Role of an Indole-Thiazolidine Molecule PPAR Pan-Agonist and COX Inhibitor on Inflammation and Microcirculatory Damage in Acute Gastric Lesions

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Santin, José Roberto ^a   Daufenback Machado, Isabel ^a   Rodrigues, Stephen F P ^a   Teixeira, Simone ^a   Muscará, Marcelo N ^a   Lins Galdino, Suely ^b   da Rocha Pitta, Ivan ^b   Farsky, Sandra H P ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BEZAFIBRATE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GRANULOCYTE ANTIBODY; INDUCIBLE NITRIC OXIDE SYNTHASE; LYSO 7; MYELOPEROXIDASE; N(G) NITROARGININE METHYL ESTER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; PROSTAGLANDIN SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; IN VIVO STUDY; INFLAMMATION; MALE; MICROCIRCULATION; MOUSE; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; STOMACH ACID SECRETION; STOMACH BLOOD FLOW; STOMACH LESION; STOMACH PH;

ANIMALS; BODY WEIGHT; CYCLOOXYGENASE INHIBITORS; ETHANOL; GASTRIC ACID; GASTRITIS; GENE EXPRESSION REGULATION; HYDROCHLORIC ACID; INDOLES; MALE; MICE; MICROCIRCULATION; NEUTROPHIL INFILTRATION; NITRIC OXIDE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PPAR GAMMA; REGIONAL BLOOD FLOW; THIAZOLIDINEDIONES;

EID: 84885034377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076894     Document Type: Article

References (68)

1. Lemos M, Santin JR, Júnior LC, Niero R, Andrade SF, (2011) Gastroprotective activity of hydroalcoholic extract obtained from the leaves of Brassica oleracea var. acephala DC in different animal models. J Ethnopharmacol 138: 503-507. doi:10.1016/j.jep.2011.09.046. PubMed: 21986229.
2. Sung NY, Choi KS, Park EC, Park K, Lee SY, et al. (2007) Smoking, alcohol and gastric cancer risk in Korean men: the National Health Insurance Corporation Study. Br J Cancer 97: 700-704. doi:10.1038/sj.bjc.6603893. PubMed: 17637680.
3. Li CY, Xu HD, Zhao BT, Chang HI, Rhee HI, (2008) Gastroprotective effect of cyaniding 3-glucoside on ethanol-induced gastric lesions in rats. Alcohol 42: 683-687. doi:10.1016/j.alcohol.2008.08.009. PubMed: 19038699.
4. Alvarez-Suarez JM, Dekanski D, Ristić S, Radonjić NV, Petronijević ND, et al. (2011) Strawberry polyphenols attenuate ethanol-induced gastric lesions in rats by activation of antioxidant enzymes and attenuation of MDA increase. PLOS ONE 6: e25878. doi:10.1371/journal.pone.0025878. PubMed: 22016781.
5. Dembinski A, Warzecha Z, Ceranowicz P, Cieszkowski J, Sendur R, et al. (2011) Involvement of Cyclooxygenase-2 Activity in Therapeutic Effect of Ghrelin in the Course of Ethanol-Induced Gastric Ulcers in Rats. Gastroenterology 140: S-315.
6. Ismail IF, Golbabapour S, Hassandarvish P, Hajrezaie M, Abdul Majid N, et al. (2012) Gastroprotective Activity of Polygonum chinense Aqueous Leaf Extract on Ethanol-Induced Hemorrhagic Mucosal Lesions in Rats. Evid Based Complement Alternat Med, 2012(2012):404012. PubMed: 23365597.
7. Ning JW, Lin GB, Ji F, Xu J, Sharify N, (2012) Preventive effects of geranylgeranylacetone on rat ethanol-induced gastritis. World J Gastroenterol 18: 2262-2269. doi:10.3748/wjg.v18.i18.2262. PubMed: 22611321.
8. Guslandi M, (1987) Effects of ethanol on the gastric mucosa. Dig Dis 5: 21-32. doi:10.1159/000171159. PubMed: 3297432.
9. Szabo S, Vattay P, (1990) Experimental gastric and duodenal ulcers. Gastroenterol Clin North Am 19: 67-85. PubMed: 2184131.
10. Medeiros JV, Gadelha GG, Lima SJ, Garcia JA, Soares PM, et al. (2008) Role of the NO/cGMP/K(ATP) pathway in the protective effects of sildenafil against ethanol-induced gastric damage in rats. Br J Pharmacol 153: 721-727. doi:10.1038/sj.bjp.0707605. PubMed: 18071300.
11. Muscará MN, Wallace JL, (1999) Nitric Oxide. V. therapeutic potential of nitric oxide donors and inhibitors. Am J Physiol 276: G1313-G1316. PubMed: 10362633.
12. Kubes P, Suzuki M, Granger DN, (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A 88: 4651-4655. doi:10.1073/pnas.88.11.4651. PubMed: 1675786.
13. Ma L, Wallace JL, (2000) Endothelial nitric oxide synthase modulates gastric ulcer healing in rats. Am J Physiol Gastrointest Liver Physiol 279: G341-G346. PubMed: 10915643.
14. Guha P, Dey A, Chatterjee A, Chattopadhyay S, Bandyopadhyay SK, (2010) Pro-ulcer effects of resveratrol in mice with indomethacin-induced gastric ulcers are reversed by L-arginine. Br J Pharmacol 159: 726-734. doi:10.1111/j.1476-5381.2009.00572.x. PubMed: 20067468.
15. Fajas L, Debril MB, Auwerx J, (2001) PPAR gamma: an essential role in metabolic control. Nutr Metab Cardiovasc Dis 11: 64-69. PubMed: 11383325.
16. Lahiri S, Sen T, Palit G, (2009) Involvement of glucocorticoid receptor and peroxisome proliferator activated receptor-gamma in pioglitazone mediated chronic gastric ulcer healing in rats. Eur J Pharmacol 609: 118-125. doi:10.1016/j.ejphar.2009.03.005. PubMed: 19281808.
17. Meissner M, Hrgovic I, Doll M, Naidenow J, Reichenbach G, et al. (2010) Peroxisome proliferator-activated receptor {delta} activators induce IL-8 expression in nonstimulated endothelial cells in a transcriptional and posttranscriptional manner. J Biol Chem 285: 33797-33804. doi:10.1074/jbc.M110.137943. PubMed: 20592029.
18. Lee JH, Kim H, Woo JH, Joe EH, Jou I, (2012):: 11,(2012) 2/MCP-1 expression in IFN-γ-stimulated astrocytes by increasing MAPK phosphatase-1 mRNA stability. J Neuroinflammation 910.1186/1742-2094-9-34. PubMed: 22339770.
19. Long EM, Klimowicz AC, Paula-Neto HA, Millen B, McCafferty DM, et al. (2011) A subclass of acylated anti-inflammatory mediators usurp Toll-like receptor 2 to inhibit neutrophil recruitment through peroxisome proliferator-activated receptor gamma. Proc Natl Acad Sci U S A 108: 16357-16362. doi:10.1073/pnas.1100702108. PubMed: 21930915.
20. Yang X, Kume S, Tanaka Y, Isshiki K, Araki S, et al. (2011) GW501516, a PPARδ agonist, ameliorates tubule interstitial inflammation in protein uric kidney disease via inhibition of TAK1-NFκB pathway in mice. PLOS ONE 6: e25271. doi:10.1371/journal.pone.0025271. PubMed: 21966476.
21. Farnesi-de-Assunção TS, Alves CF, Carregaro V, de Oliveira JR, da Silva CA, et al. (2012) PPAR-γ agonists, mainly 15d-PGJ(2), reduce eosinophil recruitment following allergen challenge. Cell Immunol 273: 23-29. doi:10.1016/j.cellimm.2011.11.010. PubMed: 22192475.
22. Wu L, Yan C, Czader M, Foreman O, Blum JS, et al. (2012) Inhibition of PPARγ in myeloid-lineage cells induces systemic inflammation, immunosuppression, and tumorigenesis. Blood 119: 115-126. doi:10.1182/blood-2011-06-363093. PubMed: 22053106.
23. Feldman PL, Lambert MH, Henke BR, (2008) PPAR modulators and PPAR pan agonists for metabolic diseases: the next generation of drugs targeting peroxisome proliferator-activated receptors? Curr Top Med Chem 8: 728-749. doi:10.2174/156802608784535084. PubMed: 18537685.
24. Zhang LS, Wang SQ, Xu WR, Wang RL, Wang JF, (2012) Scaffold-based pan-agonist design for the PPARα, PPARβ and PPARγ receptors. PLOS ONE 7: e48453. doi:10.1371/journal.pone.0048453. PubMed: 23119024.
25. Pancione M, Forte N, Sabatino L, Tomaselli E, Parente D, et al. (2009) Reduced beta-catenin and peroxisome proliferator-activated receptor-gamma expression levels are associated with colorectal cancer metastatic progression: correlation with tumor-associated macrophages, cyclooxygenase 2, and patient outcome. Hum Pathol 40: 714-725. doi:10.1016/j.humpath.2008.08.019. PubMed: 19121846.
26. Meyer S, Vogt T, Landthaler M, Berand A, Reichle A, et al. (2009) Cyclooxygenase 2 (COX2) and Peroxisome Proliferator-Activated Receptor gamma (PPARG) Are Stage-Dependent Prognostic Markers of Malignant Melanoma. PPAR Res, 2009(2009):848645. PubMed: 19639032.
27. Konturek PC, Brzozowski T, Kania J, Konturek SJ, Kwiecien S, et al. (2003) Pioglitazone, a specific ligand of peroxisome proliferator-activated receptor-gamma, accelerates gastric ulcer healing in rat. Eur J Pharmacol 472: 213-220. doi:10.1016/S0014-2999(03)01932-0. PubMed: 12871756.
28. Takagi T, Naito Y, Ichikawa H, Tomatsuri N, Katada K, et al. (2004) A PPAR-gamma ligand, 15-deoxy-Delta12, 14-prostaglandin. J Volumes 2inhibited gastric mucosal injury induced by ischemia-reperfusion in rats. Redox Rep 9:376-981.
29. Villegas I, Martín AR, Toma W, de la Lastra CA, (2004) Rosiglitazone, an agonist of peroxisome proliferator-activated receptor gamma, protects against gastric ischemia-reperfusion damage in rats: role of oxygen free radicals generation. Eur J Pharmacol 505: 195-203. doi:10.1016/j.ejphar.2004.10.020. PubMed: 15556153.
30. Brzozowski T, Konturek PC, Pajdo R, Kwiecień SN, Konturek Set al (2005) Agonist of peroxisome proliferator-activated receptor gamma (PPAR-gamma): a new compound with potent gastroprotective and ulcer healing properties. Inflammopharmacology 13: 317-330. doi:10.1163/156856005774423908. PubMed: 16259750.
31. Konturek PC, Brzozowski T, Burnat G, Szlachcic A, Koziel J, et al. (2010) Gastric ulcer healing and stress-lesion preventive properties of pioglitazone are attenuated in diabetic rats. J Physiol Pharmacol 61: 429-436. PubMed: 20814070.
32. Morsy MA, Ashour OM, Fouad AA, Abdel-Gaber SA, (2010) Gastroprotective effects of the insulin sensitizers rosiglitazone and metformin against indomethacin-induced gastric ulcers in Type 2 diabetic rats. Clin Exp Pharmacol Physiol 37: 173-177. doi:10.1111/j.1440-1681.2009.05250.x. PubMed: 19566821.
33. Santin JR, Uchôa FD, Lima MD, Rabello MM, Machado ID, et al. (2013) Chemical synthesis, docking studies and biological effects of a pan peroxisome proliferator-activated receptor agonist and cyclooxygenase inhibitor. Eur J Pharm Sci 48: 689-697. doi:10.1016/j.ejps.2012.12.029. PubMed: 23305993.
34. Mizui T, Doteuchi M, (1983) Effect of polyamines on acidified ethanol-induced gastric lesion in rats. Jpn J Pharmacol 33: 939-945. doi:10.1254/jjp.33.939. PubMed: 6580476.
35. Goso Y, Ueno M, Hotta K, Ishihara K, (2007) Protective effects of the whisky congeners on ethanol-induced gastric mucosal damage. Alcohol Clin Exp Res 31: 390-394. doi:10.1111/j.1530-0277.2006.00319.x. PubMed: 17295722.
36. Lakshmi V, Singh N, Shrivastva S, Mishra SK, Dharmani P, et al. (2010) Gedunin and photogedunin of Xylocarpus granatum show significant anti-secretory effects and protect the gastric mucosa of peptic ulcer in rats. Phytomedicine 17: 569-574. doi:10.1016/j.phymed.2009.10.016. PubMed: 19962286.
37. Shay H, Komarov SA, Fels SS, Meranze D, Gruenstein M, et al. (1945) A simple method for the uniform production of gastric ulceration in the rat. Gastroenterology 5: 43-61.
38. Bradley PP, Priebat DA, Christensen RD, Rothstein G, (1982) Measurement of cutaneous infl{ligature}ammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78: 206-209. doi:10.1111/1523-1747.ep12506462. PubMed: 6276474.
39. Conlan JW, North RJ, (1994) Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by agranulocyte-depleting monoclonal antibody. J Exp Med 179: 259-268. doi:10.1084/jem.179.1.259. PubMed: 8270870.
40. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70. PubMed: 17884993.
41. Ohno T, Katori M, Nishiyama K, Saigenji K, (1995) Direct observation of microcirculation of the basal region of rat gastric mucosa. J Gastroenterol 30: 557-564. doi:10.1007/BF02367779. PubMed: 8574325.
42. Krznaric Z, Ljubas Kelecic D, Rustemovic N, Vranesic Bender D, Ostojic R, et al. (2011) Pharmaceutical principles of acid inhibitors: unmet needs. Dig Dis 29: 469-475. doi:10.1159/000331515. PubMed: 22095012.
43. Van Beekum O, Fleskens V, Kalkhoven E, (2009) Posttranslational modifications of PPAR-gamma: fine-tuning the metabolic master regulator. Obesity 17: 213-219. doi:10.1038/oby.2008.473. PubMed: 19169221.
44. Dreijerink KM, Varier RA, Van Beekum O, Jeninga EH, Höppener JW, et al. (2009) The multiple endocrine neoplasia type 1(MEN1) tumor suppressor regulates peroxisome proliferator-activated receptor gamma-dependent adipocyte differentiation. Mol Cell Biol 29: 5060-5069. doi:10.1128/MCB.01001-08. PubMed: 19596783.
45. Naito Y, Yoshikawa T, (2010) PPARgamma as a new therapeutic target in inflammatory diseases. Nihon Rinsho 68: 341-349. PubMed: 20158107.
46. Takagi T, Naito Y, Ichikawa H, Tomatsuri N, Katada K, et al. (2004) A PPAR-gamma ligand, 15-deoxy-Delta12, 14-prostaglandin. J Volumes 2inhibited gastric mucosal injury induced by ischemia-reperfusion in rats. Redox Rep 9:376-981.
47. Reddy RC, Narala VR, Keshamouni VG, Milam JE, Newstead MW, et al. (2008) Sepsis-induced inhibition of neutrophil chemotaxis is mediated by activation of peroxisome proliferator-activated receptor-{gamma}. Blood 112: 4250-4258. doi:10.1182/blood-2007-12-128967. PubMed: 18535203.
48. Lim HA, Lee EK, Kim JM, Park MH, Kim DH, et al. (2012) PPARγ activation by baicalin suppresses NF-κB-mediated inflammation in aged rat kidney. Biogerontology 13: 133-145. doi:10.1007/s10522-011-9361-4. PubMed: 22033706.
49. Martin HL, Mounsey RB, Mustafa S, Sathe K, Teismann P, (2012) Pharmacological manipulation of peroxisome proliferator-activated receptor γ (PPARγ) reveals a role for anti-oxidant protection in a model of Parkinson's disease. Exp Neurol 235: 528-538. doi:10.1016/j.expneurol.2012.02.017. PubMed: 22417924.
50. Wallace JL, McKnight GW, Bell CJ, (1995) Adaptation of rat gastric mucosa to aspirin requires mucosal contact. Am J Physiol 268: G134-G138. PubMed: 7840196.
51. Beserra AM, Calegari PI, Souza Mdo C, Dos Santos RA, Lima JC, et al. (2011) Gastroprotective and ulcer-healing mechanisms of ellagic acid in experimental rats. J Agric Food Chem 59: 6957-6965. doi:10.1021/jf2003267. PubMed: 21644797.
52. Rocha NF, Oliveira GV, Araújo FY, Rios ER, Carvalho AM, et al. (2011) (-)-α-Bisabolol-induced gastroprotection is associated with reduction in lipid peroxidation, superoxide dismutase activity and neutrophil migration. Eur J Pharm Sci 44: 455-461. doi:10.1016/j.ejps.2011.08.020. PubMed: 21924353.
53. Bayir Y, Odabasoglu F, Cakir A, Aslan A, Suleyman H, et al. (2006) The inhibition of gastric mucosal lesion, oxidative stress and neutrophil-infiltration in rats by the lichen constituent diffractaic acid. Phytomedicine 13: 584-590. doi:10.1016/j.phymed.2005.07.002. PubMed: 16920514.
54. Celinski K, Dworzanski T, Korolczuk A, Piasecki R, Slomka M, et al. (2011) Effects of peroxisome proliferator-activated receptors-gamma ligands on dextran sodium sulphate-induced colitis in rats. J Physiol Pharmacol 62: 347-356. PubMed: 21893696.
55. Liang YJ, Jian JH, Liu YC, Juang SJ, Shyu KG, et al. (2010) Advanced glycation end products-induced apoptosis attenuated by PPAR delta activation and epigallocatechin gallate through NF-kappaB pathway in human embryonic kidney cells and human mesangial cells. Diabetes/Metab Res Rev 26: 406-416. doi:10.1002/dmrr.1100.
56. Imamoto E, Yoshida N, Uchiyama K, Kuroda M, Kokura S, et al. (2004) Inhibitory effect of pioglitazone on expression of adhesion molecules on neutrophils and endothelial cells. Biofactors 20: 37-47. doi:10.1002/biof.5520200104. PubMed: 15096659.
57. Reilly CM, Oates JC, Cook JA, Morrow JD, Halushka PV, et al. (2000) Inhibition of mesangial cell nitric oxide in MRL/lpr mice by prostaglandin J2 and proliferator activation receptor-gamma agonists. J Immunol 164: 1498-1504. PubMed: 10640767.
58. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK, (1998) The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391: 79-82. doi:10.1038/34178. PubMed: 9422508.
59. Wang AC, Dai X, Luu B, Conrad DJ, (2001) Peroxisome proliferator-activated receptor-gamma regulates airway epithelial cell activation. Am J Respir Cell Mol Biol 24: 688-693. doi:10.1165/ajrcmb.24.6.4376. PubMed: 11415933.
60. El-Demerdash E, El-Mesallamy HO, Abu-Zaid NM, Gad MZ, (2010) The potential therapeutic effect of nitric oxide modulators in experimentally-induced gastric ulcers. Drugs Discov Ther 4: 276-284. PubMed: 22491210.
61. Kato S, Ohkawa F, Ito Y, Amagase K, Takeuchi K, (2009) Role of endothelial nitric oxide synthase in aggravation of indomethacin-induced gastric damage in adjuvant arthritic rats. J Physiol Pharmacol 60: 147-155. PubMed: 20065509.
62. Guo JS, Cho CH, Wang JY, Koo MW, (2006) Differential effects of selective and non-selective inhibition of nitric oxide synthase on the expression and activity of cyclooxygenase-2 during gastric ulcer healing. Eur J Pharmacol 536: 301-308. doi:10.1016/j.ejphar.2005.12.088. PubMed: 16600210.
63. Guha P, Dey A, Sarkar B, Dhyani MV, Chattopadhyay S, et al. (2009) Improved antiulcer and anticancer properties of a trans-resveratrol analog in mice. J Pharmacol Exp Ther 328: 829-838. doi:10.1124/jpet.108.145334. PubMed: 19066340.
64. Liang C, Ren Y, Tan H, He Z, Jiang Q, et al. (2009) Rosiglitazone via up regulation of Akt/eNOS pathways attenuates dysfunction of endothelial progenitor cells, induced by advanced glycation end products. Br J Pharmacol 158: 1865-1873. doi:10.1111/j.1476-5381.2009.00450.x. PubMed: 19917066.
65. Yuen CY, Wong WT, Tian XY, Wong SL, Lau CW, et al. (2011) Telmisartan inhibits vasoconstriction via PPARγ-dependent expression and activation of endothelial nitric oxide synthase. Cardiovasc Res 90: 122-129. doi:10.1093/cvr/cvq392. PubMed: 21156825.
66. Sadaghiani MS, Javadi-Paydar M, Gharedaghi MH, Fard YY, Dehpour AR, (2011) Antidepressant-like effect of pioglitazone in the forced swimming test in mice: the role of PPAR-gamma receptor and nitric oxide pathway. Behav Brain Res 224: 336-343. doi:10.1016/j.bbr.2011.06.011. PubMed: 21704657.
67. Betz B, Schneider R, Kress T, Schick MA, Wanner C, et al. (2012) Rosiglitazone affects nitric oxide synthases and improves renal outcome in a rat model of severe ischemia/reperfusion injury. PPAR Res: pp. 2012:219319.
68. Friedland SN, Leong A, Filion KB, Genest J, Lega IC, et al. (2012) The cardiovascular effects of peroxisome proliferator-activated receptor agonists. Am J Med 125: 126-133. doi:10.1016/j.amjmed.2011.08.025. PubMed: 22269613.