Tryptamine-gallic acid hybrid prevents non-steroidal anti-inflammatory drug-induced gastropathy: Correction of mitochondrial dysfunction and inhibition of apoptosis in gastric mucosal cells

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3495-3509

  Pal, Chinmay ^a   Bindu, Samik ^a   Dey, Sumanta ^a   Alam, Athar ^a   Goyal, Manish ^a   Iqbal, Mohd Shameel ^a   Sarkar, Souvik ^a   Kumar, Rahul ^a   Halder, Kamal Krishna ^a   Debnath, Mita Chatterjee ^a   Adhikari, Susanta ^b   Bandyopadhyay, Uday ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b UNIVERSITY OF CALCUTTA   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; CASPASE-3; DEHYDROGENASE ACTIVITY; DOWN-REGULATION; ELECTRON TRANSPORT CHAIN; GASTRIC MUCOSA; GASTRIC MUCOSAL CELLS; HYBRID MOLECULES; IN-VIVO; INDOMETHACIN; LIPID PEROXIDATION; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL PATHWAYS; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL SUPEROXIDE; NON-STEROIDAL ANTI-INFLAMMATORY DRUGS; TRACER STUDY; TRANSMEMBRANE POTENTIALS; UP-REGULATION;

BIOELECTRIC POTENTIALS; CELL DEATH; GENES; OXYGEN; SYNTHESIS (CHEMICAL);

MITOCHONDRIA;

CASPASE 3; CASPASE 9; CELL DNA; GALLIC ACID DERIVATIVE; GASTROINTESTINAL AGENT; INDOMETACIN; IRON; NONSTEROID ANTIINFLAMMATORY AGENT; OXIDOREDUCTASE; PROTEIN BAX; PROTEIN BCL 2; SEGA HYBRID MOLECULE; SUPEROXIDE; TECHNETIUM 99M; THIOL; TRYPTAMINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BAX GENE; BCL 2 GENE; CONTROLLED STUDY; DNA FRAGMENTATION; DOSE RESPONSE; DOWN REGULATION; DRUG DESIGN; DRUG DOSE COMPARISON; DRUG INDUCED DISEASE; DRUG MECHANISM; DRUG POTENCY; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TRANSPORT; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; IRON CHELATION; IRON TRANSPORT; ISOTOPE LABELING; LIPID PEROXIDATION; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MUCOSA CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; STOMACH MUCOSA INJURY; STRUCTURE ACTIVITY RELATION; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; GALLIC ACID; GASTRIC MUCOSA; GENE EXPRESSION REGULATION; HUMANS; INDOMETHACIN; LIPID PEROXIDATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; STOMACH DISEASES; SUPEROXIDES; TRYPTAMINES;

EID: 84863405358     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.307199     Document Type: Article

References (68)

1. Regula, J., Butruk, E., Dekkers, C. P., de Boer, S. Y., Raps, D., Simon, L., Terjung, A., Thomas, K. B., Lühmann, R., and Fischer, R. (2006) Prevention of NSAID-associated gastrointestinal lesions. A comparison study pantoprazole versus omeprazole. Am. J. Gastroenterol. 101, 1747-1755
2. Thompson, M., and Percy, J. S. (1966) Further experience with indomethacin in the treatment of rheumatic disorders. Br. Med. J. 1, 80-83
3. Becker, J. C., Domschke, W., and Pohle, T. (2004) Current approaches to prevent NSAID-induced gastropathy. COX selectivity and beyond. Br. J. Clin. Pharmacol. 58, 587-600
4. Pal, C., Bindu, S., Dey, S., Alam, A., Goyal, M., Iqbal, M. S., Maity, P., Adhikari, S. S., and Bandyopadhyay, U. (2010) Gallic acid prevents non-steroidal anti-inflammatory drug-induced gastropathy in rat by blocking oxidative stress and apoptosis. Free Radic. Biol. Med. 49, 258-267
5. Maity, P., Bindu, S., Choubey, V., Alam, A., Mitra, K., Goyal, M., Dey, S., Guha, M., Pal, C., and Bandyopadhyay, U. (2008) Lansoprazole protects and heals gastric mucosa from non-steroidal anti-inflammatory drug (NSAID)-induced gastropathy by inhibiting mitochondrial as well as Fas-mediated death pathways with concurrent induction of mucosal cell renewal. J. Biol. Chem. 283, 14391-14401
6. Maity, P., Bindu, S., Dey, S., Goyal, M., Alam, A., Pal, C., Mitra, K., and Bandyopadhyay, U. (2009) Indomethacin, a non-steroidal anti-inflammatory drug, develops gastropathy by inducing reactive oxygen species-mediated mitochondrial pathology and associated apoptosis in gastric mucosa. Anovel role of mitochondrial aconitase oxidation. J. Biol. Chem. 284, 3058-3068
7. Biswas, K., Bandyopadhyay, U., Chattopadhyay, I., Varadaraj, A., Ali, E., and Banerjee, R. K. (2003) A novel antioxidant and antiapoptotic role of omeprazole to block gastric ulcer through scavenging of hydroxyl radical. J. Biol. Chem. 278, 10993-11001
8. Wolfe, M. M., and Soll, A. H. (1988) The physiology of gastric acid secretion. N. Engl. J. Med. 319, 1707-1715
9. Szabó, I., and Tarnawski, A. S. (2000) Apoptosis in the gastric mucosa. Molecular mechanisms, basic and clinical implications. J. Physiol. Pharmacol. 51, 3-15
10. Wallace, J. L., and Granger, D. N. (1996) The cellular and molecular basis of gastric mucosal defense. FASEB J. 10, 731-740
11. Kwiecień, S., Brzozowski, T., and Konturek, S. J. (2002) Effects of reactive oxygen species action on gastric mucosa in various models of mucosal injury. J. Physiol. Pharmacol. 53, 39-50
12. Maity, P., Bindu, S., Dey, S., Goyal, M., Alam, A., Pal, C., Reiter, R., and Bandyopadhyay, U. (2009) Melatonin reduces indomethacin-induced gastric mucosal cell apoptosis by preventing mitochondrial oxidative stress and the activation of mitochondrial pathway of apoptosis. J. Pineal. Res. 46, 314-323
13. Jacob, M., Bjarnason, I., Rafi, S., Wrigglesworth, J., and Simpson, R. J. (2001) A study of the effects of indometacin on liver mitochondria from rats, mice, and humans. Aliment. Pharmacol. Ther. 15, 1837-1842
14. Demaurex, N., and Scorrano, L. (2009) Reactive oxygen species are NOXious for neurons. Nat. Neurosci. 12, 819-820
15. Turrens, J. F. (1997) Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17, 3-8
16. Turrens, J. F. (2003) Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344
17. Fariss, M. W., Chan, C. B., Patel, M., Van Houten, B., and Orrenius, S. (2005) Role of mitochondria in toxic oxidative stress. Mol. Interv. 5, 94-111
18. Bindu, S., Pal, C., Dey, S., Goyal, M., Alam, A., Iqbal, M. S., Dutta, S., Sarkar, S., Kumar, R., Maity, P., and Bandyopadhyay, U. (2011) Translocation of heme oxygenase-1 to mitochondria is a novel cytoprotective mechanism against non-steroidal anti-inflammatory drug-induced mitochondrial oxidative stress, apoptosis, and gastric mucosal injury. J. Biol. Chem. 286, 39387-39402
19. Ceccarelli, D., Gallesi, D., Giovannini, F., Ferrali, M., and Masini, A. (1995) Relationship between free iron level and rat liver mitochondrial dysfunction in experimental dietary iron overload. Biochem. Biophys. Res. Commun. 209, 53-59
20. Britton, R. S., Ramm, G. A., Olynyk, J., Singh, R., O'Neill, R., and Bacon, B. R. (1994) Pathophysiology of iron toxicity. Adv. Exp. Med. Biol. 356, 239-253
21. Fraga, C. G., and Oteiza, P. I. (2002) Iron toxicity and antioxidant nutrients. Toxicology 180, 23-32
22. Liang, L. P., Jarrett, S. G., and Patel, M. (2008) Chelation of mitochondrial iron prevents seizure-induced mitochondrial dysfunction and neuronal injury. J. Neurosci. 28, 11550-11556
23. Link, G., Saada, A., Pinson, A., Konijn, A. M., and Hershko, C. (1998) Mitochondrial respiratory enzymes are a major target of iron toxicity in rat heart cells. J. Lab. Clin. Med. 131, 466-474
24. Ling, Y. H., Liebes, L., Zou, Y., and Perez-Soler, R. (2003) Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic response to Bortezomib, a novel proteasome inhibitor, in human H460 nonsmall cell lung cancer cells. J. Biol. Chem. 278, 33714-33723
25. Zimmerman, M. C., and Zucker, I. H. (2009) Mitochondrial dysfunction and mitochondrial-produced reactive oxygen species. New targets for neurogenic hypertension? Hypertension 53, 112-114
26. González-Flecha, B., Cutrin, J. C., and Boveris, A. (1993) Time course and mechanism of oxidative stress and tissue damage in rat liver subjected to in vivo ischemia-reperfusion. J. Clin. Invest. 91, 456-464
27. Dröge, W. (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95
28. Schapira, A. H. (2006) Mitochondrial disease. Lancet 368, 70-82
29. Lin, M. T., and Beal, M. F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795
30. Jing, X. B., Cai, X. B., Hu, H., Chen, S. Z., Chen, B. M., and Cai, J. Y. (2007) Reactive oxygen species and mitochondrial membrane potential are modulated during CDDP-induced apoptosis in EC-109 cells. Biochem. Cell Biol. 85, 265-271
31. Orrenius, S., Gogvadze, V., and Zhivotovsky, B. (2007) Mitochondrial oxidative stress. Implications for cell death. Annu. Rev. Pharmacol. Toxicol. 47, 143-183
32. Malik, F., Kumar, A., Bhushan, S., Khan, S., Bhatia, A., Suri, K. A., Qazi, G. N., and Singh, J. (2007) Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic cell death of human myeloid leukemia HL-60 cells by a dietary compound withaferin A with concomitant protection by N-acetyl cysteine. Apoptosis 12, 2115-2133
33. Parish, R., and Petersen, K. F. (2005) Mitochondrial dysfunction and type 2 diabetes. Curr. Diab. Rep. 5, 177-183
34. Carelli, V., Ross-Cisneros, F. N., and Sadun, A. A. (2004) Mitochondrial dysfunction as a cause of optic neuropathies. Prog. Retin. Eye Res. 23, 53-89
35. Naumann, M., Reiners, K., Gold, R., Schindler, R., Paulus, W., Klopstock, T., and Reichmann, H. (1995) Mitochondrial dysfunction in adult-onset myopathies with structural abnormalities. Acta Neuropathol. 89, 152-157
36. Ren, J., Pulakat, L., Whaley-Connell, A., and Sowers, J. R. (2010) Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. J. Mol. Med. 88, 993-1001
37. Serviddio, G., Bellanti, F., Sastre, J., Vendemiale, G., and Altomare, E. (2010) Targeting mitochondria. A new promising approach for the treatment of liver diseases. Curr. Med. Chem. 17, 2325-2337
38. Ko, J. K., Ma, J. J., Chow, J. Y., Ma, L., and Cho, C. H. (1998) The correlation of the weakening effect on gastric mucosal integrity by 5-HT with neutrophil activation. Free Radic. Biol. Med. 24, 1007-1014
39. Ben Farhat, M., Jordán, M. J., Chaouech-Hamada, R., Landoulsi, A., and Sotomayor, J. A. (2009) Variations in essential oil, phenolic compounds, and antioxidant activity of tunisian cultivated Salvia officinalis L. J. Agric. Food Chem. 57, 10349-10356
40. +-ATPase, oxidative damage, and apoptosis. Inflammopharmacology 12, 153-176
41. Pal, C., Kundu, M. K., Bandyopadhyay, U., and Adhikari, S. (2011) Synthesis of novel heme-interacting acridone derivatives to prevent free hememediated protein oxidation and degradation. Bioorg. Med. Chem. Lett. 21, 3563-3567
42. Kumar, S., Das, S. K., Dey, S., Maity, P., Guha, M., Choubey, V., Panda, G., and Bandyopadhyay, U. (2008) Antiplasmodial activity of [(aryl) arylsulfanylmethyl] pyridine. Antimicrob. Agents Chemother. 52, 705-715
43. Dey, S., Guha, M., Alam, A., Goyal, M., Bindu, S., Pal, C., Maity, P., Mitra, K., and Bandyopadhyay, U. (2009) Malarial infection develops mitochondrial pathology and mitochondrial oxidative stress to promote hepatocyte apoptosis. Free Radic. Biol. Med. 46, 271-281
44. Sims, N. R., and Anderson, M. F. (2008) Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat. Protoc. 3, 1228-1239
45. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
46. Rousou, A. J., Ericsson, M., Federman, M., Levitsky, S., and McCully, J. D. (2004) Opening of mitochondrial KATP channels enhances cardioprotection through the modulation of mitochondrial matrix volume, calcium accumulation, and respiration. Am. J. Physiol. Heart Circ. Physiol. 287, H1967-H1976
47. Frezza, C., Cipolat, S., and Scorrano, L. (2007) Organelle isolation. Functional mitochondria from mouse liver, muscle, and cultured fibroblasts. Nat. Protoc. 2, 287-295
48. Halder, K. K., Mandal, B., Debnath, M. C., Bera, H., Ghosh, L. K., and Gupta, B. K. (2008) Chloramphenicol-incorporated polylactide-co-glycolide (PLGA) nanoparticles. Formulation, characterization, technetium- 99m labeling, and biodistribution studies. J. Drug Target 16, 311-320
49. Basu, B., Desai, R., Balaji, J., Chaerkady, R., Sriram, V., Maiti, S., and Panicker, M. M. (2008) Serotonin in preimplantation mouse embryos is localized to the mitochondria and can modulate mitochondrial potential. Reproduction 135, 657-669
50. Mulac, D., and Humpf, H. U. (2011) Cytotoxicity and accumulation of ergot alkaloids in human primary cells. Toxicology 282, 112-121
51. Ahmed Fazary, E., Taha, M. A., and Ju, Y. H. (2009) Iron complexation equilibria studies of gallic acid. J. Chem. Eng. Data 54, 35-42
52. Robinson, K. M., Janes, M. S., Pehar, M., Monette, J. S., Ross, M. F., Hagen, T. M., Murphy, M. P., and Beckman, J. S. (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U.S.A. 103, 15038-15043
53. Musumba, C., Pritchard, D. M., and Pirmohamed, M. (2009) Review article. Cellular and molecular mechanisms of NSAID-induced peptic ulcers. Aliment. Pharmacol. Ther. 30, 517-531
54. Fornai, M., Colucci, R., Antonioli, L., Awwad, O., Ugolini, C., Tuccori, M., Fulceri, F., Natale, G., Basolo, F., and Blandizzi, C. (2011) Effects of esomeprazole on healing of nonsteroidal anti-inflammatory drug (NSAID)-induced gastric ulcers in the presence of a continued NSAID treatment. Characterization of molecular mechanisms. Pharmacol. Res. 63, 59-67
55. +-ATPase inhibition and scavenging of hydroxyl radical. Life Sci. 71, 2845-2865
56. Alarcón de la Lastra, C., Martín, M. J., and Motilva, V. (1994) Antiulcer and gastroprotective effects of quercetin. A gross and histologic study. Pharmacology 48, 56-62
57. Mukherjee, S. (2003) Diarrhea associated with lansoprazole. J. Gastroenterol. Hepatol. 18, 602-603
58. Umeno, J., Matsumoto, T., Nakamura, S., Jo, Y., Yada, S., Hirakawa, K., Yoshimura, R., Yamagata, H., Kudo, T., Hirano, A., Gushima, M., Yao, T., Nakashima, Y., and Iida, M. (2008) Linear mucosal defect may be characteristic of lansoprazole-associated collagenous colitis. Gastrointest. Endosc. 67, 1185-1191
59. Yusuke, H., Jun, T., Naotaka, M., Yuichi, T., Yutaka, E., and Kazuaki, I. (2009) Lansoprazole-associated collagenous colitis. Unique presentation, similar to ischemic colitis. Endoscopy 41, Suppl. 2, E281-E282
60. Panting, K. J., Pinto, M., and Ellison, J. (2009) Lansoprazole-induced subacute cutaneous lupus erythematosus. Clin. Exp. Dermatol. 34, 733-734
61. Fort, F. L., Miyajima, H., Ando, T., Suzuki, T., Yamamoto, M., Hamashima, T., Sato, S., Kitazaki, T., Mahony, M. C., and Hodgen, G. D. (1995) Mechanism for species-specific induction of Leydig cell tumors in rats by lansoprazole. Fundam. Appl. Toxicol. 26, 191-202
62. Jose, J., Saravu, K., Khera, K., Jimmy, B., and Shastry, B. A. (2008) Acute interstitial nephritis related to lansoprazole administration. J. Pak. Med. Assoc. 58, 206-207
63. Clark, D. W., and Strandell, J. (2006) Myopathy including polymyositis. A likely class adverse effect of proton pump inhibitors? Eur. J. Clin. Pharmacol. 62, 473-479
64. González, P., Soriano, V., López, P., and Niveiro, E. (2002) Anaphylaxis to proton pump inhibitors. Allergol. Immunopathol. 30, 342-343
65. Dial, S., Delaney, J. A., Barkun, A. N., and Suissa, S. (2005) Use of gastric acid-suppressive agents and the risk of community-acquired Clostridiumdifficile-associated disease. JAMA 294, 2989-2995
66. Laheij, R. J., Sturkenboom, M. C., Hassing, R. J., Dieleman, J., Stricker, B. H., and Jansen, J. B. (2004) Risk of community-acquired pneumonia and use of gastric acid-suppressive drugs. JAMA 292, 1955-1960
67. Wallace, J. L., Syer, S., Denou, E., de Palma, G., Vong, L., McKnight, W., Jury, J., Bolla, M., Bercik, P., Collins, S. M., Verdu, E., and Ongini, E. (2011) Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 141, 1314-1322
68. Reagan-Shaw, S., Nihal, M., and Ahmad, N. (2008) Dose translation from animal to human studies revisited. FASEB J. 22, 659-661