Receptor for advanced glycation end-products regulates lung fluid balance via protein kinase C-gp91phox signaling to epithelial sodium channels

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 1, 2015, Pages 75-87

  Downs, Charles A ^a,b   Kreiner, Lisa H ^c   Johnson, Nicholle M ^c   Brown, Lou Ann ^c   Helms, My N ^b,c  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute respiratory distress syndrome; Alveolar microenvironment; Chronic obstructive pulmonary disease; Lung injury; Pulmonary edema

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ADVANCED GLYCATION END PRODUCT RECEPTOR ANTAGONIST; EPITHELIAL SODIUM CHANNEL; PROTEIN KINASE C; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; TEMPOL; ADVANCED GLYCOSYLATION END-PRODUCT RECEPTOR; CYBB PROTEIN, HUMAN; CYBB PROTEIN, RAT; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN;

ALVEOLAR EPITHELIAL TYPE I; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EPITHELIAL LINING FLUID; FEMALE; FLUOROSCOPY; GENE SILENCING; HISTOGRAM; HUMAN; IMMUNOPRECIPITATION; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS EPITHELIUM CELL; LUNG FLUID; LUNG LAVAGE; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SALT ABSORPTION; SIGNAL TRANSDUCTION; SINGLE CHANNEL PATCH CLAMP; SMOKING; WATER ABSORPTION; WESTERN BLOTTING; ANIMAL; METABOLISM;

RATTUS;

ANIMALS; BRONCHOALVEOLAR LAVAGE; EPITHELIAL SODIUM CHANNELS; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; PROTEIN KINASE C; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SMOKING;

EID: 84920272847     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0002OC     Document Type: Article

References (54)

1. Schmidt AM, Yan SD, Yan SF, Stern DM. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 2000;1498:99-111.
2. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 2001;108:949-955.
3. Schmidt AM, Stern DM. Receptor for AGE (RAGE) is a gene within the major histocompatibility class III region: implications for host response mechanisms in homeostasis and chronic disease. Front Biosci 2001;6:D1151-D1160.
4. Crapo JD, Barry BE, Gehr P, Bachofen M, Weibel ER. Cell number and cell characteristics of the normal human lung. Am Rev Respir Dis 1982;126:332-337.
5. Fehrenbach H, Kasper M, Tschernig T, Shearman MS, Schuh D, Muller M. Receptor for advanced glycation endproducts (RAGE) exhibits highly differential cellular and subcellular localisation in rat and human lung. Cell Mol Biol (Noisy -le-grand) 1998;44:1147-1157.
6. Herold K, Moser B, Chen Y, Zeng S, Yan SF, Ramasamy R, Emond J, Clynes R, Schmidt AM. Receptor for advanced glycation end products (RAGE) in a dash to the rescue: in flammatory signals gone awry in the primal response to stress. J Leukoc Biol 2007;82:204-212.
7. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999;97:889-901.
8. Ostendorp T, Leclerc E, Galichet A, Koch M, Demling N, Weigle B, Heizmann CW, Kroneck PM, Fritz G. Structural and functional insights into RAGE activation by multimeric S100B. EMBO J 2007;26:3868-3878.
9. Abraham E, Arcaroli J, Carmody A, Wang H, Tracey KJ. HMG-1 as a mediator of acute lung inflammation. J Immunol 2000;165: 2950-2954.
10. Fukuchi Y. The aging lung and chronic obstructive pulmonary disease: similarity and difference. Proc Am Thorac Soc 2009;6:570-572.
11. Boschetto P, Campo I, Stendardo M, Casimirri E, Tinelli C, Gorrini M, Ceconi C, Fucili A, Potena A, Papi A, et al. Plasma sRAGE and N-(carboxymethyl) lysine in patients with CHF and/or COPD. Eur J Clin Invest 2013;43:562-569.
12. Sukkar MB, Wood LG, Tooze M, Simpson JL, McDonald VM, Gibson PG, Wark PA. Soluble RAGE is defi cient in neutrophilic asthma and COPD. Eur Respir J 2012;39:721-729.
13. Eaton DC, Helms MN, Koval M, Bao HF, Jain L. The contribution of epithelial sodium channels to alveolar function in health and disease. Annu Rev Physiol 2009;71:403-423.
14. Matalon S, O'Brodovich H. Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 1999;61:627-661.
15. Stewart AP, Haerteis S, Diakov A, Korbmacher C, Edwardson JM. Atomic force microscopy reveals the architecture of the epithelial sodium channel (ENaC). J Biol Chem 2011;286:31944-31952.
16. Zhao RZ, Nie HG, Su XF, Han DY, Lee A, Huang Y, Chang Y, Matalon S, Ji HL. Characterization of a novel splice variant of d ENaC subunit in human lungs. Am J Physiol Lung Cell Mol Physiol 2012;302: L1262-L1272.
17. Ji HL, Zhao RZ, Chen ZX, Shetty S, Idell S, Matalon S. δ ENaC: a novel divergent amiloride-inhibitable sodium channel. Am J Physiol Lung Cell Mol Physiol 2012;303:L1013-L1026.
18. Hummler E, Barker P, Beermann F, Gatzy J, Verdumo C, Boucher R, Rossier BC. Role of the epithelial sodium channel in lung liquid clearance. Chest 1997;111(6 suppl):113S.
19. Downs CA, Kreiner LH, Trac DQ, Helms MN. Acute effects of cigarette smoke extract on alveolar epithelial sodium channel activity and lung fluid clearance. Am J Respir Cell Mol Biol 2013;49:251-259.
20. Dekker LV, Leitges M, Altschuler G, Mistry N, McDermott A, Roes J, Segal AW. Protein kinase C-beta contributes to NADPH oxidase activation in neutrophils. Biochem J 2000;347:285-289.
21. Reddy MM, Quinton PM. ENaC activity requires CFTR channel function independently of phosphorylation in sweat duct. J Membr Biol 2005; 207:23-33.
22. Shimkets RA, Lifton R, Canessa CM. In vivo phosphorylation of the epithelial sodium channel. Proc Natl Acad Sci USA 1998;95: 3301-3305.
23. Windhager EE, Frindt G. Role of Ca11 as a regulator of Na1 permeability in epithelia. Prog Clin Biol Res 1984;168:71-75.
24. Cosentino-Gomes D, Rocco-Machado N, Meyer-Fernandes JR. Cell signaling through protein kinase C oxidation and activation. Int J Mol Sci 2012;13:10697-10721.
25. Yang J, Lane PH, Pollock JS, Carmines PK. PKC-dependent superoxide production by the renal medullary thick ascending limb from diabetic rats. Am J Physiol Renal Physiol 2009;297: F1220-F1228.
26. Yang J, Lane PH, Pollock JS, Carmines PK. Protein kinase C-dependent NAD(P)H oxidase activation induced by type 1 diabetes in renal medullary thick ascending limb. Hypertension 2010; 55:468-473.
27. Downs CA, Helms MN. Regulation of ion transport by oxidants. Am J Physiol Lung Cell Mol Physiol 2013;305:L595-L603.
28. Downs CA, Trac DQ, Kreiner LH, Eaton AF, Johnson NM, Brown LA, Helms MN. Ethanol alters alveolar fluid balance via NADPH oxidase (NOX) signaling to epithelial sodium channels (ENaC) in the lung. PLoS One 2013;8:e54750.
29. 2 signaling. Am J Physiol Lung Cell Mol Physiol 2012;302:L410-L419.
30. Deane R, Singh I, Sagare AP, Bell RD, Ross NT, LaRue B, Love R, Perry S, Paquette N, Deane RJ, et al. A multimodal RAGE-specific inhibitor reduces amyloid β-mediated brain disorder in a mouse model of Alzheimer disease. J Clin Invest 2012;122:1377-1392.
31. Fontayne A, Dang PM, Gougerot-Pocidalo MA, El-Benna J. Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 2002;41:7743-7750.
32. phox phosphorylation and translocation in activated human monocytes. J Immunol 2004;173:5730-5738.
33. Dahlin K, Mager EM, Allen L, Tigue Z, Goodglick L, Wadehra M, Dobbs L. Identifi cation of genes differentially expressed in rat alveolar type I cells. Am J Respir Cell Mol Biol 2004;31:309-316.
34. Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R, Yan SD, Brett J, Stern D. Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice: a potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 1995;96:1395-1403.
35. Schmidt AM, Weidman E, Lalla E, Yan SD, Hori O, Cao R, Brett JG, Lamster IB. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodontal Res 1996;31:508-515.
36. Demling N, Ehrhardt C, Kasper M, Laue M, Knels L, Rieber EP. Promotion of cell adherence and spreading: a novel function of RAGE, the highly selective differentiation marker of human alveolar epithelial type I cells. Cell Tissue Res 2006;323:475-488.
37. Downs CA, Kriener LH, Yu L, Eaton DC, Jain L, Helms MN. b-adrenergic agonists differentially regulate highly selective and nonselective epithelial sodium channels to promote alveolar fluid clearance in vivo. Am J Physiol Lung Cell Mol Physiol 2012;302: L1167-L1178.
38. 2 regulates lung epithelial sodium channel (ENaC) via ubiquitin-like protein Nedd8. J Biol Chem 2013;288:8136-8145.
39. Clunes LA, Davies CM, Coakley RD, Aleksandrov AA, Henderson AG, Zeman KL, Worthington EN, Gentzsch M, Kreda SM, Cholon D, et al. Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration. FASEB J 2012;26:533-545.
40. Bucciarelli LG, Wendt T, Rong L, Lalla E, Hofmann MA, Goova MT, Taguchi A, Yan SF, Yan SD, Stern DM, et al. RAGE is a multiligand receptor of the immunoglobulin superfamily: implications for homeostasis and chronic disease. Cell Mol Life Sci 2002;59: 1117-1128.
41. Wu L, Ma L, Nicholson LF, Black PN. Advanced glycation end products and its receptor (RAGE) are increased in patients with COPD. Respir Med 2011;105:329-336.
42. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, Tanji N, Lu Y, Lalla E, Fu C, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000;405: 354-360.
43. Park JY, Kim HK, Chung YE, Kim SW, Hong SK, Lee KU. Incidence and determinants of microalbuminuria in Koreans with type 2 diabetes. Diabetes Care 1998;21:530-534.
44. Wautier JL, Zoukourian C, Chappey O, Wautier MP, Guillausseau PJ, Cao R, Hori O, Stern D, Schmidt AM. Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy: soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J Clin Invest 1996;97: 238-243.
45. Cho HJ, Son SM, Jin SM, Hong HS, Shin DH, Kim SJ, Huh K, Mook-Jung I. RAGE regulates BACE1 and Abeta generation via NFAT1 activation in Alzheimer's disease animal model. FASEB J 2009;23:2639-2649.
46. Curran CS, Bertics PJ. Human eosinophils express RAGE, produce RAGE ligands, exhibit PKC-delta phosphorylation and enhanced viability in response to the RAGE ligand, S100B. Int Immunol 2011; 23:713-728.
47. Grotterod I, Maelandsmo GM, Boye K. Signal transduction mechanisms involved in S100A4-induced activation of the transcription factor NF-kappaB. BMC Cancer 2010;10:241.
48. Xu Y, Wang S, Feng L, Zhu Q, Xiang P, He B. Blockade of PKC-beta protects HUVEC from advanced glycation end products induced inflammation. Int Immunopharmacol 2010;10:1552-1559.
49. Frindt G, Windhager EE. Regulatory role of calcium in sodium transport. Prog Clin Biol Res 1984;164:403-406.
50. Frindt G, Lee CO, Yang JM, Windhager EE. Potential role of cytoplasmic calcium ions in the regulation of sodium transport in renal tubules. Miner Electrolyte Metab 1988;14:40-47.
51. Brun-Buisson C, Doyon F, Carlet J, Dellamonica P, Gouin F, Lepoutre A, Mercier JC, Offenstadt G, Ré gnier B; French ICU Group for Severe Sepsis. Incidence, risk factors, and outcome of severe sepsis and septic shock in adults: a multicenter prospective study in intensive care units. JAMA 1995;274:968-974.
52. Paletas K, Sailer X, Rizeq L, Dimitriadi A, Koliakos G, Kaloyianni M. Angiotensin-II-dependent NHE1 activation in human monocytes. J Am Soc Hypertens 2008;2:173-181.
53. Herrera M, Silva GB, Garvin JL, Angiotensin II. Angiotensin II stimulates thick ascending limb superoxide production via protein kinase C(α)-dependent NADPH oxidase activation. J Biol Chem 2010;285:21323-21328.
54. Marx N, Walcher D, Ivanova N, Rautzenberg K, Jung A, Friedl R, Hombach V, de Caterina R, Basta G, Wautier MP, et al. Thiazolidinediones reduce endothelial expression of receptors for advanced glycation end products. Diabetes 2004;53:2662-2668.