Protein kinase A-Iα regulates Na,K-ATPase endocytosis in alveolar epithelial cells exposed to high CO2 concentrations

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 5, 2013, Pages 626-634

  Lecuona, Emilia ^a   Sun, Haiying ^a   Chen, Jiwang ^a   Trejo, Humberto E ^a   Baker, Margaret A ^a   Sznajder, Jacob I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

adducin; Hypercapnia; Na,K ATPase; PKA Type I ; Soluble adenylyl cyclase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENYLATE CYCLASE; ALANINE; ALPHA ADDUCIN; BICARBONATE; CARBON DIOXIDE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; LYASE; PROTEIN KINASE A ALPHA; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADDUCIN; ATP1A1 PROTEIN, HUMAN; CALMODULIN BINDING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; PRKAR1A PROTEIN, HUMAN; PROTEIN KINASE C;

ACTIN FILAMENT; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; HYPERCAPNIA; INTRACELLULAR SIGNALING; LUNG ALVEOLUS EPITHELIUM; NONHUMAN; RNA INTERFERENCE; ANIMAL; DRUG EFFECT; ENZYMOLOGY; LUNG ALVEOLUS CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; RAT; SECOND MESSENGER; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ADENYLATE CYCLASE; ANIMALS; CALMODULIN-BINDING PROTEINS; CARBON DIOXIDE; CELL LINE, TUMOR; CELL MEMBRANE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; ENDOCYTOSIS; HUMANS; HYPERCAPNIA; PHOSPHORYLATION; PNEUMOCYTES; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; SECOND MESSENGER SYSTEMS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

MLCS; MLOWN;

EID: 84879297569     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0373OC     Document Type: Article

References (50)

1. Sznajder JI. Alveolar edema must be cleared for the acute respiratory distress syndrome patient to survive. Am J Respir Crit Care Med 2001; 163: 1293-1294.
2. Lecuona E, Trejo H, Sznajder J. Regulation of Na,K-ATPase during acute lung injury. J Bioenerg Biomembr 2007;39: 391-395.
3. Lecuona E, Saldias F, Comellas A, Ridge K, Guerrero C, Sznajder JI. Ventilator-associated lung injury decreases lung ability to clear edema in rats. Am J Respir Crit Care Med 1999;159: 603-609.
4. Litvan J, Briva A,WilsonMS, Budinger GRS, Sznajder JI, Ridge KM. Betaadrenergic receptor stimulation and adenoviral overexpression of superoxide dismutase prevent the hypoxia-mediated decrease in Na,K-ATPase and alveolar fluid reabsorption. J Biol Chem 2006;281: 19892-19898.
5. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 2012;122: 2731-2740.
6. Briva A, Vadász I, Lecuona E, Welch LC, Chen J, Dada LA, Trejo HE, Dumasius V, Azzam ZS, Myrianthefs PM, et al. High CO2 levels impair alveolar epithelial function independently of pH. PLoS ONE 2007;2:e1238.
7. Vadász I, Dada LA, Briva A, Trejo HE, Welch LC, Chen J, Tóth PT, Lecuona E, Witters LA, Schumacker PT, et al. AMP-activated protein kinase regulates CO2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na,K-ATPase endocytosis. J Clin Invest 2008; 118: 752-762.
8. Buck J, Sinclair ML, Schapal L, Cann MJ, Levin LR. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci USA 1999;96: 79-84.
9. Zippin JH, Levin LR, Buck J. CO2/HCO3-responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol Metab 2001;12: 366-370.
10. Zippin JH, Chen Y, Nahirney P, Kamenetsky M, Wuttke MS, Fischman DA, Levin LR, Buck J. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J 2003;17: 82-84.
11. Tasken K, Aandahl EM. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 2004;84: 137-167.
12. Kopperud R, Krakstad C, Selheim F, Døskeland SO. cAMP effector mechanisms: novel twists for an "old" signaling system. FEBS Lett 2003;546: 121-126.
13. Taylor SS, Kim C, Cheng CY, Brown SHJ, Wu J, Kannan N. Signaling through cAMP and cAMP-dependent protein kinase: diverse strategies for drug design. BBA Proteins Proteomics 2008;1784: 16-26.
14. Matsuoka Y, Li X, Bennett V. Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J Cell Biol 1998;142: 485-497.
15. Matsuoka Y, Li X, Bennett V. Adducin: structure, function and regulation. Cell Mol Life Sci 2000;57: 884-895.
16. Efendiev R, Krmar RT, Ogimoto G, Zwiller J, Tripodi G, Katz AI, Bianchi G, Pedemonte CH, Bertorello AM. Hypertension-linked mutation in the adducin alpha-subunit leads to higher AP2-mu2 phosphorylation and impaired Na1,K1-ATPase trafficking in response to GPCR signals and intracellular sodium. Circ Res 2004;95: 1100-1108.
17. Torielli L, Tivodar S, Montella RC, Iacone R, Padoani G, Tarsini P, Russo O, Sarnataro D, Strazzullo P, Ferrari P, et al. Alpha-adducin mutations increase Na/K pump activity in renal cells by affecting constitutive endocytosis: implications for tubular Na reabsorption. Am J Physiol Renal Physiol 2008;295:F478-F487.
18. Lecuona E, Sun H, Trejo H, Chen J, Gelfand V, Sznajder J. Diverging effects of cAMP/PKA in the traffic and function of the Na,K-ATPase in alveolar epithelial cells. Am J Respir Crit Care Med 2011;183:A4233.
19. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ. Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 2004;279: 37215-37218.
20. Gesellchen F, Stangherlin A, Surdo N, Terrin A, Zoccarato A, Zaccolo M. Measuring spatiotemporal dynamics of cyclic AMP signaling in real-time using FRET-based biosensors. Methods Mol Biol 2011;746: 297-316.
21. Kojima S, Vignjevic D, Borisy G. Improved silencing vector co-expressing GFP and small hairpin RNA. Biotechniques 2004;36: 74-79.
22. Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 2003;278: 49523-49529.
23. Cheng XJ, Fisone G, AizmanO, Aizman R, Levenson R, Greengard P, Aperia A. PKA-mediated phosphorylation and inhibition of Na1-K1-ATPase in response to b-adrenergic hormone. Am J Physiol 1997;273:C893-C901.
24. Bertorello AM, Ridge KM, Chibalin AV, Katz AI, Sznajder JI. Isoproterenol increases Na1-K1-ATPase activity by membrane insertion of alpha-subunits in lung alveolar cells. Am J Physiol 1999;276:L20-L27.
25. Lecuona E, Minin A, Trejo HE, Chen J, Comellas AP, Sun H, Grillo D, Nekrasova OE, Welch LC, Szleifer I, et al. Myosin-VA restrains the trafficking of Na1/K1-ATPase-containing vesicles in alveolar epithelial cells. J Cell Sci 2009;122: 3915-3922.
26. Zaccolo M, Pozzan T. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 2002;295: 1711-1715.
27. Willis BS, Niswender CM, Su T, Amieux PS, McKnight GS. Cell-type specific expression of a dominant negative PKA mutation in mice. PLoS ONE 2011;6:e18772.
28. Burns-Hamuro LL,Ma Y, Kammerer S, Reineke U, Self C, Cook C, Olson GL, Cantor CR, Braun A, Taylor SS. Designing isoform-specific peptide disruptors of protein kinase A localization. Proc Natl Acad Sci USA 2003;100: 4072-4077.
29. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW. Protein kinase A- anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 1997;272: 4747-4752.
30. Dada LA, Novoa E, Lecuona E, Sun H, Sznajder JI. Role of the small GTPase RhoA in the hypoxia-induced decrease of plasma membrane Na,K-ATPase in A549 cells. J Cell Sci 2007;120: 2214-2222.
31. Matsuoka Y, Hughes CA, Bennett V. Adducin regulation: definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J Biol Chem 1996;271: 25157-25166.
32. Mutlu GM, Factor P, Schwartz DE, Sznajder JI. Severe status asthmaticus: management with permissive hypercapnia and inhalation anesthesia. Crit Care Med 2002;30: 477-480.
33. Varughese M, Patole S, Shama A, Whitehall J. Permissive hypercapnia in neonates: the case of the good, the bad, and the ugly. Pediatr Pulmonol 2002;33: 56-64.
34. Belkin RA, Henig NR, Singer LG, Chaparro C, Rubenstein RC, Xie SX, Yee JY, Kotloff RM, Lipson DA, Bunin GR. Risk factors for death of patients with cystic fibrosis awaiting lung transplantation. Am J Respir Crit Care Med 2006;173: 659-666.
35. Helenius IT, Krupinski T, Turnbull DW, Gruenbaum Y, Silverman N, Johnson EA, Sporn PH, Sznajder JI, Beitel GJ. Elevated CO2 suppresses specific Drosophila innate immune responses and resistance to bacterial infection. Proc Natl Acad Sci USA 2009;106: 18710-18715.
36. Cummins EP, Oliver KM, Lenihan CR, Fitzpatrick SF, Bruning U, Scholz CC, Slattery C, Leonard MO, McLoughlin P, Taylor CT. NF-kB links CO2 sensing to innate immunity and inflammation in mammalian cells. J Immunol 2010;185: 4439-4445.
37. Wang N, Gates KL, Trejo H, Favoreto S, Schleimer RP, Sznajder JI, Beitel GJ, Sporn PHS. Elevated CO2 selectively inhibits interleukin-6 and tumor necrosis factor expression and decreases phagocytosis in the macrophage. FASEB J 2010;24: 2178-2190.
38. O'Toole D, Hassett P, Contreras M, Higgins BD, McKeown STW, McAuley DF, O'Brien T, Laffey JG. Hypercapnic acidosis attenuates pulmonary epithelial wound repair by an NF-kB dependent mechanism. Thorax 2009;64: 976-982.
39. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 2000;289: 625-628.
40. Hammer A, Hodgson DR, Cann MJ. Regulation of prokaryotic adenylyl cyclases by CO2. Biochem J 2006;396: 215-218.
41. Wang Y, Lam CS,Wu F,Wang W, Duan Y, Huang P. Regulation of CFTR channels by HCO3-sensitive soluble adenylyl cyclase in human airway epithelial cells. Am J Physiol Cell Physiol 2005;289:C1145-C1151.
42. Hallows KR, Wang H, Edinger RS, Butterworth MB, Oyster NM, Li H, Buck J, Levin LR, Johnson JP, Pastor-Soler NM. Regulation of epithelial Na1 transport by soluble adenylyl cyclase in kidney collecting duct cells. J Biol Chem 2009;284: 5774-5783.
43. Bertorello A, Sznajder JI. The dopamine paradox in lung and kidney epithelia: sharing the same target but operating different signaling networks. Am J Respir Cell Mol Biol 2005;33: 432-437.
44. Patterson C, Lum H, Schaphorst K, Verin A, Garcia J. Regulation of endothelial barrier function by the cAMP-dependent protein kinase. Endothelium 2000;7: 287-308.
45. Prasain N, Alexeyev M, Balczon R, Stevens T. Soluble adenylyl cyclase- dependent microtubule disassembly reveals a novel mechanism of endothelial cell retraction. Am J Physiol Lung Cell Mol Physiol 2009; 297:L73-L83.
46. Di Benedetto G, Zoccarato A, Lissandron V, Terrin A, Li X, Houslay MD, Baillie GS, Zaccolo M. Protein kinase A Type I and Type II define distinct intracellular signaling compartments. Circ Res 2008; 103: 836-844.
47. Day ME, Gaietta GM, Sastri M, Koller A, Mackey MR, Scott JD, Perkins GA, Ellisman MH, Taylor SS. Isoform-specific targeting of PKA to multivesicular bodies. J Cell Biol 2011;193: 347-363.
48. Qualmann B, Kessels M. Endocytosis and the cytoskeleton. Int Rev Cytol 2002;220: 93-144.
49. Woroniecki R, Ferdinand JR, Morrow JS, Devarajan P. Dissociation of spectrin-ankyrin complex as a basis for loss of Na-K-ATPase polarity after ischemia. Am J Physiol Renal Physiol 2003;284:F358-F364.
50. Barkalow KL, Italiano JE, Chou DE, Matsuoka Y, Bennett V, Hartwig JH. Alpha-adducin dissociates from F-actin and spectrin during platelet activation. J Cell Biol 2003;161: 557-570.