The role of poly(ADP-ribose) polymerase-1 inhibitor in carrageenan-induced lung inflammation in mice

Molecular Immunology

Volumn 63, Issue 2, 2015, Pages 394-405

  Ahmad, Sheikh Fayaz ^a   Zoheir, Khairy M A ^a,b   Ansari, Mushtaq Ahmad ^a   Korashy, Hesham M ^a   Bakheet, Saleh A ^a   Ashour, Abdelkader E ^a   Al Shabanah, Othman A ^a   Al harbi, Mohammed M ^a   Attia, Sabry M ^a,c  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b NATIONAL RESEARCH CENTRE   (Egypt)

^c Al Azhar University   (Egypt)

Author keywords

Carrageenan; Inflammatory mediators; Lung tissue; PARP 1 inhibitor; Pleural exudate

Indexed keywords

5 AMINOISOQUINOLINONE; ANTIINFLAMMATORY AGENT; CARRAGEENAN; CYCLOOXYGENASE 2; I KAPPA B ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; L SELECTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MALONALDEHYDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1 INHIBITOR; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 5-AMINOISOQUINOLINONE; AUTACOID; CELL ADHESION MOLECULE; CYTOKINE; ENZYME INHIBITOR; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 2 RECEPTOR ALPHA; ISOQUINOLINE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TNFRSF18 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CD25+ T LYMPHOCYTE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; LIPID PEROXIDATION; LUNG PARENCHYMA; LYMPHOCYTE COUNT; MOUSE; MOUSE MODEL; NONHUMAN; PLEURA FLUID; PLEURISY; PNEUMONIA; PROTEIN EXPRESSION; SINGLE DRUG DOSE; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; REGULATORY T LYMPHOCYTE;

MUS;

ANIMALS; CARRAGEENAN; CELL ADHESION MOLECULES; CYCLOOXYGENASE 2; CYTOKINES; ENZYME INHIBITORS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GLUCOCORTICOID-INDUCED TNFR-RELATED PROTEIN; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; ISOQUINOLINES; LIPID PEROXIDATION; MICE, INBRED BALB C; NITRIC OXIDE SYNTHASE TYPE II; PNEUMONIA; POLY(ADP-RIBOSE) POLYMERASES; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY;

EID: 84912051467     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2014.09.009     Document Type: Article

References (62)

1. Ahmad S.F., Zoheir K.M., Abdel-Hamied H.E., Attia S.M., Ashour A.E., Bakheet S.A., Abd-Allah A.R. Grape seed proanthocyanidin extract has potent anti-arthritic effects on collagen-induced arthritis by modifying the T cell balance. Int. Immunopharmacol. 2013, 17:79-87.
2. Ansari M.A., Maayah Z.H., Bakheet S.A., El-Kadi A.O., Korashy H.M. The role of aryl hydrocarbon receptor signaling pathway in cardiotoxicity of acute lead intoxication in vivo and in vitro rat model. Toxicology 2013, 306:40-49.
3. Ahmad S.F., Zoheir K.M., Bakheet S.A., Ashour A.E., Attia S.M. Poly(ADP-ribose) polymerase-1 inhibitor modulates T regulatory and IL-17 cells in the prevention of adjuvant induced arthritis in mice model. Cytokine 2014, 68:76-85.
4. Ahmad S.F., Zoheir K.M., Abdel-Hamied H.E., Alrashidi I., Attia S.M., Bakheet S.A., Ashour A.E., Abd-Allah A.R. The role of a histamine 4 receptor as an anti-inflammatory target in carrageenan-induced pleurisy in mice. Immunology 2014, 142(3):374-383.
5. Ahmad S.F., Zoheir K.M., Abdel-Hamied H.E., Attia S.M., Bakheet S.A., Ashour A.E., Abd-Allah A.R. Grape seed proanthocyanidin extract protects against carrageenan-induced lung inflammation in mice through reduction of pro-inflammatory markers and chemokine expressions. Inflammation 2014, 37:500-511.
6. Ahmad S.F., Zoheir K.M., Abdel-Hamied H.E., Attia S.M., Bakheet S.A., Ashour A.E., Abd-Allah A.R. Amelioration of autoimmune arthritis by naringin through modulation of T regulatory cells and Th1/Th2 cytokines. Cell. Immunol. 2014, 287:112-120.
7. Ahmad S.F., Attia S.M., Zoheir K.M., Ashour A.E., Bakheet S.A. Attenuation of the progression of adjuvant-induced arthritis by 3-aminobenzamide treatment. Int. Immunopharmacol. 2014, 19:52-59.
8. Ballestas M.E., Benveniste E.N. Interleukin 1-beta- and tumor necrosis factor-alpha-mediated regulation of ICAM-1 gene expression in astrocytes requires protein kinase C activity. Glia 1995, 14:267-278.
9. Barakat A., Szick-Miranda K., Chang I.F., Guyot R., Blanc G., Cooke R., Delseny M., Bailey-Serres J. The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol. 2001, 127:398-415.
10. Borish L.C., Steinke J.W. Cytokines and chemokines. J. Allergy Clin. Immunol. 2003, 111:460-475.
11. Cornelius L.A., Taylor J.T., Degitz K., Li L.J., Lawley T.J., Caughman S.W. A 5' portion of the ICAM-1 gene confers tissue-specific differential expression levels and cytokine responsiveness. J. Invest. Dermatol. 1993, 100:753-758.
12. Cuzzocrea S., Zingarelli B., Hake P., Salzman A.L., Szabo C. Anti-inflammatory effects of mercaptoethylguanidine, a combined inhibitor of nitric oxide synthase and peroxynitrite scavenger, in carrageenan-induced models of inflammation. Free Rad. Biol. Med. 1998, 24:450-459.
13. Chen Y., Yang L., Lee T.J. Oroxylin A inhibition of lipopolysaccharide-induced iNOS and COX-2 gene expression via suppression of nuclear factor-kappaB activation. Biochem. Pharmacol. 2000, 59:1445-1457.
14. Christopherson K., Hromas R. Chemokine regulation of normal and pathologic immune responses. Stem Cells 2001, 19:388-396.
15. Cuzzocrea S., Mazzon E., Dugo L., Serraino I., Di Paola R., Genovese T., De Sarro A., Caputi A.P. Absence of endogenous interleukin-10 enhances the evolution of acute lung injury. Eur. Cytokine Netw. 2002, 13:285-297.
16. Cuzzocrea S., Mazzon E., Di Paola R., Genovese T., Patel N.S., Muià C., Threadgill M.D., De Sarro A., Thiemermann C. 5-Aminoisoquinolinone reduces colon injury by experimental colitis. Naunyn Schmiedebergs Arch. Pharmacol. 2004, 370:464-473.
17. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribose) polymerase-1 reactions in the regulation of nuclear functions. Biochem. J. 1999, 342:249-268.
18. Esposito E., Cuzzocrea S. Superoxide, NO, peroxynitrite and PARP in circulatory shock and inflammation. Front. Biosci. (Landmark Ed.) 2009, 14:263-296.
19. Farombi E.O., Shrotriya S., Surh Y.-J. Kolaviron inhibits dimethyl nitrosamine-induced liver injury by suppressing COX-2 and iNOS expression via NF-kB and AP-1. Life Sci. 2009, 84:149-155.
20. Gao H., Guo R.F., Speyer C.L., Reuben J., Neff T.A., Hoesel L.M. Stat3 activation in acute lung injury. J. Immunol. 2004, 172:7703-7712.
21. Gonzalez-Rey E., Martínez-Romero R., O'Valle F., Aguilar-Quesada R., Conde C., Delgado M., Oliver F.J. Therapeutic effect of a poly(ADP-ribose) polymerase-1 inhibitor on experimental arthritis by down-regulating inflammation and Th1 response. PLoS ONE 2007, 31(2):e1071.
22. Hurst S.D., Muchamuel T., Gorman D.M., Gilbert J.M., Clifford T., Kwan S. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J. Immunol. 2002, 169:443-453.
23. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
24. Hakme A., Wong H.K., Dantzer F., Schreiber V. The expanding field of poly(ADPribosyl) action reactions. EMBO Rep. 2008, 9:1094-1100.
25. Hendryk S., Czuba Z.P., Jedrzejowska-Szypulka H., Szliszka E., Phillips V.A., Threadgill M.D. Influence of 5-aminoisoquinolin-1-one (5-AIQ) on neutrophil chemiluminescence in rats with transient and prolonged focal cerebral ischemia and after reperfusion. J. Physiol. Pharmacol. 2008, 59:811-822.
26. Hesslinger C., Strub A., Boer R., Ulrich W.R., Lehner M.D., Braun C. Inhibition of inducible nitric oxide synthase in respiratory diseases. Biochem. Soc. Trans. 2009, 37:886-891.
27. Impellizzeri D., Esposito E., Mazzon E., Paterniti I., Di Paola R., Bramanti P., Cuzzocrea S. Effect of apocynin, a NADPH oxidase inhibitor, on acute lung inflammation. Biochem. Pharmacol. 2011, 1:636-648.
28. Karin.M., Delhase M. JNK or IKK, AP-1 or NF-kappaB, which are the targets for MEK kinase 1 action?. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:9067-9069.
29. Katz Y., Nadiv O., Beer Y. Interleukin-17 enhances tumor necrosis factor alpha-induced synthesis of interleukin 1, 6, and 8 in skin and synovial fibroblasts: a possible role as a fine tuning cytokine in inflammation processes. Arthritis Rheum. 2001, 44:2176-2184.
30. Ko K., Yamazaki S., Nakamura K., Nishioka T., Hirota K., Yamaguchi T., Shimizu J., Nomura T., Chiba T., Sakaguchi S. Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3CD25CD4 regulatory T cells. J. Exp. Med. 2005, 202:885-891.
31. Kirchberger S., Vetr H., Majdic O., Stockinger H., Stockl J. Engagement of ICAM-1 by major group rhinoviruses activates the LFA-1/ICAM-3 cell adhesion pathway in mononuclear phagocytes. Immunobiology 2006, 211:537-547.
32. Kraus W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol. 2008, 202:294-302.
33. Kane A., Deenick E.K., Ma C.S., Cook M.C., Uzel G., Tangye S.G. STAT3 is a central regulator of lymphocyte differentiation and function. Curr. Opin. Immunol. 2014, 28C:49-57.
34. Lewinsohn D.M., Bargatze R.F., Butcher E.C. Leukocyte-endothelial cell recognition: evidence of a common molecular mechanism shared by neutrophils, lymphocytes, and other leukocytes. J. Immunol. 1987, 138:4313-4321.
35. Levy D.E., Lee C.K. What does STAT-3 do?. J. Clin. Invest. 2002, 109:1143-1148.
36. Lina Q., Jin L., Caob Z., Li H., Xua Y. Protective effect of Acanthopanax senticosus extract against endotoxic shock in mice. J. Ethnopharmacol. 2008, 118:495-502.
37. May C., Williams O., Milner A.D., Peacock J., Rafferty G.F., Hannam S., Greenough A. Relation of exhaled nitric oxide levels to development of bronchopulmonary dysplasia. Arch. Dis. Child Fetal Neonatal Ed. 2009, 94:F205-F209.
38. Moon D.O., Kim M.O., Kang S.H. Sulforaphane suppresses TNF-α-mediated activation of NF-kB and induces apoptosis through activation of reactive oxygen species-dependent caspase-3. Cancer Lett. 2009, 274:132-142.
39. Nishibori M., Takahashi H.K., Mori S. The regulation of ICAM-1 and LFA-1 interaction by autacoids and statins: a novel strategy for controlling inflammation and immune responses. J. Pharmacol. Sci. 2003, 92:7-12.
40. Nocentini G., Riccardi C. GITR: a multifaceted regulator of immunity belonging to the tumor necrosis factor receptor superfamily. Eur. J. Immunol. 2005, 35:1016-1022.
41. Nicolescu A.C., Holt A., Kandasamy A.D., Pacher P., Schulz R. Inhibition of matrix metalloproteinase-2 by PARP inhibitors. Biochem. Biophys. Res. Commun. 2009, 387:646-650.
42. Olabisi O.A., Soto-Nieves N., Nieves E., Yang T.T., Yang X., Yu R.Y., Suk H.Y., Macian F., Chow C.W. Regulation of transcription factor NFAT by ADP-ribosylation. Mol. Cell Biol. 2008, 28(9):2860-2871.
43. Oliveira S.H.P., Canetti C., Ribeiro R.A., Cunha F.Q. Neutrophil migration induced by IL-1β depends upon LTB4 released by macrophages and upon TNF-α and IL-1β released by mast cells. Inflammation 2008, 31:36-46.
44. Pfitzner E., Kliem S., Baus D., Litterst C.M. The role of STATs in inflammation and inflammatory diseases. Curr. Pharm. Des. 2004, 10:2839-2850.
45. Di Paola R., Mazzon E., Muia C., Terrana D., Greco S., Britti D., Santori D., Oteri G., Cordasco G., Cuzzocrea S. 5-Aminoisoquinolin-1(2H)-one, a water-soluble poly (ADP-ribose) polymerase (PARP) inhibitor reduces the evolution of experimental periodontitis in rats. J. Clin. Periodontol. 2007, 34:95-102.
46. Pacher P., Szabo C. Role of poly(ADP-ribose) polymerase-1 (PARP-1) in cardiovascular diseases: the therapeutic potential of PARP inhibitors. Cardiovasc. Drug Rev. 2007, 25:235-260.
47. Paul E.L., Lunardelli A., Caberlon E., Oliveira C.B., Santos R.C.V., Biolchi V., Bastos C.M.A., Moreira K.B., Nunes F.B., Gosmann G., Oliveira J.R. Anti-inflammatory and immunomodulatory effects of Baccharis trimera aqueous extract on induced pleurisy in rats and lymphoproliferation in vitro. Inflammation 2009, 32:419-425.
48. Renner E.D., Rylaarsdam S., Anover-Sombke S., Rack A.L., Reichenbach J., Carey J.C., Zhu Q., Jansson A.F., Barboza J., Schimke L.F. Novel signal transducer and activator of transcription 3 (STAT3) mutations, reduced T(H)17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J. Allergy Clin. Immunol. 2008, 122:181-187.
49. Molecular Cloning. A Laboratory Manual 1989, Cold Spring Harbour Laboratory Press, Plainview, NY. J. Sambrook, E.F. Fritsch, T. Maniatatis, N. Ford (Eds.).
50. Seder R.A., Paul W.E., Davis M.M., Fazekas de St., Groth B. The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4CT cells from T cell receptor transgenic mice. J. Exp. Med. 1992, 176:1091-1098.
51. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995, 155:1151-1164.
52. Shall S., De Murcia G. Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?. Mutat. Res. 2000, 460:1-15.
53. Szabo G., Bahrle S., Stumpf N. Poly(ADP-ribose) polymerase inhibition reduces reperfusion injury after heart transplantation. Circ. Res. 2002, 90:100-106.
54. Szabo C. Poly(ADP-ribose) polymerase activation by reactive nitrogen species-relevance for the pathogenesis of inflammation. Nitric Oxide 2006, 141:69-79.
55. Schymeinsky J., Mócsai A., Walzog B. Neutrophil activation via beta(2) integrins (CD11/CD18): molecular mechanisms and clinical implications. Thromb. Haemost. 2007, 98:262-273.
56. Saenz L., Lozano J.J., Valdor R., Baroja-Mazo A., Ramirez P., Parrilla P., Aparicio P., Sumoy L., Yélamos J. Transcriptional regulation by poly(ADP-ribose) polymerase-1 during T cell activation. BMC Genomics 2008, 16(9):171.
57. Seevaratnam R., Patel B.P., Hamadeh M.J. Comparison of total protein concentration in skeletal muscle as measured by the Bradford and Lowry assays. J. Biochem. 2009, 145:791-797.
58. Sun S.X., Li Y.M., Fang W.R., Cheng P. Effect and mechanism of AR-6 in experimental rheumatoid arthritis. Clin. Exp. Med. 2010, 10(2):113-121.
59. Tamura D.Y., Moore E.E., Johnson J.L., Zallen G., Aiboshi J., Silliman C.C. p38 mitogen-activated protein kinase inhibition attenuates intercellular adhesion molecule-1 up-regulation on human pulmonary microvascular endothelial cells. Surgery 1998, 124:403-407.
60. Virag L., Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 2002, 54:375-429.
61. Zingarelli B., Salzman A.L., Szabo C. Genetic disruption of poly (ADP-ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ. Res. 1998, 83:85-94.
62. Zhou H.Y., Shin E.M., Guo L.Y. Anti-inflammatory activity of 4-methoxyhonokiol is a function of the inhibition of iNOS and COX-2 expression in RAW 264.7 macrophages via NF-kB JNK and p38 MAPK inactivation. Eur. J. Pharmacol. 2008, 586:340-349.