Inducible HSP70 regulates superoxide dismutase-2 and mitochondrial oxidative stress in the endothelial cells from developing lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 4, 2014, Pages

  Afolayan, Adeleye J ^a   Teng, Ru Jeng ^a   Eis, Annie ^a   Rana, Ujala ^a   Broniowska, Katarzyna A ^a   Corbett, John A ^a   Pritchard, Kirkwood ^a   Konduri, Girija G ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Nitric oxide; Oxidative stress; Persistent pulmonary hypertension of the newborn; Pulmonary artery endothelium; Vasodilation

Indexed keywords

NITRIC OXIDE; OXIDATIVE STRESS; PERSISTENT PULMONARY HYPERTENSION OF THE NEWBORN; PULMONARY ARTERY ENDOTHELIUM; VASODILATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELLS, CULTURED; ENDOTHELIAL CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROGEN PEROXIDE; INFANT, NEWBORN; LUNG; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PERSISTENT FETAL CIRCULATION SYNDROME; PROTEIN TRANSPORT; PROTEOLYSIS; PULMONARY ARTERY; SHEEP;

EID: 84894025712     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00264.2013     Document Type: Article

References (51)

1. Abman SH, Chatfield BA, Hall SL, McMurtry IF. Role of endotheliumderived relaxing factor during transition of pulmonary circulation at birth. Am J Physiol Heart Circ Physiol 259: H1921-H1927, 1990.
2. Afolayan AJ, Eis A, Teng RJ, Bakhutashvili I, Kaul S, Davis JM, Konduri GG. Decreases in manganese superoxide dismutase expression and activity contribute to oxidative stress in persistent pulmonary hypertension of the newborn. Am J Physiol Lung Cell Mol Physiol 303: L870-L879, 2012.
3. Azem A, Oppliger W, Lustig A, Jeno ÈP, Feifel B, Schatz G, Horst M. The mitochondrial hsp70 chaperone system, Effect of adenine nucleotides, peptide substrate and mGrpE on the oligomeric state of mhsp70. J Biol Chem 272: 20901-20906, 1997.
4. Beddoe T, Lithgow T. Delivery of nascent polypeptides to the mitochondrial surface. Biochim Biophys Acta 1592: 35-39, 2002.
5. Bhatt DP, Chen X, Geiger JD, Rosenberger TA. A sensitive HPLCbased method to quantify adenine nucleotides in primary astrocyte cell cultures. J Chromatogr B Analyt Technol Biomed Life Sci 889: 110-115, 2012.
6. Black SM, Johengen MJ, Ma ZD, Bristow J, Soifer SJ. Ventilation and oxygenation induce endothelial nitric oxide synthase gene expression in the lungs of fetal lambs. J Clin Invest 100: 1448-1458, 1997.
7. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down regulated Mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277: 23977-23980, 2002.
8. Bonnet S, Michelakis ED, Porter CJ, Andrade-Navarro MA, The 'baud B, Bonnet SN, Haromy A, Harry G, Moudgil R, McMurtry MS, Weir E, Archer SL. An abnormal mitochondrial-HIF-1-Kv channel pathway disrupts oxygen-sensing and triggers pulmonary arterial hypertension (PAH) in fawn-hooded rats: similarities to human PAH. Circulation 113: 2630-2641, 2006.
9. Brennan LA, Steinhorn RH, Wedgwood S, Mata-Greenwood E, Roark EA, Russell JA, Black SM. Increased superoxide generation is associated with pulmonary hypertension in fetal lambs. A Role for NADPH oxidase. Circ Res 92: 683-691, 2003.
10. Brooks PS, Levonen AL, Shiva S, Sarti P, Darley-Usman VM. Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med 33: 755-764, 2002.
11. Brooks PS. Mitochondrial proton leak and superoxide generation: an hypothesis. Biochem Soc Trans 26: S331, 1998.
12. Brodsky JL, Chiosis G. Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 6: 1215-1225, 2006.
13. Bowers R, Cool C, Murphy RC, Tuder RM, Hopken MW, Flores SC, Voelkel NF. Oxidative stress in severe pulmonary hypertension. Am J Respir Crit Care Med 169: 764-769, 2004.
14. Cadenas E, Davis KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29: 222-230, 2000.
15. Calabrese V, Scapagnini G, Colombrita C, Ravagna A, Pennisi G, Giuffrida Stella AM, Galli F, Butterfield DA. Redox regulation of heat shock protein expression in aging and neurodegenerative disorders associated with oxidative stress: a nutritional approach. Amino Acids 25: 437-44, 2003.
16. Choi S, Park KA, Lee HJ, Park MS, Lee JH, Park KC, Kim M, Lee SH, Seo JS, Yoon BW. Expression of Cu/Zn SOD protein is suppressed in HSP 701 knockout mice. J Biochem Mol Biol 38: 111-114, 2005.
17. Craig EA, Weissman JS, Horwich AL. Heat shock proteins and molecular chaperones; mediators of protein conformation and turnover in the cell. Cell 78: 365-372, 1994.
18. Daugaard M, Rohde M, Jäättelä M. The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581: 3702-3710, 2007.
19. Doughan AK, Dikalov SI. Mitochondrial redox cycling of mitoquinone leads to superoxide production and cellular apoptosis. Antioxid Redox Signal 9: 1825-1836, 2007.
20. Faraci FM, Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol 24: 1367-1373, 2004.
21. Fink BD, O'Malley Y, Dake BL, Ross NC, Prisinzano TE, Sivitz WI. Mitochondrial targeted coenzyme Q, superoxide, and fuel selectivity in endothelial cells. PLoS One 4: e4250, 2009.
22. Franco AA, Odom RS, Rando TA. Regulation of antioxidant enzyme gene expression in response to oxidative stress and during differentiation of mouse skeletal muscle. Free Radic Biol Med 27: 1122-1132, 1999.
23. Fridovich I. The biology of oxygen radicals. Science 201: 875-880, 1978.
24. Glover LA, Lindsay JG. Targeting proteins to mitochondria: a current overview. Biochem J 284: 609-620, 1992.
25. Han ES, Muller FL, Perez VI, Qi W, Liang H, Xi L, Fu C, Doyle E, Hickey M, Cornell J, Epstein CJ, Roberts LJ, Van Remmen H, Richardson A. The in vivo gene expression signature of oxidative stress Physiol. Genomics 34: 112-126, 2008.
26. Hartl F, Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858, 2002.
27. Hitchler MJ, Oberley LW, Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 45: 1573-1580, 2008.
28. Huang Y, He T, Domann FE. Decreased expression of manganese superoxide dismutase in transformed cells is associated with increased cytosine methylation of the SOD2 gene. DNA Cell Biol 18: 643-652, 1999.
29. Huang S, Rattliff KS, Matouschek A. Protein unfolding by the mitochondrial membrane potential. Nat Struct Biol 9: 301-307, 2002.
30. Jensen RE, Johnson AE. Opening the door to mitochondria protein imports. Nat Struct Biol 8: 1008-1010, 2001.
31. Kalyanaraman B, Dranka BP, Hardy M, Michalski R, Zielonka J. HPLC-based monitoring of products formed from hydroethidine-based fluorogenic probes-The ultimate approach for intra-and extracellular superoxide detection. Biochim Biophys Acta 1840: 739-744, 2013.
32. Konduri GG, Ou J, Shi Y, Pritchard KA Jr. Decreased association of HSP90 impairs endothelial nitric oxide synthase in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 285: H204-H211, 2003.
33. Konduri GG, Mattei J. Role of oxidative phosphorylation and ATP release in mediating birth-related pulmonary vasodilation in fetal lambs. Am J Physiol Heart Circ Physiol 283: H1600-H1608, 2002.
34. Krimmer T, Rassow J, Kunau WH, Voos W, Pfanner N. Mitochondrial protein import motor: the ATPase domain of matrix Hsp70 is crucial for binding to Tim44, while the peptide binding domain and the carboxyterminal segment play a stimulatory role. Mol Cell Biol 20: 5879-5887, 2000.
35. Lassegue B, Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 30: 653-661, 2010.
36. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, Wallace DC, Epstein CJ. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11: 376-381, 1995.
37. Lim JH, Martin F, Guiard B, Pfanner N, Voos W. The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J 20: 941-950, 2001.
38. Locke M. The cellular stress response to exercise: role of stress proteins. Exerc Sport Sci Rev 25: 105-136, 1997.
39. Mayer MP, Schröder H, Rüdiger S, Paal K, Laufen T, Bukau B. Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat Struct Biol 7: 586-593, 2002.
40. Mayer MP, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62: 670-684, 2005.
41. Montezano AC, Touyz RM. Molecular mechanisms of hypertensionreactive oxygen species and antioxidants: a basic science update for the clinician. Can J Cardiol 28: 288-295, 2012.
42. 2+ regulation of mitochondrial ATP synthesis visualized at the single cell level. ACS Chem Biol 6: 709-715, 2011.
43. Powners MV, Workman P. Inhibitors of the heat shock response: biology and pharmacology. FEBS Lett 581: 3758-3769, 2007.
44. Rasbach KA, Schnellmann RG. Signaling of mitochondrial biogenesis following oxidant injury. J Biol Chem 282: 2355-2362, 2007.
45. Rudger S, Buchberger A, Bukau B. Interaction of Hsp70 with substrate. Nat Struct Biol 4: 342-349, 1997.
46. Sakao S, Tatsumi K, Voelkel NF. Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation. Respir Res 10: 95, 2009.
47. Sutton A, Imbert A, Igoudjil A, Descatoire V, Cazanave S, Pessayre D, Degoul F. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet Genomics 15: 311-319, 2005.
48. Sutton A, Khoury H, Prip-Buus C, Cepanec C, Pessayre D, Degoul F. The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria. Pharmacogenetics 13: 145-157, 2003.
49. Wiedemann N, Frazier AE, Pfanner N. The protein import machinery of mitochondria. J Biol Chem 279: 14473-14476, 2004.
50. Wispe JR, Clark JC, Burhans MS, Kropp KE, Korfhagen TR, Whitsett JA. Synthesis and processing of the precursor for human manganesesuperoxide dismutase. Biochim Biophys Acta 994: 30-36, 1989.
51. Young JC, Hoogenraad NJ, Hartl FU. Molecular chaperones hsp90 and hsp70 deliver Preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50, 2003.