iNOS-derived nitric oxide mediates the increase in TFF2 expression associated with gastric damage: Role of HIF-1

FASEB Journal

Volumn 24, Issue 1, 2010, Pages 136-145

  Ortiz Masiá, Dolores ^a,b   Hernández, Carlos ^b   Quintana, Elsa ^b   Velázquez, Miriam ^a,b   Cebrián, Sonia ^b   Riaño, Annia ^b   Calatayud, Sara ^a,b   Esplugues, Juan V ^a,b   Barrachina, Maria D ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Inducible nitric oxide synthase; Macrophage activation; Mucosal restitution; NSAID gastropathy

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEIN TFF2; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ENZYME INHIBITION; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; STOMACH INJURY; WOUND HEALING;

AMIDINES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; BASE SEQUENCE; BENZYLAMINES; CELL LINE; COCULTURE TECHNIQUES; DNA PRIMERS; ENZYME INHIBITORS; GASTRIC MUCOSA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MACROPHAGE ACTIVATION; MALE; MICE; MICRORNAS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UP-REGULATION; WOUND HEALING;

LOTUS;

EID: 75149125181     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-137489     Document Type: Article

References (47)

1. Sands, B. E., and Podolsky, D. K. (1996) The trefoil peptide family. Annu. Rev. Physiol. 58, 253-273
2. Taupin, D., and Podolsky, D. K. (2003) Trefoil factors: initiators of mucosal healing. Nat. Rev. Mol. Cell. Biol. 4, 721-732
3. Dignass, A., Lynch-Devaney, K., Kindon, H., Thim, L., and Podolsky, D. K. (1994) Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway. J. Clin. Invest. 94, 376-383
4. Playford, R. J., Marchbank, T., Chinery, R., Evison, R., Pignatelli, M., Boulton, R. A., Thim, L., and Hanby, A. M. (1995) Human spasmolytic polypeptide is a cytoprotective agent that stimulates cell migration. Gastroenterology 108, 108-116
5. Kato, K., Chen, M. C., Nguyen, M., Lehmann, F. S., Podolsky, D. K., and Soll, A. H. (1999) Effects of growth factors and trefoil peptides on migration and replication in primary oxyntic cultures. Am. J. Physiol. 276, G1105-G1116
6. Hoffmann, W. (2005) Trefoil factors TFF (trefoil factor family) peptide-triggered signals promoting mucosal restitution. Cell. Mol. Life Sci. 62, 2932-2938
7. Kubes, P., Suzuki, M., and Granger, D. N. (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. U. S. A. 88, 4651-4655
8. Longman, R. J., Douthwaite, J., Sylvester, P. A., Poulsom, R., Corfield, A. P., Thomas, M. G., and Wright, N. A. (2000) Coordinated localisation of mucins and trefoil peptides in the ulcer associated cell lineage and the gastrointestinal mucosa. Gut 47, 792-800
9. Hernandez, C., Santamatilde, E., McCreath, K. J., Cervera, A. M., Diez, I., Ortiz-Masia, D., Martinez, N., Calatayud, S., Esplugues, J. V., and Barrachina, M. D. (2009) Induction of trefoil factor (TFF)1, TFF2 and TFF3 by hypoxia is mediated by hypoxia inducible factor-1: implications for gastric mucosal healing. Br. J. Pharmacol. 156, 262-272
10. Bruick, R. K. (2003) Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible transcription factor. Genes Dev. 17, 2614-2623
11. Lando, D., Gorman, J. J., Whitelaw, M. L., and Peet, D. J. (2003) Oxygen-dependent regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation. Eur. J. Biochem. 270, 781-790
12. Sandau, K. B., Fandrey, J., and Brune, B. (2001) Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 97, 1009-1015
13. Sogawa, K., Numayama-Tsuruta, K., Ema, M., Abe, M., Abe, H., and Fujii-Kuriyama, Y. (1998) Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc. Natl. Acad. Sci. U. S. A. 95, 7368-7373
14. Yin, J. H., Yang, D. I., Ku, G., and Hsu, C. Y. (2000) iNOS expression inhibits hypoxia-inducible factor-1 activity. Biochem. Biophys. Res. Commun. 279, 30-34
15. Agani, F. H., Puchowicz, M., Chavez, J. C., Pichiule, P., and LaManna, J. (2002) Role of nitric oxide in the regulation of HIF-1alpha expression during hypoxia. Am. J. Physiol. Cell Physiol. 283, C178-C186
16. Bove, P. F., Hristova, M., Wesley, U. V., Olson, N., Lounsbury, K. M., and van der Vliet, A. (2008) Inflammatory levels of nitric oxide inhibit airway epithelial cell migration by inhibition of the kinase ERK1/2 and activation of hypoxia-inducible factor-1 alpha. J. Biol. Chem. 283, 17919-17928
17. Mateo, J., Garcia-Lecea, M., Cadenas, S., Hernandez, C., and Moncada, S. (2003) Regulation of hypoxia-inducible factor-1alpha by nitric oxide through mitochondria-dependent and -independent pathways. Biochem. J. 376, 537-544
18. Metzen, E., Zhou, J., Jelkmann, W., Fandrey, J., and Brune, B. (2003) Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol. Biol. Cell 14, 3470-3481
19. Li, F., Sonveaux, P., Rabbani, Z. N., Liu, S., Yan, B., Huang, Q., Vujaskovic, Z., Dewhirst, M. W., and Li, C. Y. (2007) Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell. 26, 63-74
20. Brune, B., and Zhou, J. (2007) Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc. Res. 75, 275-282
21. Mylonis, I., Chachami, G., Samiotaki, M., Panayotou, G., Paraskeva, E., Kalousi, A., Georgatsou, E., Bonanou, S., and Simos, G. (2006) Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxiainducible factor-1alpha. J. Biol. Chem. 281, 33095-33106
22. Ito, M., Tanaka, S., Kim, S., Kuwai, T., Matsutani, N., Kamada, T., Kitadai, Y., Sumii, M., Yoshihara, M., Haruma, K., and Chayama, K. (2003) The specific expression of hypoxia inducible factor-1alpha in human gastric mucosa induced by nonsteroidal anti-inflammatory drugs. Aliment Pharmacol. Ther. 18(Suppl. 1), 90-98
23. Kauffman, G. L., Jr. (1981) The role of prostaglandins in the regulation of gastric mucosal blood flow. Prostaglandins 21(Suppl.), 33-38
24. Wallace, J. L. (1993) Gastric ulceration: critical events at the neutrophil-endothelium interface. Can. J. Physiol. Pharmacol. 71, 98-102
25. Jimenez, D., Martin, M. J., Pozo, D., Alarcon, C., Esteban, J., Bruseghini, L., Esteras, A., and Motilva, V. (2002) Mechanisms involved in protection afforded by L-arginine in ibuprofen-induced gastric damage: role of nitric oxide and prostaglandins. Dig. Dis. Sci. 47, 44-53
26. Harvey, J. M., Clark, G. M., Osborne, C. K., and Allred, D. C. (1999) Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J. Clin. Oncol. 17, 1474-1481
27. Walker, R. A. (2006) Quantification of immunohistochemistry: issues concerning methods, utility and semiquantitative assessment I. Histopathology 49, 406-410
28. Quintana, E., Hernandez, C., Alvarez-Barrientos, A., Esplugues, J. V., and Barrachina, M. D. (2004) Synthesis of nitric oxide in postganglionic myenteric neurons during endotoxemia: implications for gastric motor function in rats. FASEB J. 18, 531-533
29. Ma, L., and Wallace, J. L. (2000) Endothelial nitric oxide synthase modulates gastric ulcer healing in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G341-G346
30. Yasuhiro, T., Konaka, A., Ukawa, H., Kato, S., and Takeuchi, K. (1997) Role of nitric oxide in pathogenesis of gastric mucosal damage induced by compound 48/80 in rats. J. Physiol. Paris 91, 131-138
31. Takeuchi, K., Suzuki, K., Araki, H., Mizoguchi, H., Sugamoto, S., and Umdeda, M. (1999) Roles of endogenous prostaglandins and nitric oxide in gastroduodenal ulcerogenic responses induced in rats by hypothermic stress. J. Physiol. Paris 93, 423-431
32. Nishida, K., Ohta, Y., and Ishiguro, I. (1998) Relation of inducible nitric oxide synthase activity to lipid peroxidation and nonprotein sulfhydryl oxidation in the development of stress-induced gastric mucosal lesions in rats. Nitric Oxide 2, 215-223
33. Souza, M. H., Lemos, H. P., Oliveira, R. B., and Cunha, F. Q. (2004) Gastric damage and granulocyte infiltration induced by indomethacin in tumour necrosis factor receptor 1 (TNF-R1) or inducible nitric oxide synthase (iNOS) deficient mice. Gut 53, 791-796
34. Garvey, E. P., Oplinger, J. A., Furfine, E. S., Kiff, R. J., Laszlo, F., Whittle, B. J., and Knowles, R. G. (1997) 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J. Biol. Chem. 272, 4959 - 4963
35. Boer, R., Ulrich, W. R., Klein, T., Mirau, B., Haas, S., and Baur, I. (2000) The inhibitory potency and selectivity of arginine substrate site nitric-oxide synthase inhibitors is solely determined by their affinity toward the different isoenzymes. Mol. Pharmacol. 58, 1026-1034
36. Hayashi, Y., Abe, M., Murai, A., Shimizu, N., Okamoto, I., Katsuragi, T., and Tanaka, K. (2005) Comparison of effects of nitric oxide synthase (NOS) inhibitors on plasma nitrite/nitrate levels and tissue NOS activity in septic organs. Microbiol. Immunol. 49, 139-147
37. Calatayud, S., Barrachina, D., and Esplugues, J. V. (2001) Nitric oxide: relation to integrity, injury, and healing of the gastric mucosa. Microsc. Res. Tech. 53, 325-335
38. Dudar, G. K., D'Andrea, L. D., Di Stasi, R., Pedone, C., and Wallace, J. L. (2008) A vascular endothelial growth factor mimetic accelerates gastric ulcer healing in an iNOS-dependent manner. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G374-G381
39. Tatemichi, M., Ogura, T., Sakurazawa, N., Nagata, H., Sugita, M., and Esumi, H. (2003) Roles of inducible nitric oxide synthase in the development and healing of experimentally induced gastric ulcers. Int. J. Exp. Pathol. 84, 213-220
40. Akiba, Y., Nakamura, M., Mori, M., Suzuki, H., Oda, M., Kimura, H., Miura, S., Tsuchiya, M., and Ishii, H. (1998) Inhibition of inducible nitric oxide synthase delays gastric ulcer healing in the rat. J. Clin. Gastroenterol. 27(Suppl. 1), S64-S73
41. Beck, K. F., Eberhardt, W., Frank, S., Huwiler, A., Messmer, U. K., Muhl, H., and Pfeilschifter, J. (1999) Inducible NO synthase: role in cellular signalling. J. Exp. Biol. 202, 645-653
42. Azarschab, P., Al Azzeh, E., Kornberger, W., and Gott, P. (2001) Aspirin promotes TFF2 gene activation in human gastric cancer cell lines. FEBS Lett. 488, 206-210
43. Louis, N. A., Hamilton, K. E., Canny, G., Shekels, L. L., Ho, S. B., and Colgan, S. P. (2006) Selective induction of mucin-3 by hypoxia in intestinal epithelia. J. Cell. Biochem. 99, 1616-1627
44. Kimura, H., Weisz, A., Kurashima, Y., Hashimoto, K., Ogura, T., D'Acquisto, F., Addeo, R., Makuuchi, M., and Esumi, H. (2000) Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 95, 189-197
45. Hagen, T., Taylor, C. T., Lam, F., and Moncada, S. (2003) Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302, 1975-1978
46. Anand, R. J., Dai, S., Rippel, C., Leaphart, C., Qureshi, F., Gribar, S. C., Kohler, J. W., Li, J., Stolz, D. B., Sodhi, C., and Hackam, D. J. (2008) Activated macrophages inhibit enterocyte gap junctions via the release of nitric oxide. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G109-G119
47. Rhoads, J. M., Liu, Y., Niu, X., Surendran, S., and Wu, G. (2008) Arginine stimulates cdx2-transformed intestinal epithelial cell migration via a mechanism requiring both nitric oxide and phosphorylation of p70 S6 kinase. J. Nutr. 138, 1652-1657