E2f1-deficient NOD/SCID mice have dry mouth due to a change of acinar/duct structure and the down-regulation of AQP5 in the salivary gland

Pflugers Archiv European Journal of Physiology

Volumn 465, Issue 2, 2013, Pages 271-281

  Satoh, Keitaro ^a   Narita, Takanori ^b   Matsuki Fukushima, Miwako ^b   Okabayashi, Ken ^b   Ito, Tatsuro ^b,c   Senpuku, Hidenobu ^c   Sugiya, Hiroshi ^b,d  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d TOKYO DENTAL COLLEGE   (Japan)

Author keywords

AQP5 protein; Disease model; Down regulation; Dry mouth; Salivary glands; Ubiquitin

Indexed keywords

AQUAPORIN 5; MESSENGER RNA; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; PILOCARPINE;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; GENE EXPRESSION REGULATION; HYPOSALIVATION; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR PATHOLOGY; MOUSE; MUSCARINIC M1 RECEPTOR GENE; MUSCARINIC M2 RECEPTOR GENE; MUSCARINIC M3 RECEPTOR GENE; NONHUMAN; NONOBESE DIABETIC MOUSE; PAROTID GLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR GENE; SALIVATION; SCID MOUSE; SUBMANDIBULAR GLAND; UBIQUITINATION; WESTERN BLOTTING; XEROSTOMIA;

ACINAR CELLS; ANIMALS; AQUAPORIN 5; CELL MEMBRANE; CYTOSOL; DOWN-REGULATION; DRINKING; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PAROTID GLAND; PILOCARPINE; SALIVARY DUCTS; SALIVATION; SUBMANDIBULAR GLAND; UBIQUITINATION; XEROSTOMIA;

EID: 84873415348     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-012-1183-y     Document Type: Article

References (49)

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(Pt 1):3-16
2. Akamatsu T, Azlina A, Purwanti N, Karabasil MR, Hasegawa T, Yao C, Hosoi K (2009) Inhibition and transcriptional silencing of a subtilisin-like proprotein convertase, PACE4/SPC4, reduces the branching morphogenesis of and AQP5expression in rat embryonic submandibular gland. Dev Biol 325(2):434-443
3. Annicotte JS, Blanchet E, Chavey C, Iankova I, Costes S, Assou S, Teyssier J, Dalle S, Sardet C, Fajas L (2009) The CDK4-pRB-E2F1 pathway controls insulin secretion. Nat Cell Biol 11(8):1017-1023
4. Blazsek J, Varga G (1999) Secretion from minor salivary glands following ablation of the major salivary glands in rats. Arch Oral Biol 44:S45-S48
5. 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
6. Chen ZJ, Sun LJ (2009) Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33(3):275-286
7. Dibas A, Yang MH, He S, Bobich J, Yorio T (2008) Changes in ocular aquaporin-4 (AQP4) expression following retinal injury. Mol Vis 14:1770-1783
8. Entesarian M, Matsson H, Klar J, Bergendal B, Olson L, Arakaki R, Hayashi Y, Ohuchi H, Falahat B, Bolstad AI, Jonsson R, Wahren-Herlenius M, Dahl N (2005) Mutations in the gene encoding fibroblast growth factor 10 are associated with aplasia of lacrimal and salivary glands. Nat Genet 37(2):125-127
9. Epstein AN, Spector D, Samman A, Goldblum C (1964) Exaggerated prandial drinking in the rat without salivary glands. Nature 201:1342-1343
10. Fox RI, Stern M, Michelson P (2000) Update in Sjögren syndrome. Curr Opin Rheumatol 12(5):391-398
11. Gresz V, Kwon TH, Gong H, Agre P, Steward MC, King LS, Nielsen S (2004) Immunolocalization of AQP-5 in rat parotid and submandibular salivary glands after stimulation or inhibition of secretion in vivo. Am J Physiol Gastrointest Liver Physiol 287(1):G151-G161
12. Hamada A, Inenaga K, Nakamura S, Terashita M, Yamashita H (2000) Disorder of salivary secretion in inbred polydipsic mouse. Am J Physiol Regul Integr Comp Physiol 278(4):R817-R823
13. Helin K, Lees JA, Vidal M, Dyson N, Harlow E, Fattaey A (1992) A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70(2):337-350
14. Henson BS, Inglehart MR, Eisbruch A, Ship JA (2001) Preserved salivary output and xerostomia-related quality of life in head and neck cancer patients receiving parotid-sparing radiotherapy. Oral Oncol 37(1):84-93
15. Hu Y, Nakagawa Y, Purushotham KR, Humphreys-Beher MG (1992) Functional changes in salivary glands of autoimmune disease-prone NOD mice. Am J Physiol 263(4 Pt 1):E607-E614
16. Iglesias A, Murge M, Laresgoiti U, Skoudy A, Bernales I, Fullaondo A, Moreno B, Lloreta J, Field SJ, Real FX, Zubiaga AM (2004) Diabetes and exocrine pancreatic insufficiency in E2F1/E2F2 double-mutant mice. J Clin Invest 113(10):1398-1407
17. Jaskoll T, Abichaker G, Witcher D, Sala FG, Bellusci S, Hajihosseini MK, Melnick M (2005) FGF10/FGFR2b signaling plays essential roles during in vivo embryonic submandibular salivary gland morphogenesis. BMC Dev Biol 5:11. doi: 10.1186/1471-213X-5-11
18. Kaelin WG Jr, Krek W, Sellers WR, DeCaprio JA, Ajchenbaum F, Fuchs CS, Chittenden T, Li Y, Farnham PJ, Blanar MA, Livingston DM, Flemington EK (1992) Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70(2):351-364
19. Karabasil MR, 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(2):69-86
20. King LS, Agre P (1996) Pathophysiology of the aquaporin water channels. Annu Rev Physiol 58:619-648
21. Konttinen YT, Tensing EK, Laine M, Porola P, Törnwall J, Hukkanen M (2005) Abnormal distribution of aquaporin-5 in salivary glands in the NOD mouse model for Sjögren's syndrome. J Rheumatol 32(6):1071-1075
22. La Thangue NB (1994) DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control. Trends Biochem Sci 19(3):108-114
23. Leitch V, Agre P, King LS (2001) Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. Proc Natl Acad Sci U S A 98(5):2894-2898
24. Leiter EH, Prochazka M, Coleman DL (1987) The non-obese diabetic (NOD) mouse. Am J Pathol 128(2):380-383
25. 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(29):20071-20074
26. Matsui-Inohara H, Uematsu H, Narita T, Satoh K, Yonezawa H, Kuroda K, Ito T, Yoneda S, Kawarai T, Sugiya H, Watanabe H, Senpuku H (2009) E2F-1-deficient NOD/SCID mice developed showing decreased saliva production. Exp Biol Med (Maywood) 234(12):1525-1536
27. 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(3):119-126
28. Matsumoto N, Salam MA, Watanabe H, Amagasa T, Senpuku H (2004) Role of gene E2f1 in susceptibility to bacterial adherence of oral streptococci to tooth surfaces in mice. Oral Microbiol Immunol 19(4):270-276
29. Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999) Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 295(3):513-521
30. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS (1998) Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12(20):3156-3161
31. 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(6):G1081-G1088
32. Nakamura T, Matsui M, Uchida K, Futatsugi A, Kusakawa S, Matsumoto N, Nakamura K, Manabe T, Taketo MM, Mikoshiba K (2004) M(3) muscarinic acetylcholine receptor plays a critical role in parasympathetic control of salivation in mice. J Physiol 558(Pt 2):561-575
33. Nandigama R, Bonitz M, Papadakis T, Schwantes U, Bschleipfer T, Kummer W (2010) Muscarinic acetylcholine receptor subtypes expressed by mouse bladder afferent neurons. Neuroscience 168(3):842-850
34. Nevins JR (1992) E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258(5081):424-429
35. Ohashi Y, Ishida R, Kojima T, Goto E, Matsumoto Y, Watanabe K, Ishida N, Nakata K, Takeuchi T, Tsubota K (2003) Abnormal protein profiles in tears with dry eye syndrome. Am J Ophthalmol 136(2):291-299
36. Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277(3):643-649
37. Quissell DO, Watson E, Dowd FJ (1992) Signal transduction mechanisms involved in salivary gland regulated exocytosis. Crit Rev Oral Biol Med 3(1-2):83-107
38. Robinson CP, Yamamoto H, Peck AB, Humphreys-Beher MG (1996) Genetically programmed development of salivary gland abnormalities in the NOD (nonobese diabetic)-scid mouse in the absence of detectable lymphocytic infiltration: a potential trigger for sialoadenitis of NOD mice. Clin Immunol Immunopathol 79(1):50-59
39. Salam MA, Matin K, Matsumoto N, Tsuha Y, Hanada N, Senpuku H (2004) E2f1 mutation induces early onset of diabetes and Sjögren's syndrome in nonobese diabetic mice. J Immunol 173(8):4908-4918
40. Satoh K, Seo Y, Matsuo S, Karabasil MR, Matsuki-Fukushima M, Nakahari T, Hosoi K (2012) 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. Pflügers Arch 464(4):375-389. doi: 10.1007/s00424-012-1141-8
41. Schein OD, Hochberg MC, Muñoz B, Tielsch JM, Bandeen-Roche K, Provost T, Anhalt GJ, West S (1999) Dry eye and dry mouth in the elderly: a population-based assessment. Arch Intern Med 159(12):1359-1363
42. Senpuku H (2010) Model mouse designed for oral biofilm formation studies. Int J Oral-Med Sci 8(3):125-131
43. Shan B, Lee WH (1994) Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol Cell Biol 14(12):8166-8173
44. Ship JA, Pillemer SR, Baum BJ (2002) Xerostomia and the geriatric patient. J Am Geriatr Soc 50(3):535-543
45. Soyfoo MS, De Vriese C, Debaix H, Martin-Martinez MD, Mathieu C, Devuyst O, Steinfeld SD, Delporte C (2007) Modified aquaporin 5 expression and distribution in submandibular glands from NOD mice displaying autoimmune exocrinopathy. Arthritis Rheum 56(8):2566-2574
46. Steinfeld S, Cogan E, King LS, Agre P, Kiss R, Delporte C (2001) Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjögren's syndrome patients. Lab Investig 81(2):143-148
47. Tashiro E, Minato Y, Maruki H, Asagiri M, Imoto M (2003) Regulation of FGF receptor-2 expression by transcription factor E2F-1. Oncogene 22(36):5630-5635
48. Turner RJ, Sugiya H (2002) Understanding salivary fluid and protein secretion. Oral Dis 8(1):3-11
49. Yuasa K, Suzue K, Nagahama M, Matsuda Y, Tsuji A (2007) Transcriptional regulation of subtilisin-like proprotein convertase PACE4 by E2F: possible role of E2F-mediated upregulation of PACE4 in tumor progression. Gene 402(1-2):103-110