Roles of lysosomal proteolytic systems in AQP5 degradation in the submandibular gland of rats following chorda tympani parasympathetic denervation

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 299, Issue 5, 2010, Pages

  Azlina, Ahmad ^a   Javkhlan, Purevjav ^a   Hiroshima, Yuka ^a   Hasegawa, Takahiro ^a   Yao, Chenjuan ^a   Akamatsu, Tetsuya ^a   Hosoi, Kazuo ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Apoptosis; Autophagy; LC3B; Lysosomal proteolysis; Protein degradation

Indexed keywords

AQUAPORIN 5; CATHEPSIN B; CATHEPSIN L; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 ISOFORM B; PROTEIN BAX; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ACINAR CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTONOMIC DENERVATION; AUTOPHAGY; CELL SIZE; CHORDA TYMPANI; IMMUNOHISTOCHEMISTRY; LYSOSOME; MALE; NICK END LABELING; NONHUMAN; ORGAN SIZE; PARASYMPATHETIC FUNCTION; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SALIVATION; SUBMANDIBULAR GLAND; VAGOTOMY; ANIMAL; INJURY; INNERVATION; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AQUAPORIN 5; BLOTTING, WESTERN; CHORDA TYMPANI NERVE; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOMES; MALE; PARASYMPATHECTOMY; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; SUBMANDIBULAR GLAND;

EID: 78149480198     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00194.2010     Document Type: Article

References (61)

1. Akamatsu T, Parvin MN, Murdiastuti K, Kosugi-Tanaka C, Yao C, Miki O, Kanamori N, Hosoi K. Expression and localization of aquaporins, members of the water channel family, during development of the rat submandibular gland. Pflügers Arch 446: 641-651, 2003.
2. Baskin-Bey ES, Canbay A, Bronk SF, Werneburg N, Guicciardi ME, Nyberg SL, Gores GJ. Cathepsin B inactivation attenuates hepatocyte apoptosis and liver damage in steatotic livers after cold ischemia-warm reperfusion injury. Am J Physiol Gastrointest Liver Physiol 288: G396-G402, 2005.
3. Bichet DG, Turner M, Morin D. Vasopressin receptor mutations causing nephrogenic diabetes insipidus. Proc Assoc Am Physicians 110: 387-394, 1998.
4. Carpenter GH, Khosravani N, Ekström J, Osailan SM, Paterson KP, Proctor GB. Altered plasticity of the parasympathetic innervation in the recovering rat submandibular gland following extensive atrophy. Exp Physiol 94: 213-219, 2009.
5. Carpenter GH, Proctor GB, Garrett JR. Preganglionic parasympathectomy decreases salivary SIgA secretion rates from the rat submandibular gland. J Neuroimmunol 160: 4-11, 2005.
6. Catalán V, Gómez-Ambrosi J, Pastor C, Rotellar F, Silva C, Rodríguez A, Gil MJ, Cienfuegos JA, Salvador J, Vendrell J, Frühbeck G. Influence of morbid obesity and insulin resistance on gene expression levels of AQP7 in visceral adipose tissue and AQP9 in liver. Obes Surg 18: 695-701, 2008.
7. Chaparro O, Yu WH, Shaw PA. Isoproterenol-induced expression of the cystatin S gene in submandibular glands of parasympathectomized rats. Brain Res Mol Brain Res 61: 136-146, 1998.
8. Dibas A, Oku H, Fukuhara M, Kurimoto T, Ikeda T, Patil RV, Sharif NA, Yorio T. Changes in ocular aquaporin expression following optic nerve crush. Mol Vis 16: 330-340, 2010.
9. Egami Y, Kiryu-Seo S, Yoshimori T, Kiyama H. Induced expressions of Rab24 GTPase and LC3 in nerve-injured motor neurons. Biochem Biophys Res Commun 337: 1206-1213, 2005.
10. Ekström J. Role of nonadrenergic, noncholinergic autonomic transmitters in salivary glandular activities in vivo, In: Neural Mechanisms of Salivary Glands. Frontiers of Oral Biology (vol. 11), edited by Garrett JR, Ekström J, Anderson LC. Basel: Karger, 1999, p. 94-130.
11. Elkjaer ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frøkiaer J, Nielsen S. Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281: F1047-F1057, 2001.
12. Endoh T. Modulation of voltage-dependent calcium channels by neurotransmitters and neuropeptides in parasympathetic submandibular ganglion neurons. Arch Oral Biol 49: 539-557, 2004.
13. Eulalio A, Huntzinger E, Nishihara T, Rehwinkel J, Fauser M, Izaurralde E. Deadenylation is a widespread effect of miRNA regulation. RNA 15: 21-32, 2009.
14. Fletcher JI, Meusburger S, Hawkins CJ, Riglar DT, Lee EF, Fairlie WD, Huang DC, Adams JM. Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax. Proc Natl Acad Sci USA 105: 18081-18087, 2008.
15. Fukasawa KM, Harada M. Purification and properties of dipeptidyl peptidase IV from Streptococcus mitis ATCC 9811. Arch Biochem Biophys 210: 230-237, 1981.
16. Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361: 549-552, 1993.
17. Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788: 1213-1228, 2009.
18. Gonen T, Sliz P, Kistler J, Cheng Y, Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429: 193-197, 2004.
19. Hironaka T, Matsuoka T, Kikuchi K, Aiyama S. Morphological changes in mouse sublingual gland parenchyma subjected to chorda tympani resection. Okajimas Folia Anat Jpn 80: 41-46, 2003.
20. Ishibashi K, Hara S, Kondo S. Aquaporin water channels in mammals. Clin Exp Nephrol 13: 107-117, 2009.
21. Izumi H, Karita K. Parasympathetic-mediated reflex salivation and vasodilatation in the cat submandibular gland. Am J Physiol Regul Integr Comp Physiol 267: R747-R753, 1994.
22. Kawedia JD, Nieman ML, Boivin GP, Melvin JE, Kikuchi K, Hand AR, Lorenz JN, Menon AG. Interaction between transcellular and paracellular water transport pathways through Aquaporin 5 and the tight junction complex. Proc Natl Acad Sci USA 104: 3621-3626, 2007.
23. King LS, Agre P. Pathophysiology of the aquaporin water channels. Annu Rev Physiol 58: 619-648, 1996.
24. King LS, Nielsen S, Agre P. Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat. Am J Physiol Cell Physiol 273: C1541-C1548, 1997.
25. Kirschke H. Cathepsin L. In: Handbook of Proteolytic Enzymes (vol. 2; 2nd ed.), edited by Barrett AJ, Rawlings ND, and Woessner JF. London: Elsevier, 2004, p. 1097-1102.
26. Kishida K, Inoue K, Kuriyama H, Nakamura T, Fushiki T, Kihara S, Shimomura I. Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc Natl Acad Sci USA 102: 10993-10998, 2005.
27. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
28. +-ATPase from the submandibular gland of rats. Biochim Biophys Acta 1039: 234-240, 1990.
29. Kuriyama H, Shimomura I, Kishida K, Kondo H, Furuyama N, Nishizawa H, Maeda N, Matsuda M, Nagaretani H, Kihara S, Nakamura T, Tochino Y, Funahashi T, Matsuzawa Y. Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9. Diabetes 51: 2915-2921, 2002.
30. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
31. Lee J, Yoo K, Kim SW, Jung KH, Ma SK, Lee YK, Kim WY, Kim J, Choi KC. Decreased expression of aquaporin water channels in denervated rat kidney. Nephron Physiol 103: 170-178, 2006.
32. Li X, Azlina A, Karabasil MR, Purwanti N, Hasegawa T, Yao C, Akamatsu T, Hosoi K. Degradation of submandibular gland AQP5 by parasympathetic denervation of chorda tympani and its recovery by cevimeline, an M3 muscarinic receptor agonist. Am J Physiol Gastrointest Liver Physiol 295: G112-G123, 2008.
33. Liu J. Control of protein synthesis and mRNA degradation by microRNAs. Curr Opin Cell Biol 20: 214-221, 2008.
34. Ma L, Huang YG, He H, Deng YC, Zhang HF, Che HL, Tian JY, Zhao G. Postnatal expression and denervation induced up-regulation of aquaporin-5 protein in rat sweat gland. Cell Tissue Res 329: 25-33, 2007.
35. Ma T, Song Y, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS. Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 274: 20071-20074, 1999.
36. Maeda N, Funahashi T, Hibuse T, Nagasawa A, Kishida K, Kuriyama H, Nakamura T, Kihara S, Shimomura I, Matsuzawa Y. Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue. Proc Natl Acad Sci USA 101: 17801-17806, 2004.
37. Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K. Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 295: 513-521, 1999.
38. Mooney SM, Miller MW. Expression of bcl-2, bax, and caspase-3 in the brain of the developing rat. Brain Res Dev Brain Res 123: 103-117, 2000.
39. Morris CA, Morris LD, Kennedy AR, Sweeney HL. Attenuation of skeletal muscle atrophy via protease inhibition. J Appl Physiol 99: 1719-1727, 2005.
40. Mort JS. Cathepsin B. In: Handbook of Proteolytic Enzymes (vol. 2; 2nd ed.), edited by Barrett AJ, Rawlings ND, and Woessner JF. London: Elsevier, 2004, p. 1079-1086.
41. Murakami M, Murdiastuti K, Hosoi K, Hill AE. AQP and the control of fluid transport in a salivary gland. J Membr Biol 210: 91-103, 2006.
42. Murdiastuti K, Miki O, Yao C, Parvin MN, Kosugi-Tanaka C, Akamatsu T, Kanamori N, Hosoi K. Divergent expression and localization of aquaporin 5, an exocrine-type water channel, in the submandibular gland of Sprague-Dawley rats. Pflügers Arch 445: 405-412, 2002.
43. Murdiastuti K, Purwanti N, Karabasil MR, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K. 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, 2006.
44. Nielsen S, DiGiovanni SR, Christensen EI, Knepper MA, Harris HW. Cellular and subcellular immunolocalization of vasopressin-regulated water channel in rat kidney. Proc Natl Acad Sci USA 90: 11663-11667, 1993.
45. Németh-Cahalan KL, Hall JE. pH and calcium regulate the water permeability of aquaporin 0. J Biol Chem 275: 6777-6782, 2000.
46. 2+ regulation of aquaporin water permeability. J Gen Physiol 123: 573-580, 2004.
47. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74: 609-619, 1993.
48. Parisier SC, Blitzer A, Binder WJ, Friedman WF, Marovitz WF. Tympanic neurectomy and chorda tympanectomy for the control of drooling. Arch Otolaryngol 104: 273-277, 1978.
49. Peronace AA, Davison TA, Housay AB, Perec J. Alterations in submandibular and retrolingual glands following parasympathetic denervation in rats. Anat Rec 150: 25-34, 1964.
50. Proctor GB, Carpenter GH. Regulation of salivary gland function by autonomic nerves. Auton Neurosci 133: 3-18, 2007.
51. Raina S, Preston GM, Guggino WB, Agre P. Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. J Biol Chem 270: 1908-1912, 1995.
52. Rossé T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B, Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391: 496-499, 1998.
53. Sahara N, Suzuki K. Ultrastructural localization of dipeptidyl peptidase IV in rat salivary glands by immunocytochemistry. Cell Tissue Res 235: 427-432, 1984.
54. Sidhaye V, Hoffert JD, King LS. cAMP has distinct acute and chronic effects on aquaporin-5 in lung epithelial cells. J Biol Chem 280: 3590-3596, 2005.
55. Silver N, Proctor GB, Arno M, Carpenter GH. Activation of mTOR coincides with autophagy during ligation-induced atrophy in the rat submandibular gland. Cell Death Dis 1: 1-10, 2010.
56. Siu PM, Alway SE. Mitochondria-associated apoptotic signaling in denervated rat skeletal muscle. J Physiol 565: 309-323, 2005.
57. Van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, van der Sluijs P, Deen PM. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J Biol Chem 277: 41473-41479, 2002.
58. Wellner RB, Redman RS, Swaim WD, Baum BJ. Further evidence for AQP8 expression in the myoepithelium of rat submandibular and parotid glands. Pflügers Arch 451: 642-645, 2006.
59. Yao C, Li X, Murdiastuti K, Kosugi-Tanaka C, Akamatsu T, Kanamori N, Hosoi K. Lipopolysaccharide-induced elevation and secretion of interleukin-1β in the submandibular gland of male mice. Immunology 116: 213-222, 2005.
60. Yao C, Purwanti N, Karabasil MR, Azlina A, Javkhlan P, Hasegawa T, Akamatsu T, Hosoi T, Ozawa K, Hosoi K. Potential down-regulation of salivary gland AQP5 by LPS via cross-coupling of NF-κB and p-c- Jun/c-Fos. Am J Pathol 177: 724-734, 2010.
61. Zha H, Aimé-Sempé C, Sato T, Reed JC. Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J Biol Chem 271: 7440-7444, 1996.