Arsenic inhibits SGK1 activation of CFTR Cl- channels in the gill of killifish, Fundulus heteroclitus

Aquatic Toxicology

Volumn 98, Issue 2, 2010, Pages 157-164

  Shaw, Joseph R ^a,b   Bomberger, Jennifer M ^c   VanderHeide, John ^b   LaCasse, Taylor ^b   Stanton, Sara ^b   Coutermarsh, Bonita ^c   Barnaby, Roxanna ^c   Stanton, Bruce A ^b,c  

^a INDIANA UNIVERSITY   (United States)

^b MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Abcc7; Acclimation; Environmental toxicant; Lysosome; Ubiquitination

Indexed keywords

ARSENIC; CHLORIDE CHANNEL; FRESH WATER; MESSENGER RNA; SEA WATER; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ACCLIMATION; ARSENIC; ENZYME ACTIVITY; FISH; GENE EXPRESSION; PROTEIN; SEAWATER;

ACCLIMATIZATION; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CELL MEMBRANE; CONTROLLED STUDY; CYPRINODONTIFORMES; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; GILL; INHIBITION KINETICS; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOXICOKINETICS; UBIQUITINATION; WESTERN BLOTTING;

ACCLIMATIZATION; ANIMALS; ARSENIC; ATP-BINDING CASSETTE TRANSPORTERS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DOWN-REGULATION; FUNDULIDAE; GENE EXPRESSION REGULATION; GILLS; IMMEDIATE-EARLY PROTEINS; LYSOSOMES; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEAWATER; TIME FACTORS; UBIQUITINATION; WATER POLLUTANTS, CHEMICAL;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

EID: 77953683634     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.02.001     Document Type: Article

References (49)

1. Abernathy C.O., Liu Y.P., Longfellow D., Aposhian H.V., Beck B., Fowler B., Goyer R., Menzer R., Rossman T., Thompson C., Waalkes M. Arsenic: health effects, mechanisms of actions, and research issues. Environ. Health Perspect. 1999, 107:593-597.
2. Ameen N., Silvis M., Bradbury N.A. Endocytic trafficking of CFTR in health and disease. J. Cys. Fibrosis 2007, 6:1-14.
3. American Society for Testing and Materials Annual Book of ASTM Standards. Water and Environmental Technology. Water (I) 1985, American Society for Testing and Materials, Philadelphia, PA, p. v.
4. Bears H., Richards J.G., Schulte P.M. Arsenic exposure alters hepatic arsenic species composition and stress-mediated gene expression in the common killifish (Fundulus heteroclitus). Aquat. Toxicol. 2006, 77:257-266.
5. Bhalla V., Soundararajan R., Pao A.C., Li H., Pearce D. Disinhibitory pathways for control of sodium transport: regulation of ENaC by SGK1 and GILZ. Am. J. Physiol. Renal Physiol. 2006, 291:F714-F721.
6. Bomberger J.M., Barnaby R.L., Stanton B.A. The deubiquitinating enzyme USP10 regulates the post-endocytic sorting of cystic fibrosis transmembrane conductance regulator in airway epithelial cells. J. Biol. Chem. 2009, 284:18778-18789.
7. Boyle R.W., Jonasson I.R. Geochemistry of Arsenic and Antimony 1973, National Research Council of Canada Ottawa, Canada. G. Canada (Ed.).
8. Bredfeldt T.G., Kopplin M.J., Gandolfi A.J. Effects of arsenite on UROtsa cells: low-level arsenite causes accumulation of ubiquitinated proteins that is enhanced by reduction in cellular glutathione levels. Toxicol. Appl. Pharmacol. 2004, 198:412-418.
9. Caohuy H., Jozwik C., Pollard H.B. Rescue of DeltaF508-CFTR by the SGK1/Nedd4-2 signaling pathway. J. Biol. Chem. 2009, 284:25241-25253.
10. Ernst S.A., Dodson W.C., Karnaky K.J. Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J. Cell Biol. 1980, 87:488-497.
11. Gentzsch M., Chang X., Cui L., Wu Y., Ozols V.V., Choudhury A., Pagano R.E., Riordan J.R. Endocytic trafficking routes of wild-type and ΔF508 CFTR. Mol. Biol. Cell 2004, 15:2684-2696.
12. Henke K.R. Arsenic: Environmental Chemistry, Health Threats and Waste Treatment 2009, vol. xviii. Wiley, Chichester, UK, 569 pp.
13. - transport in the operculum epithelium of Fundulus heteroclitus: long- and short-term salinity adaptation. Biochim. Biophys. Acta 2002, 1566:129-139.
14. Karagas M.R., Tosteson T.D., Blum J., Morris J.S., Baron J.A., Klaue B. Design of an epidemiologic study of drinking water arsenic exposure and skin and bladder cancer risk in a U.S. population. Environ. Health Perspect. 1998, 106(Suppl. 4):1047-1050.
15. Karnaky K.G., Kinter W.B. Killifish opercular skin: a flat epithelium with a high density of chloride cells. J. Exp. Zool. 1977, 199:355-364.
16. Kendziorski C.M., Zhang Y., Lan H., Attie A.D. The efficiency of pooling mRNA in microarray experiments. Biostatistics 2003, 4:465-477.
17. Kirkpatrick D.S., Dale K.V., Catania J.M., Gandolfi A.J. Low-level arsenite causes accumulation of ubiquitinated proteins in rabbit renal cortical slices and HEK293 cells. Toxicol. Appl. Pharmacol. 2003, 186:101-109.
18. Lang F., Henke G., Embark H.M., Waldegger S., Palmada M., Bohmer C., Vallon V. Regulation of channels by the serum and glucocorticoid-inducible kinase-implications for transport, excitability and cell proliferation. Cell. Physiol. Biochem. 2003, 13:41-50.
19. Lang F., Bohmer C., Palmada M., Seebohm G., Strutz-Seebohm N., Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol. Rev. 2006, 86:1151-1178.
20. Li Y., Qu X., Qu J., Zhang Y., Liu J., Teng Y., Hu X., Hou K., Liu Y. Arsenic trioxide induces apoptosis and G2/M phase arrest by inducing Cbl to inhibit PI3K/Akt signaling and thereby regulate p53 activation. Cancer Lett. 2009, 284:208-215.
21. Loffing J., Flores S.Y., Staub O. Sgk kinases and their role in epithelial transport. Annu. Rev. Physiol. 2006, 68:461-490.
22. Marshall W.S., Emberley T.R., Singer T.D., Bryson S.E., McCormick S.D. Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J. Exp. Biol. 1999, 202(Pt 11):1535-1544.
23. Marshall W.S. Na(+), Cl(-), Ca(2+) and Zn(2+) transport by fish gills: retrospective review and prospective synthesis. J. Exp. Zool. 2002, 293:264-283.
24. Marshall W.S., Singer T.D. Cystic fibrosis transmembrane conductance regulator in teleost fish. Biochim. Biophys. Acta 2002, 1566:16-27.
25. Marshall W.S. Rapid regulation of NaCl secretion by estuarine teleost fish: coping strategies for short-duration freshwater exposures. Biochim. Biophys. Acta 2003, 1618:95-105.
26. Marshall W.S., Cozzi R.R., Pelis R.M., McCormick S.D. Cortisol receptor blockade and seawater adaptation in the euryhaline teleost Fundulus heteroclitus. J. Exp. Zool. A: Comp. Exp. Biol. 2005, 303:132-142.
27. Mattingly C.J., Hampton T.H., Brothers K.M., Griffin N.E., Planchart A. Perturbation of defense pathways by low-dose arsenic exposure in zebrafish embryos. Environ. Health Perspect. 2009, 117:981-987.
28. Moeller A., MacNeil S.D., Ambrose R.F., Que Hee S.S. Elements in fish of Malibu Creek and Malibu Lagoon near Los Angeles, California. Mar. Pollut. Bull. 2003, 46:424-429.
29. Moyer B.D., Loffing J., Schwiebert E.M., Loffing-Cueni D., Halpin P.A., Karlson K.H., Ismailov I.I., Guggino W.B., Langford G.M., Stanton B.A. Membrane trafficking of the cystic fibrosis gene product, cystic fibrosis transmembrane conductance regulator, tagged with green fluorescent protein in madin-darby canine kidney cells. J. Biol. Chem. 1998, 273:21759-21768.
30. National Research Council (U.S.).Subcommittee on Arsenic in Drinking Water, NetLibrary Inc. Arsenic in Drinking Water 1999, vol. xvii. National Academy Press, Washington, DC, 310 pp.
31. Neff J.M. Ecotoxicology of arsenic in the marine environment. Environ. Toxicol. Chem. 1997, 16:917-927.
32. Pearce D. SGK1 regulation of epithelial sodium transport. Cell. Physiol. Biochem. 2003, 13:13-20.
33. Sato J.D., Chapline M.C., Thibodeau R., Frizzell R.A., Stanton B.A. Regulation of human cystic fibrosis transmembrane conductance regulator (CFTR) by serum- and glucocorticoid-inducible kinase (SGK1). Cell. Physiol. Biochem. 2007, 20:91-98.
34. Scott G.R., Richards J.G., Forbush B., Isenring P., Schulte P.M. Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am. J. Physiol. Cell Physiol. 2004, 287:C300-C309.
35. Shaw J.R., Jackson B., Gabor K., Stanton S., Hamilton J.W., Stanton B.A. The influence of exposure history on arsenic accumulation and toxicity in the killifish, Fundulus heteroclitus. Environ. Toxicol. Chem. 2007, 26:2704-2709.
36. Shaw J.R., Gabor K., Hand E., Lankowski A., Durant L., Thibodeau R., Stanton C.R., Barnaby R., Coutermarsh B., Karlson K.H., Sato J.D., Hamilton J.W., Stanton B.A. Role of glucocorticoid receptor in acclimation of killifish (Fundulus heteroclitus) to seawater and effects of arsenic. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R1052-R1060.
37. Shaw J.R., Sato J.D., VanderHeide J., LaCasse T., Stanton C.R., Lankowski A., Stanton S.E., Chapline C., Coutermarsh B., Barnaby R., Karlson K., Stanton B.A. The role of SGK and CFTR in acute adaptation to seawater in Fundulus heteroclitus. Cell. Physiol. Biochem. 2008, 22:69-78.
38. Singer T.D., Tucker S.J., Marshall W.S., Higgins C.F. A divergent CFTR homologue: highly regulated salt transport in the euryhaline teleost F. heteroclitus. Am. J. Physiol. 1998, 274:C715-C723.
39. Stanton C.R., Thibodeau R., Lankowski A., Shaw J.R., Hamilton J.W., Stanton B.A. Arsenic inhibits CFTR-mediated chloride secretion by killifish (Fundulus heteroclitus) opercular membrane. Cell. Physiol. Biochem. 2006, 17:269-278.
40. Swiatecka-Urban A., Duhaime M., Coutermarsh B., Karlson K.H., Collawn J., Milewski M., Cutting G.R., Guggino W.B., Langford G., Stanton B.A. PDZ domain interaction controls the endocytic recycling of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 2002, 277:40099-40105.
41. Swiatecka-Urban A., Brown A., Moreau-Marquis S., Coutermarsh B., Barnaby R., Karlson K.H., Flotte T.R., Fukuda M., Langford G., Stanton B.A. The short apical membrane half-life of resuced Δ508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated encocytosis of Δ508-CFTR in polarized human airway epithelial cells. J. Biol. Chem. 2005, 280:36762-36772.
42. Tatham M.H., Geoffroy M.C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., Palvimo J.J., Hay R.T. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 2008, 10:538-546.
43. Tessier M., Woodgett J.R. Serum and glucocorticoid-regulated protein kinases: variations on a theme. J. Cell. Biochem. 2006, 98:1391-1407.
44. Thomas C.P., Itani O.A. New insights into epithelial sodium channel function in the kidney: site of action, regulation by ubiquitin ligases, serum- and glucocorticoid-inducible kinase and proteolysis. Curr. Opin. Nephrol. Hypertens. 2004, 13:541-548.
45. United States.Environmental Protection Agency.Office of Water Regulations and Standards.Criteria & Standards Division Ambient Water Quality Criteria for Arsenic 1980, Springfield, Va., Washington, DC, 211 p. in various pagings.
46. Vallon V., Wulff P., Huang D.Y., Loffing J., Volkl H., Kuhl D., Lang F. Role of Sgk1 in salt and potassium homeostasis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R4-R10.
47. Wagner J.A., Nepomuceno I.B., Messner A.H., Moran M.L., Batson E.P., Dimiceli S., Brown B.W., Desch J.K., Norbash A.M., Conrad C.K., Guggino W.B., Flotte T.R., Wine J.J., Carter B.J., Reynolds T.C., Moss R.B., Gardner P. A phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum. Gene Ther. 2002, 13:1349-1359.
48. - transport in the intact killifish after rapid salinity transfer. Biochim. Biophys. Acta 2003, 1618:106-119.
49. Zheng X.H., Watts G.S., Vaught S., Gandolfi A.J. Low-level arsenite induced gene expression in HEK293 cells. Toxicology 2003, 187:39-48.