High CO₂ Leads to Na,K-ATPase Endocytosis via c-Jun Amino-Terminal Kinase-Induced LMO7b Phosphorylation

REFERENCES

• Kessler R, Faller M, Fourgaut G, Mennecier B, Weitzenblum E. 1999. Predictive factors of hospitalization for acute exacerbation in a series of 64 patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 159:158–164. http://dx.doi.org/10.1164/ajrccm.159.1.9803117.
   PubMed Web of Science ®Google Scholar
• Vitacca M, Bianchi L, Barbano L, Ziliani M, Ambrosino N. 2005. Effects of acute on chronic respiratory failure on hypercapnia and 3-month survival. Chest 128:1209–1215. http://dx.doi.org/10.1378/chest.128.3.1209.
   PubMedGoogle Scholar
• Vadasz I, Hubmayr RD, Nin N, Sporn PH, Sznajder JI. 2012. Hypercapnia: a nonpermissive environment for the lung. Am J Respir Cell Mol Biol 46:417–421. http://dx.doi.org/10.1165/rcmb.2011-0395PS.
   PubMedGoogle Scholar
• Kohnlein T, Windisch W, Wegscheider K, Welte T. 2014. Non-invasive positive pressure ventilation for severe COPD. Authors' reply. Lancet Respir Med 2:e19.
   PubMedGoogle Scholar
• Briva A, Vadasz I, Lecuona E, Welch LC, Chen J, Dada LA, Trejo HE, Dumasius V, Azzam ZS, Myrianthefs PM, Batlle D, Gruenbaum Y, Sznajder JI. 2007. High CO2 levels impair alveolar epithelial function independently of pH. PLoS One 2:e1238. http://dx.doi.org/10.1371/journal.pone.0001238.
   PubMedGoogle Scholar
• Vadasz I, Dada LA, Briva A, Helenius IT, Sharabi K, Welch LC, Kelly AM, Grzesik BA, Budinger GR, Liu J, Seeger W, Beitel GJ, Gruenbaum Y, Sznajder JI. 2012. Evolutionary conserved role of c-Jun-N-terminal kinase in CO2-induced epithelial dysfunction. PLoS One 7:e46696. http://dx.doi.org/10.1371/journal.pone.0046696.
   PubMedGoogle Scholar
• Vadasz I, Dada LA, Briva A, Trejo HE, Welch LC, Chen J, Toth PT, Lecuona E, Witters LA, Schumacker PT, Chandel NS, Seeger W, Sznajder JI. 2008. AMP-activated protein kinase regulates CO2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na,K-ATPase endocytosis. J Clin Investig 118:752–762.
   PubMedGoogle Scholar
• 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. http://dx.doi.org/10.1164/ajrccm.163.6.ed1801d.
   PubMedGoogle Scholar
• Berthiaume Y, Folkesson HG, Matthay MA. 2002. Lung edema clearance: 20 years of progress: invited review: alveolar edema fluid clearance in the injured lung. J Appl Physiol 93:2207–2213. http://dx.doi.org/10.1152/japplphysiol.01201.2001.
   PubMed Web of Science ®Google Scholar
• Dada LA, Chandel NS, Ridge KM, Pedemonte C, Bertorello AM, Sznajder JI. 2003. Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J Clin Investig 111:1057–1064. http://dx.doi.org/10.1172/JCI16826.
   PubMed Web of Science ®Google Scholar
• Mutlu GM, Sznajder JI. 2005. Mechanisms of pulmonary edema clearance. Am J Physiol Lung Cell Mol Physiol 289:L685–L695. http://dx.doi.org/10.1152/ajplung.00247.2005.
   PubMed Web of Science ®Google Scholar
• Factor P, Senne C, Dumasius V, Ridge K, Jaffe HA, Uhal B, Gao Z, Sznajder JI. 1998. Overexpression of the Na+,K+-ATPase alpha1 subunit increases Na+,K+-ATPase function in A549 cells. Am J Respir Cell Mol Biol 18:741–749. http://dx.doi.org/10.1165/ajrcmb.18.6.2918.
   PubMed Web of Science ®Google Scholar
• Shull GE, Schwartz A, Lingrel JB. 1985. Amino-acid sequence of the catalytic subunit of the (Na+ + K+)ATPase deduced from a complementary DNA. Nature 316:691–695. http://dx.doi.org/10.1038/316691a0.
   PubMed Web of Science ®Google Scholar
• Looney MR, Sartori C, Chakraborty S, James PF, Lingrel JB, Matthay MA. 2005. Decreased expression of both the alpha1- and alpha2-subunits of the Na-K-ATPase reduces maximal alveolar epithelial fluid clearance. Am J Physiol Lung Cell Mol Physiol 289:L104–L110. http://dx.doi.org/10.1152/ajplung.00464.2004.
   PubMedGoogle Scholar
• Sznajder JI, Factor P, Ingbar DH. 2002. Invited review: lung edema clearance: role of Na(+)-K(+)-ATPase. J Appl Physiol 93:1860–1866. http://dx.doi.org/10.1152/japplphysiol.00022.2002.
   PubMed Web of Science ®Google Scholar
• Gusarova GA, Dada LA, Kelly AM, Brodie C, Witters LA, Chandel NS, Sznajder JI. 2009. Alpha1-AMP-activated protein kinase regulates hypoxia-induced Na,K-ATPase endocytosis via direct phosphorylation of protein kinase C zeta. Mol Cell Biol 29:3455–3464. http://dx.doi.org/10.1128/MCB.00054-09.
   PubMedGoogle Scholar
• Lecuona E, Sun H, Chen J, Trejo HE, Baker MA, Sznajder JI. 2013. Protein kinase A-Ialpha regulates Na,K-ATPase endocytosis in alveolar epithelial cells exposed to high CO(2) concentrations. Am J Respir Cell Mol Biol 48:626–634. http://dx.doi.org/10.1165/rcmb.2012-0373OC.
   PubMedGoogle Scholar
• Raman M, Chen W, Cobb MH. 2007. Differential regulation and properties of MAPKs. Oncogene 26:3100–3112. http://dx.doi.org/10.1038/sj.onc.1210392.
   PubMed Web of Science ®Google Scholar
• Bogoyevitch MA, Kobe B. 2006. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 70:1061–1095. http://dx.doi.org/10.1128/MMBR.00025-06.
   PubMed Web of Science ®Google Scholar
• Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K. 2003. JNK phosphorylates paxillin and regulates cell migration. Nature 424:219–223. http://dx.doi.org/10.1038/nature01745.
   PubMed Web of Science ®Google Scholar
• Mengistu M, Brotzman H, Ghadiali S, Lowe-Krentz L. 2011. Fluid shear stress-induced JNK activity leads to actin remodeling for cell alignment. J Cell Physiol 226:110–121. http://dx.doi.org/10.1002/jcp.22311.
   PubMedGoogle Scholar
• Chen Z, Gibson TB, Robinson F, Silvestro L, Pearson G, Xu B, Wright A, Vanderbilt C, Cobb MH. 2001. MAP kinases. Chem Rev 101:2449–2476. http://dx.doi.org/10.1021/cr000241p.
   PubMed Web of Science ®Google Scholar
• Lee MH, Koria P, Qu J, Andreadis ST. 2009. JNK phosphorylates beta-catenin and regulates adherens junctions. FASEB J 23:3874–3883. http://dx.doi.org/10.1096/fj.08-117804.
   PubMed Web of Science ®Google Scholar
• Lee MH, Padmashali R, Koria P, Andreadis ST. 2011. JNK regulates binding of alpha-catenin to adherens junctions and cell-cell adhesion. FASEB J 25:613–623. http://dx.doi.org/10.1096/fj.10-161380.
   PubMed Web of Science ®Google Scholar
• Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153–183.
   PubMed Web of Science ®Google Scholar
• Katz S, Aronheim A. 2002. Differential targeting of the stress mitogen-activated protein kinases to the c-Jun dimerization protein 2. Biochem J 368:939–945. http://dx.doi.org/10.1042/bj20021127.
   PubMedGoogle Scholar
• Ooshio T, Irie K, Morimoto K, Fukuhara A, Imai T, Takai Y. 2004. Involvement of LMO7 in the association of two cell-cell adhesion molecules, nectin and E-cadherin, through afadin and alpha-actinin in epithelial cells. J Biol Chem 279:31365–31373. http://dx.doi.org/10.1074/jbc.M401957200.
   PubMedGoogle Scholar
• Tanaka-Okamoto M, Hori K, Ishizaki H, Hosoi A, Itoh Y, Wei M, Wanibuchi H, Mizoguchi A, Nakamura H, Miyoshi J. 2009. Increased susceptibility to spontaneous lung cancer in mice lacking LIM-domain only 7. Cancer Sci 100:608–616. http://dx.doi.org/10.1111/j.1349-7006.2009.01091.x.
   PubMedGoogle Scholar
• Ridge KM, Olivera WG, Saldias F, Azzam Z, Horowitz S, Rutschman DH, Dumasius V, Factor P, Sznajder JI. 2003. Alveolar type 1 cells express the alpha2 Na,K-ATPase, which contributes to lung liquid clearance. Circ Res 92:453–460. http://dx.doi.org/10.1161/01.RES.0000059414.10360.F2.
   PubMedGoogle Scholar
• Chen Z, Krmar RT, Dada L, Efendiev R, Leibiger IB, Pedemonte CH, Katz AI, Sznajder JI, Bertorello AM. 2006. Phosphorylation of adaptor protein-2 mu2 is essential for Na+,K+-ATPase endocytosis in response to either G protein-coupled receptor or reactive oxygen species. Am J Respir Cell Mol Biol 35:127–132. http://dx.doi.org/10.1165/rcmb.2006-0044OC.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• 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–C1308. http://dx.doi.org/10.1152/ajpcell.00227.2002.
   PubMedGoogle Scholar
• Vagin O, Tokhtaeva E, Garay PE, Souda P, Bassilian S, Whitelegge JP, Lewis R, Sachs G, Wheeler L, Aoki R, Fernandez-Salas E. 2014. Recruitment of septin cytoskeletal proteins by botulinum toxin A protease determines its remarkable stability. J Cell Sci 127:3294–3308. http://dx.doi.org/10.1242/jcs.146324.
   PubMedGoogle Scholar
• Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ. 2009. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4:484–494. http://dx.doi.org/10.1038/nprot.2009.21.
   PubMed Web of Science ®Google Scholar
• Rappsilber J, Mann M, Ishihama Y. 2007. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2:1896–1906. http://dx.doi.org/10.1038/nprot.2007.261.
   PubMed Web of Science ®Google Scholar
• Al-Khalili L, Kotova O, Tsuchida H, Ehren I, Feraille E, Krook A, Chibalin AV. 2004. ERK1/2 mediates insulin stimulation of Na(+),K(+)-ATPase by phosphorylation of the alpha-subunit in human skeletal muscle cells. J Biol Chem 279:25211–25218. http://dx.doi.org/10.1074/jbc.M402152200.
   PubMedGoogle Scholar
• Khundmiri SJ, Bertorello AM, Delamere NA, Lederer ED. 2004. Clathrin-mediated endocytosis of Na+,K+-ATPase in response to parathyroid hormone requires ERK-dependent phosphorylation of Ser-11 within the alpha1-subunit. J Biol Chem 279:17418–17427. http://dx.doi.org/10.1074/jbc.M311715200.
   PubMedGoogle Scholar
• Chibalin AV, Ogimoto G, Pedemonte CH, Pressley TA, Katz AI, Feraille E, Berggren PO, Bertorello AM. 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. http://dx.doi.org/10.1074/jbc.274.4.1920.
   PubMed Web of Science ®Google Scholar
• Ohno H. 2006. Clathrin-associated adaptor protein complexes. J Cell Sci 119:3719–3721. http://dx.doi.org/10.1242/jcs.03085.
   PubMedGoogle Scholar
• Ohno H. 2006. Physiological roles of clathrin adaptor AP complexes: lessons from mutant animals. J Biochem 139:943–948. http://dx.doi.org/10.1093/jb/mvj120.
   PubMedGoogle Scholar
• Szymkiewicz I, Shupliakov O, Dikic I. 2004. Cargo- and compartment-selective endocytic scaffold proteins. Biochem J 383:1–11. http://dx.doi.org/10.1042/BJ20040913.
   PubMedGoogle Scholar
• Schiavo G, Greensmith L, Hafezparast M, Fisher EM. 2013. Cytoplasmic dynein heavy chain: the servant of many masters. Trends Neurosci 36:641–651. http://dx.doi.org/10.1016/j.tins.2013.08.001.
   PubMed Web of Science ®Google Scholar
• Ninkovic M, Mitkovski M, Kohl T, Stuhmer W, Pardo LA. 2012. Physical and functional interaction of KV10.1 with Rabaptin-5 impacts ion channel trafficking. FEBS Lett 586:3077–3084. http://dx.doi.org/10.1016/j.febslet.2012.07.055.
   PubMedGoogle Scholar
• Kaksonen M, Toret CP, Drubin DG. 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7:404–414. http://dx.doi.org/10.1038/nrm1940.
   PubMed Web of Science ®Google Scholar
• Sun Y, Martin AC, Drubin DG. 2006. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev Cell 11:33–46. http://dx.doi.org/10.1016/j.devcel.2006.05.008.
   PubMed Web of Science ®Google Scholar
• Okreglak V, Drubin DG. 2007. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J Cell Biol 178:1251–1264. http://dx.doi.org/10.1083/jcb.200703092.
   PubMed Web of Science ®Google Scholar
• McMurray MA, Stefan CJ, Wemmer M, Odorizzi G, Emr SD, Thorner J. 2011. Genetic interactions with mutations affecting septin assembly reveal ESCRT functions in budding yeast cytokinesis. Biol Chem 392:699–712.
   PubMedGoogle Scholar
• Mostowy S, Cossart P. 2012. Septins: the fourth component of the cytoskeleton. Nat Rev Mol Cell Biol 13:183–194.
   PubMed Web of Science ®Google Scholar
• Engqvist-Goldstein AE, Warren RA, Kessels MM, Keen JH, Heuser J, Drubin DG. 2001. The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. J Cell Biol 154:1209–1223. http://dx.doi.org/10.1083/jcb.200106089.
   PubMed Web of Science ®Google Scholar
• Berryman M, Bretscher A. 2000. Identification of a novel member of the chloride intracellular channel gene family (CLIC5) that associates with the actin cytoskeleton of placental microvilli. Mol Biol Cell 11:1509–1521. http://dx.doi.org/10.1091/mbc.11.5.1509.
   PubMedGoogle Scholar
• Bannert N, Vollhardt K, Asomuddinov B, Haag M, Konig H, Norley S, Kurth R. 2003. PDZ domain-mediated interaction of interleukin-16 precursor proteins with myosin phosphatase targeting subunits. J Biol Chem 278:42190–42199. http://dx.doi.org/10.1074/jbc.M306669200.
   PubMed Web of Science ®Google Scholar
• Nakamura H, Hori K, Tanaka-Okamoto M, Higashiyama M, Itoh Y, Inoue M, Morinaka S, Miyoshi J. 2011. Decreased expression of LMO7 and its clinicopathological significance in human lung adenocarcinoma. Exp Ther Med 2:1053–1057.
   PubMedGoogle Scholar
• Derijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025–1037. http://dx.doi.org/10.1016/0092-8674(94)90380-8.
   PubMed Web of Science ®Google Scholar
• Tanoue T, Adachi M, Moriguchi T, Nishida E. 2000. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol 2:110–116. http://dx.doi.org/10.1038/35000065.
   PubMed Web of Science ®Google Scholar
• Bjorkblom B, Ostman N, Hongisto V, Komarovski V, Filen JJ, Nyman TA, Kallunki T, Courtney MJ, Coffey ET. 2005. Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 25:6350–6361. http://dx.doi.org/10.1523/JNEUROSCI.1517-05.2005.
   PubMedGoogle Scholar
• Ogimoto G, Yudowski GA, Barker CJ, Kohler M, Katz AI, Feraille E, Pedemonte CH, Berggren PO, Bertorello AM. 2000. G protein-coupled receptors regulate Na+,K+-ATPase activity and endocytosis by modulating the recruitment of adaptor protein 2 and clathrin. Proc Natl Acad Sci U S A 97:3242–3247. http://dx.doi.org/10.1073/pnas.97.7.3242.
   PubMed Web of Science ®Google Scholar