Display options
Cite
Bogdanova A, Petrushanko IY, Hernansanz-Agustín P, et al. "Oxygen Sensing" by Na,K-ATPase: These Miraculous Thiols. Front Physiol. 2016;7:314doi: 10.3389/fphys.2016.00314.
Bogdanova, A., Petrushanko, I. Y., Hernansanz-Agustín, P., & Martínez-Ruiz, A. (2016). "Oxygen Sensing" by Na,K-ATPase: These Miraculous Thiols. Frontiers in physiology, 7314. https://doi.org/10.3389/fphys.2016.00314
Bogdanova, Anna, et al. ""Oxygen Sensing" by Na,K-ATPase: These Miraculous Thiols." Frontiers in physiology vol. 7 (2016): 314. doi: https://doi.org/10.3389/fphys.2016.00314
Bogdanova A, Petrushanko IY, Hernansanz-Agustín P, Martínez-Ruiz A. "Oxygen Sensing" by Na,K-ATPase: These Miraculous Thiols. Front Physiol. 2016 Aug 02;7:314. doi: 10.3389/fphys.2016.00314. eCollection 2016. PMID: 27531981; PMCID: PMC4970491.
Copy Download .nbib Format: NLM
Share it on

Front Physiol. 2016 Aug 02;7:314. doi: 10.3389/fphys.2016.00314. eCollection 2016.

"Oxygen Sensing" by Na,K-ATPase: These Miraculous Thiols.

Frontiers in physiology

Anna Bogdanova, Irina Y Petrushanko, Pablo Hernansanz-Agustín, Antonio Martínez-Ruiz

Affiliations

  1. Institute of Veterinary Physiology, Vetsuisse Faculty and the Zurich Center for Integrative Human Physiology (ZIHP), University of Zurich Zurich, Switzerland.
  2. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences Moscow, Russia.
  3. Servicio de Inmunología, Instituto de Investigación Sanitaria Princesa (IIS-IP), Hospital Universitario de La PrincesaMadrid, Spain; Departamento de Bioquímica, Universidad Autónoma de MadridMadrid, Spain.
  4. Servicio de Inmunología, Instituto de Investigación Sanitaria Princesa (IIS-IP), Hospital Universitario de La Princesa Madrid, Spain.

PMID: 27531981 PMCID: PMC4970491 DOI: 10.3389/fphys.2016.00314

Abstract

Control over the Na,K-ATPase function plays a central role in adaptation of the organisms to hypoxic and anoxic conditions. As the enzyme itself does not possess O2 binding sites its "oxygen-sensitivity" is mediated by a variety of redox-sensitive modifications including S-glutathionylation, S-nitrosylation, and redox-sensitive phosphorylation. This is an overview of the current knowledge on the plethora of molecular mechanisms tuning the activity of the ATP-consuming Na,K-ATPase to the cellular metabolic activity. Recent findings suggest that oxygen-derived free radicals and H2O2, NO, and oxidized glutathione are the signaling messengers that make the Na,K-ATPase "oxygen-sensitive." This very ancient signaling pathway targeting thiols of all three subunits of the Na,K-ATPase as well as redox-sensitive kinases sustains the enzyme activity at the "optimal" level avoiding terminal ATP depletion and maintaining the transmembrane ion gradients in cells of anoxia-tolerant species. We acknowledge the complexity of the underlying processes as we characterize the sources of reactive oxygen and nitrogen species production in hypoxic cells, and identify their targets, the reactive thiol groups which, upon modification, impact the enzyme activity. Structured accordingly, this review presents a summary on (i) the sources of free radical production in hypoxic cells, (ii) localization of regulatory thiols within the Na,K-ATPase and the role reversible thiol modifications play in responses of the enzyme to a variety of stimuli (hypoxia, receptors' activation) (iii) redox-sensitive regulatory phosphorylation, and (iv) the role of fine modulation of the Na,K-ATPase function in survival success under hypoxic conditions. The co-authors attempted to cover all the contradictions and standing hypotheses in the field and propose the possible future developments in this dynamic area of research, the importance of which is hard to overestimate. Better understanding of the processes underlying successful adaptation strategies will make it possible to harness them and use for treatment of patients with stroke and myocardial infarction, sleep apnoea and high altitude pulmonary oedema, and those undergoing surgical interventions associated with the interruption of blood perfusion.

Keywords: S-glutathionylation; S-nitrosylation; Sodium-Potassium-Exchanging ATPase; hypoxia; redox regulation; thiols

References

  1. Acta Physiol (Oxf). 2016 Apr;216(4):447-53 - PubMed
  2. PLoS One. 2014 Oct 13;9(10):e110514 - PubMed
  3. Am J Physiol Renal Physiol. 2006 Feb;290(2):F241-50 - PubMed
  4. Br J Pharmacol. 2013 Aug;169(7):1417-29 - PubMed
  5. PLoS One. 2014 Nov 06;9(11):e110597 - PubMed
  6. Cell Biochem Funct. 2005 Mar-Apr;23(2):115-23 - PubMed
  7. Br J Pharmacol. 2010 May;160(2):346-54 - PubMed
  8. Comp Biochem Physiol C Toxicol Pharmacol. 2008 Nov;148(4):355-62 - PubMed
  9. Neurobiol Aging. 2005 Jun;26(6):907-16 - PubMed
  10. Science. 2003 Dec 12;302(5652):1975-8 - PubMed
  11. Eur J Biochem. 1999 Mar;260(3):904-10 - PubMed
  12. Cell Mol Life Sci. 2013 Jan;70(2):205-22 - PubMed
  13. Mol Cell. 1999 May;3(5):555-63 - PubMed
  14. Sci Signal. 2015 Apr 21;8(373):ra37 - PubMed
  15. Cell Metab. 2005 Jun;1(6):393-9 - PubMed
  16. J Biol Chem. 2012 Sep 14;287(38):32195-205 - PubMed
  17. Arch Pharm Res. 2007 Oct;30(10):1216-24 - PubMed
  18. Hypertension. 1998 May;31(5):1097-103 - PubMed
  19. J Biol Chem. 1995 Dec 1;270(48):28495-8 - PubMed
  20. J Biol Chem. 2012 Apr 6;287(15):12353-64 - PubMed
  21. J Cereb Blood Flow Metab. 2006 Sep;26(9):1148-56 - PubMed
  22. Proc Natl Acad Sci U S A. 2012 Jan 24;109 (4):1239-44 - PubMed
  23. Cell Metab. 2005 Jun;1(6):401-8 - PubMed
  24. Chin J Nat Med. 2015 Apr;13(4):264-73 - PubMed
  25. Free Radic Biol Med. 2008 Jun 15;44(12):2013-8 - PubMed
  26. Anim Reprod Sci. 2011 Dec;129(3-4):152-61 - PubMed
  27. Biochemistry. 2001 Nov 27;40(47):14134-42 - PubMed
  28. Nat Prod Res. 2010 Feb;24(3):274-85 - PubMed
  29. Mol Biosyst. 2015 Mar;11(3):923-9 - PubMed
  30. J Biol Chem. 2005 Jan 28;280(4):2750-8 - PubMed
  31. Antioxid Redox Signal. 2012 Dec 15;17(12):1748-63 - PubMed
  32. Antioxid Redox Signal. 2008 Mar;10(3):445-73 - PubMed
  33. Biochemistry (Mosc). 2014 Feb;79(2):158-64 - PubMed
  34. Biochem Biophys Res Commun. 1999 Jan 19;254(2):424-9 - PubMed
  35. Pathophysiology. 2007 Dec;14(3-4):159-66 - PubMed
  36. Free Radic Biol Med. 2011 Jul 1;51(1):17-29 - PubMed
  37. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11715-20 - PubMed
  38. J Biol Chem. 2007 Apr 6;282(14):10585-93 - PubMed
  39. Nature. 2014 Nov 20;515(7527):431-5 - PubMed
  40. Arch Biochem Biophys. 1977 Apr 30;180(2):248-57 - PubMed
  41. Antioxid Redox Signal. 2006 Sep-Oct;8(9-10):1693-705 - PubMed
  42. J Bioenerg Biomembr. 2008 Oct;40(5):533-9 - PubMed
  43. J Biol Chem. 1990 Jul 15;265(20):11409-12 - PubMed
  44. Respir Physiol Neurobiol. 2010 Dec 31;174(3):192-200 - PubMed
  45. J Physiol. 2015 Mar 15;593(6):1361-82 - PubMed
  46. J Biol Chem. 1998 May 15;273(20):12558-66 - PubMed
  47. Circ Res. 2009 Mar 27;104(6):720-3 - PubMed
  48. J Neurosci. 2003 Jan 1;23 (1):43-51 - PubMed
  49. Biochem Pharmacol. 2014 May 1;89(1):20-30 - PubMed
  50. Free Radic Biol Med. 2000 Dec 15;29(12 ):1280-90 - PubMed
  51. Antioxid Redox Signal. 2014 Nov 20;21(15):2061-82 - PubMed
  52. Antioxid Redox Signal. 2014 Jan 1;20(1):1-14 - PubMed
  53. Am J Physiol. 1998 Nov;275(5 Pt 2):F633-50 - PubMed
  54. Ann N Y Acad Sci. 2003 Apr;986:58-62 - PubMed
  55. Nat Methods. 2006 Apr;3(4):281-6 - PubMed
  56. J Biol Chem. 2011 May 20;286(20):18056-65 - PubMed
  57. Biochemistry. 1995 Aug 8;34(31):9893-6 - PubMed
  58. Physiol Rep. 2015 Aug;3(8):null - PubMed
  59. Ann N Y Acad Sci. 2003 Apr;986:541-2 - PubMed
  60. Biochemistry (Mosc). 2005 Feb;70(2):120-7 - PubMed
  61. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9493-8 - PubMed
  62. Circ Res. 2009 Jul 17;105(2):185-93 - PubMed
  63. Oncogene. 2008 Aug 21;27(36):4877-87 - PubMed
  64. J Insect Physiol. 2008 Jun;54(6):1023-7 - PubMed
  65. Circ Res. 2005 Aug 5;97(3):252-9 - PubMed
  66. Science. 2014 Mar 7;343(6175):1137-40 - PubMed
  67. Cardiovasc Res. 2003 Mar 15;57(4):1044-51 - PubMed
  68. Circulation. 1999 Apr 27;99(16):2105-12 - PubMed
  69. J Mol Cell Cardiol. 2013 Aug;61:164-71 - PubMed
  70. J Hypertens. 1998 Dec;16(12 Pt 2):1953-8 - PubMed
  71. Gen Physiol Biophys. 2002 Mar;21(1):31-7 - PubMed
  72. J Bioenerg Biomembr. 2007 Dec;39(5-6):391-5 - PubMed
  73. J Biol Chem. 2009 Oct 23;284(43):29773-83 - PubMed
  74. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6758-62 - PubMed
  75. Antioxid Redox Signal. 2008 Nov;10(11):1941-88 - PubMed
  76. Antioxid Redox Signal. 2013 Oct 10;19(11):1220-35 - PubMed
  77. Oxid Med Cell Longev. 2016;2016:9092328 - PubMed
  78. Thorax. 2005 Apr;60(4):265-7 - PubMed
  79. J Exp Biol. 2006 Feb;209(Pt 4):677-88 - PubMed
  80. Sci Rep. 2014 Jun 04;4:5165 - PubMed
  81. Front Biosci (Landmark Ed). 2011 Jan 01;16:553-67 - PubMed
  82. Physiol Rev. 2007 Jan;87(1):315-424 - PubMed
  83. Philos Trans R Soc Lond B Biol Sci. 2013 Jun 10;368(1622):20130088 - PubMed
  84. Proc Natl Acad Sci U S A. 2010 Jun 8;107(23 ):10719-24 - PubMed
  85. Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15560-5 - PubMed
  86. Annu Rev Biochem. 1995;64:97-112 - PubMed
  87. Adv Exp Med Biol. 2012;748:145-69 - PubMed
  88. Exp Physiol. 2006 Sep;91(5):807-19 - PubMed
  89. Am J Physiol Heart Circ Physiol. 2007 Mar;292(3):H1470-8 - PubMed
  90. J Clin Invest. 2003 Apr;111(7):1057-64 - PubMed
  91. Arch Biochem Biophys. 2001 Apr 1;388(1):74-80 - PubMed
  92. Nature. 1961 Jul 8;191:144-8 - PubMed
  93. J Neurochem. 2009 Aug;110(4):1170-9 - PubMed
  94. FEBS Lett. 1997 Oct 13;416(1):15-8 - PubMed
  95. J Cell Physiol. 2014 Mar;229(3):343-52 - PubMed
  96. Am J Respir Cell Mol Biol. 1996 Nov;15(5):633-44 - PubMed
  97. Nat Commun. 2014 Oct 21;5:5222 - PubMed
  98. Eur J Biochem. 2000 Aug;267(16):4928-44 - PubMed
  99. J Cereb Blood Flow Metab. 1996 Mar;16(2):290-5 - PubMed
  100. Ann N Y Acad Sci. 1997 Nov 3;834:479-88 - PubMed
  101. Lancet. 2015 Jun 13;385(9985):2363-70 - PubMed
  102. Cell Metab. 2015 Nov 3;22(5):825-37 - PubMed
  103. Hypertension. 2010 Nov;56(5):914-9 - PubMed
  104. Cardiovasc Res. 2004 Apr 1;62(1):43-52 - PubMed
  105. Am J Physiol. 1998 Jan;274(1 Pt 2):F182-8 - PubMed
  106. News Physiol Sci. 2001 Oct;16:217-21 - PubMed
  107. IUBMB Life. 2007 Apr-May;59(4-5):243-8 - PubMed
  108. Biochim Biophys Acta. 2016 Jul;1857(7):863-71 - PubMed
  109. J Biol Chem. 1994 Dec 2;269(48):30436-44 - PubMed
  110. Biochim Biophys Acta. 2014 Aug;1844(8):1344-54 - PubMed
  111. Methods Enzymol. 1996;269:37-41 - PubMed
  112. Am J Physiol Heart Circ Physiol. 2012 Dec 1;303(11):H1332-43 - PubMed
  113. Cell Mol Neurobiol. 1999 Feb;19(1):133-40 - PubMed
  114. J Biol Chem. 2013 Nov 22;288(47):34249-58 - PubMed
  115. Chem Rev. 2013 Jan 9;113(1):596-698 - PubMed
  116. J Biol Chem. 2000 Nov 3;275(44):34693-700 - PubMed
  117. Semin Nephrol. 2005 Sep;25(5):292-303 - PubMed
  118. Am J Physiol Cell Physiol. 2015 Aug 15;309(4):C239-50 - PubMed
  119. Science. 2015 Jan 2;347(6217):44-9 - PubMed
  120. J Biol Chem. 2013 Sep 6;288(36):25769-79 - PubMed
  121. J Biol Chem. 2010 Oct 8;285(41):31277-84 - PubMed
  122. Antioxid Redox Signal. 2013 May 1;18(13):1623-41 - PubMed
  123. Am J Physiol Regul Integr Comp Physiol. 2006 Apr;290(4):R916-25 - PubMed
  124. Antioxid Redox Signal. 2015 Feb 10;22(5):377-97 - PubMed
  125. J Biol Chem. 2010 Apr 30;285(18):13712-20 - PubMed
  126. Br J Pharmacol. 2006 Jul;148(6):871-80 - PubMed
  127. Free Radic Biol Med. 2013 Dec;65:563-72 - PubMed
  128. PLoS One. 2013;8(2):e55512 - PubMed
  129. Carcinogenesis. 2001 Aug;22(8):1221-9 - PubMed
  130. Am J Physiol Cell Physiol. 2009 Apr;296(4):C693-700 - PubMed
  131. J Biol Chem. 2004 Mar 26;279(13):13044-53 - PubMed
  132. Biochemistry. 2000 Aug 22;39(33):10319-29 - PubMed
  133. Curr Opin Cell Biol. 2015 Aug;35:1-6 - PubMed
  134. Am J Physiol. 1997 Sep;273(3 Pt 1):C893-901 - PubMed
  135. Free Radic Biol Med. 2007 Sep 15;43(6):883-98 - PubMed
  136. J Biol Chem. 2016 May 13;291(20):10934-47 - PubMed
  137. J Neurosci. 2014 Jan 15;34(3):963-8 - PubMed
  138. Structure. 2011 Dec 7;19(12):1732-8 - PubMed
  139. Biochem Biophys Res Commun. 1995 Feb 6;207(1):155-9 - PubMed
  140. Science. 2010 Jul 23;329(5990):448-51 - PubMed
  141. J Exp Med. 2007 Sep 3;204(9):2089-102 - PubMed
  142. J Physiol. 2003 Oct 15;552(Pt 2):335-44 - PubMed
  143. J Biol Chem. 2006 Aug 4;281(31):21827-36 - PubMed
  144. Free Radic Res. 2016;50(2):172-94 - PubMed
  145. Cardiovasc Res. 2005 Jan 1;65(1):93-103 - PubMed
  146. Cardiovasc Res. 2007 Jul 15;75(2):220-8 - PubMed
  147. Neuroscience. 1997 May;78(2):589-601 - PubMed
  148. Cell Metab. 2005 Jun;1(6):409-14 - PubMed
  149. FASEB J. 2004 Jan;18(1):197-9 - PubMed
  150. J Biol Chem. 2001 Feb 2;276(5):3098-105 - PubMed
  151. Redox Biol. 2015;4:180-3 - PubMed
  152. Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13742-7 - PubMed
  153. Pharmacol Rev. 2009 Mar;61(1):9-38 - PubMed
  154. Annu Rev Pharmacol Toxicol. 2011;51:169-87 - PubMed
  155. Antioxid Redox Signal. 2012 Feb 1;16(3):203-16 - PubMed
  156. Biochim Biophys Acta. 2015 Oct;1848(10 Pt A):2430-6 - PubMed
  157. Trends Biochem Sci. 2009 Feb;34(2):85-96 - PubMed
  158. PLoS One. 2014 Oct 27;9(10):e111448 - PubMed
  159. J Cardiovasc Pharmacol. 2011 Jan;57(1):65-71 - PubMed
  160. J Physiol Pharmacol. 2003 Jun;54(2):191-210 - PubMed
  161. Pflugers Arch. 2009 Jan;457(3):635-44 - PubMed
  162. Am J Physiol Cell Physiol. 2000 Sep;279(3):C541-66 - PubMed
  163. Mol Cell. 2008 May 23;30(4):393-402 - PubMed
  164. J Exp Biol. 2005 May;208(Pt 10):1793-801 - PubMed
  165. Am J Physiol. 1993 Nov;265(5 Pt 2):R1020-5 - PubMed
  166. J Biol Chem. 2002 Nov 8;277(45):43505-11 - PubMed
  167. Science. 2005 Apr 22;308(5721):518 - PubMed
  168. Respir Physiol. 2001 Nov 15;128(3):263-76 - PubMed
  169. Mol Cell Biol. 2009 Jul;29(13):3455-64 - PubMed
  170. Am J Respir Cell Mol Biol. 2006 Jul;35(1):127-32 - PubMed
  171. J Cell Sci. 2004 Jan 15;117(Pt 2):131-2 - PubMed
  172. Am J Physiol Cell Physiol. 2015 Jan 1;308(1):C51-60 - PubMed
  173. J Neurosci. 2007 Jan 31;27(5):1129-38 - PubMed
  174. Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5379-84 - PubMed
  175. FASEB J. 1999 Sep;13(12):1481-90 - PubMed
  176. Oxid Med Cell Longev. 2014;2014:343154 - PubMed
  177. Front Biosci. 2007 Jan 01;12:1072-8 - PubMed
  178. Crit Care Med. 2003 Apr;31(4 Suppl):S248-52 - PubMed
  179. J Gen Physiol. 2007 Oct;130(4):389-98 - PubMed
  180. Ann N Y Acad Sci. 2007 Mar;1099:119-34 - PubMed
  181. FEBS Lett. 2015 Sep 14;589(19 Pt B):2668-74 - PubMed
  182. Amino Acids. 2003 Dec;25(3-4):295-311 - PubMed
  183. Physiol Rev. 2006 Apr;86(2):583-650 - PubMed
  184. FASEB J. 1999 Oct;13(13):1751-61 - PubMed
  185. Biomed Pharmacother. 2009 Feb;63(2):79-85 - PubMed
  186. Comp Biochem Physiol B Biochem Mol Biol. 1996 Jan;113(1):3-13 - PubMed
  187. J Biol Chem. 2000 Aug 18;275(33):25130-8 - PubMed
  188. Am J Physiol Cell Physiol. 2009 Jun;296(6):C1346-55 - PubMed
  189. Free Radic Biol Med. 2014 Jun;71:146-56 - PubMed
  190. Biochim Biophys Acta. 2000 Apr 5;1464(2):177-87 - PubMed
  191. Biochem J. 2009 Jan 1;417(1):1-13 - PubMed
  192. Cardiovasc Res. 2006 Jul 15;71(2):195-207 - PubMed
  193. Am J Physiol Cell Physiol. 2011 Oct;301(4):C833-40 - PubMed
  194. Neurosci Lett. 1997 Oct 10;235(1-2):89-92 - PubMed
  195. J Proteomics. 2012 Sep 18;75(17):5449-62 - PubMed
  196. Circulation. 2010 Dec 21;122(25):2699-708 - PubMed
  197. J Hypertens. 2012 Sep;30(9):1817-26 - PubMed
  198. Redox Biol. 2013 Feb 08;1:244-57 - PubMed
  199. Comp Biochem Physiol A Mol Integr Physiol. 1999 Sep;124(1):1-17 - PubMed
  200. Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19579-86 - PubMed
  201. J Neurosci. 2008 Sep 17;28(38):9463-72 - PubMed
  202. Nature. 1967 Jan 14;213(5072):137-9 - PubMed
  203. Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):903-15 - PubMed
  204. J Biol Chem. 1997 Jul 11;272(28):17726-33 - PubMed
  205. Biochem J. 1976 May 15;156(2):435-44 - PubMed
  206. Curr Opin Chem Biol. 2012 Dec;16(5-6):498-506 - PubMed
  207. Cell Signal. 2007 Sep;19(9):1893-8 - PubMed
  208. J Biol Chem. 2011 May 27;286(21):18562-72 - PubMed
  209. Antioxid Redox Signal. 2013 Jan 20;18(3):239-49 - PubMed
  210. Ann N Y Acad Sci. 1997 Nov 3;834:680-3 - PubMed

Publication Types