Vasoactive intestinal peptide, forskolin, and genistein increase apical CFTR trafficking in the rectal gland of the spiny dogfish, Squalus acanthias: Acute regulation of CFTR trafficking in an intact epithelium

Journal of Clinical Investigation

Volumn 101, Issue 4, 1998, Pages 737-745

  Lehrich, Rüdiger W ^a,b,d   Aller, Stephen G ^a,d   Webster, Paul ^a   Marino, Christopher R ^c   Forrest Jr , John N ^a,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

Author keywords

CFTR; Cystic fibrosis transmembrane conductance regulator; Forskolin; Genistein; Membrane trafficking; Shark rectal gland

Indexed keywords

CHLORIDE; FORSKOLIN; GENISTEIN; HORMONE; TRANSMEMBRANE CONDUCTANCE REGULATOR; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; HORMONAL REGULATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MALE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RECTUM GLAND; SHARK;

EID: 0032519924     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI803     Document Type: Article

References (42)

1. Kerem, B., J.M. Rommens, J.A. Buchanan, D. Markiewicz, T.K. Cox, A. Chakravarti, M. Buchwald, and L.C. Tsui. 1989. Identification of the cystic fibrosis gene: genetic analysis. Science. 245:1073-1080.
2. Kartner, N., O. Augustinas, T.J. Jensen, A.L. Naismith, and J.R. Riordan. 1992. Mislocalization of delta F508 CFTR in cystic fibrosis sweat gland. Nat. Genet. 1:321-327.
3. Dalemans, W., J. Hinnrasky, P. Slos, D. Dreyer, C. Fuchey, A. Pavirani, and E. Puchelle. 1992. Immunocytochemical analysis reveals differences between the subcellular localization of normal and delta Phe508 recombinant cystic fibrosis transmembrane conductance regulator. Exp. Cell Res. 201-.235-240.
4. Marino, C.R., L.M. Matovcik, F.S. Gorelick, and J.A. Cohn. 1991. Localization of the cystic fibrosis transmembrane conductance regulator in pancreas [published erratum appears in J. Clin. Invest. 1991. 88:1433]. J. Clin. Invest. 88: 712-716.
5. Cohn, J.A., A.C. Nairn, C.R. Marino, O. Melhus, and J. Kole. 1992. Characterization of the cystic fibrosis transmembrane conductance regulator in a colonocyte cell line. Proc. Natl Acad. Sci. USA. 89:2340-2344.
6. Webster, P., L. Vanacore, A.C. Nairn, and C.R. Marino. 1994. Subcellular localization of CFTR to endosomes in a ductal epithelium. Am. J. Physiol. 267:C340-C348.
7. Bradbury, N.A., J.A. Cohn, C.J. Venglarik, and R.J. Bridges. 1994. Biochemical and biophysical identification of cystic fibrosis transmembrane conductance regulator chloride channels as components of endocytic clathrin-coated vesicles. J. Biol. Chem. 269:8296-8302.
8. Bradbury, N.A., T. Jilling, G. Berta, E.J. Sorscher, R.J. Bridges, and K.L. Kirk. 1992. Regulation of plasma membrane recycling by CFTR. Science. 256: 530-532.
9. Schwiebert, E.M., F. Gesek, L. Ercolani, C. Wjasow, D.C. Gruenert, K. Karlson, and B.A. Stanton. 1994. Heterotrimeric G proteins, vesicle trafficking, and CFTR Cl-channels. Am. J. Physiol. 267:C272-C281.
10. Denning, G.M., L.S. Ostedgaard, S.H. Cheng, A.E. Smith, and MJ. Welsh. 1992. Localization of cystic fibrosis transmembrane conductance regulator in chloride secretory epithelia. J. Clin. Invest. 89:339-349.
11. Prince, L.S., A. Tousson, and R.B. Marchase. 1993. Cell surface labeling of CFTR in T84 cells. Am. J. Physiol. 264:C491-C498.
12. Dho, S., S. Grinstein, and J.K. Foskett. 1993. Plasma membrane recycling in CFTR-expressing CHO cells. Biochim. Biophys. Acta. 1225:78-82.
13. Tousson, A., C.M. Fuller, and D.J. Benos. 1996. Apical recruitment of CFTR in T84 cells is dependent on cAMP and microtubules but not Ca2+ or microfilaments. J. Cell Sci. 109:1325-1334.
14. Forrest, J.N. 1996. Cellular and molecular biology of chloride secretion in the shark rectal gland: regulation by adenosine receptors. Kidney Int. 49: 1557-1562.
15. Silva, P., R.J. Solomon, and F.H. Epstein. 1996. The rectal gland of Squalus acanthias: a model for the transport of chloride. Kidney Int. 49:1552-1556.
16. Eveloff, J., R. Kinne, E. Kinne-Saffran, H. Murer, P. Silva, F.H. Epstein, J. Stoff, and W.B. Kinter. 1978. Coupled sodium and chloride transport into plasma membrane vesicles prepared from dogfish rectal gland. Pflugers Arch. 378:87-92.
17. Lytle, C., and B. Forbush 3d. 1992. The Na-K-Cl cotransport protein of shark rectal gland. II. Regulation by direct phosphorylation. J. Biol. Chem. 267: 25438-25443.
18. Marshall, J., K.A. Martin, M. Picciotto, S. Hockfield, A.C. Nairn, and L.K. Kaczmarek. 1991. Identification and localization of a dogfish homolog of human cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 266:22749-22754.
19. Devor, D.C., J.N. Forrest, Jr., W.K. Suggs, and R.A. Frizzell. 1995. cAMP-activated Cl-channels in primary cultures of spiny dogfish (Squalus acanthias) rectal gland. Am. J. Physiol. 268-.C70-C79.
20. Kelley, G.G., E.M. Poeschla, H.V. Barron, and J.N. Forrest, Jr. 1990. A1 adenosine receptors inhibit chloride transport in the shark rectal gland. Dissociation of inhibition and cyclic AMP. J. Clin. Invest. 85:1629-1636.
21. Kelley, G.G., O.S. Aassar, and J.N. Forrest, Jr. 1991. Endogenous adenosine is an autacoid feedback inhibitor of chloride transport in the shark rectal gland. J. Clin. Invest. 88:1933-1939.
22. French, P.J., J.H. van Doorninck, R.H. Peters, E. Verbeek, N.A. Ameen, C.R. Marino, H.R. de Jonge, J. Bijman, and B.J. Scholte. 1996. A delta F508 mutation in mouse cystic fibrosis transmembrane conductance regulator results in a temperature-sensitive processing defect in vivo. J. Clin. Invest. 98:1304-1312.
23. Kozak, M. 1984. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 12:857-872.
24. Mattfeld, T., G. Mall, A. Von Herbay, and P. Moeller. 1989. Stereological investigation of anisotropic structures with the orientator. Acta Stereol. 8:671-676.
25. Stoff, J.S., R. Rosa, R. Hallac, P. Suva, and F.H. Epstein. 1979. Hormonal regulation of active chloride transport in the dogfish rectal gland. Am. J. Physiol. 237:F138-F144.
26. Seamon, K.B., and J.W. Daly. 1986. Forskolin: its biological and chemical properties. Adv. Cyclic Nucleotide Protein Phosphorylation Res. 20:1-150.
27. Lehrich, R.W., and J.N. Forrest, 1995. Tyrosine phosphorylation is a novel pathway for regulation of chloride secretion in the shark rectal gland. Am. J. Physiol. 269:F594-F600.
28. Illek, B., H. Fischer, G.F. Santos, J.H. Widdicombe, T.E. Machen, and W.W. Reenstra. 1995. cAMP-independent activation of CFTR Cl channels by the tyrosine kinase inhibitor genistein. Am. J. Physiol. 268:C886-C893.
29. Illek, B., H. Fischer, and T.E. Machen. 1996. Alternate stimulation of apical CFTR by genistein in epithelia. Am. J. Physiol. 270:C265-C275.
30. Reenstra, W.W., K. Yurko-Mauro, A. Dam, S. Raman, and S. Shorten. 1996. CFTR chloride channel activation by genistein: the role of serine/threonine protein phosphatases. Am. J. Physiol. 271:C650-C657.
31. Sears, C.L., F. Firoozmand, A. Mellander, F.G. Chambers, I.G. Eromar, A.C. Bot, B. Scholte, H.R. De Jonge, and M. Donowitz. 1995. Genistein and tyrphostin 47 stimulate CFTR-mediated Cl-secretion in T84 cell monolayers, Am. J. Physiol. 269:G874-G882.
32. Lytle, C., and B. Forbush 3d. 1992. Na-K-Cl cotransport in the shark rectal gland. II. Regulation in isolated tubules. Am. J. Physiol. 262:C1009-C1017.
33. Takahaschi, A., S.C. Watkins, M. Howard, and R.A. Frizzell. 1996. CFTR-dependent membrane insertion is linked to stimulation of the CFTR chloride conductance. Am. J. Physiol. 271:C1887-C1894.
34. Cheng, S.H., R.J. Gregory, J. Marshall, S. Paul, D.W. Souza, G.A. White, C.R. O'Riordan, and A.E. Smith, 1990. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell. 63: 827-834.
35. Lehrich, R.W., C. Marino, H. Henschel, C. Kelmenson, M. Ratner, and J.N. Forrest. 1995. Immunolocalization of DFTR with the rodent CFTR antibody R3195 in the rectal gland of the dogfish shark, Squalus acanthias. Bull. Mt. Desert Isl. Biol. Lab. 35:28-31.
36. Sorscher, E.J., C.M. Fuller, R.J. Bridges, A. Tousson, R.B. Marchase, B.R. Brinkley, R.A. Frizzell, and D.J. Benos. 1992. Identification of a membrane protein from T84 cells using antibodies made against a DIDS-binding peptide. Am. J. Physiol. 262:C136-C147.
37. Santos, G.F., and W.W. Reenstra. 1994. Activation of the cystic fibrosis transmembrane regulator by cyclic AMP is not correlated with inhibition of endocytosis. Biochim. Biophys. Acta. 1195:96-102.
38. Kachadorian, W.A., S.D. Levine, J.B. Wade, V.A. DiScala, and R.M. Hays. 1977. Relationship of aggregated intramembranous particles to water permeability in vasopressin-treated toad urinary bladder. J. Clin. Invest. 59: 576-581.
39. Deen, P.M., H. Croes, R.A. van Aubel, L.A. Ginsel, and C.H. van Os. 1995. Water channels encoded by mutant aquaporin-2 genes in nephrogenic diabetes insipidus are impaired in their cellular routing. J. Clin. Invest. 95:2291-2296.
40. Cushman, S.W., and L.J. Wardzala. 1980. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. J. Biol. Chem. 255:4758-4762.
41. 4L Kono, T., K. Suzuki, E. Dansey, W. Robinson, and T.L. Belvins. 1981. Energy-dependent and protein synthesis-independent recycling of the insulin-sensitive glucose transport mechanism in fat cells. J. Biol. Chem. 256:6400-6407.
42. Brown, D., S. Gluck, and J. Hartwig. 1987. Structure of the novel membrane-coating material in proton-secreting epithelial cells and identification as an H+ATPase. J. Cell Biol. 105:1637-1648.