Salnikow K, An WG, Melillo G, et al. Nickel-induced transformation shifts the balance between HIF1 and p53 transcription factors. Carcinogenesis. 1999;20(9):1819–1823. DOI: 10.1093/carcin/20.9.1819 |
| [120] |
Salnikow K., An W.G., Melillo G., et al. Nickel-induced transformation shifts the balance between HIF1 and p53 transcription factors//Carcinogenesis. 1999. Vol. 20. No. 9. P. 1819–1823. DOI: 10.1093/carcin/20.9.1819 |
| [121] |
Salnikow K, Blagosklonny MV, Ryan H, et al. Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Res. 2000;60:38–41. |
| [122] |
Salnikow K., Blagosklonny M.V., Ryan H., et al. Carcinogenic nickel induces genes involved with hypoxic stress//Cancer Res. 2000. Vol. 60. P. 38–41. |
| [123] |
Kim D, Dai J, Park YH, et al. Activation of Epidermal Growth Factor Receptor/p38/Hypoxia-inducible Factor-1α Is Pivotal for Angiogenesis and Tumorigenesis of Malignantly Transformed Cells Induced by Hexavalent Chromium. J Biol Chem. 2016;291(31):16271–16281. DOI: 10.1074/jbc.M116.715797 |
| [124] |
Kim D., Dai J., Park Y.H., et al. Activation of Epidermal Growth Factor Receptor/p38/Hypoxia-inducible Factor-1α Is Pivotal for Angiogenesis and Tumorigenesis of Malignantly Transformed Cells Induced by Hexavalent Chromium//J Biol Chem. 2016. Vol. 291. No. 31. P. 16271–16281. DOI: 10.1074/jbc.M116.715797 |
| [125] |
Gao N, Jiang BH, Leonard SS, et al. p38 Signaling-mediated hypoxia-inducible factor 1α and vascular endothelial growth factor induction by Cr(VI) in DU145 human prostate carcinoma cells. J Biol Chem. 2002;277(47):45041–45048. DOI: 10.1074/jbc.M202775200 |
| [126] |
Gao N., Jiang B.H., Leonard S.S., et al. p38 Signaling-mediated hypoxia-inducible factor 1α and vascular endothelial growth factor induction by Cr(VI) in DU145 human prostate carcinoma cells//J Biol Chem. 2002. Vol. 277. No. 47. P. 45041–45048. DOI: 10.1074/jbc.M202775200 |
| [127] |
Agani F, Semenza GL. Mersalyl is a novel inducer of vascular endothelial growth factor gene expression and hypoxia-inducible factor 1 activity. Mol Pharmacol. 1998;54(5):749–754. DOI: 10.1124/mol.54.5.749 |
| [128] |
Agani F., Semenza G.L. Mersalyl is a novel inducer of vascular endothelial growth factor gene expression and hypoxia-inducible factor 1 activity//Mol Pharmacol. 1998. Vol. 54. No. 5. P. 749–754. DOI: 10.1124/mol.54.5.749 |
| [129] |
Salnikow K, Donald SP, Bruick RK, et al. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem. 2004;279(39):40337–40344. DOI: 10.1074/jbc.M403057200 |
| [130] |
Salnikow K., Donald S.P., Bruick R.K., et al. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress//J Biol Chem. 2004. Vol. 279. No. 39. P. 40337–40344. DOI: 10.1074/jbc.M403057200 |
| [131] |
Wu Z, Zhang W, Kang YJ. Copper affects the binding of HIF1α to the critical motifs of its target genes. Metallomics. 2019;11(2):429–438. DOI: 10.1039/c8mt00280k |
| [132] |
Wu Z., Zhang W., Kang Y.J. Copper affects the binding of HIF1α to the critical motifs of its target genes//Metallomics. 2019. Vol. 11. No. 2. P. 429–438. DOI: 10.1039/c8mt00280k |
| [133] |
Zelzer E, Levy Y, Kahana C, et al. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF1α/ARNT. EMBO J. 1998;17(17):5085–5094. DOI: 10.1093/emboj/17.17.5085 |
| [134] |
Zelzer E., Levy Y., Kahana C., et al. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF1α/ARNT//EMBO J. 1998. Vol. 17. No. 17. P. 5085–5094. DOI: 10.1093/emboj/17.17.5085 |
| [135] |
Feldser D, Agani F, Iyer NV, et al. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res. 1999;59:3915–3918. |
| [136] |
Feldser D., Agani F., Iyer N.V., et al. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2//Cancer Res. 1999. Vol. 59. P. 3915–3918. |
| [137] |
Cherkashin DV, Lyubimov AV. The molecular marker of the preconditioning phenomenon HIF1α is a new pathway for early detection of visceral hypoxic conditions. Therapeutic archive. 2020;92(4):121–126. (In Russ.) DOI: 10.26442/00403660.2020.04.000473 |
| [138] |
Черкашин Д.В., Любимов А.В. HIF1α как молекулярный маркер феномена прекондиционирования ранней висцеральной гипоксемии//Терапевтический архив. 2020. Т. 92, № 4. С. 121–126. DOI: 10.26442/00403660.2020.04.000473 |
| [139] |
Lyubimov AV, Ivanov AO, Bezkishkii EN, et al. Assessment of the effect of long-term continuous stay in the artificial hypoxic gas-air environment at normal atmospheric pressure on the functional state of the cardiovascular system. Reviews on Clinical Pharmacology and Drug Therapy. 2018;16(3):47–53. (In Russ.) DOI: 10.17816/RCF16347-53 |
| [140] |
Любимов А.В., Иванов А.О., Безкишкий Э.Н., и др. Оценка влияния длительного непрерывного пребывания в искусственной гипоксической газовоздушной среде при нормальном атмосферном давлении на функциональное состояние сердечно-сосудистой системы человека//Обзоры по клинической фармакологии и лекарственной терапии. 2018. Т. 16, № 3. С. 47–53. DOI: 10.17816/RCF16347-53 |
| [141] |
Mabjeesh NJ, Post DE, Willard MT, et al. Geldanamycin induces degradation of hypoxia-inducible factor 1α protein via the proteosome pathway in prostate cancer cells. Cancer Res. 2002;62:2478–2482. |
| [142] |
Mabjeesh N.J., Post D.E., Willard M.T., et al. Geldanamycin induces degradation of hypoxia-inducible factor 1α protein via the proteosome pathway in prostate cancer cells//Cancer Res. 2002. Vol. 62. P. 2478–2482. |
Lyubimov A.V., Cherkashin D.V., Efimov S.V., Alanichev A.E., Ivanov V.S., Kutelev G.G.
/
| 〈 |
|
〉 |