A potential role for reactive oxygen species and the HIF-1α-VEGF pathway in hypoxia-induced pulmonary vascular leak

Free Radical Biology and Medicine

Volumn 47, Issue 1, 2009, Pages 55-61

  Irwin, David C ^a   McCord, Joe M ^a,b   Nozik Grayck, Eva ^a   Beckly, Ginny ^a   Foreman, Ben ^a   Sullivan, Tim ^a   White, Molly ^a   T Crossno Jr , Joseph ^a,b   Bailey, Damian ^c   Flores, Sonia C ^a   Majka, Susan ^a   Klemm, Dwight ^a,b   Tissot van Patot, Martha C ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Faculty of Health Sport and Science   (United Kingdom)

Author keywords

Free radicals; HIF; Hypoxia; Pulmonary edema; Reactive oxygen species; VEGF

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; GLUTATHIONE; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN SFLT 1; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG BLOOD VESSEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANOXIA; ANTIOXIDANTS; CAPILLARY PERMEABILITY; CELL NUCLEUS; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; PULMONARY ARTERY; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS;

EID: 67349199628     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.03.027     Document Type: Article

References (36)

1. Bartsch P., Mairbaurl H., Maggiorini M., and Swenson E. Physiological aspects of high-altitude pulmonary edema. J. Appl. Physiol. 98 (2005) 1101-1110
2. Fagan K.A., McMurtry I.F., and Rodman D. Role of endothelin-1in lung disease. Respir. Res. 2 (2001) 90-101
3. Goyal P., Weissmann N., Grimminger F., Hegel C., Badar L., Rose F., Fink L., Ghofrani H., Schermuly R., Schimdt H.H., Seeger W., and Hanze J. Upregulation of NAD(P) oxidase 1 in hypoxia activates hypoxia-inducible factor 1 via increase in reactive oxygen species. Free Radic. Biol. Med. 36 (2004) 1279-1288
4. Lum H., and Roebuck K.A. Oxidant stress and endothelial cell dysfunction. Am. J. Cell Physiol. 280 (2001) 719-741
5. Maulik N., and Das D.K. Redox signaling in vascular angiogenesis. Free Radic. Biol. Med. 33 (2002) 1047-1060
6. Moldovan L., Mythreye K., Goldschmidt-Clermont P., and Satterwhite L.L. Reactive oxygen species in vascular endothelial cell motility: roles of NAD(P)H oxidase and Rac1. Cardiovasc. Res. 71 (2006) 236-246
7. Bell E., and Chandel N. Mitochondrial oxygen sensing: regulation of hypoxia-inducible factor by mitochondrial reactive oxygen species. Essays Biochem. 43 (2007) 17-27
8. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., and Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95 (1998) 11715-11720
9. Gorlach A., and Kietzmann T. Superoxide and derived reactive oxygen species in the regulation of hypoxia-inducible factors. Methods Enzymol. 435 (2007) 421-446
10. Guzy R., and Schumacker P.T. Oxygen sensing by mitochondria at complex III: the paradox of increased ROS during hypoxia. Exp. Physiol. 91 (2006) 807-819
11. Simon M. Mitochondrial reactive oxygen species are required for hypoxic HIF alpha stabilization. Adv. Exp. Med. Biol. 588 (2006) 165-170
12. Fischer S., Clauss M., Wiesnet M., and Karliczek G. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am. J. Physiol. 276 (1999) C812-C820
13. Fischer S., Wobben M., Marti H.H., Renz D., and Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in expression of zonula occludens-1. Microvasc. Res. 63 (2002) 70-80
14. Carpenter T., Schomberg S., and Stenmark K. Endothelin-mediated increases in lung VEGF content promote vascular leak in young rats exposed to viral infection and hypoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 289 (2005) 1075-1082
15. Godzich M., Hodnett M., Frank J.A., Su G., Pespeni M., Angel M., Howard B., Matthay A., and Pittet J.F. Activation of stress protein response prevents the development of pulmonary edema by inhibiting VEGF cell signaling in a model of lung ischemia-reperfusion injury in rats. FASEB J. 20 (2006) 757-768
16. Kohl R., Zhou J., and Brune B. Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1α stabilization. Free Radic. Biol. Med. 40 (2006) 1430-1442
17. Mura M., dos Santos C., Stewart D., and Liu M. Vascular endothelial growth factor and related molecules in acute lung injury. J. Appl. Physiol. 97 (2004) 1605-1617
18. Irwin D.C., Tissot van Patot M., Tucker A., and Bowen R. Direct ANP inhibition of hypoxia-induced inflammatory pathways in pulmonary microvascular and macrovascular endothelial cells. Am. J. Physiol. 288 (2005) 849-859
19. Hu T., Ramachandra Rao S.P., Siva S., Valancius C., Zhu Y., Mahadev K., Toh I., Goldstein B.J., Woolkalis M., and Sharma K. Reactive oxygen species production via NADPH oxidase mediates TGF-β-induced cytoskeletal alterations in endothelial cells. Am. J. Renal Physiol. 289 (2005) 816-825
20. Mura M., Han B., Andrade C.F., Seth R., Hwang D., Waddell T., Keshavjee S., and Liu M. The early responses of VEGF and its receptors during acute lung injury: implication of VEGF in alveolar epithelial cell survival. Crit. Care 10 (2006) R130
21. Semenza G.L. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88 (2000) 1474-1480
22. Votyakova T.V., and Reynolds I.J. Detection of hydrogen peroxide with Amplex red: interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biophys. 431 (2004) 138-144
23. Stevens T., Garcia J.G.N., Shasby M., Bhattacharya J., and Malik A.B. Mechanisms regulating endothelial cell barrier function. Am. J Physiol. 279 (2000) L419-L422
24. Aird W.C. Endothelial cell heterogeneity. Crit. Care Med. 31 (2003) S221-S230
25. Nico B., Mangieri D., Crivellato E., Longo V., De Giorgis M., Capobianco C., Corsi P., Benagiano V., Roncali L., and Ribatti D. HIF activation and VEGF overexpression are coupled with ZO-1 up-phosphorylation in the brain of dystrophic MDX mouse. Brain Pathol. 17 (2007) 399-406
26. Shoshani T., Faerman A., Mett I., Zelin E., Tenne T., Gorodin S., Moshel Y., Elbaz S., Budanov A., Chajut A., Kalinski H., Kamer I., Rozen A., Mor O., Keshet E., Leshkowitz D., Einat P., Skaliter R., and Feinstein E. Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 22 (2002) 2283-2293
27. 2 induces paracellular permeability of porcine brain-derived microvascular endothelial cells by activation of the p44/42 MAP kinase pathway. Eur. J. Cell Biol. 84 (2005) 687-697
28. Bailey D., and Davies B. Acute mountain sickness: prophylactic benefits of antioxidant vitamin supplementation at high altitude. High Alt. Med. Biol. 2 (2001) 21-29
29. Tissot van Patot M.C., Leadbetter G., Keyes L.E., Bendrick-Peart J., Beckey V.E., Christians U., and Hackett P. Greater free plasma VEGF and lower soluble VEGF receptor-1 in acute mountain sickness. J. Appl. Physiol. 98 (2005) 1626-1629
30. Wilson J.N., Pierce J.D., and Clancy R.L. Reactive oxygen species in acute respiratory distress syndrome. Heart Lung 30 (2001) 370-375
31. Shibuya M. Vascular endothelial growth factor receptor-1 (VEGF-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 9 (2006) 225-230
32. Hastings J.M., Licence D.R., Burton G.J., Charnock-Jones D.S., and Smith S.K. Soluble vascular endothelial growth factor receptor 1 inhibits edema and epithelial proliferation induced by 17{beta}-estradiol in the mouse uterus. Endocrinology 144 (2003) 326-334
33. Patel N., Sun L., Moshinsky D., Chen H., Leahy K.M., Le P., Moss K.G., Wang X., Rice A., Tam D., Laird A.D., Yu X., Zhang Q., Tang C., McMahon G., and Howlett A.A. selective and oral small molecule inhibitor of vascular epithelial growth factor receptor (VEGFR)-2 and VEGFR-1 inhibits neovascularization and vascular permeability. J. Pharmacol. Exp. Ther. 306 (2003) 838-845
34. Sugimoto H., Hamano Y., Charytan D., Cosgrove D., Kieran M., Sudhakar A., and Kalluri R. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J. Biol. Chem. 278 (2003) 12605-12608
35. Shapiro, N.; Yano, K.; Okada, H.; Fischer, C.; Howell, M.; Spokes, K.; Ngo, L.; Angus, D.; Aird, W. A prospective, observational study of soluble FLT-1 and vascular endothelial growth factor in sepsis. Shock E-pub ahead of print; 2007.
36. Tsao P., Chan F., Wei S., Hsieh W., Chou H., Su Y., Chen C., Hsu W., Hsieh F., and Hsu S. Soluble vascular endothelial growth factor receptor-1 protects mice in sepsis. Crit. Care Med. 35 (2007) 1955-1960