Sirtuin 3 deficiency does not augment hypoxia-induced pulmonary hypertension

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 6, 2013, Pages 885-891

  Waypa, Gregory B ^a   Osborne, Scott W ^a   Marks, Jeremy D ^b   Berkelhamer, Sara K ^a   Kondapalli, Jyothisri ^a   Schumacker, Paul T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Hypoxia inducible factor 1; Hypoxic pulmonary vasoconstriction; Reactive oxygen species; Redox sensitive, ratiometric fluorescent protein sensor; Sirtuins

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; REACTIVE OXYGEN METABOLITE; SIRTUIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; CALCIUM SIGNALING; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GENE DELETION; GENOTYPE; HEART LEFT VENTRICLE HYPERTROPHY; HEART RIGHT VENTRICLE HYPERTROPHY; HYPOXIA INDUCED PULMONARY HYPERTENSION; HYPOXIC LUNG VASOCONSTRICTION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER;

ANIMALS; ANOXIA; CALCIUM SIGNALING; FEMALE; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; REACTIVE OXYGEN SPECIES; SIRTUIN 3; VASOCONSTRICTION;

EID: 84890046645     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0191OC     Document Type: Article

References (43)

1. Waypa GB, Guzy R, Mungai PT, Mack MM, Marks JD, Roe MW, Schumacker PT. Increases in mitochondrial reactive oxygen species trigger hypoxia-induced calcium responses in pulmonary artery smooth muscle cells. Circ Res 2006;99:970-978.
2. Waypa GB, Marks JD, Mack MM, Boriboun C, Mungai PT, Schumacker PT. Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ Res 2002;91:719-726.
3. Waypa GB, Chandel NS, Schumacker PT. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circ Res 2001;88:1259-1266.
4. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT. Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 2008;28:718-731.
5. Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schumacker PT, Simon MC. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 2005;1:393-399.
6. Pastukh V, Ruchko M, Gorodnya O, Wilson GL, Gillespie MN. Sequence-specific oxidative base modifications in hypoxia-inducible genes. Free Radic Biol Med 2007;43:1616-1626.
7. 2 during reperfusion of ischemic cardiomyocytes modifies mitochondrial oxidant injury. Crit Care Med 2007;35:1709-1716.
8. Gusarova GA, Dada LA, Kelly AM, Brodie C, Witters LA, Chandel NS, Sznajder JI. Alpha1-AMP-activated protein kinase regulates hypoxiainduced Na, K-ATPase endocytosis via direct phosphorylation of protein kinase C zeta. Mol Cell Biol 2009;29:3455-3464.
9. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxiainduced transcription. Proc Natl Acad Sci USA 1998;95:11715-11720.
10. Korde AS, Yadav VR, Zheng YM, Wang YX. Primary role of mitochondrial Rieske iron-sulfur protein in hypoxic ROS production in pulmonary artery myocytes. Free Radic Biol Med 2011;50:945-952.
11. Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 2005;1:409-414.
12. Leach RM, Hill HM, Snetkov VA, Robertson TP, Ward JP. Divergent roles of glycolysis and the mitochondrial electron transport chain in hypoxic pulmonary vasoconstriction of the rat: identity of the hypoxic sensor. J Physiol 2001;536:211-224.
13. Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J, Dokic D, Schumacker PT. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res 2010;106:526-535.
14. 2+ responses to acute hypoxia in pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 2009;297:L17-L25.
15. 2+ responses to hypoxia. Am J Physiol Lung Cell Mol Physiol 2008;295:L104-L113.
16. Robertson TP, Hague D, Aaronson PI, Ward JP. Voltage-independent calcium entry in hypoxic pulmonary vasoconstriction of intrapulmonary arteries of the rat. J Physiol 2000;525:669-680.
17. + channels, Kv1. 5 and Kv2.1, in hypoxic pulmonary vasoconstriction and control of resting membrane potential in rat pulmonary artery myocytes. J Clin Invest 1998;101:2319-2330.
18. Morio Y, McMurtry IF. Ca (2+) release from ryanodine-sensitive store contributes to mechanism of hypoxic vasoconstriction in rat lungs. J Appl Physiol 2002;92:527-534.
19. Chandel NS, Schumacker PT. Cells depleted of mitochondrial DNA (rho0) yield insight into physiological mechanisms. FEBS Lett 1999;454:173-176.
20. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000;275:25130-25138.
21. Semenza GL. Surviving ischemia: adaptive responses mediated by hypoxia-inducible factor 1. J Clin Invest 2000;106:809-812.
22. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000;88:1474-1480.
23. Semenza GL. HIF-1, O (2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 2001;107:1-3.
24. Yu AY, Shimoda LA, Iyer NV, Huso DL, Sun X, McWilliams R, Beaty T, Sham JS, Wiener CM, Sylvester JT, et al. Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxiainducible factor 1alpha. J Clin Invest 1999;103:691-696.
25. Guarente L. Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 2008;132:171-176.
26. Giralt A, Villarroya F. SIRT3, a pivotal actor in mitochondrial functions: metabolism, cell death and aging. Biochem J 2012;444:1-10.
27. Rose G, Dato S, Altomare K, Bellizzi D, Garasto S, Greco V, Passarino G, Feraco E, Mari V, Barbi C, et al. Variability of the SIRT3 gene, human silent information regulator Sir2 homologue, and survivorship in the elderly. Exp Gerontol 2003;38:1065-1070.
28. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, et al. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 2007;27:8807-8814.
29. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD, Van Der Meer R, Nguyen P, Savage J, Owens KM, et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 2010;17:41-52.
30. Jacobs KM, Pennington JD, Bisht KS, Aykin-Burns N, Kim HS, Mishra M, Sun L, Nguyen P, Ahn BH, Leclerc J, et al. SIRT3 interacts with the daf-16 homolog FOXO3a in the mitochondria, as well as increases FOXO3a dependent gene expression. Int J Biol Sci 2008;4:291-299.
31. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, Gupta MP. Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J Clin Invest 2009;119:2758-2771.
32. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardoso SM, Clish CB, et al. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1a destabilization. Cancer Cell 2011;19:416-428.
33. Bell EL, Emerling BM, Ricoult SJ, Guarente L. SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production. Oncogene 2011;30:2986-2996.
34. Marshall C, Mamary AJ, Verhoeven AJ, Marshall BE. Pulmonary artery NADPH-oxidase is activated in hypoxic pulmonary vasoconstriction. Am J Respir Cell Mol Biol 1996;15:633-644.
35. Wallenstein S, Zucker CL, Fleiss JL. Some statistical methods useful in circulation research. Circ Res 1980;47:1-9.
36. Thibault HB, Kurtz B, Raher MJ, Shaik RS, Waxman A, Derumeaux G, Halpern EF, Bloch KD, Scherrer-Crosbie M. Noninvasive assessment of murine pulmonary arterial pressure: validation and application to models of pulmonary hypertension. Circ Cardiovasc Imaging 2010;3:157-163.
37. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, Kim HS, Flynn CR, Hill S, Hayes McDonald W, et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 2010;40:893-904.
38. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000;279:L1005-L1028.
39. Sheldon RA, Sedik C, Ferriero DM. Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res 1998;810:114-122.
40. Ikeda S, Hawes NL, Chang B, Avery CS, Smith RS, Nishina PM. Severe ocular abnormalities in C57BL/6 but not in 129/Sv p53-deficient mice. Invest Ophthalmol Vis Sci 1999;40:1874-1878.
41. Ward NL, Moore E, Noon K, Spassil N, Keenan E, Ivanco TL, La Manna JC. Cerebral angiogenic factors, angiogenesis, and physiological response to chronic hypoxia differ among four commonly used mouse strains. J Appl Physiol 2007;102:1927-1935.
42. Adachi T, Ogawa H, Okabe S, Kitamuro T, Kikuchi Y, Shibahara S, Shirato K, Hida W. Mice with blunted hypoxic ventilatory response are susceptible to respiratory disturbance during hypoxia. Tohoku J Exp Med 2006;209:125-134.
43. Zwemer CF, Song MY, Carello KA, D'Alecy LG. Strain differences in response to acute hypoxia: CD-1 versus C57BL/6J mice. J Appl Physiol 2007;102:286-293.