Aberrant chloride intracellular channel 4 expression contributes to endothelial dysfunction in pulmonary arterial hypertension

Circulation

Volumn 129, Issue 17, 2014, Pages 1770-1780

  Wojciak Stothard, Beata ^a   Abdul Salam, Vahitha B ^a   Lao, Ka Hou ^a   Tsang, Hilda ^a   Irwin, David C ^b   Lisk, Christina ^b   Loomis, Zoe ^b   Stenmark, Kurt R ^b   Edwards, John C ^c   Yuspa, Stuart H ^d   Howard, Luke S ^e   Edwards, Robert J ^a   Rhodes, Christopher J ^a   Gibbs, J Simon R ^e   Wharton, John ^a   Zhao, Lan ^a   Wilkins, Martin R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COLORADO   (United States)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Centre for Cancer Research   (United States)

^e NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

angiogenesis inducing agents; endothelium; hypertension, pulmonary; hypoxia inducible factor 1; nuclear factor kappaB

Indexed keywords

ADENOVIRUS VECTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CD31 ANTIGEN; ENDOTHELIN 1; F ACTIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MONOCROTALINE; MYOSIN ADENOSINE TRIPHOSPHATASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR RELA; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL JUNCTION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL STRUCTURE; CELL SURVIVAL; CHLORIDE INTRACELLULAR CHANNEL 4 GENE; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE; GENE DELETION; GENE OVEREXPRESSION; GENE TRANSFER; HEART RIGHT VENTRICLE HYPERTROPHY; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; LUNG BLOOD VESSEL; MALE; MOUSE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SYSTOLIC BLOOD PRESSURE; TANDEM MASS SPECTROMETRY; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; WILD TYPE;

ANGIOGENESIS INDUCING AGENTS; ENDOTHELIUM; HYPERTENSION, PULMONARY; HYPOXIA-INDUCIBLE FACTOR 1; NUCLEAR FACTOR-KAPPAB;

ANIMALS; CELLS, CULTURED; CHLORIDE CHANNELS; ENDOTHELIUM, VASCULAR; HUMANS; HYPERTENSION, PULMONARY; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; MUSCLE, SMOOTH, VASCULAR; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTOR RELA;

EID: 84899987572     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.006797     Document Type: Article

References (42)

1. Littler DR, Harrop SJ, Goodchild SC, Phang JM, Mynott AV, Jiang L, Valenzuela SM, Mazzanti M, Brown LJ, Breit SN, Curmi PM. The enigma of the CLIC proteins: ion channels, redox proteins, enzymes, scaffolding proteins? FEBS Lett. 2010;584:2093-2101.
2. Bohman S, Matsumoto T, Suh K, Dimberg A, Jakobsson L, Yuspa S, Claesson-Welsh L. Proteomic analysis of vascular endothelial growth factor-induced endothelial cell differentiation reveals a role for chloride intracellular channel 4 (CLIC4) in tubular morphogenesis. J Biol Chem. 2005;280:42397-42404.
3. Tung JJ, Hobert O, Berryman M, Kitajewski J. Chloride intracellular channel 4 is involved in endothelial proliferation and morphogenesis in vitro. Angiogenesis. 2009;12:209-220.
4. Chalothorn D, Zhang H, Smith JE, Edwards JC, Faber JE. Chloride intracellular channel-4 is a determinant of native collateral formation in skeletal muscle and brain. Circ Res. 2009;105:89-98.
5. Abdul-Salam VB, Wharton J, Cupitt J, Berryman M, Edwards RJ, Wilkins MR. Proteomic analysis of lung tissues from patients with pulmonary arterial hypertension. Circulation. 2010;122:2058-2067.
6. Tuder RM, Voelkel NF. Angiogenesis and pulmonary hypertension: a unique process in a unique disease. Antioxid Redox Signal. 2002;4:833-843.
7. Fernandez-Salas E, Sagar M, Cheng C, Yuspa SH, Weinberg WC. p53 and tumor necrosis factor alpha regulate the expression of a mitochondrial chloride channel protein. J Biol Chem. 1999;274:36488-36497.
8. Yao Q, Qu X, Yang Q, Wei M, Kong B. CLIC4 mediates TGF- beta1-induced fibroblast-to-myofibroblast transdifferentiation in ovarian cancer. Oncol Rep. 2009;22:541-548.
9. Suh KS, Mutoh M, Gerdes M, Yuspa SH. CLIC4, an intracellular chloride channel protein, is a novel molecular target for cancer therapy. J Investig Dermatol Symp Proc. 2005;10:105-109.
10. Spiekerkoetter E, Guignabert C, de Jesus Perez V, Alastalo TP, Powers JM, Wang L, Lawrie A, Ambartsumian N, Schmidt AM, Berryman M, Ashley RH, Rabinovitch M. S100A4 and bone morphogenetic protein- 2 codependently induce vascular smooth muscle cell migration via phospho- extracellular signal-regulated kinase and chloride intracellular channel 4. Circ Res. 2009;105:639-647, 13 p following 647.
11. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood. 2007;109:1801-1809.
12. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752-2760.
13. Ulmasov B, Bruno J, Gordon N, Hartnett ME, Edwards JC. Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway. Am J Pathol. 2009;174:1084-1096.
14. Abe K, Toba M, Alzoubi A, Ito M, Fagan KA, Cool CD, Voelkel NF, McMurtry IF, Oka M. Formation of plexiform lesions in experimental severe pulmonary arterial hypertension. Circulation. 2010;121:2747-2754.
15. Suh KS, Mutoh M, Nagashima K, Fernandez-Salas E, Edwards LE, Hayes DD, Crutchley JM, Marin KG, Dumont RA, Levy JM, Cheng C, Garfield S, Yuspa SH. The organellular chloride channel protein CLIC4/mtCLIC translocates to the nucleus in response to cellular stress and accelerates apoptosis. J Biol Chem. 2004;279:4632-4641.
16. Wojciak-Stothard B, Tsang LY, Haworth SG. Rac and Rho play opposing roles in the regulation of hypoxia/reoxygenation-induced permeability changes in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2005;288:L749-L760.
17. Fiedler LR, Bachetti T, Leiper J, Zachary I, Chen L, Renn T, Wojciak- Stothard B. The ADMA/DDAH pathway regulates VEGF-mediated angiogenesis. Arterioscler Thromb Vasc Biol. 2009;29:2117-2124.
18. Chau NM, Rogers P, Aherne W, Carroll V, Collins I, McDonald E, Workman P, Ashcroft M. Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1alpha induction in response to hypoxic stress and growth factors. Cancer Res. 2005;65:4918-4928.
19. Wojciak-Stothard B, Haworth SG. Perinatal changes in pulmonary vascular endothelial function. Pharmacol Ther. 2006;109:78-91.
20. Toshner M, Voswinckel R, Southwood M, Al-Lamki R, Howard LS, Marchesan D, Yang J, Suntharalingam J, Soon E, Exley A, Stewart S, Hecker M, Zhu Z, Gehling U, Seeger W, Pepke-Zaba J, Morrell NW. Evidence of dysfunction of endothelial progenitors in pulmonary arterial hypertension. Am J Respir Crit Care Med. 2009;180:780-787.
21. Diller GP, van Eijl S, Okonko DO, Howard LS, Ali O, Thum T, Wort SJ, Bdard E, Gibbs JS, Bauersachs J, Hobbs AJ, Wilkins MR, Gatzoulis MA, Wharton J. Circulating endothelial progenitor cells in patients with Eisenmenger syndrome and idiopathic pulmonary arterial hypertension. Circulation. 2008;117:3020-3030.
22. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, Grimminger F. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest. 2005;115:2811-2821.
23. Hess P, Clozel M, Clozel JP. Telemetry monitoring of pulmonary arterial pressure in freely moving rats. J Appl Physiol (1985). 1996;81:1027-1032.
24. Sebkhi A, Strange JW, Phillips SC, Wharton J, Wilkins MR. Phosphodiesterase type 5 as a target for the treatment of hypoxia-induced pulmonary hypertension. Circulation. 2003;107:3230-3235.
25. Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev. 2005;11:127-152.
26. Fijalkowska I, Xu W, Comhair SA, Janocha AJ, Mavrakis LA, Krishnamachary B, Zhen L, Mao T, Richter A, Erzurum SC, Tuder RM. Hypoxia inducible- factor1alpha regulates the metabolic shift of pulmonary hypertensive endothelial cells. Am J Pathol. 2010;176:1130-1138.
27. Gorlach A, Bonello S. The cross-talk between NF-kappaB and HIF-1: further evidence for a significant liaison. Biochem J. 2008;412:e17-e19.
28. Lu X, An H, Jin R, Zou M, Guo Y, Su PF, Liu D, Shyr Y, Yarbrough WG. PPM1A is a RelA phosphatase with tumor suppressor-like activity [published online ahead of print July 1, 2013]. Oncogene. doi: 10.1038/ onc.2013.246. http://www.nature.com/onc/journal/vaop/ncurrent/full/ onc2013246a.html. Accessed December 10, 2013.
29. Burton VJ, Ciuclan LI, Holmes AM, Rodman DM, Walker C, Budd DC. Bone morphogenetic protein receptor II regulates pulmonary artery endothelial cell barrier function. Blood. 2011;117:333-341.
30. Budhiraja R, Tuder RM, Hassoun PM. Endothelial dysfunction in pulmonary hypertension. Circulation. 2004;109:159-165.
31. Stenmark KR, Meyrick B, Galie N, Mooi WJ, McMurtry IF. Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. Am J Physiol Lung Cell Mol Physiol. 2009;297:L1013-L1032.
32. Bowers R, Cool C, Murphy RC, Tuder RM, Hopken MW, Flores SC, Voelkel NF. Oxidative stress in severe pulmonary hypertension. Am J Respir Crit Care Med. 2004;169:764-769.
33. Burke DL, Frid MG, Kunrath CL, Karoor V, Anwar A, Wagner BD, Strassheim D, Stenmark KR. Sustained hypoxia promotes the development of a pulmonary artery-specific chronic inflammatory microenvironment. Am J Physiol Lung Cell Mol Physiol. 2009;297:L238-L250.
34. Machado RD, Eickelberg O, Elliott CG, Geraci MW, Hanaoka M, Loyd JE, Newman JH, Phillips JA 3rd, Soubrier F, Trembath RC, Chung WK. Genetics and genomics of pulmonary arterial hypertension. J Am Coll Cardiol. 2009;54(suppl):S32-S42.
35. Morty RE, Nejman B, Kwapiszewska G, Hecker M, Zakrzewicz A, Kouri FM, Peters DM, Dumitrascu R, Seeger W, Knaus P, Schermuly RT, Eickelberg O. Dysregulated bone morphogenetic protein signaling in monocrotaline-induced pulmonary arterial hypertension. Arterioscler Thromb Vasc Biol. 2007;27:1072-1078.
36. Kourembanas S, Marsden PA, McQuillan LP, Faller DV. Hypoxia induces endothelin gene expression and secretion in cultured human endothelium. J Clin Invest. 1991;88:1054-1057.
37. Tuder RM, Chacon M, Alger L, Wang J, Taraseviciene-Stewart L, Kasahara Y, Cool CD, Bishop AE, Geraci M, Semenza GL, Yacoub M, Polak JM, Voelkel NF. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol. 2001;195:367-374.
38. Yeh WL, Lu DY, Lin CJ, Liou HC, Fu WM. Inhibition of hypoxia-induced increase of blood-brain barrier permeability by YC-1 through the antagonism of HIF-1alpha accumulation and VEGF expression. Mol Pharmacol. 2007;72:440-449.
39. Skuli N, Simon MC. HIF-1alpha versus HIF-2alpha in endothelial cells and vascular functions: is there a master in angiogenesis regulation? Cell Cycle. 2009;8:3252-3253.
40. Skuli N, Liu L, Runge A, Wang T, Yuan L, Patel S, Iruela-Arispe L, Simon MC, Keith B. Endothelial deletion of hypoxia-inducible factor-2alpha (HIF-2alpha) alters vascular function and tumor angiogenesis. Blood. 2009;114:469-477.
41. Shukla A, Yuspa SH. CLIC4 and Schnurri-2: a dynamic duo in TGF-beta signaling with broader implications in cellular homeostasis and disease. Nucleus. 2010;1:144-149.
42. Hu X, Janssen WE, Moscinski LC, Bryington M, Dangsupa A, Rezai- Zadeh N, Babbin BA, Zuckerman KS. An IkappaBalpha inhibitor causes leukemia cell death through a p38 MAP kinase-dependent, NF-kappaB-independent mechanism. Cancer Res. 2001;61:6290-6296.