Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway

American Journal of Pathology

Volumn 174, Issue 3, 2009, Pages 1084-1096

  Ulmasov, Barbara ^a   Bruno, Jonathan ^b   Gordon, Nicarter ^b   Hartnett, M Elizabeth ^b   Edwards, John C ^b  

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

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; CHLORIDE INTRACELLULAR CHANNEL PROTEIN 4; FIBRIN; MATRIGEL; UNCLASSIFIED DRUG;

ACIDIFICATION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; LYSOSOME; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN TOXICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA BLOOD VESSEL; WILD TYPE;

EID: 62549164694     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080625     Document Type: Article

References (42)

1. Lubarsky B, Krasnow MA: Tube morphogenesis: making and shaping biological tubes. Cell 2003, 112:19-28
2. Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE, Weinstein BM: Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 2006, 442:453-456
3. Béraud-Dufour S, Balch W: A journey through the exocytic pathway. J Cell Sci 2002, 115:1779-1780
4. Mellman I: The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 1992, 172:39-45
5. Ashley RH: Challenging accepted ion channel biology: p64 and the CLIC family of putative intracellular anion channel proteins. Mol Membr Biol 2003, 20:1-11
6. Berry KL, Bulow HE, Hall DH, Hobert O: AC. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 2003, 302:2134-2137
7. 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
8. Tulk BM, Schlesinger PH, Kapadia SA, Edwards JC: CLIC-1 functions as a chloride channel when expressed and purified from bacteria. J Biol Chem 2000, 275:26986-26993
9. Bowman EJ, Siebers A, Altendorf K: Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 1988, 85:7972-7976
10. Albig AR, Neil JR, Schiemann WP: Fibulins 3 and 5 antagonize tumor angiogenesis in vivo. Cancer Res 2006, 66:2621-2629
11. Yi M, Sakai T, Fassler R, Ruoslahti E: Antiangiogenic proteins require plasma fibronectin or vitronectin for in vivo activity. Proc Natl Acad Sci USA 2003, 100:11435-11438
12. McColm JR, Geisen P, Peterson LJ, Hartnett ME: Exogenous leukemia inhibitory factor (LIF) attenuates retinal vascularization reducing cell proliferation not apoptosis. Exp Eye Res 2006, 83:438-446
13. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R, D'Amore PA: Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 1994, 35:101-111
14. Chikaraishi Y, Shimazawa M, Hara H: New quantitative analysis, using high-resolution images, of oxygen-induced retinal neovascularization in mice. Exp Eye Res 2007, 84:529-536
15. Lim YC, Garcia-Cardena G, Allport JR, Zervoglos M, Connolly AJ, Gimbrone Jr MA, Luscinskas FW: Heterogeneity of endothelial cells from different organ sites in T-cell subset recruitment. Am J Pathol 2003, 162:1591-1601
16. Bayless KJ, Salazar R, Davis GE: RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha (v) beta(3) and alpha(5)beta(1) integrins. Am J Pathol 2000, 156:1673-1683
17. Bayless KJ, Davis GE: The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 2002, 115:1123-1136
18. Ulmasov B, Bruno J, Woost PG, Edwards JC: Tissue and subcellular distribution of CLIC1. BMC Cell Biol 2007, 8:8
19. Shah N, Ulmasov B, Waheed A, Becker T, Makani S, Svichar N, Chesler M, Sly WS: Carbonic anhydrase IV and XIV knockout mice: roles of the respective carbonic anhydrases in buffering the extracellular space in brain. Proc Natl Acad Sci USA 2005, 102:16771-16776
20. Armitage P: Statistical Methods in Medical Research, ed 4. Oxford, Blackwell Scientific Publications, 1971, pp 99-216
21. Bunting M, Bernstein KE, Greer JM, Capecchi MR, Thomas KR: Targeting genes for self-excision in the germ line. Genes Dev 1999, 13:1524-1528
22. Auerbach R, Lewis R, Shinner B, Kubai L, Akhtar N: Angiogenesis assays: a critical overview. Clin Chem 2003, 49:32-40
23. Uemura A, Kusuhara S, Katsuta H, Nishikawa S: Angiogenesis in the mouse retina: a model system for experimental manipulation. Exp Cell Res 2006, 312:676-683
24. Chen J, Smith LE: Retinopathy of prematurity. Angiogenesis 2007, 10:133-140
25. Davis GE, Camarillo CW: An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 1996, 224:39-51
26. Bach TL, Barsigian C, Chalupowicz DG, Busler D, Yaen CH, Grant DS, Martinez J: VE-cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp Cell Res 1998, 238:324-334
27. Yang S, Graham J, Kahn JW, Schwartz EA, Gerritsen ME: Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am J Pathol 1999, 155:887-895
28. Davis GE, Bayless KJ: An integrin and Rho GTPase-dependent pinocytic vacuole mechanism controls capillary lumen formation in collagen and fibrin matrices. Microcirculation 2003, 10:27-44
29. Zen K, Biwersi J, Perisasamy N, Verkman A: Second messengers regulate endosomal acidification in Swiss 3T3 fibroblasts. J Cell Biol 1992, 119:99-110
30. van Weert AWM, Dunn KW, Gueze HJ, Maxfield FR, Stoorvogel W: Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995, 130:821-834
31. Haughland RP: Handbook of Fluorescent Probes and Research Products, ed 9. Eugene, Molecular Probes, 2002, p 844
32. Berry KL, Hobert O: Mapping functional domains of chloride intracellular channel (CLIC) proteins in vivo. J Mol Biol 2006, 359:1316-1333
33. Gasser KW, DiDomenico J, Hoper U: Secretatgogues activate chloride transport pathways in pancreatic zymogen granules. Am J Physiol 1988, 254:G93-G99
34. Dayanithi G, Nordmann JJ: Chloride and magnesium dependence of vasopressin release from rat permeabilized neurohypophysial nerve endings. Neurosci Lett 1989, 106:305-309
35. Fuller CM, Eckhardt L, Schultz I: Ionic and osmotic dependence of secretion from permeabilized acini of the rat pancreas. Pflugers Arch 1989, 413:385-394
36. Takuma T, Ichida T: Roles of potassium and chloride ions in cAMP-mediated amylase exocytosis from rat parotid acini. Cell Struct Funct 1991, 16:405-409
37. Berryman M, Bretscher A: 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 2000, 11:1509-1521
38. Edwards JC, Kapadia S: Regulation of the bovine kidney microsomal chloride channel p64 by p59fyn, a src family tyrosine kinase. J Biol Chem 2000, 275:31826-31832
39. Suginta W, Karoulias N, Aitkin A, Ashley RH: Chloride intracellular channel protein CLIC4 (p64H1) binds directly to brain dynamin I in a complex containing actin, tubulin and 14-3-3 isoforms. Biochem J 2001, 359:55-64
40. Shanks RA, Larocca MC, Berryman M, Edwards JC, Urushidani T, Navarre J, Goldenring JR: AKAP350 at the Golgi apparatus. J Biol Chem 2002, 277:40973-40980
41. Park JS, Lee KM, Jeong MS, Jin GE, Jang SB: The binding of human CLIC1 with SEDL and its characterization in vitro. Bull Korean Chem Soc 2007, 28:574-580
42. Edwards JC: A novel member of the p64 Cl channel family: subcellular distribution and nephron segment-specific expression. Am J Physiol 1999, 276:F398-F408