Carbonic Anhydrases and Mucosal Vanilloid Receptors Help Mediate the Hyperemic Response to Luminal CO2 in Rat Duodenum

Gastroenterology

Volumn 131, Issue 1, 2006, Pages 142-152

  Akiba, Yasutada ^a,b   Ghayouri, Sara ^c   Takeuchi, Tetsu ^a,b   Mizumori, Misa ^a,b   Guth, Paul H ^c   Engel, Eli ^a   Swenson, Erik R ^d   Kaunitz, Jonathan D ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Brentwood Biomedical Research Institute Los Angeles   (United States)

^c VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^d VA Puget Sound Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N,N DIMETHYL)AMILORIDE; BENZOLAMIDE; CAPSAICIN; CAPSAZEPINE; CARBON DIOXIDE; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; CARBONATE DEHYDRATASE IV; CARBONATE DEHYDRATASE IX; CARBONATE DEHYDRATASE XII; CARBONATE DEHYDRATASE XIV; ISOENZYME; METHAZOLAMIDE; PROTEIN INHIBITOR; RECEPTOR BLOCKING AGENT; SODIUM CHLORIDE; SODIUM PROTON EXCHANGE PROTEIN 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1;

ACIDIFICATION; ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PH; CYTOSOL; DENERVATION; DUODENUM; EPITHELIUM CELL; EXPOSURE; HYPEREMIA; IMAGE ANALYSIS; IMAGING; INTESTINE BLOOD FLOW; LASER DOPPLER FLOWMETRY; MALE; NODOSE GANGLION; NONHUMAN; NUCLEOTIDE SEQUENCE; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; STOMACH;

EID: 33744940067     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.04.018     Document Type: Article

References (76)

1. Rune S.J., and Henriksen F.W. Carbon dioxide tensions in the proximal part of the canine gastrointestinal tract. Gastroenterology 56 (1969) 758-762
2. Simon S.A., and Gutknecht J. Solubility of carbon dioxide in lipid bilayer membranes and organic solvents. Biochim Biophys Acta 596 (1980) 352-358
3. 2 on intracellular pH in in vitro frog gastric mucosa. Am J Physiol 256 (1989) G206-G213
4. Kivilaakso E., and Kiviluoto T. Intracellular pH in isolated Necturus antral mucosa in simulated ulcerogenic conditions. Gastroenterology 95 (1988) 1198-1205
5. Boron W.F., McCormick W.C., and Roos A. pH regulation in barnacle muscle fibers. dependence on intracellular and extracellular pH. Am J Physiol 237 (1979) C185-C193
6. Richardson C.T., and Feldman M. Effects of transdermal scopolamine, alone or in combination with cimetidine, on total 24 hour gastric acid secretion in patients with duodenal ulcer. Gut 27 (1986) 1493-1497
7. + back-diffusion. Nature 313 (1985) 52-54
8. 2 diffusion. Am J Physiol 253 (1987) G527-G530
9. Javaheri S., and Nardell E.A. Severe metabolic alkalosis. a case report. Br Med J (Clin Res Ed) 283 (1981) 1016-1017
10. Barriere H., Poujeol C., Tauc M., Blasi J.M., Counillon L., and Poujeol P. CFTR modulates programmed cell death by decreasing intracellular pH in Chinese hamster lung fibroblasts. Am J Physiol Cell Physiol 281 (2001) C810-C824
11. Nedergaard M., Goldman S.A., Desai S., and Pulsinelli W.A. Acid-induced death in neurons and glia. J Neurosci 11 (1991) 2489-2497
12. Kaunitz J.D., and Akiba Y. Acid-sensing protective mechanisms of duodenum. J Physiol Pharmacol 54 (2003) 19-26
13. Kaunitz J.D., and Akiba Y. Luminal acid elicits a protective duodenal mucosal response. Keio J Med 51 (2002) 29-35
14. + back diffusion stimulating gastric mucosal blood flow in the rabbit fundus. Surgery 89 (1981) 232-236
15. Holm M., Johansson B., Pettersson A., and Fändriks L. Carbon dioxide mediates duodenal mucosal alkaline secretion in response to luminal acidity in the anesthetized rat. Gastroenterology 115 (1998) 680-685
16. 2. Am J Physiol Gastrointest Liver Physiol 288 (2005) G557-G563
17. Flemström G., and Isenberg J.I. Gastroduodenal mucosal alkaline secretion and mucosal protection. News Physiol Sci 16 (2001) 23-28
18. Kaunitz J.D., and Akiba Y. Gastroduodenal mucosal defense. role of endogenous mediators. Curr Opin Gastroenterol 20 (2004) 526-532
19. Akiba Y., and Kaunitz J.D. Regulation of intracellular pH and blood flow in rat duodenal epithelium in vivo. Am J Physiol Gastrointest Liver Physiol 276 (1999) G293-G302
20. Akiba Y., Guth P.H., Engel E., Nastaskin I., and Kaunitz J.D. Acid-sensing pathways of rat duodenum. Am J Physiol Gastrointest Liver Physiol 277 (1999) G268-G274
21. Paimela H., Kiviluoto T., Mustonen H., and Kivilaakso E. Intracellular pH in isolated Necturus duodenal mucosa exposed to luminal acid. Gastroenterology 102 (1992) 862-867
22. Akiba Y., Furukawa O., Guth P.H., Engel E., Nastaskin I., and Kaunitz J.D. Sensory pathways and cyclooxygenase regulate mucus gel thickness in rat duodenum. Am J Physiol Gastrointest Liver Physiol 280 (2001) G470-G474
23. Sugai N., Okamura H., and Tsunoda R. Histochemical localization of carbonic anhydrase in the rat duodenal epithelium. Fukushima J Med Sci 40 (1994) 103-117
24. Mori K., Ogawa Y., Ebihara K., Tamura N., Tashiro K., Kuwahara T., Mukoyama M., Sugawara A., Ozaki S., Tanaka I., and Nakao K. Isolation and characterization of CA XIV, a novel membrane-bound carbonic anhydrase from mouse kidney. J Biol Chem 274 (1999) 15701-15705
25. Kivela A.J., Kivela J., Saarnio J., and Parkkila S. Carbonic anhydrases in normal gastrointestinal tract and gastrointestinal tumours. World J Gastroenterol 11 (2005) 155-163
26. Goldfarb D.S., Sly W.S., Waheed A., and Charney A.N. Acid-base effects on electrolyte transport in CA II-deficient mouse colon. Am J Physiol 278 (2000) G409-G415
27. Parkkila S., Parkkila A.K., Juvonen T., and Rajaniemi H. Distribution of the carbonic anhydrase isoenzymes I, II, and VI in the human alimentary tract. Gut 35 (1994) 646-650
28. Geers C., and Gros G. Carbon dioxide transport and carbonic anhydrase in blood and muscle. Physiol Rev 80 (2000) 681-715
29. Supuran C.T., and Scozzafava A. Benzolamide is not a membrane-impermeant carbonic anhydrase inhibitor. J Enzyme Inhib Med Chem 19 (2004) 269-273
30. Saarikoski J., and Kaila K. Simultaneous measurement of intracellular and extracellular carbonic anhydrase activity in intact muscle fibres. Pflugers Arch 421 (1992) 357-363
31. Akiba Y., Kato S., Katsube K., Nakamura M., Takeuchi K., Ishii H., and Hibi T. Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet beta cells modulates insulin secretion in rats. Biochem Biophys Res Commun 321 (2004) 219-225
32. Akiba Y., Nakamura M., Oda M., Kimura H., Miura S., Tsuchiya M., and Ishii H. Basic fibroblast growth factor increases constitutive nitric oxide synthase during healing of rat gastric ulcers. J Clin Gastroenterol 25 (1997) S122-S128
33. Leung F.W., Itoh M., Hirabayashi K., and Guth P.H. Role of blood flow in gastric and duodenal mucosal injury in the rat. Gastroenterology 88 (1985) 281-289
34. Cheung L.Y., and Ashley S.W. Gastric blood flow and mucosal defense mechanisms. Clin Invest Med 10 (1987) 201-208
35. Akiba Y., Nakamura M., Nagata H., Kaunitz J.D., and Ishii H. Acid-sensing pathways in rat gastrointestinal mucosa. J Gastroenterol 37 (2002) 133-138
36. Horie S., Yamamoto H., Michael G.J., Uchida M., Belai A., Watanabe K., Priestley J.V., and Murayama T. Protective role of vanilloid receptor type 1 in HCl-induced gastric mucosal lesions in rats. Scand J Gastroenterol 39 (2004) 303-312
37. Kato S., Aihara E., Nakamura A., Xin H., Matsui H., Kohama K., and Takeuchi K. Expression of vanilloid receptors in rat gastric epithelial cells. role in cellular protection. Biochem Pharmacol 66 (2003) 1115-1121
38. Tashima K., Nakashima M., Kagawa S., Kato S., and Takeuchi K. Gastric hyperemic response induced by acid back-diffusion in rat stomachs following barrier disruption-relation to vanilloid type-1 receptors. Med Sci Monit 8 (2002) BR157-BR163
39. Abdel-Salam O.M., Czimmer J., Debreceni A., Szolcsanyi J., and Mozsik G. Gastric mucosal integrity: gastric mucosal blood flow and microcirculation. An overview. J Physiol Paris 95 (2001) 105-127
40. Danzer M., Jocic M., Samberger C., Painsipp E., Bock E., Pabst M.A., Crailsheim K., Schicho R., Lippe I.T., and Holzer P. Stomach-brain communication by vagal afferents in response to luminal acid backdiffusion, gastrin, and gastric acid secretion. Am J Physiol Gastrointest Liver Physiol 286 (2004) G403-G411
41. Schicho R., Florian W., Liebmann I., Holzer P., and Lippe I.T. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci 19 (2004) 1811-1818
42. Nozawa Y., Nishihara K., Yamamoto A., Nakano M., Ajioka H., and Matsuura N. Distribution and characterization of vanilloid receptors in the rat stomach. Neurosci Lett 309 (2001) 33-36
43. Holzer P. Gastroduodenal mucosal defense. coordination by a network of messengers and mediators. Curr Opin Gastroenterol 17 (2001) 489-496
44. Kivilaakso E., Fromm D., and Silen W. Effect of the acid secretory state on intramural pH of rabbit gastric mucosa. Gastroenterology 75 (1978) 641-648
45. Starlinger M., Matthews J., Yoon C., Wenzl E., Feil W., and Schiessel R. The effect of acid perfusion on mucosal blood flow and intramural pH of rabbit duodenum. Surgery 101 (1987) 433-438
46. Muallem R., Reimer R., Odes H.S., Schwenk M., Beil W., and Sewing K.F. Role of carbonic anhydrase in basal and stimulated bicarbonate secretion by the guinea pig duodenum. Dig Dis Sci 39 (1994) 1078-1084
47. - secretion in the human proximal duodenum. Gastroenterology 108 (1995) 102-107
48. - secretion across murine duodenum. Am J Physiol 274 (1998) G718-G726
49. + exchanger NHE1, and carbonic anhydrase in rabbit duodenal bicarbonate secretion. Gastroenterology 119 (2000) 406-419
50. Leppilampi M., Parkkila S., Karttunen T., Ortova G.M., Gros G., and Sjöblom M. Carbonic anhydrase isozyme-II-deficient mice lack the duodenal bicarbonate secretory response to prostaglandin E2. Proc Natl Acad Sci U S A 102 (2005) 15247-15252
51. Robert A., Lancaster C., Davis J.P., Kolbasa K.P., and Nezamis J.E. Ulcer formation and cytoprotection by acetazolamide. Eur J Pharmacol 118 (1985) 193-201
52. Garner A., Flemström G., Allen A., Heylings J.R., and McQueen S. Gastric mucosal protective mechanisms. roles of epithelial bicarbonate and mucus secretions. Scand J Gastroenterol Suppl 101 (1984) 79-86
53. +. Scand J Gastroenterol Suppl 67 (1981) 219-221
54. + exchange. Am J Physiol Regul Integr Comp Physiol 284 (2003) R1551-R1559
55. Purkerson J.M., and Schwartz G.J. Expression of membrane-associated carbonic anhydrase isoforms IV, IX, XII, and XIV in the rabbit. induction of CA IV and IX during maturation. Am J Physiol Regul Integr Comp Physiol 288 (2005) R1256-R1263
56. Amasaki T., Amasaki H., Nagasao J., Ichihara N., Asari M., Nishita T., Taniguchi K., and Mutoh K. Immunohistochemical localization of carbonic anhydrase isoenzymes in salivary gland and intestine in adult and suckling pigs. J Vet Med Sci 63 (2001) 967-970
57. Lehtonen J., Shen B., Vihinen M., Casini A., Scozzafava A., Supuran C.T., Parkkila A.K., Saarnio J., Kivela A.J., Waheed A., Sly W.S., and Parkkila S. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J Biol Chem 279 (2004) 2719-2727
58. Saarnio J., Parkkila S., Parkkila A.K., Waheed A., Casey M.C., Zhou X.Y., Pastorekova S., Pastorek J., Karttunen T., Haukipuro K., Kairaluoma M.I., and Sly W.S. Immunohistochemistry of carbonic anhydrase isozyme IX (MN/CA IX) in human gut reveals polarized expression in the epithelial cells with the highest proliferative capacity. J Histochem Cytochem 46 (1998) 497-504
59. Fleming R.E., Parkkila S., Parkkila A.K., Rajaniemi H., Waheed A., and Sly W.S. Carbonic anhydrase IV expression in rat and human gastrointestinal tract regional, cellular, and subcellular localization. J Clin Invest 96 (1995) 2907-2913
60. Hilvo M., Rafajova M., Pastorekova S., Pastorek J., and Parkkila S. Expression of carbonic anhydrase IX in mouse tissues. J Histochem Cytochem 52 (2004) 1313-1322
61. Kleinke T., Wagner S., John H., Hewett-Emmett D., Parkkila S., Forssmann W.G., and Gros G. A distinct carbonic anhydrase in the mucus of the colon of humans and other mammals. J Exp Biol 208 (2005) 487-496
62. Endeward V., Kleinke T., and Gros G. Carbonic anhydrase in the gastrointestinal mucus of mammals-possible protective role against carbon dioxide. Comp Biochem Physiol A Mol Integr Physiol 136 (2003) 281-287
63. Pastorekova S., Casini A., Scozzafava A., Vullo D., Pastorek J., and Supuran C.T. Carbonic anhydrase inhibitors. the first selective, membrane-impermeant inhibitors targeting the tumor-associated isozyme IX. Bioorg Med Chem Lett 14 (2004) 869-873
64. Torrance R.W. Carbonic anhydrase near central chemoreceptors. Adv Exp Med Biol 337 (1993) 235-239
65. 2 transduction mechanisms in avian intrapulmonary chemoreceptors. experiments and models. Respir Physiol Neurobiol 144 (2004) 203-214
66. 2 chemoreceptors. Respir Physiol 129 (2001) 219-229
67. 2 chemoreception. J Comp Physiol [A] 182 (1998) 163-174
68. - exchanger binds carbonic anhydrase IV. J Biol Chem 277 (2002) 25239-25246
69. Sterling D., Brown N.J., Supuran C.T., and Casey J.R. The functional and physical relationship between the DRA bicarbonate transporter and carbonic anhydrase II. Am J Physiol Cell Physiol 283 (2002) C1522-C1529
70. Woehlck H.J., Otterson M., Yun H., Connolly L.A., Eastwood D., and Colpaert K. Acetazolamide reduces referred postoperative pain after laparoscopic surgery with carbon dioxide insufflation. Anesthesiology 99 (2003) 924-928
71. Anavi-Goffer S., McKay N.G., Ashford M.L., and Coutts A.A. Vanilloid receptor type 1-immunoreactivity is expressed by intrinsic afferent neurones in the guinea-pig myenteric plexus. Neurosci Lett 319 (2002) 53-57
72. Patterson L.M., Zheng H., Ward S.M., and Berthoud H.R. Vanilloid receptor (VR1) expression in vagal afferent neurons innervating the gastrointestinal tract. Cell Tissue Res 311 (2003) 277-287
73. Ward S.M., Bayguinov J., Won K.J., Grundy D., and Berthoud H.R. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol 465 (2003) 121-135
74. 2-receptor antagonist, on reflux esophagitis in rats through capsaicin-sensitive afferent neurons. J Pharmacol Sci 93 (2003) 55-61
75. Matthews P.J., Aziz Q., Facer P., Davis J.B., Thompson D.G., and Anand P. Increased capsaicin receptor TRPV1 nerve fibres in the inflamed human oesophagus. Eur J Gastroenterol Hepatol 16 (2004) 897-902
76. Yu S., Undem B.J., and Kollarik M. Vagal afferent nerves with nocioceptive properties in guinea-pig oesophagus. J Physiol 563 (2005) 831-842