The lectin-like domain of TNF increases ENaC open probability through a novel site at the interface between the second transmembrane and C-terminal domains of the α-subunit

Journal of Biological Chemistry

Volumn 291, Issue 45, 2016, Pages 23440-23451

  Lucas, Rudolf ^a   Yue, Qiang ^b   Alli, Abdel ^b,c   Duke, Billie Jeanne ^b   Al Khalili, Otor ^b   Thai, Tiffany L ^b   Hamacher, Jürg ^d   Sridhar, Supriya ^a   Lebedyeva, Iryna ^e   Su, Huabo ^a   Tzotzos, Susan ^f   Fischer, Bernhard ^f   Gameiro, Armanda Formigao ^e   Loose, Maria ^g   Chakraborty, Trinad ^g   Shabbir, Waheed ^h   Aufy, Mohammed ^h   Lemmens Gruber, Rosa ^h   Eaton, Douglas C ^b   Czikora, Istvan ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b AUGUSTA UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e SAARLAND UNIVERSITY   (Germany)

^f APEPTICO GmbH   (Austria)

^g JUSTUS LIEBIG UNIVERSITY   (Germany)

^h UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; BLOOD PRESSURE; CELL MEMBRANES; ENZYME ACTIVITY; PROBABILITY; PROTEINS;

BINDING CAPACITIES; C-TERMINAL DOMAINS; EPITHELIAL SODIUM CHANNELS; EXTRACELLULAR LOOPS; FUNCTIONAL CHANNELS; MOLECULAR DOCKING; TRANSMEMBRANES; UBIQUITINATION;

PEPTIDES;

EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL ALPHA SUBUNIT; SOLNATIDE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AP301 PEPTIDE; CYCLOPEPTIDE; EPITHELIAL SODIUM CHANNEL STIMULATING AGENT; PROTEIN SUBUNIT;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; LECTIN LIKE DOMAIN; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SECOND TRANSMEMBRANE DOMAIN; UBIQUITINATION; CHEMISTRY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; POINT MUTATION; PROTEIN SUBUNIT; TUMOR CELL LINE;

CELL LINE, TUMOR; EPITHELIAL SODIUM CHANNEL AGONISTS; EPITHELIAL SODIUM CHANNELS; HEK293 CELLS; HUMANS; MOLECULAR DOCKING SIMULATION; PEPTIDES, CYCLIC; POINT MUTATION; PROTEIN DOMAINS; PROTEIN SUBUNITS; UBIQUITINATION;

EID: 84994201989     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.718163     Document Type: Article

References (54)

1. Eaton, D. C., Helms, M. N., Koval, M., Bao, H. F., and Jain, L. (2009) The contribution of epithelial sodium channels to alveolar function in health and disease. Annu. Rev. Physiol. 71, 403-423
2. Eaton, D. C., Malik, B., Bao, H. F., Yu, L., and Jain, L. (2010) Regulation of epithelial sodium channel trafficking by ubiquitination. Proc. Am. Thorac. Soc. 7, 54-64
3. Ji, H. L., Zhao, R. Z., Chen, Z. X., Shetty, S., Idell, S., and Matalon, S. (2012) γ ENaC: a novel divergent amiloride-inhibitable sodium channel. Am. J. Physiol. Lung Cell Mol. Physiol. 303, L1013-L1026
4. Shi, S., Carattino, M. D., Hughey, R. P., and Kleyman, T. R. (2013) ENaC regulation by proteases and shear stress. Curr. Mol. Pharmacol. 6, 28-34
5. + channel (ENaC) intersubunit Clγ inhibitory residues suggests a trimeric αγβ channel architecture. J. Biol. Chem. 286, 6027-6032
6. Kashlan, O. B., and Kleyman, T. R. (2011) ENaC structure and function in the wake of a resolved structure of a family member. Am. J. Physiol. Renal Physiol. 301, F684-F696
7. Butterworth, M. B., Edinger, R. S., Frizzell, R. A., and Johnson, J. P. (2009) Regulation of the epithelial sodium channel by membrane trafficking. Am. J. Physiol. Renal Physiol. 296, F10-F24
8. + channel (ENaC) by phosphatidylinositides. Am. J. Physiol. Renal Physiol. 290, F949-F957
9. + channel by binding to a site in an extracellular acidic cleft. J. Biol. Chem. 290, 568-576
10. + channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life 60, 620-628
11. Collier, D. M., Tomkovicz, V. R., Peterson, Z. J., Benson, C. J., and Snyder, P. M. (2014) Intersubunit conformational changes mediate epithelial sodium channel gating. J. Gen. Physiol. 144, 337-348
12. Snyder, P. M. (2009) Down-regulating destruction: phosphorylation regulates the E3 ubiquitin ligase Nedd4-2. Sci. Signal. 2, pe41
13. Chraïbi, A., and Horisberger, J. D. (2002) Na self inhibition of human epithelial Na channel: temperature dependence and effect of extracellular proteases. J. Gen. Physiol. 120, 133-145
14. Hughey, R. P., Carattino, M. D., and Kleyman, T. R. (2007) Role of proteolysis in the activation of epithelial sodium channels. Curr. Opin. Nephrol. Hypertens. 16, 444-450
15. + channels are activated by laminar shear stress. J. Biol. Chem. 279, 4120-4126
16. Mukherjee, A., Mueller, G. M., Kinlough, C. L., Sheng, N., Wang, Z., Mustafa, S. A., Kashlan, O. B., Kleyman, T. R., and Hughey, R. P. (2014) Cysteine palmitoylation of the γ subunit has a dominant role in modulating activity of the epithelial sodium channel. J. Biol. Chem. 289, 14351-14359
17. Pavlov, T. S., Ilatovskaya, D. V., Levchenko, V., Mattson, D. L., Roman, R. J., and Staruschenko, A. (2011) Effects of cytochrome P-450 metabolites of arachidonic acid on the epithelial sodium channel (ENaC). Am. J. Physiol. Renal Physiol. 301, F672-F681
18. Pochynyuk, O., Bugaj, V., and Stockand, J. D. (2008) Physiologic regulation of the epithelial sodium channel by phosphatidylinositides. Curr. Opin. Nephrol. Hypertens. 17, 533-540
19. Alli, A. A., Bao, H. F., Aldrugh, Y., Song, J. Z., Ma, H. P., Yu, L., Al-Khalili, O., and Eaton, D. C. (2012) Phosphatidylinositol phosphate-dependent regulation of Xenopus ENaC by MARCKS protein. Am. J. Physiol. Renal Physiol. 303, F800-F811
20. Alli, A. A., Bao, H. F., Liu, B. C., Yu, L., Aldrugh, S., Montgomery, D. S., Ma, H. P., and Eaton, D. C. (2015) Calmodulin and CaMKII modulate ENaC activity by regulating the association of MARCKS and the cytoskeleton with the apical membrane. Am. J. Physiol. Renal Physiol. 309, F456-F463
21. Reifenberger, M. S., Yu, L., Bao, H. F., Duke, B. J., Liu, B. C., Ma, H. P., Alli, A. A., Eaton, D. C., and Alli, A. A. (2014) Cytochalasin E alters the cytoskeleton and decreases ENaC activity in Xenopus 2F3 cells. Am. J. Physiol. Renal Physiol. 307, F86-F95
22. Copeland, S. J., Berdiev, B. K., Ji, H. L., Lockhart, J., Parker, S., Fuller, C. M., and Benos, D. J. (2001) Regions in the carboxy terminus of α-bENaC involved in gating and functional effects of actin. Am. J. Physiol. Cell Physiol. 281, C231-C240
23. Mazzochi, C., Bubien, J. K., Smith, P. R., and Benos, D. J. (2006) The carboxyl terminus of the α-subunit of the amiloride-sensitive epithelial sodium channel binds to F-actin. J. Biol. Chem. 281, 6528-6538
24. Åstrand, A. B., Hemmerling, M., Root, J., Wingren, C., Pesic, J., Johansson, E., Garland, A. L., Ghosh, A., and Tarran, R. (2015) Linking increased airway hydration, ciliary beating, and mucociliary clearance through ENaC inhibition. Am. J. Physiol. Lung Cell Mol. Physiol. 308, L22-L32
25. Mall, M. A., and Galietta, L. J. (2015) Targeting ion channels in cystic fibrosis. J. Cyst Fibros 14, 561-570
26. Matalon, S., Bartoszewski, R., and Collawn, J. F. (2015) Role of epithelial sodium channels in the regulation of lung fluid homeostasis. Am. J. Physiol. Lung Cell Mol. Physiol. 309, L1229-L1238
27. Ware, L. B., and Matthay, M. A. (2001) Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am. J. Respir. Crit Care Med. 163, 1376-1383
28. Boncoeur, E., Tardif, V., Tessier, M. C., Morneau, F., Lavoie, J., Gendreau-Berthiaume, E., Grygorczyk, R., Dagenais, A., and Berthiaume, Y. (2010) Modulation of epithelial sodium channel activity by lipopolysaccharide in alveolar type II cells: involvement of purinergic signaling. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L417-L426
29. Czikora, I., Alli, A., Bao, H. F., Kaftan, D., Sridhar, S., Apell, H. J., Gorshkov, B., White, R., Zimmermann, A., Wendel, A., Pauly-Evers, M., Hamacher, J., Garcia-Gabay, I., Fischer, B., Verin, A., et al. (2014) A novel tumor necrosis factor-mediated mechanism of direct epithelial sodium channel activation. Am. J. Resp. Crit. Care Med. 190, 522-532
30. Lucas, R., Sridhar, S., Rick, F. G., Gorshkov, B., Umapathy, N. S., Yang, G., Oseghale, A., Verin, A. D., Chakraborty, T., Matthay, M. A., Zemskov, E. A., White, R., Block, N. L., and Schally, A. V. (2012) Agonist of growth hormone-releasing hormone reduces pneumolysin-induced pulmonary permeability edema. Proc. Natl. Acad. Sci. U. S. A. 109, 2084-2089
31. Migneault, F., Boncoeur, E., Morneau, F., Pascariu, M., Dagenais, A., and Berthiaume, Y. (2013) Cycloheximide and lipopolysaccharide downregulate αENaC mRNA via different mechanisms in alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 305, L747-L755
32. Peters, D. M., Vadász, I., Wujak, L., Wygrecka, M., Olschewski, A., Becker, C., Herold, S., Papp, R., Mayer, K., Rummel, S., Brandes, R. P., Günther, A., Waldegger, S., Eickelberg, O., Seeger, W., et al. (2014) TGF-β directs trafficking of the epithelial sodium channel ENaC which has implications for ion and fluid transport in acute lung injury. Proc. Natl. Acad. Sci. U. S. A. 111, E374-E383
33. Bao, H. F., Zhang, Z. R., Liang, Y. Y., Ma, J. J., Eaton, D. C., and Ma, H. P. (2007) Ceramide mediates inhibition of the renal epithelial sodium channel by tumor necrosis factor-α through protein kinase C. Am. J. Physiol. Renal Physiol. 293, F1178-F1186
34. Braun, C., Hamacher, J., Morel, D. R., Wendel, A., and Lucas, R. (2005) Dichotomal role of TNF in experimental pulmonary edema reabsorption. J. Immunol. 175, 3402-3408
35. Yamagata, T., Yamagata, Y., Nishimoto, T., Hirano, T., Nakanishi, M., Minakata, Y., Ichinose, M., Dagenais, A., and Berthiaume, Y. (2009) The regulation of amiloride-sensitive epithelial sodium channels by tumor necrosis factor-α in injured lungs and alveolar type II cells. Respir. Physiol. Neurobiol. 166, 16-23
36. Bertok, S., Wilson, M. R., Morley, P. J., de Wildt, R., Bayliffe, A., and Takata, M. (2012) Selective inhibition of intra-alveolar p55 TNF receptor attenuates ventilator-induced lung injury. Thorax 67, 244-251
37. Dagenais, A., Fréchette, R., Yamagata, Y., Yamagata, T., Carmel, J. F., Clermont, M. E., Brochiero, E., Massé, C., and Berthiaume, Y. (2004) Downregulation of ENaC activity and expression by TNF-α in alveolar epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 286, L301-L311
38. Shabbir, W., Tzotzos, S., Bedak, M., Aufy, M., Willam, A., Kraihammer, M., Holzner, A., Czikora, I., Scherbaum-Hazemi, P., Fischer, H., Pietschmann, H., Fischer, B., Lucas, R., and Lemmens-Gruber, R. (2015) Glycosylation-dependent activation of epithelial sodium channel by solnatide. Biochem. Pharmacol. 98, 740-753
39. Marquardt, A., Bernevic, B., and Przybylski, M. (2007) Identification, affinity characterisation and biological interactions of lectin-like peptidecarbohydrate complexes derived from human TNF-α using high-resolution mass spectrometry. J. Pept Sci. 13, 803-810
40. Lopitz-Otsoa, F., Rodriguez-Suarez, E., Aillet, F., Casado-Vela, J., Lang, V., Matthiesen, R., Elortza, F., and Rodriguez, M. S. (2012) Integrative analysis of the ubiquitin proteome isolated using Tandem Ubiquitin Binding Entities (TUBEs). J. Proteomics 75, 2998-3014
41. Keane, J. (2005) TNF-blocking agents and tuberculosis: new drugs illuminate an old topic. Rheumatology (Oxford) 44, 714-720
42. Lucas, R., Verin, A. D., Black, S. M., and Catravas, J. D. (2009) Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochem. Pharmacol. 77, 1763-1772
43. Matthay, M. A., Robriquet, L., and Fang, X. (2005) Alveolar epithelium: role in lung fluid balance and acute lung injury. Proc. Am. Thorac. Soc. 2, 206-213
44. Roux, J., McNicholas, C. M., Carles, M., Goolaerts, A., Houseman, B. T., Dickinson, D. A., Iles, K. E., Ware, L. B., Matthay, M. A., and Pittet, J. F. (2013) IL-8 inhibits cAMP-stimulated alveolar epithelial fluid transport via a GRK2/PI3K-dependent mechanism. FASEB J. 27, 1095-1106
45. Wagener, B. M., Roux, J., Carles, M., and Pittet, J. F. (2015) Synergistic inhibition of β2-adrenergic receptor-mediated alveolar epithelial fluid transport by interleukin-8 and transforming growth factor-β. Anesthesiology 122, 1084-1092
46. Chen, X. J., Seth, S., Yue, G., Kamat, P., Compans, R. W., Guidot, D., Brown, L. A., Eaton, D. C., and Jain, L. (2004) Influenza virus inhibits ENaC and lung fluid clearance. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L366-L373
47. Cholon, D. M., O'Neal, W. K., Randell, S. H., Riordan, J. R., and Gentzsch, M. (2010) Modulation of endocytic trafficking and apical stability of CFTR in primary human airway epithelial cultures. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L304-L314
48. Zhu, J., Yan, J., and Thornhill, W. B. (2012) N-Glycosylation promotes the cell surface expression of Kv1.3 potassium channels. FEBS J. 279, 2632-2644
49. Baldwin, R. L., Stolowitz, M. L., Hood, L., and Wisnieski, B. J. (1996) Structural changes of tumor necrosis factor α associated with membrane insertion and channel formation. Proc. Natl. Acad. Sci. U. S. A. 93, 1021-1026
50. Elia, N., Tapponnier, M., Matthay, M. A., Hamacher, J., Pache, J. C., Brundler, M. A., Totsch, M., De Baetselier, P., Fransen, L., Fukuda, N., Morel, D. R., and Lucas, R. (2003) Functional identification of the alveolar edema reabsorption activity of murine tumor necrosis factor-α. Am. J. Respir. Crit Care Med. 168, 1043-1050
51. Sieck, G. C., and Wylam, M. E. (2014) Paradoxical use of tumor necrosis factor in treating pulmonary edema. Am. J. Respir. Crit Care Med. 190, 595-596
52. Alli, A. A., Song, J. Z., Al-Khalili, O., Bao, H. F., Ma, H. P., Alli, A. A., and Eaton, D. C. (2012) Cathepsin B is secreted apically from Xenopus 2F3 cells and cleaves the epithelial sodium channel (ENaC) to increase its activity. J. Biol. Chem. 287, 30073-30083
53. Alli, A. A., and Gower, W. R., Jr. (2010) Molecular approaches to examine the phosphorylation state of the C type natriuretic peptide receptor. J. Cell Biochem. 110, 985-994
54. Malik, B., Schlanger, L., Al-Khalili, O., Bao, H. F., Yue, G., Price, S. R., Mitch, W. E., and Eaton, D. C. (2001) ENaC degradation in A6 cells by the ubiquitin-proteosome proteolytic pathway. J. Biol. Chem. 276, 12903-12910