Glucagon induces the gene expression of aquaporin-8 but not that of aquaporin-9 water channels in the rat hepatocyte

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 4, 2009, Pages

  Soria, Leandro R ^a   Gradilone, Sergio A ^a   Larocca, M Cecilia ^a   Marinelli, Raúl A ^a,b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Aquaporins; Calpains; Liver; Phosphatidylinositol 3 kinase; Protein kinase A

Indexed keywords

AQUAPORIN 8; AQUAPORIN 9; CALPAIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOHEXIMIDE; DACTINOMYCIN; GLUCAGON; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; LIVER CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AQUAPORINS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLUCAGON; HEPATOCYTES; INJECTIONS, INTRAPERITONEAL; MALE; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEASE INHIBITORS; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, WISTAR; RNA, MESSENGER; TIME FACTORS; UP-REGULATION;

EID: 65949103390     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90783.2008     Document Type: Article

References (55)

1. - channels in rat hepatocytes. J Physiol 573: 611-625, 2006.
2. Baker A, Kaplan M, Kimberg DV. Alkaline phosphatase possible induction by cyclic AMP after cholera enterotoxin administration. J Clin Invest 52: 2928-2934, 1973.
3. Blommaart EFC, Krause U, Schellens JPM, Vreeling-Sindelarova H, Melier AJ. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246, 1996.
4. Calamita G, Ferri D, Gena P, Liquori GE, Cavalier A, Thomas D, Svelto M. The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J Biol Chem 280: 17149-17153, 2005. (Pubitemid 41389180)
5. Calamita G, Mazzone A, Bizzoca A, Cavalier A, Cassano G, Thomas D, Svelto M. Expression and immunolocalization of the aquaporin-8 water channel in rat gastrointestinal tract. Eur J Cell Biol 80: 711-719, 2001. (Pubitemid 34092939)
6. Caperna TJ, Shannon AE, Richards MP, Garrett WM, Talbot NC. Identification and characterization of aquaporin-9 (AQP9) in porcine hepatic tissue and hepatocytes in monolayer culture. Domest Anim Endocrinol 32: 273-286, 2007. (Pubitemid 46437292)
7. Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P. Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA 100: 2945-2950, 2003. (Pubitemid 36297603)
8. Carreras FI, Gradilone SA, Mazzone A, Garcia F, Huang BQ, Ochoa JE, Tietz PS, LaRusso NF, Calamita G, Marinelli RA. Rat hepatocyte aquaporin-8 water channels are down-regulated in extrahepatic cholestasis. Hepatology 37: 1026-1033, 2003. (Pubitemid 36538679)
9. Carreras FI, Lehmann GL, Ferri D, Tioni MF, Calamita G, Marinelli RA. Defective hepatocyte aquaporin-8 expression and reduced canalicular membrane water permeability in estrogen-induced cholestasis. Am J Physiol Gastrointest Liver Physiol 292: G905-G912, 2007. (Pubitemid 46440394)
10. Cosentino C, Di Domenico M, Porcellini A, Cuozzo C, De Gregorio G, Santillo MR, Agnese S, Di Stasio R, Feliciello A, Migliaccio A, Avvedimento EV. p85 regulatory subunit of PI3K mediates cAMP-PKA and estrogens biological effects on growth and survival. Oncogene 26: 2095-2103, 2007. (Pubitemid 46514751)
11. Duca L, Debelle L, Debret R, Antonicelli F, Hornebeck W, Haye B. The elastin peptides-mediated induction of pro-collagenase-1 production by human fibroblasts involves activation of MEK/ERK pathway via PKA- and PI(3)K-dependent signaling. FEBS Lett 524: 193-198, 2002.
12. Elkjaer ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frokiaer J, Nielsen S. Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281: F1047-F1057, 2001. (Pubitemid 33716572)
13. Elkjaer ML, Vajda Z, Nejsum LN, Kwon TH, Jensen UB, Amiry- Moghaddam M, Frokiaer J, Nielsen S. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276: 1118-1128, 2000.
14. Ferri D, Mazzone A, Liquori GE, Cassano G, Svelto M, Calamita G. Ontogeny, distribution, and possible functional implications of an unusual aquaporin, AQP8, in mouse liver. Hepatology 38: 947-957, 2003. (Pubitemid 37221678)
15. Folli F, Alvaro D, Gigliozzi A, Bassotti C, Kahn CR, Pontiroli AE, Capocaccia L, Jezequel AM, Benedetti A. Regulation of endocytictranscytotic pathways and bile secretion by phosphatidylinositol 3-kinase in rats. Gastroenterology 113: 954-965, 1997. (Pubitemid 27381157)
16. Garcia F, Kierbel A, Larocca MC, Gradilone SA, Splinter P, LaRusso NF, Marinelli RA. The water channel aquaporin-8 is mainly intracellular in rat hepatocytes and its plasma membrane insertion is stimulated by cyclic AMP. J Biol Chem 276: 12147-12152, 2001. (Pubitemid 37385381)
17. Gorelick DA, Praetorius J, Tsunenari T, Nielsen S, Agre P. Aquaporin- 11: a channel protein lacking apparent transport function expressed in brain [Online]. BMC Biochem 7: 14, 2006. (Pubitemid 43865107)
18. Gradilone SA, Carreras FI, Lehmann GL, Marinelli RA. Phosphatidylinositol- 3-kinase is involved in the glucagon-induced translocation of aquaporin-8 to hepatocyte plasma membrane. Biol Cell 97: 831-836, 2005.
19. Gradilone SA, Garcia F, Huebert RC, Tietz PS, Larocca MC, Kierbel A, Carreras FI, LaRusso NF, Marinelli RA. Glucagon induces the plasma membrane insertion of functional aquaporin-8 water channels in isolated rat hepatocytes. Hepatology 37: 1435-1441, 2003. (Pubitemid 36667324)
20. Hasler U, Mordasini D, Bens M, Bianchi M, Cluzeaud F, Rousselot M, Vandewalle A, Feraille E, Martin PY. Long term regulation of aquaporin- 2 expression in vasopressin-responsive renal collecting duct principal cells. J Biol Chem 277: 10379-10386, 2002.
21. Hilding A, Moller C, Hall KE. Glucagon and GLP-1 stimulate IGFBP-1 secretion in Hep G2 cells without effect on IGFBP-1 mRNA. Growth Horm IGF Res 12: 60-68, 2002.
22. Huebert RC, Splinter PL, García F, Marinelli RA, LaRusso NF. Expression and localization of aquaporin water channels in rat hepatocytes. Evidence for a role in canalicular bile secretion. J Biol Chem 277: 22710-22717, 2002.
23. Immenschuh S, Kietzmann T, Hinke V, Wiederhold M, Katz N, Muller-Eberhard U. The rat heme oxygenase-1 gene is transcriptionally induced via the protein kinase A signaling pathway in rat hepatocyte cultures. Mol Pharmacol 53: 483-491, 1998. (Pubitemid 28162871)
24. Ishibashi K, Kuwahara M, Kageyama Y, Tohsaka A, Marumo F, Sasaki S. Cloning and functional expression of a second new aquaporin abundantly expressed in testis. Biochem Biophys Res Commun 237: 714-718, 1997. (Pubitemid 27434753)
25. Iynedjian PB, Auberger P, Guigoz Y, Le Cam A. Pretranslational regulation of tyrosine aminotransferase and phosphoenolpyruvate carboxykinase (GTP) synthesis by glucagon and dexamethasone in adult rat hepatocytes. Biochem J 225: 77-84, 1985. (Pubitemid 15151958)
26. Kagawa T, Varticovski L, Yoshimichi S, Arias IM. Mechanism by wich cAMP activates PI3-kinase and increases bile acid secretion in WIF-B9 cells. Am J Physiol Cell Physiol 283: C1655-C1666, 2002. (Pubitemid 35340597)
27. King LS, Kozono D, Agre P. From structure to disease: The evolving tale of aquaporin biology. Molec Cell Biol 5: 687-698, 2004. (Pubitemid 39208179)
28. Kojima T, Mitaka T, Shibata Y, Mochizuki Y. Induction and regulation of connexin26 by glucagon in primary cultures of adult rat hepatocytes. J Cell Sci 108: 2771-2780, 1995.
29. Larocca MC, Soria LR, Espelt MV, Lehmann GL, Marinelli RA. The knockdown of hepatocyte aquaporin-8 by RNA interference induces defective bile canalicular water transport. Am J Physiol Gastrointest Liver Physiol 296: G93-G100, 2009.
30. Lee CM, Kim BY, Li L, Morgan ET. Nitric oxide-dependent proteasomal degradation of cytochrome P450 2B proteins. J Biol Chem 283: 889-898, 2008.
31. Lehmann GL, Carreras FI, Soria LR, Gradilone SA, Marinelli RA. LPS induces the TNFα-mediated down-regulation of rat liver aquaporin-8: Role in sepsis-associated cholestasis. Am J Physiol Gastrointest Liver Physiol 294: G567-G575, 2008.
32. Lehmann GL, Marinelli RA. Peritoneal sepsis downregulates liver expression of Aquaporin-8: a water channel involved in bile secretion. Liver Int 29: 317-318, 2009.
33. Lenzen R, Hruby V, Tavoloni N. Mechanism of glucagon choleresis in guinea pigs. Am J Physiol Gastrointest Liver Physiol 259: G736-G744, 1990. (Pubitemid 20385808)
34. Li L, Qi HB. Relationship between cyclic adenosine monophosphate and aquaporin 8 expression and distribution in human amnion-derived cells. Zhonghua Fu Chan Ke Za Zhi 43: 685-689, 2008.
35. Liu X, Harriman JF, Schnellmann RG. Cytoprotective properties of novel nonpeptide calpain inhibitors in renal cells. J Pharmacol Exp Ther 302: 88-94. 2002. (Pubitemid 34680425)
36. Lowry OH, Rosebrough NJ, Farr AL, Randall RJJ. Protein measurements with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
37. Marinelli RA, Tietz PS, Caride AJ, Huang BQ, LaRusso NF. Water transporting properties of hepatocyte basolateral and canalicular plasma membrane domains. J Biol Chem 31: 43157-43162, 2003.
38. Misra S, Ujházy P, Varticovski L, Arias IM. Phosphoinositide 3-kinase lipid products regulate ATP-dependent transport by sister of P-glycoprotein and multidrug resistance associated protein 2 in bile canalicular membrane vesicles. Proc Natl Acad Sci USA 96: 5814-5819, 1999. (Pubitemid 29234701)
39. Nakamura T, Shibata N, Nishimoto-Shibata T, Feng D, Ikemoto M, Motojima K, Iso-O N, Tsukamoto K, Tsujimoto M, Arai H. Regulation of SR-BI protein levels by phosphorylation of its associated protein, PDZK1. Proc Natl Acad Sci USA 102: 13404-13409, 2005. (Pubitemid 41420860)
40. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92: 1013-1017, 1995.
41. Oshima I, Hirota M, Ohboshi C, Shima K. Comparison of half-disappearance times, distribution volumes and metabolic clearance rates of exogenous glucagon-like peptide 1 and glucagon in rats. Regul Pept 21: 85-93, 1988. (Pubitemid 18117754)
42. Puliyanda DP, Ward DT, Baum MA, Hammond TG, Harris HW Jr. Calpain-mediated AQP2 proteolysis in inner medullary collecting duct. Biochem Biophys Res Commun 303: 52-58, 2003.
43. Rudling M, Angelin B. Stimulation of rat hepatic low density lipoprotein receptors by glucagon. Evidence of a novel regulatory mechanism in vivo. J Clin Invest 91: 2796-2805, 1993. (Pubitemid 23182538)
44. Schliess F, Kurz AK, Haussinger D. Glucagon-induced expression of the MAP kinase phosphatase MKP-1 in rat hepatocytes. Gastroenterology 118: 929-936, 2000. (Pubitemid 30243756)
45. Sekar N, Veldhuis JD. Concerted transcriptional activation of the low density lipoprotein receptor gene by insulin and luteinizing hormone in cultured porcine granulosa-luteal cells: possible convergence of protein kinase a, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase signaling pathways. Endocrinology 142: 2921-2928, 2001. (Pubitemid 32575529)
46. Snodgrass PJ, Lin RC, Müller WA, Aoki TT. Induction of urea cycle enzymes of rat liver by glucagon. J Biol Chem 253: 2748-2753, 1978.
47. Tian X, Zamek-Gliszczynski MJ, Zhang P, Brouwer KL. Modulation of multidrug resistance-associated protein 2 (Mrp2) and Mrp3 expression and function with small interfering RNA in sandwich-cultured rat hepatocytes. Mol Pharmacol 66: 1004-1010, 2004. (Pubitemid 39319472)
48. Wang S, Chen J, Au KT, Ross MG. Expression of aquaporin 8 and its up-regulation by cyclic adenosine monophosphate in human WISH cells. Am J Obstet Gynecol 188: 997-1001, 2003. (Pubitemid 36530052)
49. Webster CRL, Anwer MS. Role of the PI3K/PKB signaling pathway in cAMP-mediated translocation of rat liver Ntcp. Am J Physiol Gastrointest Liver Physiol 277: G1165-G1172, 1999.
50. Wei LH, Yang Y, Wu G, Ignarro LJ. IL-4 and IL-13 upregulate ornithine decarboxylase expression by PI3K and MAP kinase pathways in vascular smooth muscle cells. Am J Physiol Cell Physiol 294: C1198-C1205, 2008.
51. Woodcroft KJ, Novak RF. The role of phosphatidylinositol 3-kinase, Src kinase, and protein kinase A signaling pathways in insulin and glucagon regulation of CYP2E1 expression. Biochem Biophys Res Commun 266: 304-307, 1999.
52. Yang F, Kawedia JD, Menon AG. Cyclic AMP regulates aquaporin 5 expression at both transcriptional and post-transcriptional levels through a protein kinase A pathway. J Biol Chem 278: 32173-32180, 2003. (Pubitemid 37048408)
53. Yano Y, Cesar KR, Araujo M, Rodrigues AC Jr, Andrade LC, Magaldi AJ. Aquaporin 2 expression increased by glucagon in normal rat inner medullary collecting ducts. Am J Physiol Renal Physiol 296: F54-F59, 2009.
54. Zhang F, Cheng J, Lam G, Jin DK, Vincent L, Hackett NR, Wang S, Young LM, Hempstead B, Crystal RG, Rafii S. Adenovirus vector E4 gene regulates connexin 40 and 43 expression in endothelial cells via PKA and PI3K signal pathways. Circ Res 96: 950-957, 2005. (Pubitemid 40712794)
55. Zhao AZ, Shinohara MM, Huang D, Shimizu M, Eldar-Finkelman H, Krebs EG, Beavo JA, Bornfeldt KE. Leptin induces insulin-like signaling that antagonizes cAMP elevation by glucagon in hepatocytes. J Biol Chem 275: 11348-11354, 2000. (Pubitemid 30212785)