Cell-specific effects of luminal acid, bicarbonate, cAMP, and carbachol on transporter trafficking in the intestine

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 8, 2012, Pages

  Jakab, Robert L ^a   Collaco, Anne M ^a   Ameen, Nadia A ^a,b  

^a Departments of Pediatrics/Gastroenterology and Hepatology   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cystic fibrosis transmembrane conductance regulator; Electrogenic sodium bicarbonate cotransporter; Goblet cell; Membrane trafficking; Sodium and potassium coupled chloride cotransporter; Sodium proton exchanger

Indexed keywords

8 BROMO CYCLIC AMP; BICARBONATE; BICARBONATE SODIUM COTRANSPORTER; CARBACHOL; CYCLIC AMP; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM PROTON EXCHANGE PROTEIN 3; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; CELL SPECIFICITY; CELL VACUOLE; CONTROLLED STUDY; CRYPT CELL; DUODENUM; HUMAN; HUMAN TISSUE; ILEUM; IN VIVO STUDY; INTERNALIZATION; INTESTINE ABSORPTION; INTESTINE BRUSH BORDER MEMBRANE; INTESTINE CELL; INTESTINE VILLUS; JEJUNUM; MALE; MEMBRANE TRANSPORT; NONHUMAN; PH; PRIORITY JOURNAL; RAT; SECOND MESSENGER; SMALL INTESTINE;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ACIDS; ANIMALS; BICARBONATES; CARBACHOL; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; INTESTINAL MUCOSA; INTESTINES; MALE; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; SODIUM-BICARBONATE SYMPORTERS; SODIUM-HYDROGEN ANTIPORTER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS;

EID: 84867605411     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00452.2011     Document Type: Article

References (65)

1. Akiba Y, Guth PH, Engel E, Nastaskin I, Kaunitz JD. Dynamic regulation of mucus gel thickness in rat duodenum. Am J Physiol Gastro-intest Liver Physiol 279: G437-G447, 2000.
2. Allen A, Flemstrom G. Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am J Physiol Cell Physiol 288: C1-C19, 2005.
3. Ambort D, Johansson ME, Gustafsson JK, Nilsson HE, Ermund A, Johansson BR, Koeck PJ, Hebert H, Hansson GC. Calcium and pH-dependent packing and release of the gel-forming MUC2 mucin. Proc Natl Acad Sci USA 109: 5645-5650, 2012.
4. Ameen N, Apodaca G. Defective CFTR apical endocytosis and entero-cyte brush border in myosin VI-deficient mice. Traffic 8: 998-1006, 2007.
5. Ameen NA, Ardito T, Kashgarian M, Marino CR. A unique subset of rat and human intestinal villus cells express the cystic fibrosis transmembrane conductance regulator. Gastroenterology 108: 1016-1023, 1995.
6. Ameen NA, Marino C, Salas PJ. cAMP-dependent exocytosis and vesicle traffic regulate CFTR and fluid transport in rat jejunum in vivo. Am J Physiol Cell Physiol 284: C429-C438, 2003.
7. Ameen NA, Martensson B, Bourguinon L, Marino C, Isenberg J. CFTR channel insertion to the apical surface in rat duodenal villus epithelial cells is upregulated by VIP in vivo. J Cell Sci 112: 887-894, 1999.
8. Ameen NA, van Donselaar E, Posthuma G, de Jonge H, McLaughlin G, Geuze HJ, Marino C, Peters PJ. Subcellular distribution of CFTR in rat intestine supports a physiologic role for CFTR regulation by vesicle traffic. Histochem Cell Biol 114: 219-228, 2000.
9. Atuma C, Strugala V, Allen A, Holm L. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol Gastrointest Liver Physiol 280: G922-G929, 2001.
10. 2+/calmodulin-, and PKC-dependent manner. Am J Physiol Gastrointest Liver Physiol 291: G650-G657, 2006.
11. +/HCO3 cotransporter subtype pNBC1. Am J Physiol Gastrointest Liver Physiol 284: G37-G45, 2003.
12. +-2Cl~ cotransporter NKCC1 in the normal and CFTR-deficient murine colon. J Physiol 549: 525-536, 2003.
13. Bell S, Kamm MA. Antibodies to tumour necrosis factor-a as treatment for Crohn's disease. Lancet 355: 858-860, 2000.
14. Binder HJ, Sandle GI. Electrolyte transport in the mammalian colon. In: Physiology of the Gastrointestinal Tract (3rd ed.), edited by Johnson LR. New York: Raven, 1994, p. 2133-2171.
15. Chang EB, Rao MC. Intestinal water and electrolyte transport: mechanisms of physiological and adaptive responses. In: Physiology of the Gastrointestinal Tract (3rd ed.), edited by Johnson LR. New York: Raven, 1994, p. 2027-2081.
16. Chen EY, Yang N, Quinton PM, Chin WC. A new role for bicarbonate in mucus formation. Am J Physiol Lung Cell Mol Physiol 299: L542-L549, 2010.
17. Ciancio MJ, Chang EB. Epithelial secretory response to inflammation. Ann NY Acad Sci 664: 210-221, 1992.
18. Clarke LL, Harline MC. Dual role of CFTR in cAMP-stimulated HCO3 secretion across murine duodenum. Am J Physiol Gastrointest Liver Physiol 274: G718-G726, 1998.
19. Cuthbert AW, Hickman ME, MacVinish LJ, Evans MJ, Colledge WH, Ratcliff R, Seale PW, Humphrey PP. Chloride secretion in response to guanylin in colonic epithelial from normal and transgenic cystic fibrosis mice. Br J Pharmacol 112: 31-36, 1994.
20. D'Andrea L, Lytle C, Matthews JB, Hofman P, Forbush B 3rd, Madara JL. Na:K:2Cl cotransporter (NKCC) of intestinal epithelial cells. Surface expression in response to cAMP. J Biol Chem 271: 28969-28976, 1996.
21. de Jonge HR. The response of small intestinal villus and crypt epithelium to cholera toxin in rat. Evidence against a specific role of the crypt cells in choleragen induced secretion. Biochimica Biphysica Acta 381: 128-143, 1975.
22. Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29: 1035-1041, 1988.
23. Field M, Semrad CE. Toxigenic diarrheas, congenital diarrheas and cystic fibrosis: disorders of intestinal ion transport. Ann Rev Physiol 55: 631-655, 1993.
24. Flagella M, Clarke LL, Miller ML, Erway LC, Giannella RA, An-dringa A, Gawenis LR, Kramer J, Duffy JJ, Doetschman T, Lorenz JN, Yamoah EN, Cardell EL, Shull GE. Mice lacking the basolateral Na-K-2Cl cotransporter have impaired epithelial chloride secretion and are profoundly deaf. J Biol Chem 274: 26946-26955, 1999.
25. Furukawa O, Bi LC, Guth PH, Engel E, Hirokawa M, Kaunitz JD. NHE3 inhibition activates duodenal bicarbonate secretion in the rat. Am J Physiol Gastrointest Liver Physiol 286: G102-G109, 2004.
26. Furukawa O, Hirokawa M, Zhang L, Takeuchi T, Bi LC, Guth PH, Engel E, Akiba Y, Kaunitz JD. Mechanism of augmented duodenal HCO3 secretion after elevation of luminal CO2. Am J Physiol Gastrointest Liver Physiol 288: G557-G563, 2005.
27. Gabriel SE, Brigman KN, Koller BH, Boucher RC, Stutts MJ. Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 266: 107-109, 1994.
28. Garcia MA, Yang N, Quinton PM. Normal mouse intestinal mucus release requires cystic fibrosis transmembrane regulator-dependent bicarbonate secretion. J Clin Invest 119: 2613-2622, 2009.
29. +/HCO3 cotransporter. J Biol Chem 282: 9042-9052, 2007.
30. Gawenis LR, Franklin CL, Simpson JE, Palmer BA, Walker NM, Wiggins TM, Clarke LL. cAMP inhibition of murine intestinal Na/H exchange requires CFTR-mediated cell shrinkage of villus epithelium. Gastroenterology 125: 1148-1163, 2003.
31. Gelfond D, Ma C, Semler J, Borowitz D. Intestinal pH and gastrointestinal transit profiles in cystic fibrosis patients measured by wireless motility capsule. Dig Dis Sci 2012 May 17 (Epub ahead of print).
32. Goldstein JL, Sahi J, Bhuva M, Layden TJ, Rao MC. Escherichia coli heat-stable enterotoxin-mediated colonic Cl~ secretion is absent in cystic fibrosis. Gastroenterology 107: 950-956, 1994.
33. Golin-Bisello F, Bradbury NA, Ameen NA. Heat stable enterotoxin (STa) and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G. Am J Physiol Cell Physiol 289: C708-C716, 2005.
34. Gustafsson JK, Ermund A, Ambort D, Johansson ME, Nilsson HE, Thorell K, Hebert H, Sjovall H, Hansson GC. Bicarbonate and functional CFTR channel are required for proper mucin secretion and link cystic fibrosis with its mucus phenotype. J Exp Med 209: 1263-1272, 2012.
35. Hogan DL, Crombie DL, Isenberg JI, Svendsen P, Schaffalitzky de Muckadell OB, Ainsworth MA. CFTR mediates cAMP and calcium activated duodenal epithelial bicarbonate secretion. Am J Physiol Gastrointest Liver Physiol 272: G872-G878, 1997.
36. Holm M, Johansson B, Pettersson A, Fandriks L. Carbon dioxide mediates duodenal mucosal alkaline secretion in response to luminal acidity in the anesthetized rat. Gastroenterology 115: 680-685, 1998.
37. Isenberg J, Hogan D, Koss MA, Selling J. Human duodenal mucosal bicarbonate secretion. Gastroenterology 91: 370-378, 1986.
38. Jacob P, Rossmann H, Lamprecht G, Kretz A, Neff C, Lin-Wu E, Gregor M, Groneberg DA, Kere J, Seidler U. Down-regulated in adenoma mediates apical Cl~/HCO3 exchange in rabbit, rat, and human duodenum. Gastroenterology 122: 709-724, 2002.
39. Jakab RL, Collaco AM, Ameen NA. Lubiprostone targets prostanoid signaling and promotes ion transporter trafficking, mucus exocytosis, and contractility. Dig Dis Sci 2012 Aug 25 (Epub ahead of print).
40. Jakab RL, Collaco AM, Ameen NA. Physiological relevance of cell-specific distribution patterns of CFTR, NKCC1, NBCe1, and NHE3 along the crypt-villus axis in the intestine. Am J Physiol Gastrointest Liver Physiol 300: G82-G98, 2011.
41. Kreusel KM, Fromm M, Schulzke JD, Hegel U. Cl secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am J Physiol Cell Physiol 261: C574-C582, 1991.
42. 2+-activated Cl~ channels bestrophin and anoctamin in epithelial cells. Biol Chem 392: 125-134, 2011.
43. + exchanger 3 (NHE3) occurs through changes in NHE3 trafficking and complex formation and is Src dependent. J Physiol 556: 791-804, 2004.
44. Mizumori M, Choi Y, Guth PH, Engel E, Kaunitz JD, Akiba Y. CFTR inhibition augments NHE3 activity during luminal high CO2 exposure in rat duodenal mucosa. Am J Physiol Gastrointest Liver Physiol 294: G1318-G1327, 2008.
45. Moritz M, Iber F, Moore E. Rabbit cholera: effects of cycloheximide on net water and ion fluxes and transmural electric potentials. Gastroenterology 63: 76-82, 1972.
46. Musch MW, Arvans DL, Wang Y, Nakagawa Y, Solomaha E, Chang EB. Cyclic AMP-mediated endocytosis of intestinal epithelial NHE3 requires binding to synaptotagmin 1. Am J Physiol Gastrointest Liver Physiol 298: G203-G211, 2010.
47. Poulsen J, Fischer H, Illek B, Machen TE. Bicarbonate conductance and pH regulatory capabilty of cystic fibrosis transmembrane conductance regulator. Physiology 91: 5340-5344, 1994.
48. Press AG, Hauptmann IA, Hauptmann L, Fuchs B, Fuchs M, Ewe K, Ramadori G. Gastrointestinal pH profiles in patients with inflammatory bowel disease. Aliment Pharmacol Ther 12: 673-678, 1998.
49. Pye G, Evans DF, Ledingham S, Hardcastle JD. Gastrointestinal intraluminal pH in normal subjects and those with colorectal adenoma or carcinoma. Gut 31: 1355-1357, 1990.
50. Seidler U, Blumenstein I, Kretz A, Viellard-Baron D, Rossman H, Colledge WH, Evans M, Ratcliff R, Gregor M. A functional CFTR protein is required for mouse intestinal cAMP, cGMP and calcium-dependent HCO3 secretion. J Physiol 505: 411-423, 1997.
51. Simpson JE, Gawenis LR, Walker NM, Boyle KT, Clarke LL. Chloride conductance of CFTR facilitates basal Cl~/HCO3 exchange in the villous epithelium of intact murine duodenum. Am J Physiol Gastrointest Liver Physiol 288: G1241-G1251, 2005.
52. -~/HCO3 exchanger in the upper villous epithelium of the murine duodenum. Am J Physiol Gastrointest Liver Physiol 292: G1079-G1088, 2007.
53. +-dipeptide transport in duodenal villous epithelium. Am J Physiol Gastrointest Liver Physiol 298: G683-G691, 2010.
54. Singh AK, Riederer B, Chen M, Xiao F, Krabbenhoft A, Engelhardt R, Nylander O, Soleimani M, Seidler U. The switch of intestinal Slc26 exchangers from anion absorptive to HCO3 secretory mode is dependent on CFTR anion channel function. Am J Physiol Cell Physiol 298: C1057-C1065, 2010.
55. Sjoblom M, Singh AK, Zheng W, Wang J, Tuo BG, Krabbenhoft A, Riederer B, Gros G, Seidler U. Duodenal acidity "sensing" but not epithelial HCO3 supply is critically dependent on carbonic anhydrase II expression. Proc Natl Acad Sci USA 106: 13094-13099, 2009.
56. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, Koller BH. An animal model for cystic fibrosis made by gene targeting. Science 257: 1083-1088, 1992.
57. Stewart CP, Turnberg LA. A microelectrode study of responses to secretagogues by epithelial cells in villus and crypt of rat small intestine. Am J Physiol Gastrointest Liver Physiol 257: G334-G343, 1989.
58. Tuo B, Wen G, Zhang Y, Liu X, Wang X, Dong H. Involvement of phosphatidylinositol 3-kinase in cAMP- and cGMP-induced duodenal epithelial CFTR activation in mice. Am J Physiol Cell Physiol 297: C503-C515, 2009.
59. Walker NM, Simpson JE, Brazill JM, Gill RK, Dudeja PK, Schweinfest CW, Clarke LL. Role of down-regulated in adenoma anion exchanger in HCO3 secretion across murine duodenum. Gastroenterology 136: 893-901, 2009.
60. Walker NM, Simpson JE, Hoover EE, Brazill JM, Schweinfest CW, Soleimani M, Clarke LL. Functional activity of Pat-1 (Slc26a6) Cl~/ HCO3 exchange in the lower villus epithelium of murine duodenum. Acta Physiol (Oxf) 201: 21-31, 2011.
61. Ward FW, Coates ME. Gastrointestinal pH measurement in rats: influence of the microbial flora, diet and fasting. Lab Anim 21: 216-222, 1987.
62. Wilschanski M, Durie PR. Patterns of GI disease in adulthood associated with mutations in the CFTR gene. Gut 56: 1153-1163, 2007.
63. Youngberg CA, Berardi RR, Howatt WF, Hyneck ML, Amidon GL, Meyer JH, Dressman JB. Comparison of gastrointestinal pH in cystic fibrosis and healthy subjects. Dig Dis Sci 32: 472-480, 1987.
64. Yu K, Lujan R, Marmorstein A, Gabriel S, Hartzell HC. Bestrophin-2 mediates bicarbonate transport by goblet cells in mouse colon. J Clin Invest 120: 1722-1735, 2010.
65. Zhang K, Yin L, Zhang M, Parker MD, Binder HJ, Salzman P, Zhang L, Okunieff P, Vidyasagar S. Radiation decreases murine small intestinal HCO3 secretion. Int J Radiat Biol 87: 878-888, 2011.