Evolutionary Conserved Role of c-Jun-N-Terminal Kinase in CO2-Induced Epithelial Dysfunction

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Vadász, István ^a,b   Dada, Laura A ^a   Briva, Arturo ^a,c   Helenius, Iiro Taneli ^a   Sharabi, Kfir ^d   Welch, Lynn C ^a   Kelly, Aileen M ^a   Grzesik, Benno A ^b   Budinger, G R Scott ^a   Liu, Jing ^a   Seeger, Werner ^b   Beitel, Greg J ^a   Gruenbaum, Yosef ^d   Sznajder, Jacob I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^c DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CARBON DIOXIDE; HELMINTH PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MUTANT PROTEIN; PROTEIN KINASE C; PROTEIN KINASE C ZETA; SERINE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DIPTERA; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE; GENETIC CONSERVATION; HYPERCAPNIA; INFERTILITY; JNK 1 GENE; KGB 2 GENE; LUNG; LUNG ALVEOLUS EPITHELIUM; MAMMAL CELL; NEMATODE; NONHUMAN; PHARYNGEAL PUMPING DEFECT; PHARYNX DISEASE; RAT; RNA INTERFERENCE; RODENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BURKITT LYMPHOMA; CAENORHABDITIS ELEGANS; CARBON DIOXIDE; DROSOPHILA; ENZYME ACTIVATION; EPITHELIAL CELLS; EVOLUTION, MOLECULAR; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE C; PULMONARY ALVEOLI; RATS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84867291423     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046696     Document Type: Article

References (40)

1. Matthay MA, Folkesson HG, Clerici C, (2002) Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600.
2. Vadasz I, Raviv S, Sznajder JI, (2007) Alveolar epithelium and Na,K-ATPase in acute lung injury. Intensive Care Med 33: 1243-1251.
3. Sznajder JI, (2001) Alveolar edema must be cleared for the acute respiratory distress syndrome patient to survive. Am J Respir Crit Care Med 163: 1293-1294.
4. Briva A, Vadasz I, Lecuona E, Welch LC, Chen J, et al. (2007) High CO2 levels impair alveolar epithelial function independently of pH. PLoS ONE 2: e1238.
5. Vadasz I, Dada LA, Briva A, Trejo HE, Welch LC, et al. (2008) AMP-activated protein kinase regulates CO2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na,K-ATPase endocytosis. J Clin Invest 118: 752-762.
6. Putnam RW, (2010) CO2 chemoreception in cardiorespiratory control. J Appl Physiol 108: 1796-1802.
7. Sharabi K, Lecuona E, Helenius IT, Beitel GJ, Sznajder JI, et al. (2009) Sensing, physiological effects and molecular response to elevated CO2 levels in eukaryotes. J Cell Mol Med 13: 4304-4318.
8. Vadasz I, Hubmayr RD, Nin N, Sporn PH, Sznajder JI, (2012) Hypercapnia- a non-permissive environment for the lung. Am J Respir Cell Mol Biol 46: 417-21.
9. Vohwinkel CU, Lecuona E, Sun H, Sommer N, Vadasz I, et al. (2011) Elevated CO2 Levels Cause Mitochondrial Dysfunction and Impair Cell Proliferation. J Biol Chem 286: 37067-37076.
10. Wang N, Gates KL, Trejo H, Favoreto S Jr, Schleimer RP, et al. (2010) Elevated CO2 selectively inhibits interleukin-6 and tumor necrosis factor expression and decreases phagocytosis in the macrophage. FASEB J 24: 2178-2190.
11. Zhou Y, Zhao J, Bouyer P, Boron WF, (2005) Evidence from renal proximal tubules that HCO3- and solute reabsorption are acutely regulated not by pH but by basolateral HCO3- and CO2. Proc Natl Acad Sci U S A 102: 3875-3880.
12. Chang L, Karin M, (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
13. Davis RJ, (2000) Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
14. Hibi M, Lin A, Smeal T, Minden A, Karin M, (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7: 2135-2148.
15. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, et al. (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369: 156-160.
16. Liu J, Yang D, Minemoto Y, Leitges M, Rosner MR, et al. (2006) NF-kappaB is required for UV-induced JNK activation via induction of PKCdelta. Mol Cell 21: 467-480.
17. Lopez-Bergami P, Habelhah H, Bhoumik A, Zhang W, Wang LH, et al. (2005) RACK1 mediates activation of JNK by protein kinase C. Mol Cell. 19: 309-320.
18. Lopez-Bergami P, Ronai Z, (2008) Requirements for PKC-augmented JNK activation by MKK4/7. Int J Biochem Cell Biol 40: 1055-1064.
19. Bretscher AJ, Busch KE, de Bono M, (2008) A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 8044-8049.
20. Fischler W, Kong P, Marella S, Scott K, (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448: 1054-1057.
21. Hallem EA, Sternberg PW, (2008) Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105: 8038-8043.
22. Sharabi K, Hurwitz A, Simon AJ, Beitel GJ, Morimoto RI, et al. (2009) Elevated CO2 levels affect development, motility, and fertility and extend life span in Caenorhabditis elegans. Proc Natl Acad Sci U S A 106: 4024-4029.
23. Helenius IT, Krupinski T, Turnbull DW, Gruenbaum Y, Silverman N, et al. (2009) Elevated CO2 suppresses specific Drosophila innate immune responses and resistance to bacterial infection. Proc Natl Acad Sci U S A 106: 18710-18715.
24. Chibalin AV, Ogimoto G, Pedemonte CH, Pressley TA, Katz AI, et al. (1999) Dopamine-induced endocytosis of Na+,K+-ATPase is initiated by phosphorylation of Ser-18 in the rat alpha subunit and Is responsible for the decreased activity in epithelial cells. J Biol Chem 274: 1920-1927.
25. Dada LA, Chandel NS, Ridge KM, Pedemonte C, Bertorello AM, et al. (2003) Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J Clin Invest 111: 1057-1064.
26. Chen J, Lecuona E, Briva A, Welch LC, Sznajder JI, (2008) Carbonic anhydrase II and alveolar fluid reabsorption during hypercapnia. Am J Respir Cell Mol Biol 38: 32-37.
27. Myrianthefs PM, Briva A, Lecuona E, Dumasius V, Rutschman DH, et al. (2005) Hypocapnic but not metabolic alkalosis impairs alveolar fluid reabsorption. Am J Respir Crit Care Med 171: 1267-1271.
28. Klein JD, Lamitina ST, O'Neill WC, (1999) JNK is a volume-sensitive kinase that phosphorylates the Na-K-2Cl cotransporter in vitro. Am J Physiol 277: C425-431.
29. Donnellan F, Keating N, Geoghegan P, Murray FE, Harvey BJ, et al. (2010) JNK mitogen-activated protein kinase limits calcium-dependent chloride secretion across colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 298: G37-44.
30. Kassardjian A, Kreydiyyeh SI, (2008) JNK modulates the effect of caspases and NF-kappaB in the TNF-alpha-induced down-regulation of Na+/K+ATPase in HepG2 cells. J Cell Physiol 216: 615-620.
31. Ramia N, Kreydiyyeh SI, (2010) TNF-alpha reduces the Na+/K+ ATPase activity in LLC-PK1 cells by activating caspases and JNK and inhibiting NF-kappaB. Cell Biol Int 34: 607-613.
32. Vadasz I, Morty RE, Olschewski A, Konigshoff M, Kohstall MG, et al. (2005) Thrombin impairs alveolar fluid clearance by promoting endocytosis of Na+,K+-ATPase. Am J Respir Cell Mol Biol 33: 343-354.
33. Welch LC, Lecuona E, Briva A, Trejo HE, Dada LA, et al. (2010) Extracellular signal-regulated kinase (ERK) participates in the hypercapnia-induced Na,K-ATPase downregulation. FEBS Lett 584: 3985-3989.
34. Chibalin AV, Pedemonte CH, Katz AI, Feraille E, Berggren PO, et al. (1998) Phosphorylation of the catalyic alpha-subunit constitutes a triggering signal for Na+,K+-ATPase endocytosis. J Biol Chem 273: 8814-8819.
35. Daire V, Giustiniani J, Leroy-Gori I, Quesnoit M, Drevensek S, et al. (2009) Kinesin-1 regulates microtubule dynamics via a c-Jun N-terminal kinase-dependent mechanism. J Biol Chem 284: 31992-32001.
36. Shumay E, Tao J, Wang HY, Malbon CC, (2007) Lysophosphatidic acid regulates trafficking of beta2-adrenergic receptors: the Galpha13/p115RhoGEF/JNK pathway stimulates receptor internalization. J Biol Chem 282: 21529-21541.
37. Bertorello AM, Komarova Y, Smith K, Leibiger IB, Efendiev R, et al. (2003) Analysis of Na+,K+-ATPase motion and incorporation into the plasma membrane in response to G protein-coupled receptor signals in living cells. Mol Biol Cell 14: 1149-1157.
38. Comellas AP, Dada LA, Lecuona E, Pesce LM, Chandel NS, et al. (2006) Hypoxia-Mediated Degradation of Na,K-ATPase via Mitochondrial Reactive Oxygen Species and the Ubiquitin-Conjugating System. Circ Res 98: 1314-22.
39. Lee VY, Schroedl C, Brunelle JK, Buccellato LJ, Akinci OI, et al. (2005) Bleomycin induces alveolar epithelial cell death through JNK-dependent activation of the mitochondrial death pathway. Am J Physiol Lung Cell Mol Physiol 289: L521-528.
40. Hallows KR, Kobinger GP, Wilson JM, Witters LA, Foskett JK, (2003) Physiological modulation of CFTR activity by AMP-activated protein kinase in polarized T84 cells. Am J Physiol Cell Physiol 284: C1297-1308.