Structure and function of CLCA proteins

Physiological Reviews

Volumn 85, Issue 3, 2005, Pages 1061-1092

  Loewen, Matthew E ^a   Forsyth, George W ^a,b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b NONE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; BETA4 INTEGRIN; BINDING PROTEIN; CHLORIDE CHANNEL; MEMBRANE PROTEIN; PROTEIN; PROTEIN BESTROPHIN; PROTEIN CLCA; UNCLASSIFIED DRUG;

APOPTOSIS; ASTHMA; BLOOD PRESSURE; BLOOD VESSEL TONE; CANCER INHIBITION; CANCER INVASION; CELL ADHESION; CELL CYCLE; CHLORIDE CONDUCTANCE; COW; CYSTIC FIBROSIS; EPITHELIUM; GENE CLUSTER; GENE LOCUS; HUMAN; HYPERTENSION; ION TRANSPORT; METASTASIS; MOLECULAR CLONING; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RETINOPATHY; REVIEW; SECRETORY CELL; SMALL INTESTINE; SMOOTH MUSCLE; TRACHEA; TUMOR CELL;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM SIGNALING; CATTLE; CHLORIDE CHANNELS; CLONING, MOLECULAR; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN CONFORMATION; SWINE;

EID: 21244486285     PISSN: 00319333     EISSN: None     Source Type: Journal    
DOI: 10.1152/physrev.00016.2004     Document Type: Review

References (215)

1. Abdel-Ghany M, Cheng HC, Elble RC, Lin H, DiBiasio J, and Pauli BU. The interacting binding domains of the beta-4 Integrin and calcium-activated chloride channels (CLCAs) in metastasis. J Biol Chem 278: 49406-49416, 2003.
2. Abdel-Ghany M, Cheng HC, Elble RC, and Pauli BU. The breast cancer beta-4 integrin and endothelial human CLCA2 mediate lung metastasis. J Biol Chem 276: 25438-25446, 2001.
3. Abdel-Ghany M, Cheng HC, Elble RC, and Pauli BU. Focal adhesion kinase activated by beta-4 integrin ligation to mCLCA1 mediates early metastatic growth. J Biol Chem 277: 34391-34400, 2002.
4. Agnel M, Vermat T, and Culouscou JM. Identification of three novel members of the calcium-dependent chloride channel (CaCC) family predominantly expressed in the digestive tract and trachea. FEBS Lett 455: 295-301, 1999.
5. Alberola-Ila J and Hernandez-Hoyos G. The Ras/MAPK cascade and the control of positive selection. Immunol Rev 191: 79-96, 2003.
6. Allikmets R, Seddon JM, Bernstein PS, Hutchinson A, Atkinson A, Sharma S, Gerrard B, Li W, Metzker ML, Wadelius C, Caskey CT, Dean M, and Petrukhin K. Evaluation of the Best disease gene in patients with age-related macular degeneration and other maculopathies. Hum Genet 104: 449-453, 1999.
7. Amberg GC, Bonev AD, Rossow CF, Nelson MT, and Santana LF. Modulation of the molecular composition of large conductance, Ca(2+) activated K(+) channels in vascular smooth muscle during hypertension. J Clin Invest 112: 717-724, 2003.
8. Amberg GC and Santana LF. Downregulation of the BK channel betal subunit in genetic hypertension. Circ Res 93: 965-971, 2003.
9. Anderson MP and Welsh MJ. Calcium and cAMP activate different chloride channels in the apical membrane of normal and cystic flbrosis epithelia. Proc Natl Acad Sci USA 88: 6003-6007, 1991.
10. Arima K, Umeshita-Suyama R, Sakata Y, Akaiwa M, Mao XQ, Enomoto T, Dake Y, Shimazu S, Yamashita T, Sugawara N, Brodeur S, Geha R, Puri RK, Sayegh MH, Adra CN, Hamasaki N, Hopkin JM, Shirakawa T, and Izuhara K. Upregulation of IL-13 concentration in vivo by the IL13 variant associated with bronchial asthma. J Allergy Clin Immunol 109: 980-987, 2002.
11. Atherton H, Mesher J, Poll CT, and Danahay H. Preliminary pharmacological characterisation of an interleukin-13-enhanced calcium-activated chloride conductance in the human airway epithelium. Naunyn-Schmiedebergs Arch Pharmacol 367: 214-217, 2003.
12. Atherton HC, Jones G, and Danahay H. IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am J Physiol Lung Cell Mol Physiol 285: L730-L739, 2003.
13. Bakall B, Marknell T, Ingvast S, Koisti MJ, Sandgren O, Li W, Bergen AA, Andreasson S, Rosenberg T, Petrukhin K, and Wadelius C. The mutation spectrum of the bestrophin protein-functional implications. Hum Genet 104: 383-389, 1999.
14. Beckley JR, Pauli BU, and Elble RC. Re-expression of detachment-inducible chloride channel mCLCAo suppresses growth of metastatic breast cancer cells. J Biol Chem. In press.
15. Benson WE, Kolker AE, Enoch JM, Van Loo JA Jr, and Honda Y. Best's vitelliform macular dystrophy. Am J Ophthalmol 79: 59-66, 1975.
16. Bertrand CA, Danahay H, Poll CT, Laboisse C, Hopfer U, and Bridges RJ. Niflumic acid inhibits ATP-stimulated exocytosis in a mucin-secreting epithelial cell line. Am J Physiol Cell Physiol 286: C247-C255, 2003.
17. - transport mechanisms in bovine pigment epithelium that could modulate subretinal space volume and composition. J Physiol 475: 401-417, 1994.
18. +-ATPase and nasal potential in pseudohypoaldosteronism. Clin Endocrinol 56: 575-580, 2002.
19. - conductances mediate CP secretion in a mouse renal inner medullary collecting duct cell line. J Physiol 523: 325-338, 2000.
20. Boucher RC, Cheng EH, Paradiso AM, Stutts MJ, Knowles MR, and Earp HS. Chloride secretory response of cystic fibrosis human airway epithelia. Preservation of calcium but not protein kinase C- and A-dependent mechanisms. J Clin Invest 84: 1424-1431, 1989.
21. Bremner SA, Carey IM, DeWilde S, Richards N, Maier WC, Hilton SR, Strachan DP, and Cook DG. Early-life exposure to antibacterials and the subsequent development of hayfever in childhood in the UK: case-control studies using the General Practice Research Database and the Doctors' Independent Network. Clin Exp Allergy 33: 1518-1525, 2003.
22. Brenner C and Kroemer G. Apoptosis. Mitochondria-the death signal integrators. Science 289: 1150-1151, 2000.
23. Brenner R, Perez GJ, Bonev AD, Eckman DM, Kosek JC, Wiler SW, Patterson AJ, Nelson MT, and Aldrich RW. Vaso-regulation by the betal subunit of the calcium-activated potassium channel. Nature 407: 870-876, 2000.
24. Breyer MD and Harris RC. Cyclooxygenase 2 and the kidney. Curr Opin Nephrol Hypertens 10: 89-98, 2001.
25. Britton FC, Ohya S, Horowitz B, and Greenwood IA. Comparison of the properties of CLCA1 generated currents and 1[Cl(Ca)] in murine portal vein smooth muscle cells. J Physiol 539: 107-117, 2002.
26. Brusselle GG, Kips JC, Tavernier JH, van der Heyden JG, Cuvelier CA, Pauwels RA, and Bluethmann H. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin Exp Allergy 24: 73-80, 1994.
27. Busse WW and Lemanske RF Jr. Asthma. N Engl J Med 344: 350-362, 2001.
28. Caldwell GM, Kakuk LE, Griesinger IB, Simpson SA, Nowak NJ, Small KW, Maumenee IH, Rosenfeld PJ, Sieving PA, Shows TB, and Ayyagari R. Bestrophin gene mutations in patients with Best vitelliform macular dystrophy. Genomics 58: 98-101, 1999.
29. Cheng HF, Wang JL, Zhang MZ, Miyazaki Y, Ichikawa I, McKanna JA, and Harris RC. Angiotensin II attenuates renal cortical cyclooxygenase-2 expression. J Clin Invest 103: 953-961, 1999.
30. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, and Smith AE. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834, 1990.
31. Chipperfield AR and Harper AA. Chloride in smooth muscle. Prog Biophys Mol Biol 74: 175-221, 2000.
32. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr, and Roccella EJ. Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 42: 1206-1252, 2003.
33. Chung J, Bachelder RE, Lipscomb EA, Shaw LM, and Mercurio AM. Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J Cell Biol 158: 165-174, 2002.
34. Clarke LL, Grubb BR, Gabriel SE, Smithies O, Koller BH, and Boucher RC. Defective epithelial chloride transport in a gene-targeted mouse model of cystic fibrosis. Science 257: 1125-1128, 1992.
35. Connon CJ, Yamasaki K, Kawasaki S, Quantock AJ, Koizumi N, and Kinoshita S. Calcium-activated chloride channel-2 in human epithelia. J Histochem Cytochem 52: 415-418, 2004.
36. Cotton CU and Russ L. Characterization of epithelial ion transport. In: Epithelial Transport: A Guide to Methods and Experimental Analysis (1st ed.), edited by Wills NKRL and Lewis SA. London: Chapman & Hall, 1996, p. 70-92.
37. Cotton CU, Stutts MJ, Knowles MR, Gatzy JT, and Boucher RC. Abnormal apical cell membrane in cystic flbrosis respiratory epithelium. An in vitro electrophysiologic analysis. J Clin Invest 79: 80-85, 1987.
38. Cross HE and Bard L. Electro-oculography in Best's macular dystrophy. Am J Ophthalmol 77: 46-50, 1974.
39. Cunningham SA, Awayda MS, Bubien JK, Ismailov II, Arrate MP, Berdiev BK, Benos DJ, and Fuller CM. Cloning of an epithelial chloride channel from bovine trachea. J Biol Chem 270: 31016-31026, 1995.
40. Danahay H, Atherton H, Jones G, Bridges RJ, and Poll CT. Interleukin-13 induces a hypersecretory ion transport phenotype in human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 282: L226-L236, 2002.
41. Dans M, Gagnoux-Palacios L, Blaikie P, Klein S, Mariotti A, and Giancotti FG. Tyrosine phosphorylation of the beta 4 integrin cytoplasmic domain mediates She signaling to extracellular signal-regulated kinase and antagonizes formation of hemidesmosomes. J Biol Chem 276: 1494-1502, 2001.
42. - binding motif on aen-related proteins to stimulate mitogenesis. Eur J Immunol 22: 1165-1171, 1992.
43. + channels in human T lymphocytes: a role in mitogenesis? Nature 307: 465-468, 1984.
44. Devi L. Consensus sequence for processing of peptide precursors at monobasic sites. FEBS Lett 280: 189-194, 1991.
45. Downward J. Control of ras activation. Cancer Surv 27: 87-100, 1996.
46. Eksandh L, Bakall B, Bauer B, Wadelius C, and Andreasson S. Best's vitelliform macular dystrophy caused by a new mutation (Val89Ala) in the VMD2 gene. Ophthalmic Genet 22: 107-115, 2001.
47. El Biaze M, Boniface S, Koscher V, Mamessier E, Dupuy P, Milhe F, Ramadour M, Vervloet D, and Magnan A. T cell activation, from atopy to asthma: more a paradox than a paradigm. Allergy 58: 844-853, 2003.
48. Elble RC, Ji G, Nehrke K, DeBiasio J, Kingsley PD, Kotlikoff MI, and Pauli BU. Molecular and functional characterization of a murine calcium-activated chloride channel expressed in smooth muscle. J Biol Chem 277: 18586-18591, 2002.
49. Elble RC and Pauli BU. Tumor suppression by a proapoptotic calcium-activated chloride channel in mammary epithelium. J Biol Chem 276: 40510-40517, 2001.
50. Elble RC, Widom J, Gruber AD, Abdel-Ghany M, Levine R, Goodwin A, Cheng HC, and Pauli BU. Cloning and characterization of lung-endothelial cell adhesion molecule-1 suggest it is an endothelial chloride channel. J Biol Chem 272: 27853-27861, 1997.
51. Emsley J, King SL, Bergelson JM, and Liddington RC. Crystal structure of the I domain from integrin alpha2beta1. J Biol Chem 272: 28512-28517, 1997.
52. Emsley J, Knight CG, Farndale RW, Barnes MJ, and Liddington RC. Structural basis of collagen recognition by integrin alpha2betal. Cell 101: 47-56, 2000.
53. Espinosa M, Noe G, Troncoso C, Ho SB, and Villalon M. Acidic pH and increasing [Ca(2+)] reduce the swelling of mucins in primary cultures of human cervical cells. Hum Reprod 17: 1964-1972, 2002.
54. Evans SR, Thoreson WB, and Beck CL. Molecular and functional analysis of two new CLCA family members from mouse intestine. J Biol Chem. In press.
55. Fagard RH and Van den Enden M. Treatment and blood pressure control in isolated systolic hypertension vs diastolic hypertension in primary care. J Hum Hypertens 17: 681-687, 2003.
56. Fong P, Argent BE, Guggino WB, and Gray MA. Characterization of vectorial chloride transport pathways in the human pancreatic duct adenocarcinoma cell line HPAF. Am, J Physiol Cell Physiol 285: C433-C445, 2003.
57. Foster PS, Hogan SP, Ramsay AJ, Matthaei KI, and Young IG. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity and lung damage in a mouse asthma model. J Exp Med 183: 195-201, 1996.
58. Frangieh GT, Green WE, and Fine SL. A histopathologic study of Best's macular dystrophy. Arch Ophthalmol 100: 1115-1121, 1982.
59. Fuller CM and Benos DJ. Ca(2-)-activated Cl(-) channels: a newly emerging anion transport family. News Physiol Sci 15: 165-171, 2000.
60. Fuller CM, Ji HL, Tousson A, Elble RC, Pauli BU, and Benos DJ. Ca(2+)-activated Cl(-) channels: a newly emerging anion transport family. Pflügers Arch 443 Suppl 1: S107-S110, 2001.
61. Gabriel SE and Forsyth GW. Candidate proteins for conductive chloride transport in porcine ileal brush-border membrane. J Biol Chem 266: 17764-17769, 1991.
62. - conductance in the apical membrane of murine tracheal epithelial cells. J Biol Chem 275: 35028-35033, 2000.
63. Gabriel SE, Racette KJ, Gaspar KJ, and Forsyth GW. Inhibition of ileal brush-border chloride conductance by specific anti-body. J Membr Biol 129: 323-328, 1992.
64. Gallemore RP, Griff ER, and Steinberg RH. Evidence in support of a photoreceptoral origin for the "light-peak substance." Invest Ophthalmol Vis Sci 29: 566-571, 1988.
65. Gallemore RP, Steinberg RH, and Griff ER. Effects of DIDS on the chick retinal pigment epithelium. II. Mechanism of the light peak and other responses originating at the basal membrane. J Neurosci 9: 1977-1984, 1989.
66. Gambaletta D, Marchetti A, Benedetti L, Mercuric AM, Sacchi A, and Falcioni R. Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J Biol Chem 275: 10604-10610, 2000.
67. Gandhi R, Elble RC, Gruber AD, Schreur KD, Ji HL, Fuller CM, and Pauli BU. Molecular and functional characterization of a calcium-sensitive chloride channel from mouse lung. J Biol Chem 273: 32096-32101, 1998.
68. Gaspar KJ, Racette KJ, Gordon JR, Loewen ME, and Forsyth GW. Cloning a chloride conductance mediator from the apical membrane of porcine ileal enterocytes. Physiol Gen 3: 101-111, 2000.
69. Ghosh S, Mendoza T, Ortiz LA, Hoyle GW, Fermin CD, Brody AR, Friedman M, and Morris GF. Bleomycin sensitivity of mice expressing dominant-negative p53 in the lung epithelium. Am J Respir Crit Care Med 166: 890-897, 2002.
70. Goetz DJ, el-Sabban ME, Hammer DA, and Pauli BU. Lu-ECAM-1-mediated adhesion of melanoma cells to endothelium under conditions of flow. Int J Cancer 65: 192-199, 1996.
71. Gottlieb RA and Dosanjh A. Mutant cystic fibrosis transmembrane conductance regulator inhibits acidification and apoptosis in C127 cells: possible relevance to cystic fibrosis. Proc Natl Acad Sci USA 93: 3587-3591, 1996.
72. Greenberg SG, Lorenz JN, He XR, Schnermann JB, and Briggs JP. Effect of prostaglandin synthesis inhibition on macula densa-stimulated renin secretion. Am J Physiol Renal Fluid Electrolyte Physiol 265: F578-F583, 1993.
73. Greenwood IA, Miller LJ, Ohya S, and Horowitz B. The large conductance potassium channel beta-subunit can interact with and modulate the functional properties of a calcium-activated chloride channel, CLCA1. J Biol Chem 277: 22119-22122, 2002.
74. - secretion in nasal epithelia of CF mice. Am J Physiol Cell Physiol 266: C1478-C1483, 1994.
75. - channel proteins. Genomics 54: 200-214, 1998.
76. Gruber AD, Elble RC, and Pauli BU. Discovery and cloning of the CLCA gene family. In: Calcium-Activated, Chloride Channels, edited by Fuller CM. San Diego, CA: Academic, 2002, p. 367-387.
77. Gruber AD, Gandhi R, and Pauli BU. The murine calcium-sensitive chloride channel (mCaCC) is widely expressed in secretory epithelia and in other select tissues. Histochem Cell Biol 110: 43-49, 1998.
78. - channels. Biochim Biophys Acta 1444: 418-423, 1999.
79. 2+-activated chloride channel CLCA2. Cancer Res 59: 5488-5491, 1999.
80. Gruber AD, Schreur KD, Ji HL, Fuller CM, and Pauli BU. Molecular cloning and transmembrane structure of hCLCA2 from human lung, trachea, and mammary gland. Am J Physiol Cell Physiol 276: C1261-C1270, 1999.
81. 2+ dependence and physiological implication. Cell Calcium 21: 421-429, 1997.
82. Harris RC and Breyer MD. Physiological regulation of cyclooxygenase-2 in the kidney. Am J Physiol Renal Physiol 281: F1-F11, 2001.
83. Hauber HP, Manoukian JJ, Nguyen LH, Sobol SE, Levitt RC, Holroyd KJ, McElvaney NG, Griffin S, and Hamid Q. Increased expression of interleukin-9, interleukin-9 receptor, and the calcium-activated chloride channel hCLCA1 in the upper airways of patients with cystic fibrosis. Laryngoscope 113: 1037-1042, 2003.
84. Hauber HP, Tsicopoulos A, Wallaert B, Griffin S, McElvaney NG, Daigneault P, Mueller Z, Olivenstein R, Holroyd KJ, Levitt RC, and Hamid Q. Expression of hCLCA1 in cystic fibrosis lungs is associated with mucus overproduction. Eur Respir J 23: 846-850, 2004.
85. Hirakawa Y, Gericke M, Cohen RA, and Bolotina VM. Ca(2+)-dependent Cl(-) channels in mouse and rabbit aortic smooth muscle cells: regulation by intracellular Ca(2+) and NO. Am J Physiol Heart Circ Physiol 277: H1732-H1744, 1999.
86. Hobom M, Dai S, Marais E, Lacinova L, Hofmann F, and Klugbauer N. Neuronal distribution and functional characterization of the calcium channel alpha(2)delta-2 subunit. Eur J Neurosci 12: 1217-1226, 2000.
87. Hoggard N, Hey Y, Brintnell B, James L, Jones D, Mitchell E, Weissenbach J, and Varley JM. Identification and cloning in yeast artificial chromosomes of a region of elevated loss of heterozygosity on chromosome 1p31.1 in human breast cancer. Genomics 30: 233-243, 1995.
88. - channel 1 (CaCC1) gene in the asthmatic airway. Am J Respir Crit Care Med 165: 1132-1136, 2002.
89. Hughes AD. Calcium channels in vascular smooth muscle cells. J Vasc Res 32: 353-370, 1995.
90. Humbert M, Durham SR, Ying S, Kimmitt P, Barkans J, Assoufi B, Pfister R, Menz G, Robinson DS, Kay AB, and Corrigan CJ. IL-4 and IL-5 mRNA and protein in bronchial biopsies from patients with atopic and nonatopic asthma: evidence against "intrinsic" asthma being a distinct immunopathologic entity. Am J Respir Crit Care Med 154: 1497-1504, 1996.
91. Jackson WF. Ion channels and vascular tone. Hypertension 35: 173-178, 2000.
92. Jaggar JH, Porter VA, Lederer WJ, and Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol 278: C235-C256, 2000.
93. Kad NM, Rovner AS, Fagnant PM, Joel PB, Kennedy GG, Patlak JB, Warshaw DM, and Trybus KM. A mutant heterodimeric myosin with one inactive head generates maximal displacement. J Cell Biol 162: 481-488, 2003.
94. - channels in corpus cavernosum smooth muscle: a novel mechanism for control of penile erection. J Appl Physiol 94: 301-313, 2003.
95. Keegan LP, Haerry TE, Crotty DA, Packer AI, Wolgemuth DJ, and Gehring WJ. A sequence conserved in vertebrate Hox gene introns functions as an enhancer regulated by posterior homeotic genes in Drosophila imaginal discs. Mech Dev 63: 145-157, 1997.
96. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, Chakravarti A, Buchwald M, and Tsui LC. Identification of the cystic fibrosis gene: genetic analysis. Science 245: 1073-1080, 1989.
97. Kerem E, Bistritzer T, Hanukoglu A, Hofmann T, Zhou Z, Bennett W, MacLaughlin E, Barker P, Nash M, Quittell L, Boucher R, and Knowles MR. Pulmonary epithelial sodium-channel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med 341: 156-162, 1999.
98. Kim JA, Kang YS, Lee SH, Lee EH, Yoo BH, and Lee YS. Glibenclamide induces apoptosis through inhibition of cystic fibrosis transmembrane conductance regulator (CFTR) Cl(-) channels and intracellular Ca(2+) release in HepG2 human hepatoblastoma cells. Biochem Biophys Res Commun 261: 682-688, 1999.
99. - channels in the mechanism of apoptosis induced by cyclosporin A in a human hepatoma cell line. Biochem Biophys Res Commun 309: 291-297, 2003.
100. Kim MO, Yun SJ, Kim IS, Sohn S, and Lee EH. Transforming growth factor-beta-inducible gene-h3 [beta(ig)-h3] promotes cell adhesion of human astrocytoma cells in vitro: implication of alpha6beta4 integrin. Neurosci Lett 336: 93-96, 2003.
101. Kirk KL, Halm DR, and Dawson DC. Active sodium transport by turtle colon via an electrogenic Na-K exchange pump. Nature 287: 237-239, 1980.
102. Klaassen CHW and Depont J. Gastric ATPase. Cell Physiol Biochem 4: 115-134, 1994.
103. Komiya T, Tanigawa Y, and Hirohashi S. Cloning and identification of the gene gob-5, which is expressed in intestinal goblet cells in mice. Biochem Biophys Res Commun 255: 347-351, 1999.
104. Kramer F, White K, Pauleikhoff D, Gehrig A, Passmore L, Rivera A, Rudolph G, Kellner U, Andrassi M, Lorenz B, Rohrschneider K, Blankenagel A, Jurklies B, Schilling H, Schutt F, Holz FG, and Weber BH. Mutations in the VMD2 gene are associated with juvenile-onset vitelliform macular dystrophy (Best disease) and adult vitelliform macular dystrophy but not age-related macular degeneration. Eur J Hum Genet 8: 286-292, 2000.
105. + conductance in cystic-fibrosis. Pflugers Arch 431: 1-9, 1995.
106. Lapis K, Paku S, and Liotta LA. Endothelialization of embolized tumor cells during metastasis formation. Clin Exp Metastasis 6: 73-89, 1988.
107. Lee D, Ha S, Kho Y, Kim J, Cho K, Baik M, and Choi Y. Induction of mouse Ca(2+)-sensitive chloride channel 2 gene during involution of mammary gland. Biochem Biophys Res Commun 264: 933-937, 1999.
108. Leverkoehne I and Gruber AD. Assignment of the murine calcium-activated chloride channel genes Clca1 and Clca3 (alias gob-5) to chromosome 3 band H2-H3 using somatic cell hybrids. Cytogenet Cell Genet 88: 208-209, 2000.
109. Leverkoehne I and Gruber AD. The murine mCLCA3 (alias gob-5) protein is located in the mucin granule membranes of intestinal, respiratory, and uterine goblet cells. J Histochem Cytochem 50: 829-838, 2002.
110. Leverkoehne I, Horstmeier BA, von Samson-Himmelstjerna G, Scholte BJ, and Gruber AD. Real-time RT-PCR quantitation of mCLCA1 and mCLCA2 reveals differentially regulated expression in pre- and postnatal murine tissues. Histochem Cell Biol 118: 11-17, 2002.
111. Lewis SA. Epithelial structure and function. In: Epithelial Transport: A Guide to Methods and Experimental Analysis (1st ed.), edited by Wills NKRL and Lewis SA. London: Chapman & Hall, 1996, p. 1-20.
112. Li X, Cowell JK, and Sossey-Alaoui K. CLCA2 tumour suppressor gene in 1p31 is epigenetically regulated in breast cancer. Oncogene 23: 1474-1480, 2004.
113. Loewen ME, Bekar LK, Gabriel SE, Walz W, and Forsyth GW. pCLCA1 becomes a cAMP-dependent chloride conductance mediator in Caco-2 cells. Biochem Biophys Res Commun 298: 531-536, 2002.
114. Loewen ME, Bekar LK, Walz W, Forsyth GW, and Gabriel SE. pCLCA1 lacks inherent chloride channel activity in an epithelial colon carcinoma cell line. Am J Physiol Gastrointest Liver Physiol 287: G33-G41, 2004.
115. Loewen ME, Gabriel SE, and Forsyth GW. The calcium-dependent chloride conductance mediator pCLCA1. Am J Physiol Cell Physiol 283: C412-C421, 2002.
116. Loewen ME, MacDonald DW, Gaspar KJ, and Forsyth GW. Isoform-specific exon skipping in a variant form of ClC-2. Biochim Biophys Acta 1493: 284-288, 2000.
117. Loewen ME, Smith NK, Hamilton DL, Grahn BH, and Forsyth GW. CLCA protein and chloride transport in canine retinal pigment epithelium. Am J Physiol Cell Physiol 285: C1314-C1321, 2003.
118. Lotery AJ, Munier FL, Fishman GA, Weleber RG, Jacobson SG, Affatigato LM, Nichols BE, Schorderet DF, Sheffield VC, and Stone EM. Allelic variation in the VMD2 gene in Best disease and age-related macular degeneration. Invest Ophthalmol Vis Sci 41: 1291-1296, 2000.
119. Lyczak JB, Cannon CL, Pier GB, Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, and Smith AE. Lung infections associated with cystic fibrosis. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Clin Microbiol Rev 15: 194-222, 2002.
120. Mainiero F, Pepe A, Wary KK, Spinardi L, Mohammadi M, Schlessinger J, and Giancotti FG. Signal transduction by the alpha 6 beta 4 integrin: distinct beta 4 subunit sites mediate recruitment of Shc/Grb2 and association with the cytoskeleton of hemidesmosomes. EMBO J 14: 4470-4481, 1995.
121. Malhi H, Irani AN, Rajvanshi P, Suadicani SO, Spray DC, McDonald TV, and Gupta S. K-ATP channels regulate mitogenically induced proliferation in primary rat hepatocytes and human liver cell lines: implications for liver growth control and potential therapeutic targeting. J Biol Chem 275: 26050-26057, 2000.
122. + channels in human normal and cystic fibrosis airway epithelia. Pediatr Res 53: 608-618, 2003.
123. Marchant D, Gogat K, Boutboul S, Pequignot M, Sternberg C, Dureau P, Roche O, Uteza Y, Hache JC, Puech B, Puech V, Dumur V, Mouillon M, Munier FL, Schorderet DF, Marsac C, Dufler JL, and Abitbol M. Identification of novel VMD2 gene mutations in patients with best vitelliform macular dystrophy. Hum Mutat 17: 235, 2001.
124. Marmorstein AD, Marmorstein LY, Rayborn M, Wang X, Hollyfield JG, and Petrukhin K. Bestrophin, the product of the Best vitelliform macular dystrophy gene (VMD2), localizes to the basolateral plasma membrane of the retinal pigment epithelium. Proc Natl Acad Sci USA 97: 12758-12763, 2000.
125. Marmorstein LY, McLaughlin PJ, Stanton JB, Yan L, Crabb JW, and Marmorstein AD. Bestrophin interacts physically and functionally with protein phosphatase 2A. J Biol Chem 277: 30591-30597, 2002.
126. Marquardt A, Stohr H, Passmore LA, Kramer F, Rivera A, and Weber BH. Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best's disease). Hum Mol Genet 7: 1517-1525, 1998.
127. Matricardi PM, Rosmini F, Ferrigno L, Nisini R, Rapicetta M, Chionne P, Stroffolini T, Pasquini P, and D'Amelio R. Cross sectional retrospective study of prevalence of atopy among Italian military students with antibodies against hepatitis A virus. Bone Miner J 314: 999-1003, 1997.
128. Matsui H, Davis CW, Tarran R, and Boucher RC. Osmotic water permeabilities of cultured, well-differentiated normal and cystic fibrosis airway epithelia. J Clin Invest 105: 1419-1427, 2000.
129. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, and Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015, 1998.
130. Mattes J and Karmaus W. The use of antibiotics in the first year of life and development of asthma: which comes first? Clin Exp Allergy 29: 729-732, 1999.
131. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, Paumet F, Sollner TH, and Rothman JE. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407: 144-146, 2000.
132. Mekid H, Tounekti O, Spatz A, Cemazar M, El Kebir FZ, and Mir LM. In vivo evolution of tumour cells after the generation of double-strand DNA breaks. Br J Cancer 88: 1763-1771, 2003.
133. Murray AW. Cyclin-dependent kinases: regulators of the cell cycle and more. Chem Biol 1: 191-195, 1994.
134. Nakamura Y, Ghaffar O, Olivenstein R, Taha RA, Soussi-Gounni A, Zhang DH, Ray A, and Hamid Q. Gene expression of the GATA-3 transcription factor is increased in atopic asthma. J Allergy Clin Immunol 103: 215-222, 1999.
135. Nakanishi A, Morita S, Iwashita H, Sagiya Y, Ashida Y, Shirafuji H, Fujisawa Y, Nishimura O, and Fujino M. Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma. Proc Natl Acad Sci USA 98: 5175-5180, 2001.
136. Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, and Lederer WJ. Relaxation of arterial smooth muscle by calcium sparks. Science 270: 633-637, 1995.
137. Nelson MT, Conway MA, Knot HJ, and Brayden JE. Chloride channel blockers inhibit myogenic tone in rat cerebral arteries. J Physiol 502: 259-264, 1997.
138. Nelson MT, Patlak JB, Worley JF, and Standen NB. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol Cell Physiol 259: C3-C18, 1990.
139. Nilius B and Wohlrab W. Potassium channels and regulation of proliferation of human-melanoma cells. J Physiol 445: 537-548, 1992.
140. O'Gorman S, Flaherty WA, Fishman GA, and Berson EL. Histopathologic findings in Best's vitelliform macular dystrophy. Arch Ophthalmol 106: 1261-1268, 1988.
141. O'Grady SM, Musch MW, and Field M. Stoichiometry and ion affinities of the Na-K-Cl cotransport system in the intestine of the winter flounder (Pseudopleuronectes americanus). J Membr Biol 91: 33-41, 1986.
142. O'Grady SM, Palfrey HC, Field M, and Musch MW. Characteristics and functions of Na-K-Cl cotransport in epithelial tissues. Am J Physiol Cell Physiol 253: C177-C192, 1987.
143. Orrenius S, Zhivotovsky B, and Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4: 552-565, 2003.
144. Palomba G, Rozzo C, Angius A, Pierrottet CO, Orzalesi N, and Pirastu M. A novel spontaneous missense mutation in VMD2 gene is a cause of a best macular dystrophy sporadic case. Am J Ophthalmol 129: 260-262, 2000.
145. Parlati F, McNew JA, Fukuda R, Miller R, Sollner TH, and Rothman JE. Topological restriction of SNARE-dependent membrane fusion. Nature 407: 194-198, 2000.
146. Pauli BU, Abdel-Ghany M, Cheng HC, Gruber AD, Archibald HA, and Elble RC. Molecular characteristics and functional diversity of CLCA family members. Clin Exp Pharmacol Physiol 27: 901-905, 2000.
147. Peerce BE, Seifert S, and Clarke R. Partial-purification and reconstitution of an anion conductance from rabbit intestinal brush-border membranes (Abstract). FASEB J 5: A1761, 1991.
148. Petrukhin K, Koisti MJ, Bakall B, Li W, Xie G, Marknell T, Sandgren O, Foreman K, Holmgren G, Andreasson S, Vujic M, Bergen AA, McGarty-Dugan V, Figueroa D, Austin CP, Metzker ML, Caskey CT, and Wadelius C. Identification of the gene responsible for Best macular dystrophy. Nat Genet 19: 241-247, 1998.
149. Pfitzer G. Invited review: regulation of myosin phosphorylation in smooth muscle. J Appl Physiol 91: 497-503, 2001.
150. Pier GB. CFTR mutations and host susceptibility to Pseudomonas aeruginosa lung infection. Curr Opin Microbiol 5: 81-86, 2002.
151. Puzon-McLaughlin W and Takada Y. Critical residues for ligand binding in an I domain-like structure of the integrin beta1 subunit. J Biol Chem 271: 20438-20443, 1996.
152. - channel: identification of a residue important in anion binding and conduction. J Gen Physiol 123: 327-340, 2004.
153. Qu Z, Wei RW, Mann W, and Hartzell HC. Two bestrophins cloned from Xenopus laevis oocytes express Ca(2+)-activated Cl(-) currents. J Biol Chem 278: 49563-49572, 2003.
154. Racette KJ, Gabriel SE, Gaspar KJ, and Forsyth GW. Monoclonal antibody against conductive chloride transport in pig ileal apical membrane vesicles. Am J Physiol Cell Physiol 271: C478-C485, 1996.
155. Ran S, Fuller CM, Arrate MP, Latorre R, and Benos DJ. Functional reconstitution of a chloride channel protein from bovine trachea. J Biol Chem 267: 20630-20637, 1992.
156. Rashid P, Leonardi-Bee J, and Bath P. Blood pressure reduction and secondary prevention of stroke and other vascular events: a systematic review. Stroke 34: 2741-2748, 2003.
157. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL, Drumm ML, Iannuzzi MC, Collins FS, and Tsui LC. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245; 1066-1073, 1989.
158. Ritzka M, Weinel C, Stanke F, and Tummler B. Sequence comparisons of the whole murine and human CLCA locus reveals conserved synteny between both species. Genome Lett 2: 149-154, 2003.
159. Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, Corrigan C, Durham SR, and Kay AB. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med 326: 298-304, 1992.
160. Romio L, Musante L, Cinti R, Seri M, Moran O, Zegarra-Moran O, and Galietta LJ. Characterization of a murine gene homologous to the bovine CaCC chloride channel. Gene 228: 181-188, 1999.
161. Rozakis-Adcock M, Fernley R, Wade J, Pawson T, and Bowtell D. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature 363: 83-85, 1993.
162. Ruoslahti E and Rajotte D. An address system in the vasculature of normal tissues and tumors. Annu Rev Immunol 18: 813-827, 2000.
163. + cotransport. Pflügers Arch 414: 286-290, 1989.
164. Schwartz TW and Devi L. The processing of peptide precursors. "Proline-directed arginyl cleavage" and other monobasic processing mechanisms: consensus sequence for processing of peptide precursors at monobasic sites. FEBS Lett 200: 1-10, 1986.
165. Segal MS and Beem E. Effect of pH, ionic charge, and osmolality on cytochrome c-mediated caspase-3 activity. Am J Physiol Cell Physiol 281: C1196-C1204, 2001.
166. Shaw LM, Rabinovitz I, Wang HH, Toker A, and Mercurio AM. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell 91: 949-960, 1997.
167. Shirakawa T, Enomoto T, Shimazu S, and Hopkin JM. The inverse association between tuberculin responses and atopic disorder. Science 275: 77-79, 1997.
168. Smalley KS. A pivotal role for ERK in the oncogenic behaviour of malignant melanoma? Int J Cancer 104: 527-532, 2003.
169. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, and Koller BH. An animal-model for cystic-fibrosis made by gene targeting. Science 257: 1083-1088, 1992.
170. Stohr H, Marquardt A, Nanda I, Schmid M, and Weber BH. Three novel human VMD2-like genes are members of the evolutionary highly conserved RFP-TM family. Eur J Hum Genet 10: 281-284, 2002.
171. Strachan DP. Hay fever, hygiene, and household size. Bone Miner J 299: 1259-1260, 1989.
172. Stutts MJ, Canessa CM, Olsen JC, Hamrick M, Cohn JA, Rossier BC, and Boucher RC. CFTR as a cAMP-dependent regulator of sodium-channels. Science 269: 847-850, 1995.
173. Sun H, Tsunenari T, Yau KW, and Nathans J. The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci USA 99: 4008-4013, 2002.
174. Szabo I, Lepple-Wienhues A, Kaba KN, Zoratti M, Gulbins E, and Lang F. Tyrosine kinase-dependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. Proc Natl Acad Sci USA 95: 6169-6174, 1998.
175. Takagi J, Kamata T, Meredith J, Puzon-McLaughlin W, and Takada Y. Changing ligand specificities of alphavbeta1 and alphavbeta3 integrins by swapping a short diverse sequence of the beta subunit. J Biol Chem 272: 19794-19800, 1997.
176. Tang K, Nie D, Cai Y, and Honn KV. The beta4 integrin subunit rescues A431 cells from apoptosis through a PI3K/Akt kinase signaling pathway. Biochem Biophys Res Commun 264: 127-132, 1999.
177. - conductances. J Gen Physiol 120: 407-418, 2002.
178. Thevenod F. Ion channels in secretory granules of the pancreas and their role in exocytosis and release of secretory proteins. Am J Physiol Cell Physiol 283: C651-C672, 2002.
179. --permeable conductance and a CLCA protein from rat pancreatic zymogen granules. Biochem Biophys Res Commun 300: 546-554, 2003.
180. - currents in CF and normal mouse tracheal epithelial cell lines. Am J Physiol Cell Physiol 279: C1578-C1586, 2000.
181. Toda M, Tulic MK, Levitt RC, and Hamid Q. A calcium-activated chloride channel (HCLCA1) is strongly related to IL-9 expression and mucus production in bronchial epithelium of patients with asthma. J Allergy Clin Immunol 109: 246-250, 2002.
182. Trusolino L, Bertotti A, and Comoglio PM. A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 107: 643-654, 2001.
183. Tsuboi S. Measurement of the volume flow and hydraulic conductivity across the isolated dog retinal pigment epithelium. Invest Ophthalmol Vis Sci 28: 1776-1782, 1987.
184. Tsuboi S, Manabe R, and Iizuka S. Aspects of electrolyte transport across isolated dog retinal pigment epithelium. Am J Physiol Renal Fluid Electrolyte Physiol 250: F781-F784, 1986.
185. Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P, Yau KW, and Nathans J. Structure-function analysis of the bestrophin family of anion channels. J Biol Chem 278: 41114-41125, 2003.
186. Tsuruta D, Hopkinson SB, Lane KD, Werner ME, Cryns VL, and Jones JC. Crucial role of the specificity-determining loop of the integrin beta4 subunit in the binding of cells to laminin-5 and outside-in signal transduction. J Biol Chem 278: 38707-38714, 2003.
187. Tyska MJ, Dupuis DE, Guilford WH, Patlak JB, Waller GS, Trybus KM, Warshaw DM, and Lowey S. Two heads of myosin are better than one for generating force and motion. Proc Natl Acad Sci USA 96: 4402-4407, 1999.
188. Ullrich N and Sontheimer H. Cell cycle-dependent expression of a glioma-specific chloride current: proposed link to cytoskeletal changes. Am J Physiol Cell Physiol 273: C1290-C1297, 1997.
189. Vaage J and Harlos JP. Spontaneous metastasis from primary C3H mouse mammary tumors. Cancer Res 47: 547-550, 1987.
190. Verdugo P. Mucin exocytosis. Am Rev Respir Dis 144: S33-S37, 1991.
191. Villaz M, Cinniger JC, and Moody WJ. A voltage-gated chloride channel in ascidian embryos modulated by both the cell-cycle clock and cell-volume. J Physiol 488: 689-699, 1995.
192. Walker C, Bauer W, Braun RK, Menz G, Braun P, Schwarz F, Hansel TT, and Villiger B. Activated T cells and cytokines in bronchoalveolar lavages from patients with various lung diseases associated with eosinophilia. Am J Respir Crit Care Med 150: 1038-1048, 1994.
193. 1 ionic event necessary for cell cycle progression and survival in the MCF-7 human breast carcinoma cell line. J Cell Physiol 176: 456-464, 1998.
194. Wang YX and Kotlikoff MI. Inactivation of calcium-activated chloride channels in smooth muscle by calcium/calmodulin-dependent protein Kinase. Proc Natl Acad Sci USA 94: 14918-14923, 1997.
195. Watson B Jr. Genetics of the kidney and hypertension. Curr Hypertens Rep 5: 273-276, 2003.
196. Weingeist TA, Kobrin JI, and Watzke RC. Histopathology of Best's macular dystrophy. Arch Ophthalmol 100: 1108-1114, 1982.
197. Whittaker CA and Hynes RO. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13: 3369-3387, 2002.
198. WHO. 1999 World Health Organization-International Society of Hypertension Guidelines for the Management of Hypertension. Guidelines Subcommittee J Hypertens 17: 151-183, 1999.
199. 2+ ionophores in cystic fibrosis airway epithelia. Am J Physiol Cell Physiol 256: C226-C233, 1989.
200. Willumsen NJ, Boucher RC, and Davis CW. Shunt resistance and ion permeabilities in normal and cystic fibrosis airway epithelia. Am J Physiol Cell Physiol 256: C1054-C1063, 1989.
201. - pathways in cultured human airway epithelium. Am J Physiol Cell Physiol 256: C1033-C1044, 1989.
202. Wilson GF and Chiu SY. Mitogenic factors regulate ion channels in Schwann-cells cultured from newborn rat sciatic-nerve. J Physiol 470: 501-520, 1993.
203. Winpenny JP, Lavery WL, Watson N, and Chazot PL. Biochemical and electrophysiological characterisation of the GOB5 (mCLCA3) chloride ion channel protein after expression in HEK293 cells. J Physiol 539: 2P, 2002.
204. 2+ concentration of human keratinocytes. Skin Pharmacol Appl Skin Physiol 12: 257-265, 1999.
205. Woodfork KA, Wonderlin WF, Peterson VA, and Strobl JS. Inhibition of ATP-sensitive potassium channels causes reversible cell-cycle arrest of human breast-cancer cells in tissue-culture. J Cell Physiol 162: 163-171, 1995.
206. Ye C, Rogers K, Bai M, Quinn SJ, Brown EM, and Vassilev PM. Agonists of the Ca(2+)-sensing receptor (CaR) activate nonselective cation channels in HEK293 cells stably transfected with the human CaR. Biochem Biophys Res Commun 226: 572-579, 1996.
207. Yerxa BR, Sabater JR, Davis CW, Stutts MJ, Lang-Furr M, Picher M, Jones AC, Cowlen M, Dougherty R, Boyer J, Abraham WM, and Boucher RC. Pharmacology of INS37217 P-1-(uridine 5′)-P-4-(2′-deoxycytidine 5′) tetraphosphate, tetrasodium salt, a next-generation P2Y(2) receptor agonist for the treatment of cystic fibrosis. J Pharmacol Exp Ther 302: 871-880, 2002.
208. Zhang LF, Ding JH, Yang BZ, He GC, and Roe C. Characterization of the bidirectional promoter region between the human genes encoding VLCAD and PSD-95. Genomics 82: 660-668, 2003.
209. Zhou Y, Dong Q, Louahed J, Dragwa C, Savio D, Huang M, Weiss C, Tomer Y, McLane MP, Nicolaides NC, and Levitt RC. Characterization of a calcium-activated chloride channel as a shared target of Th2 cytokine pathways and its potential involvement in asthma. Am J Respir Cell Mol Biol 25: 486-491, 2001.
210. Zhou Y, Shapiro M, Dong Q, Louahed J, Weiss C, Wan S, Chen Q, Dragwa C, Savio D, Huang M, Fuller C, Tomer Y, Nicolaides NC, McLane M, and Levitt RC. A calcium-activated chloride channel blocker inhibits goblet cell metaplasia and mucus overproduction. Novartis Found Symp 248: 150-170, 2002.
211. Zhu D, Cheng CF, and Pauli BU. Blocking of lung endothelial cell adhesion molecule-1 (Lu-ECAM-1) inhibits murine melanoma lung metastasis. J Clin Invest 89: 1718-1724, 1992.
212. Zhu D and Pauli BU. Correlation between the lung distribution patterns of Lu-ECAM-1 and melanoma experimental metastases. Int J Cancer 53: 628-633, 1993.
213. Zhu DZ, Cheng CF, and Pauli BU. Mediation of lung metastasis of murine melanomas by a lung-specific endothelial cell adhesion molecule. Proc Natl Acad Sci USA 88: 9568-9572, 1991.
214. Zhu DZ and Pauli BU. Generation of monoclonal antibodies directed against organ-specific endothelial cell surface determinants. J Histochem Cytochem 39: 1137-1142, 1991.
215. Zhu GY, Zhang Y, Xu HX, and Jiang C. Identification of endogenous outward currents in the human embryonic kidney (HEK293) cell line. J Neurosci Methods 81: 73-83, 1998.