Roles of AQP5/AQP5-G103D in carbamylcholine-Induced volume decrease and in reduction of the activation energy for water transport by rat parotid acinar cells

Pflugers Archiv European Journal of Physiology

Volumn 464, Issue 4, 2012, Pages 375-389

  Satoh, Keitaro ^a   Seo, Yoshiteru ^a   Matsuo, Shinsuke ^d   Karabasil, Mileva Ratko ^d,e   Matsuki Fukushima, Miwako ^b   Nakahari, Takashi ^c   Hosoi, Kazuo ^d  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c OSAKA MEDICAL COLLEGE   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

^e UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

1H NMR; Activation energy; Cell volume; Parotid gland; Salivary secretion; Water permeability

Indexed keywords

AQUAPORIN 5; CARBACHOL;

ACINAR CELL; ACTIVATION ENERGY; ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL LEVEL; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; ENERGY; IMMUNOHISTOCHEMISTRY; MUTANT; NONHUMAN; PAROTID GLAND; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; WATER PERMEABILITY; WATER TRANSPORT; WILD TYPE;

ACINAR CELLS; ANIMALS; AQUAPORIN 5; CARBACHOL; CELL MEMBRANE PERMEABILITY; CELL SIZE; MUTATION; PAROTID GLAND; RATS; RATS, MUTANT STRAINS; WATER;

EID: 84866733915     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-012-1141-8     Document Type: Article

References (45)

1. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels from atomic structure to clinical medicine. J Physiol 542:3-16
2. Baker OJ (2010) Tight junctions in salivary epithelium. J Biomed Biotechnol 2010:278948
3. Bernfeld P (1955) Amylase α and β. Methods Enzymol 1:149-158
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
5. Carbrey JM, Agre P (2009) Discovery of the aquaporins and development of the field. Handb Exp Pharmacol 190:3-28
6. Carpi-Medina P, Leon V, Espidel J,Whittembury G (1988) Diffusive water permeability in isolated kidney proximal tubular cells: nature of the cellular water pathways. J Membr Biol 104:35-43
7. Delporte C (2009) Aquaporins in secretory glands and their role in Sjögren's syndrome. In: Beitz E (ed) Aquaporins: handbook of experimental pharmacology 190. Springer, Berlin, pp 185-201
8. Echevarría M, Windhager EE, Frindt G (1996) Selectivity of the renal collecting duct water channel aquaporin-3. J Biol Chem 271:25079-25082
9. Fabry ME, Eisenstadt M (1975) Water exchange between red cells and plasma. Measurement by nuclear magnetic relaxation. Biophys J 15:1101-1110
10. Hasegawa T, Azlina A, Javkhlan P, Yao C, Akamatsu T, Hosoi K (2011) Novel phosphorylation of aquaporin-5 at its threonine 259 through cAMP signaling in salivary gland cells. Am J Physiol Cell Physiol 301:C667-C678
11. Hashizume A, Ueno T, Furuse M, Tsukita S, Nakanishi Y, Hieda Y (2004) Expression patterns of claudin family of tight junction membrane proteins in developing mouse submandibular gland. Dev Dyn 231:425-431
12. Imai Y, Nishikawa H, Yoshizaki K, Watari H (1973) Evidence for the osmotic flow across dog submaxillary gland epithelia as a cause of salivary secretion. Jpn J Physiol 23:635-644
13. Ishikawa Y, Eguchi T, Skowronski MT, Ishida H (1998) Acetylcholine acts on M3 muscarinic receptors and induces the translocation of aquaporin5 water channel via cytosolic Ca2+ elevation in rat parotid glands. Biochem Biophys Res Commun 245:835-840
14. KarabasilMR, Hasegawa T, Azlina A, Purwanti N,Yao C, Akamatsu T, Tomioka S, Hosoi K (2011) Effects of naturally occurring G103D point mutation of AQP5 on its water permeability, trafficking and cellular localization in the submandibular gland of rats. Biol Cell 103:69-86
15. Kawedia JD, Nieman ML, Boivin GP, Melvin JE, Kikuchi K, Hand AR, Lorenz JN, Menon AG (2007) Interaction between transcellular and paracellular water transport pathways through Aquaporin 5 and the tight junction complex. Proc Natl Acad Sci USA 104:3621-3626
16. Koenig SH, Ahkong QF, Brown RD 3rd, Lafleur M, Spiller M, Unger E, Tilcock C (1992) Permeability of liposomal membranes to water: results from the magnetic field dependence of T1 of solvent protons in suspensions of vesicles with entrapped paramagnetic ions. Magn Reson Med 23:275-286
17. Kosugi-Tanaka C, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K (2006) Protein kinase A-regulated membrane trafficking of a green fluorescent protein-aquaporin 5 chimera in MDCK cells. Biochim Biophys Acta, Mol Cell Res 1763:337-344
18. Lavelle JP, Negrete HO, Poland PA, Kinlough CL, Meyers SD, Hughey RP, Zeidel ML (1997) Low permeabilities of MDCK cell monolayers: a model barrier epithelium. Am J Physiol 273:F67-F75
19. Lee MD, King LS, Agre P (1999) The aquaporin family of water channel proteins in clinical medicine. Medicine (Baltimore) 76: 141-156
20. Ma T, Song Y, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1999) Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 274:20071-20074
21. Mathai JC, Mori S, Smith BL, Preston GM, Mohandas N, Collins M, van Zijl PC, Zeidel ML, Agre P (1996) Functional analysis of aquaporin-1 deficient red cells. The Colton-null phenotype. J Biol Chem 271:1309-1313
22. Matsuki M, Hashimoto S, Shimono M, Murakami M, Fujita-Yoshigaki J, Furuyama S, Sugiya H (2005) Involvement of aquaporin-5 water channel in osmoregulation in parotid secretory granules. J Membr Biol 203:119-126
23. Murakami M, Murdiastuti K, Hosoi K, Hill AE (2006) AQP and the control of fluid transport in a salivary gland. J Membr Biol 210:91-103
24. Murakami M, Shachar-Hill B, Steward MC, Hill AE (2001) The paracellular component of water flow in the rat submandibular salivary gland. J Physiol 537:899-906
25. Murakami M, Suzuki E, Miyamoto S, Seo Y, Watari H (1989) Direct measurement of K movement by 39K NMR in perfused rat mandibular salivary gland stimulated with acetylcholine. Pflugers Arch 414:385-392
26. Murdiastuti K, Miki O, Yao C, Parvin MN, Kosugi-Tanaka C, Akamatsu T, Kanamori N, Hosoi K (2002) Divergent expression and localization of aquaporin 5, an exocrine-type water channel, in the submandibular gland of Sprague-Dawley rats. Pflugers Arch 445:405-412
27. Murdiastuti K, Purwanti N, Karabasil MR, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K (2006) A naturally occurring point mutation in the rat aquaporin 5 gene, influencing its protein production by and secretion of water from salivary glands. Am J Physiol Gastrointest Liver Physiol 291:G1081-G1088
28. Nakahari T, Imai Y (1998) Transient swelling of salivary acinus induced by acetylcholine stimulation: water secretion pathway in rat submandibular gland. J Membr Biol 161:287-296
29. Nakahari T, Murakami M, Kataoka T (1989) Shrinkage of rat mandibular acinar cell with acetylcholine detected by videoenhanced contrast in microscopy. Jpn J Physiol 39:609-615
30. Nakahari T, Murakami M, Yoshida H, Miyamoto M, Sohma Y, Imai Y (1990) Decrease in rat submandibular acinar cell volume during ACh stimulation. Am J Physiol 258:G878-G886
31. Nauntofte B (1992) Regulation of electrolyte and fluid secretion in salivary acinar cells. Am J Physiol 263:G823-G837
32. Novak I, Dave CC, Young JA (1984) The anionic basis of secretion by rat and rabbit mandibular glands. In: Case RM, Lingard JA, Young JA (eds) Secretion: mechanisms and control. Manchester University Press, Manchester, pp 77-80
33. Price HD, Thompson TE (1969) Properties of liquid bilayer membranes separating two aqueous phases: temperature dependence of water permeability. J Mol Biol 41:443-457
34. Raina S, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. J Biol Chem 270:1908-1912
35. Redwood WR, Haydon DA (1969) Influence of temperature and membrane composition on the water permeability of lipid bilayers. J Theor Biol 22:1-8
36. Rosenberg PA, Finkelstein A (1978) Water permeability of gramicidin A-treated lipid bilayer membranes. J Gen Physiol 72:341-350
37. Satoh K, Matsuki-Fukushima M, Qi B, Guo M, Narita T, Fujita-Yoshigaki J, Sugiya H (2009) Phosphorylation of myristoylated alanine-rich C kinase substrate is involved in the cAMP-dependent amylase release in parotid acinar cells. Am J Physiol Gastrointest Liver Physiol 296:G1382-G1390
38. Schwarzbauer C, Morrissey SP, Deichmann R, Hillenbrand C, Syha J, Adolf H, Noth U, Haase A (1997) Quantitative magnetic resonance imaging of capillary water permeability and regional blood volume with an intravascular MR contrast agent. Magn Reson Med 37:769-777
39. Segawa A (1994) Tight junctional permeability in living cells: dynamic changes directly visualized by confocal laser microscopy. J Electron Microsc (Tokyo) 43:290-298
40. Solenov E, Watanabe H, Manley GT, Verkman AS (2004) Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286:C426-C232
41. Steward MC, Seo Y, Rawlings JM, Case RM (1990) Water permeability of acinar cell membranes in the isolated perfused rabbit mandibular salivary gland. J Physiol 431:571-583
42. Suzuki Y, Ohtsuyama M, Samman G, Sata F, Sato K (1991) Ionic basis of methacholine-induced shrinkage of dissociated eccrine clear cells. J Membr Biol 123:33-41
43. Tada J, Sawa T, Yamanaka N, Shono M, Akamatsu T, Tsumura K, Parvin MN, Kanamori N, Hosoi K (1999) Involvement of vesicle-cytoskeleton interaction in AQP5 trafficking in AQP5-genetransfected HSG cells. Biochem Biophys Res Commun 266:443-447
44. Verkman AS (2000) Water permeability measurement in living cells and complex tissues. J Membr Biol 173:73-87
45. Yasui M (2009) pH regulated anion permeability of aquaporin-6. In: Beitz E (ed) Aquaporins: handbook of experimental pharmacology 190. Springer, Berlin, pp 299-308