physiology and Pathophysiology of bicarbonate secretion by pancreatic duct epithelium

Nagoya Journal of Medical Science

Volumn 74, Issue 1-2, 2012, Pages 1-18

  Ishiguro, Hiroshi ^a,b   Yamamoto, Akiko ^a   Nakakuki, Miyuki ^a   Yi, Lanjuan ^a   Ishiguro, Mariko ^a   Yamaguchi, Makoto ^a   Kondo, Shiho ^a   Mochimaru, Yuka ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Alcoholic pancreatitis; CFTR; Cystic fibrosis; Isolated pancreatic duct

Indexed keywords

ALCOHOL; BICARBONATE; GLUCOSE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ACTIVE TRANSPORT; ANIMAL; CYSTIC FIBROSIS; DRUG EFFECT; EPITHELIUM CELL; HUMAN; METABOLISM; PANCREAS DISEASE; PANCREAS DUCT; PANCREAS JUICE; PATHOPHYSIOLOGY; REVIEW; SECRETION;

ANIMALS; BICARBONATES; BIOLOGICAL TRANSPORT, ACTIVE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; ETHANOL; GLUCOSE; HUMANS; PANCREATIC DISEASES; PANCREATIC DUCTS; PANCREATIC JUICE;

EID: 84860615898     PISSN: 00277622     EISSN: 21863326     Source Type: Journal    
DOI: None     Document Type: Article

References (84)

1. Kopelman H, Corey M, Gaskin K, Durie P, Weizman Z, Forstner G. Impaired chloride secretion, as well as bicarbonate secretion, underlies the fluid secretory defect in the cystic fibrosis pancreas. Gastroenterology, 1988; 95: 349-55.
2. Freedman SD. New concepts in understanding the pathophysiology of chronic pancreatitis. Int J Pancreatol, 1998; 24: 1-8.
3. Ashizawa N, Sakai T, Yoneyama T, Naora H, Kinoshita Y. Three-dimensional structure of peripheral exocrine gland in rat pancreas: reconstruction using transmission electron microscopic examination of serial sections. Pancreas, 2005; 31: 401-404.
4. Fanjul M, Alvarez L, Salvador C, Gmyr V, Kerr-Conte J, Pattou F, Carter N, Hollande E. Evidence for a membrane carbonic anhydrase IV anchored by its C-terminal peptide in normal human pancreatic ductal cells. Histochem Cell Biol, 2004; 121: 91-99.
5. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL, Drumm ML, Iannuzzi MC, Collins FS, Tsui LC. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science, 1989; 245: 1066-1073.
6. Quinton PM. Chloride impermeability in cystic fibrosis. Nature, 1983; 301: 421-422.
7. Steward MC, Ishiguro H, Case RM. Mechanisms of bicarbonate secretion in the pancreatic duct. Annu Rev Physiol, 2005; 67: 377-409.
8. Burghardt B, Nielsen S, Steward MC. The role of aquaporin water channels in fluid secretion by the exocrine pancreas. J Membr Biol, 2006; 210: 143-153.
9. Burghardt B, Elkaer ML, Kwon TH, Rácz GZ, Varga G, Steward MC, Nielsen S. Distribution of aquaporin water channels AQP1 and AQP5 in the ductal system of the human pancreas. Gut, 2003; 52: 1008-1016.
10. Case RM, Argent BE. Pancreatic duct cell secretion: control and mechanisms of transport. In: The Pancreas: Biology, Pathobiology and Disease, 2nd edition, edited by Go VLW, DiMagno EP, Gardner JD, Labenthal E, Reher HA, and Scheele GA. pp. 301-350, 1993, Raven, New York.
11. Lightwood R, Reber HA. Micropuncture study of pancreatic secretion in the cat. Gastroenterology, 1977; 72: 61-66.
12. Arkle S, Lee CM, Cullen MJ, Argent BE. Isolation of ducts from the pancreas of copper-deficient rats. Q J Exp Physiol, 1986; 71: 249-265.
13. Argent BE, Arkle S, Cullen MJ, Green R. Morphological, biochemical and secretory studies on rat pancreatic ducts maintained in tissue culture. Q J Exp Physiol, 1986; 71: 633-648.
14. Yamamoto A, Ishiguro H, Ko SBH, Suzuki A, Wang Y, Hamada H, Mizuno N, Kitagawa M, Hayakawa T, and Naruse S. Ethanol induces fluid hypersecretion in guinea-pig pancreatic duct cells. J Physiol, 2003; 551: 917-926.
15. Ishiguro H, Naruse S, Steward MC, Kitagawa M, Ko SB, Hayakawa T, Case RM. Fluid secretion in interlobular ducts isolated from guinea-pig pancreas. J Physiol, 1998; 511: 407-422.
16. Ishiguro H, Steward MC, Yamamoto A. Microperfusion and micropuncture analysis of ductal secretion. In; THE PANCREAPEDIA (http://www.lib.umich.edu/spo/panc/), University of Michigan Library, 2011; DOI: 10.3998/panc.2011.16
17. Gray MA, Plant S, Argent BE. cAMP-regulated whole cell chloride currents in pancreatic duct cells. Am J Physiol, 1993; 264: C591-602.
18. Gray MA, Greenwell JR, Garton AJ, Argent BE. Regulation of maxi-K+ channels on pancreatic duct cells by cyclic AMP-dependent phosphorylation. J Membr Biol, 1990; 115: 203-215.
19. Novak I, Greger R. Properties of the luminal membrane of isolated perfused rat pancreatic ducts; effect of cyclic AMP and blockers of chloride transport. Pflügers Arch, 1988; 411: 546-553.
20. Novak I, Greger R. Electrophysiological study of transport systems in isolated perfused pancreatic ducts: properties of the basolateral membrane. Pflügers Arch, 1988; 411: 58-68.
21. Kumpulainen T, Jalovaara P. Immunohistochemical localization of carbonic anhydrase isoenzymes in the human pancreas. Gastroenterology, 1981; 80: 796-799.
22. Gray MA, Pollard CE, Harris A, Coleman L, Greenwell JR, Argent BE. Anion selectivity and block of the small-conductance chloride channel on pancreatic duct cells. Am J Physiol, 1990; 259: C752-761.
23. Ishiguro H, Naruse S, Kitagawa M, Suzuki A, Yamamoto A, Hayakawa T, Case RM, Steward MC. CO2 permeability and bicarbonate transport in microperfused interlobular ducts isolated from guinea-pig pancreas. J Physiol, 2000; 528: 305-315.
24. Ishiguro H, Naruse S, Kitagawa M, Mabuchi T, Kondo T, Hayakawa T, Case RM, Steward MC. Chloride transport in microperfused interlobular ducts isolated from guinea-pig pancreas. J Physiol, 2002; 539: 175-189.
25. Ishiguro H, Steward MC, Sohma Y, Kubota T, Kitagawa M, Kondo T, Case RM, Hayakawa T, Naruse S. Membrane potential and bicarbonate secretion in isolated interlobular ducts from guinea-pig pancreas. J Gen Physiol, 2002; 120: 617-628.
26. Steward MC, Ishiguro H. Molecular and cellular regulation of pancreatic duct cell function. Curr Opin Gastroenterol, 2009; 25: 447-453.
27. Ishiguro H, Steward MC, Naruse S, Ko SB, Goto H, Case RM, Kondo T, Yamamoto A. CFTR functions as a bicarbonate channel in pancreatic duct cells. J Gen Physiol, 2009; 133: 315-326.
28. 3 secretion: relevance to cystic fibrosis. EMBO J, 2006; 25: 5049-5057.
29. 3 exchanger activity and cAMP-stimulated bicarbonate secretion in pancreatic duct. Am J Physiol Gastrointest Liver Physiol, 2007; 292: G447-455.
30. Ohana E, Yang D, Shcheynikov N, Muallem S. Diverse transport modes by the solute carrier 26 family of anion transporters. J Physiol, 2009; 587: 2179-2185.
31. 3 transport in a mathematical model of the pancreatic ductal epithelium. J Membr Biol, 2000; 176: 77-100.
32. 3 transport in cystic fibrosis. EMBO J, 2002; 21: 5662-5672.
33. 3 secretion by pancreatic duct cells. Sheng Li Xue Bao, 2007; 59: 465-476.
34. 3 secretion and pathogenesis of cystic fibrosis/chronic pancreatitis. Journal of the Japan Pancreas Society (in Japanese), 2006; 21: 13-25.
35. Highlights from the literature. Physiology 2009; 24: 77.
36. -]i and its role in pancreatic bicarbonate secretion. Gastroenterology, 2010; 139: 620-631.
37. Ko SBH, Naruse S, Kitagawa M, Ishiguro H, Furuya S, Mizuno N, Wang Y, Yoshikawa T, Suzuki A, Shimano S, Hayakawa T. Aquaporins in rat pancreatic interlobular ducts. Am J Physiol Gastrointest Liver Physiol, 2002; 282: G324-G331.
38. Krane CM, Melvin JE, Nguyen HV, Richardson L, Towne JE, Doetschman T, Menon AG. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation. J Biol Chem, 2001; 276: 23413-23420.
39. Verkman AS. Role of aquaporins in lung liquid physiology. Respir Physiol Neurobiol, 2007; 159: 324-330.
40. Furuya S, Naruse S, Ko SBH, Ishiguro H, Yoshikawa T, Hayakawa T. Distribution of aquaporin 1 in the rat pancreatic duct system examined with light and electron microscopic immunohistochemistry. Cell Tissue Res, 2002; 308: 75-86.
41. Argent B, Gray M, Steward M, Case M. Cell Physiology of Pancreatic Ducts. In: Physiology of the Gastrointestinal Tract, edited by Johnson LR, Barrett KE, Ghishan FK, Merchant JL, Said HM, Wood JD. pp. 1371-1396. 2006, Elsevier Academic Press.
42. Nathan JD, Patel AA, McVey DC, Thomas JE, Prpic V, Vigna SR, Liddle RA. Capsaicin vanilloid receptor-1 mediates substance P release in experimental pancreatitis. Am J Physiol Gastrointest Liver Physiol, 2001; 281: G1322-1328.
43. Hegyi P, Gray MA, Argent BE. Substance P inhibits bicarbonate secretion from guinea pig pancreatic ducts by modulating an anion exchanger. Am J Physiol Cell Physiol, 2003; 285: C268-276.
44. Ko SB, Naruse S, Kitagawa M, Ishiguro H, Murakami M, Hayakawa T. Arginine vasopressin inhibits fluid secretion in guinea pig pancreatic duct cells. Am J Physiol, 1999; 277: G48-54.
45. Kitagawa M, Hayakawa T, Kondo T, Shibata T, Oiso Y. Plasma osmolality and exocrine pancreatic secretion. Int J Pancreatol, 1990; 6: 25-32.
46. Bruce JI, Yang X, Ferguson CJ, Elliott AC, Steward MC, Case RM, Riccardi D. Molecular and functional identification of a Ca2+ (polyvalent cation)-sensing receptor in rat pancreas. J Biol Chem, 1999; 274: 20561-20568.
47. Novak I. Purinergic receptors in the endocrine and exocrine pancreas. Purinergic Signal, 2008; 4: 237-253.
48. 3 secretion in guinea-pig pancreatic duct. J Physiol, 1999; 519: 551-558.
49. Suzuki A, Naruse S, Kitagawa M, Ishiguro H, Yoshikawa T, Ko SB, Yamamoto A, Hamada H, Hayakawa T. 5-hydroxytryptamine strongly inhibits fluid secretion in guinea pig pancreatic duct cells. J Clin Invest, 2001; 108: 749-756.
50. Hallenbeck GA. Biliary and pancreatic intraductal pressures. In: Handbook of Physiology. Alimentary Canal. Secretion. pp.1007-1025. 1967, American Physiological Society, Washington D.C.
51. Czakó L, Yamamoto M, Otsuki M. Pancreatic fluid hypersecretion in rats after acute pancreatitis. Dig Dis Sci, 1997; 42: 265-272.
52. Czakó L, Yamamoto M, Otsuki M. Exocrine pancreatic function in rats after acute pancreatitis. Pancreas, 1997; 15: 83-90.
53. Venglovecz V, Rakonczay Z Jr, Ozsvári B, Takács T, Lonovics J, Varró A, Gray MA, Argent BE, Hegyi P. Effects of bile acids on pancreatic ductal bicarbonate secretion in guinea pig. Gut, 2008; 57: 1102-1112.
54. Venglovecz V, Hegyi P, Rakonczay Z Jr, Tiszlavicz L, Nardi A, Grunnet M, Gray MA. Pathophysiological relevance of apical large-conductance Ca2+-activated potassium channels in pancreatic duct epithelial cells. Gut, 2011; 60: 361-369.
55. Kawabata A, Kuroda R, Nishida M, Nagata N, Sakaguchi Y, Kawao N, Nishikawa H, Arizono N, Kawai K. Protease-activated receptor-2 (PAR-2) in the pancreas and parotid gland: immunolocalization and involvement of nitric oxide in the evoked amylase secretion. Life Sci, 2002; 71: 2435-2446.
56. Nguyen TD, Moody MW, SteinhoffM, Okolo C, Koh DS, Bunnett NW. Trypsin activates pancreatic duct epithelial cell ion channels through proteinase-activated receptor-2. J Clin Invest, 1999; 103: 261-269.
57. Masamune A, Kikuta K, Satoh M, Suzuki N, Shimosegawa T. Protease-activated receptor-2-mediated proliferation and collagen production of rat pancreatic stellate cells. J Pharmacol Exp Ther, 2005; 312: 651-658.
58. Hoogerwerf WA, Shenoy M, Winston JH, Xiao SY, He Z, Pasricha PJ. Trypsin mediates nociception via the proteinase-activated receptor 2: a potentially novel role in pancreatic pain. Gastroenterology, 2004; 127: 883-891.
59. Sharma A, Tao X, Gopal A, Ligon B, Andrade-Gordon P, Steer ML, Perides G. Protection against acute pancreatitis by activation of protease-activated receptor-2. Am J Physiol Gastrointest Liver Physiol, 2005; 288: G388-395.
60. Laukkarinen JM, Weiss ER, van Acker GJ, Steer ML, Perides G. Protease-activated receptor-2 exerts contrasting model-specific effects on acute experimental pancreatitis. J Biol Chem, 2008; 283: 20703-20712.
61. Namkung W, Han W, Luo X, Muallem S, Cho KH, Kim KH, Lee MG. Protease-activated receptor 2 exerts local protection and mediates some systemic complications in acute pancreatitis. Gastroenterology 2004; 126: 1844-1859.
62. - channels and luminal anion exchangers. Gastroenterology, 2011; 40: 2228-2239.
63. Gukovskaya AS, Mouria M, Gukovsky I, Reyes CN, Kasho VN, Faller LD, Pandol SJ. Ethanol metabolism and transcription factor activation in pancreatic acinar cells in rats. Gastroenterology, 2002; 122: 106-118.
64. Lu Z, Karne S, Kolodecik T, Gorelick FS. Alcohols enhance caerulein-induced zymogen activation in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol, 2002; 282: G501-507.
65. Laurence DR, Bennett PN. Central nervous system. Non-medical use of drags. Ethyl alcohol (ethanol). In: Clinical Pharmacology. pp. 411-422, 1987, Churchill Livingstone.
66. Deitrich RA, Harris RA. How much alcohol should I use in my experiments? Alcohol Clin Exp Res, 1996; 20: 1-2.
67. Sarles H. Alcoholic pancreatitis. In: Disorders of the Pancreas. pp. 273-282, 1992, McGraw-Hill, New York.
68. Gerasimenko JV, Lur G, Ferdek P, Sherwood MW, Ebisui E, Tepikin AV, Mikoshiba K, Petersen OH, Gerasimenko OV. Calmodulin protects against alcohol-induced pancreatic trypsinogen activation elicited via Ca2+ release through IP3 receptors. Proc Natl Acad Sci U S A, 2011; 108: 5873-5878.
69. Little HJ. The contribution of electrophysiology to knowledge of the acute and chronic effects of ethanol. Pharmacol Ther, 1999; 84: 333-353.
70. Korpi ER, Mäkelä R, Uusi-Oukari M. Ethanol: Novel actions on nerve cell physiology explain impaired functions. News Physiol Sci, 1998; 13: 164-170.
71. Hamada H, Ishiguro H, Yamamoto A, Shimano-Futakuchi S, Ko SB, Yoshikawa T, Goto H, Kitagawa M, Hayakawa T, Seo Y, Naruse S. Dual effects of n-alcohols on fluid secretion from guinea pig pancreatic ducts. Am J Physiol Cell Physiol, 2005; 288: C1431-1439.
72. Benjamin K, Matzner MJ, Sobel AE. A study of external pancreatic secretion in man. J Clin Invest, 1936; 15: 393-396.
73. 3 and fluid secretion in rat pancreatic ducts. Pflügers Arch, 2009; 459: 215-226.
74. Creutzfeldt W, Gleichmann D, Otto J, Stöckmann F, Maisonneuve P, Lankisch PG. Follow-up of exocrine pancreatic function in type-1 diabetes mellitus. Digestion, 2005; 72: 71-75.
75. Busik JV, Hootman SR, Greenidge CA, Henry DN. Glucose-specific regulation of aldose reductase in capan-1 human pancreatic duct cells in vitro. J Clin Invest, 1997; 100: 1685-1692.
76. Imaizumi Y. Incidence and mortality rates of cystic fibrosis in Japan, 1969-1992. Am J Med Genet, 1995; 58: 161-168.
77. Yamashiro Y, Shimizu T, Oguchi S, Shioya T, Nagata S, Ohtsuka Y. The estimated incidence of cystic fibrosis in Japan. J Pediatr Gastroenterol Nutr, 1997; 24: 544-547.
78. Naruse S, Kitagawa M, Ishiguro H, Fujiki K, Hayakawa T. Cystic fibrosis and related diseases of the pancreas. Best Pract Res Clin Gastroenterol, 2002; 16: 511-526.
79. Hanawa M, Takebe T, Takahashi S, Koizumi M, Endo K. The significance of the sweat test in chronic pancreatitis. Tohoku J Exp Med, 1978; 125: 59-69.
80. Naruse S, Ishiguro H, Suzuki Y, Fujiki K, Ko SB, Mizuno N, Takemura T, Yamamoto A, Yoshikawa T, Jin C, Suzuki R, Kitagawa M, Tsuda T, Kondo T, Hayakawa T. A finger sweat chloride test for the detection of a high-risk group of chronic pancreatitis. Pancreas, 2004; 28: e80-85.
81. Fujiki K, Ishiguro H, Ko SB, Mizuno N, Suzuki Y, Takemura T, Yamamoto A, Yoshikawa T, Kitagawa M, Hayakawa T, Sakai Y, Takayama T, Saito M, Kondo T, Naruse S. Genetic evidence for CFTR dysfunction in Japanese: background for chronic pancreatitis. J Med Genet, 2004; 41: e55.
82. Quinton PM. The sweat gland. In: Cystic fibrosis in adults, edited by Yankaskas JR and Knowles MR. pp. 419-437, 1999, Lippincott-Raven, Philadelphia.
83. Tsuda T, Noda S, Kitagawa S, Morishita T. Proposal of sampling process for collecting human sweat and determination of caffeine concentration in it by using GC/MS. Biomed Chromatogr, 2000; 14: 505-510.
84. Nakakuki M, Ishiguro H, Shirota K, Yamamoto A, Ko SB, Goto H, Fujiki K, Kondo T, Naruse S. Measurement of chloride concentrations of insensible sweat collected from thumb. J Jpn Pancreas Soc (in Japanese), 2008; 23: 486-493.