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Molecular fingerprints of neutrophil-dependent oxidative stress in inflammatory bowel disease

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Abstract

Neutrophil accumulation within epithelial crypts and in the intestinal mucosa directly correlates with clinical disease activity and epithelial injury in inflammatory bowel disease (IBD). Current advances have defined the mechanisms by which neutrophils are activated or migrate across endothelial and mucosal epithelial cells. A better understanding of this process will likely provide new insights into novel treatment strategies for IBD. Especially, activated neutrophils produce reactive oxygen and nitrogen species and myeloperoxidase within intestinal mucosa, which induce oxidative stress. Posttranslational modification of proteins generated by these reactive species serves as a “molecular fingerprint” of protein modification by lipid peroxidation-, nitric oxide-, and myeloperoxidase-derived oxidants. Measurement of these modified proteins may serve both as a quantitative index of oxidative stress and an important new biological marker of clinical relevance to IBD. We have succeeded in the clinical development of a novel granulocyte adsorptive apheresis therapy for IBD. In this review, we discuss current advances in defining the role of neutrophil-dependent oxidative stress in IBD.

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References

  1. T Hibi H Ogata (2006) ArticleTitleNovel pathophysiological concepts of inflammatory bowel disease J Gastroenterol 41 10–6 Occurrence Handle16501852 Occurrence Handle10.1007/s00535-005-1744-3

    Article  PubMed  Google Scholar 

  2. N Yoshida T Yamaguchi S Nakagawa Y Nakamura Y Naito T Yoshikawa (2001) ArticleTitleRole of P-selectin and intercellular adhesion molecule-1 in TNB-induced colitis in rats Digestion 1 81–6 Occurrence Handle10.1159/000051916

    Article  Google Scholar 

  3. S Kokura RE Wolf T Yoshikawa DN Granger TY Aw (1999) ArticleTitleMolecular mechanisms of neutrophil-endothelial cell adhesion induced by redox imbalance Circ Res 84 516–24 Occurrence Handle10082473 Occurrence Handle1:CAS:528:DyaK1MXitVSrsr4%3D

    PubMed  CAS  Google Scholar 

  4. TF Tedder DA Steeber A Chen P Engel (1995) ArticleTitleThe selectins: vascular adhesion molecules FASEB J 9 866–73 Occurrence Handle7542213 Occurrence Handle1:CAS:528:DyaK2MXntFyrsLg%3D

    PubMed  CAS  Google Scholar 

  5. S Nakamura H Ohtani Y Watanabe K Fukushima T Matsumoto A Kitano et al. (1993) ArticleTitleIn situ expression of the cell adhesion molecules in inflammatory bowel disease. Evidence of immunologic activation of vascular endothelial cells Lab Invest 69 77–85 Occurrence Handle7687311 Occurrence Handle1:STN:280:DyaK3szitlCmtw%3D%3D

    PubMed  CAS  Google Scholar 

  6. GM Schurmann AE Bishop P Facer M Vecchio JC Lee DS Rampton et al. (1995) ArticleTitleIncreased expression of cell adhesion molecule P-selectin in active inflammatory bowel disease Gut 36 411–8 Occurrence Handle7535284 Occurrence Handle10.1136/gut.36.3.411 Occurrence Handle1:STN:280:DyaK2M3ht12ltA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  7. OH Nielsen E Langholz J Hendel J Brynskov (1994) ArticleTitleCirculating soluble intercellular adhesion molecule-1 (sICAM-1) in active inflammatory bowel disease Dig Dis Sci 39 1918–23 Occurrence Handle7521822 Occurrence Handle10.1007/BF02088125 Occurrence Handle1:CAS:528:DyaK2cXmslOqt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  8. M Goke JC Hoffmann J Evers H Kruger MP Manns (1997) ArticleTitleElevated serum concentrations of soluble selectin and immunoglobulin type adhesion molecules in patients with inflammatory bowel disease J Gastroenterol 32 480–6 Occurrence Handle9250894 Occurrence Handle1:STN:280:DyaK2szpsVGltA%3D%3D

    PubMed  CAS  Google Scholar 

  9. G van Assche P Rutgeerts (2002) ArticleTitleAntiadhesion molecule therapy in inflammatory bowel disease Inflamm Bowel Dis 8 291–300 Occurrence Handle12131614 Occurrence Handle10.1097/00054725-200207000-00009

    Article  PubMed  Google Scholar 

  10. T Taniguchi H Tsukada H Nakamura M Kodama K Fukuda T Saito et al. (1998) ArticleTitleEffects of the anti-ICAM-1 monoclonal antibody on dextran sodium sulphate-induced colitis in rats J Gastroenterol Hepatol 13 945–9 Occurrence Handle9794195 Occurrence Handle1:CAS:528:DyaK1cXntVGrtLc%3D

    PubMed  CAS  Google Scholar 

  11. SJ van Deventer JA Tami MK Wedel (2004) ArticleTitleA randomised, controlled, double blind, escalating dose study of alicaforsen enema in active ulcerative colitis Gut 53 1646–51 Occurrence Handle15479686 Occurrence Handle10.1136/gut.2003.036160 Occurrence Handle1:CAS:528:DC%2BD2cXhtVajtrvJ

    Article  PubMed  CAS  Google Scholar 

  12. PB Miner SuffixJr MK Wedel S Xia BF Baker (2006) ArticleTitleSafety and efficacy of two dose formulations of alicaforsen enema compared with mesalazine enema for treatment of mild to moderate left-sided ulcerative colitis: a randomized, double-blind, active-controlled trial Aliment Pharmacol Ther 23 1403–13 Occurrence Handle16669955 Occurrence Handle10.1111/j.1365-2036.2006.02837.x Occurrence Handle1:CAS:528:DC%2BD28Xms1Olt78%3D

    Article  PubMed  CAS  Google Scholar 

  13. B Yacyshyn WY Chey MK Wedel RZ Yu D Paul E Chuang (2007) ArticleTitleA randomized, double-masked, placebo-controlled study of alicaforsen, an antisense inhibitor of intercellular adhesion molecule 1, for the treatment of subjects with active Crohn's disease Clin Gastroenterol Hepatol 5 215–20 Occurrence Handle17296530 Occurrence Handle10.1016/j.cgh.2006.11.001 Occurrence Handle1:CAS:528:DC%2BD2sXjtlKjsrg%3D

    Article  PubMed  CAS  Google Scholar 

  14. OH Nielsen J Brynskov B Vainer (1996) ArticleTitleIncreased mucosal concentrations of soluble intercellular adhesion molecule-1 (sICAM-1), sE-selectin, and interleukin-8 in active ulcerative colitis Dig Dis Sci 41 1780–5 Occurrence Handle8794794 Occurrence Handle10.1007/BF02088745 Occurrence Handle1:STN:280:DyaK28zoslamuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  15. T Katsuta C Lim K Shimoda K Shibuta P Mitra BF Banner et al. (2000) ArticleTitleInterleukin-8 and SDF1-alpha mRNA expression in colonic biopsies from patients with inflammatory bowel disease Am J Gastroenterol 95 3157–64 Occurrence Handle11095335 Occurrence Handle1:CAS:528:DC%2BD3cXos1ygsL4%3D

    PubMed  CAS  Google Scholar 

  16. Y Umehara M Kudo R Nakaoka T Kawasaki M Shiomi (2006) ArticleTitleSerum proinflammatory cytokines and adhesion molecules in ulcerative colitis Hepatogastroenterology 53 879–82 Occurrence Handle17153445 Occurrence Handle1:CAS:528:DC%2BD28XhtlCisbvP

    PubMed  CAS  Google Scholar 

  17. A Ando A Ogawa S Bamba Y Fujiyama (2007) ArticleTitleInteraction between interleukin-17-producing CD4+ T cells and colonic subepithelial myofibroblasts: what are they doing in mucosal inflammation? J Gastroenterol 42 IssueIDSuppl 17 29–33 Occurrence Handle10.1007/s00535-006-1926-7 Occurrence Handle1:CAS:528:DC%2BD2sXnvVSluw%3D%3D

    Article  CAS  Google Scholar 

  18. S Fujino A Andoh S Bamba A Ogawa K Hata Y Araki et al. (2003) ArticleTitleIncreased expression of interleukin 17 in inflammatory bowel disease Gut 52 65–70 Occurrence Handle12477762 Occurrence Handle10.1136/gut.52.1.65 Occurrence Handle1:CAS:528:DC%2BD3sXmtVyqsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  19. LE Harrington PR Mangan CT Weaver (2006) ArticleTitleExpanding the effector CD4 T-cell repertoire: the Th17 lineage Curr Opin Immunol 18 349–56 Occurrence Handle16616472 Occurrence Handle10.1016/j.coi.2006.03.017 Occurrence Handle1:CAS:528:DC%2BD28XktVGhsbg%3D

    Article  PubMed  CAS  Google Scholar 

  20. H Park Z Li XO Yang SH Chang R Nurieva YH Wang et al. (2005) ArticleTitleA distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17 Nat Immunol 6 1133–41 Occurrence Handle16200068 Occurrence Handle10.1038/ni1261 Occurrence Handle1:CAS:528:DC%2BD2MXhtFamsb%2FO

    Article  PubMed  CAS  Google Scholar 

  21. PR Mangan LE Harrington DB O'Quinn WS Helms DC Bullard CO Elson et al. (2006) ArticleTitleTransforming growth factor-beta induces development of the T(H)17 lineage Nature 441 231–4 Occurrence Handle16648837 Occurrence Handle10.1038/nature04754 Occurrence Handle1:CAS:528:DC%2BD28XksVGns7k%3D

    Article  PubMed  CAS  Google Scholar 

  22. J Witowski K Ksiazek A Jorres (2004) ArticleTitleInterleukin-17: a mediator of inflammatory responses Cell Mol Life Sci 61 567–79 Occurrence Handle15004696 Occurrence Handle10.1007/s00018-003-3228-z Occurrence Handle1:CAS:528:DC%2BD2cXjt1Ors70%3D

    Article  PubMed  CAS  Google Scholar 

  23. S Danese C de la Motte A Sturm JD Vogel GA West SA Strong et al. (2003) ArticleTitlePlatelets trigger a CD40-dependent inflammatory response in the microvasculature of inflammatory bowel disease patients Gastroenterology 124 1249–64 Occurrence Handle12730866 Occurrence Handle10.1016/S0016-5085(03)00289-0 Occurrence Handle1:CAS:528:DC%2BD3sXktVSktrs%3D

    Article  PubMed  CAS  Google Scholar 

  24. O Ludwiczek A Kaser H Tilg (2003) ArticleTitlePlasma levels of soluble CD40 ligand are elevated in inflammatory bowel diseases Int J Colorectal Dis 18 142–7 Occurrence Handle12548417 Occurrence Handle1:STN:280:DC%2BD3s%2FjvF2isg%3D%3D

    PubMed  CAS  Google Scholar 

  25. IE Koutroubakis A Theodoropoulou C Xidakis A Sfiridaki G Notas G Kolios et al. (2004) ArticleTitleAssociation between enhanced soluble CD40 ligand and prothrombotic state in inflammatory bowel disease Eur J Gastroenterol Hepatol 16 1147–52 Occurrence Handle15489574 Occurrence Handle10.1097/00042737-200411000-00011 Occurrence Handle1:CAS:528:DC%2BD2cXos1aqs7k%3D

    Article  PubMed  CAS  Google Scholar 

  26. S Danese C Fiocchi (2005) ArticleTitlePlatelet activation and the CD40/CD40 ligand pathway: mechanisms and implications for human disease Crit Rev Immunol 25 103–21 Occurrence Handle15952932 Occurrence Handle10.1615/CritRevImmunol.v25.i2.20 Occurrence Handle1:CAS:528:DC%2BD2sXktleit7Y%3D

    Article  PubMed  CAS  Google Scholar 

  27. T Vowinkel C Anthoni KC Wood KY Stokes J Russell L Gray et al. (2007) ArticleTitleCD40-CD40 ligand mediates the recruitment of leukocytes and platelets in the inflamed murine colon Gastroenterology 132 955–65 Occurrence Handle17324402 Occurrence Handle10.1053/j.gastro.2006.12.027 Occurrence Handle1:CAS:528:DC%2BD2sXkslCju70%3D

    Article  PubMed  CAS  Google Scholar 

  28. CA Parkos SP Colgan AE Bacarra A Nusrat C Delp-Archer S Carlson et al. (1995) ArticleTitleIntestinal epithelia (T84) possess basolateral ligands for CD11b/CD18-mediated neutrophil adherence Am J Physiol 268 C472–9 Occurrence Handle7532360 Occurrence Handle1:CAS:528:DyaK2MXktFGns7g%3D

    PubMed  CAS  Google Scholar 

  29. KM Blake SO Carrigan AC Issekutz AW Stadnyk (2004) ArticleTitleNeutrophils migrate across intestinal epithelium using beta2 integrin (CD11b/CD18)-independent mechanisms Clin Exp Immunol 136 262–8 Occurrence Handle15086389 Occurrence Handle10.1111/j.1365-2249.2004.02429.x Occurrence Handle1:CAS:528:DC%2BD2cXksVSjsrY%3D

    Article  PubMed  CAS  Google Scholar 

  30. SO Carrigan AL Weppler AC Issekutz AW Stadnyk (2005) ArticleTitleNeutrophil differentiated HL-60 cells model Mac-1 (CD11b/CD18)-independent neutrophil transepithelial migration Immunology 115 108–17 Occurrence Handle15819703 Occurrence Handle10.1111/j.1365-2567.2005.02131.x Occurrence Handle1:CAS:528:DC%2BD2MXjvFaqt7s%3D

    Article  PubMed  CAS  Google Scholar 

  31. I Okayasu S Hatakeyama M Yamada T Ohkusa Y Inagaki R Nakaya (1990) ArticleTitleA novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice Gastroenterology 98 694–702 Occurrence Handle1688816 Occurrence Handle1:STN:280:DyaK3c7ivVSnuw%3D%3D

    PubMed  CAS  Google Scholar 

  32. MA Breider M Eppinger A Gough (1997) ArticleTitleIntercellular adhesion molecule-1 expression in dextran sodium sulfate-induced colitis in rats Vet Pathol 34 598–604 Occurrence Handle9396141 Occurrence Handle1:CAS:528:DyaK2sXnslyrt7o%3D Occurrence Handle10.1177/030098589703400608

    Article  PubMed  CAS  Google Scholar 

  33. B Vainer (2005) ArticleTitleIntercellular adhesion molecule-1 (ICAM-1) in ulcerative colitis: presence, visualization, and significance Inflamm Res 54 313–27 Occurrence Handle16158332 Occurrence Handle10.1007/s00011-005-1363-8 Occurrence Handle1:CAS:528:DC%2BD2MXhtVKnurbI

    Article  PubMed  CAS  Google Scholar 

  34. M Natsui K Kawasaki H Takizawa S Hayashi Y Matsuda K Sugimura et al. (1997) ArticleTitleSelective depletion of neutrophils by a monoclonal antibody, RP-3, suppresses dextran sulphate sodium-induced colitis in rats J Gastroenterol Hepatol 12 801–8 Occurrence Handle9504889 Occurrence Handle1:CAS:528:DyaK1cXhvVyltbc%3D

    PubMed  CAS  Google Scholar 

  35. Y Naito T Takagi O Handa T Ishikawa N Matsumoto N Yagi et al. (2001) ArticleTitleRole of superoxide and lipid peroxidation in the pathogenesis of dextran sulfate sodium-colitis in mice ITE Lett 2 663–7 Occurrence Handle1:CAS:528:DC%2BD38XhsVegtA%3D%3D

    CAS  Google Scholar 

  36. Y Morohoshi K Matsuoka H Chinen N Kamada T Sato T Hisamatsu et al. (2006) ArticleTitleInhibition of neutrophil elastase prevents the development of murine dextran sulfate sodium-induced colitis J Gastroenterol 41 318–24 Occurrence Handle16741610 Occurrence Handle10.1007/s00535-005-1768-8 Occurrence Handle1:CAS:528:DC%2BD28Xlt1Kqtr8%3D

    Article  PubMed  CAS  Google Scholar 

  37. MB Grisham LA Hernandez DN Granger (1986) ArticleTitleXanthine oxidase and neutrophil infiltration in intestinal ischemia Am J Physiol 252 G567–74

    Google Scholar 

  38. H Hanai K Takeuchi T Iida N Kashiwagi AR Saniabadi I Matsushita et al. (2004) ArticleTitleRelationship between fecal calprotectin, intestinal inflammation, and peripheral blood neutrophils in patients with active ulcerative colitis Dig Dis Sci 49 1438–43 Occurrence Handle15481316 Occurrence Handle10.1023/B:DDAS.0000042243.47279.87

    Article  PubMed  Google Scholar 

  39. DA McCarthy DS Rampton YC Liu (1991) ArticleTitlePeripheral blood neutrophils in inflammatory bowel disease: morphological evidence of in vivo activation in active disease Clin Exp Immunol 86 489–93 Occurrence Handle1684141 Occurrence Handle1:STN:280:DyaK38%2FotlKmug%3D%3D Occurrence Handle10.1111/j.1365-2249.1991.tb02958.x

    Article  PubMed  CAS  Google Scholar 

  40. A D'Odorico R D'Inca C Mestriner V Di Leo A Ferronato GC Sturniolo (2000) ArticleTitleInfluence of disease site and activity on peripheral neutrophil function in inflammatory bowel disease Dig Dis Sci 45 1594–600 Occurrence Handle11007111 Occurrence Handle10.1023/A:1005521212948

    Article  PubMed  Google Scholar 

  41. K Anezaki H Asakura T Honma K Ishizuka K Funakoshi Y Tsukada et al. (1998) ArticleTitleCorrelations between interleukin-8, and myeloperoxidase or luminol-dependent chemiluminescence in inflamed mucosa of ulcerative colitis Intern Med 37 253–8 Occurrence Handle9617859 Occurrence Handle1:STN:280:DyaK1c3nvVChsw%3D%3D

    PubMed  CAS  Google Scholar 

  42. L Mazzucchelli C Hauser K Zgraggen H Wagner M Hess JA Laissue et al. (1994) ArticleTitleExpression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation Am J Pathol 144 997–1007 Occurrence Handle8178948 Occurrence Handle1:STN:280:DyaK2c3jsVaqsg%3D%3D

    PubMed  CAS  Google Scholar 

  43. KL Isaacs RB Sartor S Haskill (1992) ArticleTitleCytokine messenger RNA profiles in inflammatory bowel disease mucosa detected by polymerase chain reaction amplification Gastroenterology 103 1587–95 Occurrence Handle1426879 Occurrence Handle1:CAS:528:DyaK38XmsVKhsLc%3D

    PubMed  CAS  Google Scholar 

  44. M Carlson Y Raab L Seveus S Xu R Hallgren P Venge (2002) ArticleTitleHuman neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis Gut 50 501–6 Occurrence Handle11889070 Occurrence Handle10.1136/gut.50.4.501 Occurrence Handle1:CAS:528:DC%2BD38XislOqsLg%3D

    Article  PubMed  CAS  Google Scholar 

  45. T Yoshikawa Y Naito (2002) ArticleTitleWhat is oxidative stress? Jpn Med Assoc J 45 271–6

    Google Scholar 

  46. Y Naito H Takano T Yoshikawa (2005) ArticleTitleOxidative stress-related molecules as a therapeutic target for inflammatory and allergic diseases Curr Drug Targets Inflamm Allergy 4 511–5 Occurrence Handle16101531 Occurrence Handle10.2174/1568010054526269 Occurrence Handle1:CAS:528:DC%2BD2MXmvV2iu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  47. T Yoshikawa T Yamaguchi N Yoshida H Yamamoto S Kitazumi S Takahashi et al. (1997) ArticleTitleEffect of Z-103 on TNB-induced colitis in rats Digestion 58 464–8 Occurrence Handle9383638 Occurrence Handle1:CAS:528:DyaK2sXmvFOitL0%3D Occurrence Handle10.1159/000201484

    Article  PubMed  CAS  Google Scholar 

  48. Y Naito T Takagi K Matsuyama N Yagi N Yoshida H Murase et al. (2002) ArticleTitleEffect of a novel water-soluble vitamin E derivative, 2-(a-D-glucopyranoyl)methyl-2,5,7,8-tetramethylchroman-6-ol, on dextran sulfate sodium-induced colitis in mice J Clin Biochem Nutr 31 59–67 Occurrence Handle1:CAS:528:DC%2BD3sXjt1ejsr4%3D

    CAS  Google Scholar 

  49. G Leonarduzzi F Robbesyn G Poli (2004) ArticleTitleSignaling kinases modulated by 4-hydroxynonenal Free Radic Biol Med 37 1694–702 Occurrence Handle15528028 Occurrence Handle10.1016/j.freeradbiomed.2004.08.027 Occurrence Handle1:CAS:528:DC%2BD2cXpsFWku7c%3D

    Article  PubMed  CAS  Google Scholar 

  50. K Uchida (2005) ArticleTitleProtein-bound 4-hydroxy-2-nonenal as a marker of oxidative stress J Clin Biochem Nutr 36 1–10 Occurrence Handle10.3164/jcbn.36.1 Occurrence Handle1:CAS:528:DC%2BD2MXjvF2ls7k%3D

    Article  CAS  Google Scholar 

  51. S Dwivedi A Sharma B Patrick R Sharma YC Awasthi (2007) ArticleTitleRole of 4-hydroxynonenal and its metabolites in signaling Redox Rep 12 4–10 Occurrence Handle17263900 Occurrence Handle10.1179/135100007X162211 Occurrence Handle1:CAS:528:DC%2BD2sXhs1antLw%3D

    Article  PubMed  CAS  Google Scholar 

  52. H Bartsch J Nair (2005) ArticleTitleAccumulation of lipid peroxidation-derived DNA lesions: potential lead markers for chemoprevention of inflammation-driven malignancies Mutat Res 591 34–44 Occurrence Handle16099477 Occurrence Handle1:CAS:528:DC%2BD2MXht1Gnu7zF

    PubMed  CAS  Google Scholar 

  53. J Nair F Gansauge H Beger P Dolara G Winde H Bartsch (2006) ArticleTitleIncreased etheno-DNA adducts in affected tissues of patients suffering from Crohn's disease, ulcerative colitis, and chronic pancreatitis Antioxid Redox Signal 8 1003–10 Occurrence Handle16771690 Occurrence Handle10.1089/ars.2006.8.1003 Occurrence Handle1:CAS:528:DC%2BD28XlsFOntbo%3D

    Article  PubMed  CAS  Google Scholar 

  54. H Kimura M Mukaida K Kuwabara T Ito K Hashino K Uchida et al. (2006) ArticleTitle4-Hydroxynonenal modifies IgA in rat intestine after lipopolysaccharide injection Free Radic Biol Med 41 973–8 Occurrence Handle16934680 Occurrence Handle10.1016/j.freeradbiomed.2006.06.005 Occurrence Handle1:CAS:528:DC%2BD28XovVWqsbs%3D

    Article  PubMed  CAS  Google Scholar 

  55. F Biasi B Vizio C Mascia E Gaia N Zarkovic E Chiarpotto et al. (2006) ArticleTitlec-Jun N-terminal kinase upregulation as a key event in the proapoptotic interaction between transforming growth factor-beta1 and 4-hydroxynonenal in colon mucosa Free Radic Biol Med 41 443–54 Occurrence Handle16843825 Occurrence Handle10.1016/j.freeradbiomed.2006.04.005 Occurrence Handle1:CAS:528:DC%2BD28XntFWru7g%3D

    Article  PubMed  CAS  Google Scholar 

  56. CC Winterbourn AJ Kettle (2000) ArticleTitleBiomarkers of myeloperoxidase-derived hypochlorous acid Free Radic Biol Med 29 403–9 Occurrence Handle11020661 Occurrence Handle10.1016/S0891-5849(00)00204-5 Occurrence Handle1:CAS:528:DC%2BD3cXntVWgsLo%3D

    Article  PubMed  CAS  Google Scholar 

  57. JS Gujral JA Hinson H Jaeschke (2004) ArticleTitleChlorotyrosine protein adducts are reliable biomarkers of neutrophil-induced cytotoxicity in vivo Comp Hepatol 3 IssueIDSuppl 1 S48 Occurrence Handle14960200 Occurrence Handle10.1186/1476-5926-2-S1-S48

    Article  PubMed  Google Scholar 

  58. JK Ryu KC Tran JG McLarnon (2007) ArticleTitleDepletion of neutrophils reduces neuronal degeneration and inflammatory responses induced by quinolinic acid in vivo Glia 55 439–51 Occurrence Handle17203474 Occurrence Handle10.1002/glia.20479

    Article  PubMed  Google Scholar 

  59. B Shao MN Oda C Bergt X Fu PS Green N Brot et al. (2006) ArticleTitleMyeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I J Biol Chem 281 9001–4 Occurrence Handle16497665 Occurrence Handle10.1074/jbc.C600011200 Occurrence Handle1:CAS:528:DC%2BD28XjtVSktrY%3D

    Article  PubMed  CAS  Google Scholar 

  60. AJ Kettle T Chan I Osberg R Senthilmohan AL Chapman TJ Mocatta et al. (2004) ArticleTitleMyeloperoxidase and protein oxidation in the airways of young children with cystic fibrosis Am J Respir Crit Care Med 170 1317–23 Occurrence Handle15466253 Occurrence Handle10.1164/rccm.200311-1516OC

    Article  PubMed  Google Scholar 

  61. Y Naito T Takagi T Ishikawa O Handa N Matsumoto N Yagi et al. (2001) ArticleTitleThe inducible nitric oxide synthase inhibitor ONO-1714 blunts dextran sulfate sodium colitis in mice Eur J Pharmacol 412 91–9 Occurrence Handle11166740 Occurrence Handle10.1016/S0014-2999(00)00926-2 Occurrence Handle1:CAS:528:DC%2BD3MXptFSgtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  62. E Mazzon C Muia RD Paola T Genovese M Menegazzi A De Sarro et al. (2005) ArticleTitleGreen tea polyphenol extract attenuates colon injury induced by experimental colitis Free Radic Res 39 1017–25 Occurrence Handle16087483 Occurrence Handle10.1080/10715760500197177 Occurrence Handle1:CAS:528:DC%2BD2MXpslyrt70%3D

    Article  PubMed  CAS  Google Scholar 

  63. S Cuzzocrea E Mazzon L Dugo AP Caputi DP Riley D Salvemini (2001) ArticleTitleProtective effects of M40403, a superoxide dismutase mimetic, in a rodent model of colitis Eur J Pharmacol 432 79–89 Occurrence Handle11734191 Occurrence Handle10.1016/S0014-2999(01)01427-3 Occurrence Handle1:CAS:528:DC%2BD3MXovVCgsbo%3D

    Article  PubMed  CAS  Google Scholar 

  64. I Singer DW Kawka S Scott JR Weidner RA Mumford TE Riehl et al. (1996) ArticleTitleExpression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease Gastroenterology 111 871–85 Occurrence Handle8831582 Occurrence Handle10.1016/S0016-5085(96)70055-0 Occurrence Handle1:STN:280:DyaK28vivVCkuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  65. L Kruidenier I Kuiper CB Lamers HW Verspaget (2003) ArticleTitleIntestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants J Pathol 201 28–36 Occurrence Handle12950014 Occurrence Handle10.1002/path.1409 Occurrence Handle1:CAS:528:DC%2BD3sXotFyqs7g%3D

    Article  PubMed  CAS  Google Scholar 

  66. A Keshavarzian A Banan A Farhadi S Komanduri E Mutlu Y Zhang et al. (2003) ArticleTitleIncreases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease Gut 52 720–8 Occurrence Handle12692059 Occurrence Handle10.1136/gut.52.5.720 Occurrence Handle1:CAS:528:DC%2BD3sXjvVeiu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  67. M Schmid K Fellermann P Fritz O Wiedow EF Stange J Wehkamp (2007) ArticleTitleAttenuated induction of epithelial and leukocyte serine antiproteases elafin and secretory leukocyte protease inhibitor in Crohn's disease J Leukoc Biol 81 907–15 Occurrence Handle17200145 Occurrence Handle10.1189/jlb.0906581 Occurrence Handle1:CAS:528:DC%2BD2sXkt1Oitro%3D

    Article  PubMed  CAS  Google Scholar 

  68. RE Young RD Thompson KY Larbi M La CE Roberts SD Shapiro et al. (2004) ArticleTitleNeutrophil elastase (NE)-deficient mice demonstrate a nonredundant role for NE in neutrophil migration, generation of proinflammatory mediators, and phagocytosis in response to zymosan particles in vivo J Immunol 172 4493–502 Occurrence Handle15034066 Occurrence Handle1:CAS:528:DC%2BD2cXitlOqtLs%3D

    PubMed  CAS  Google Scholar 

  69. AW Stadnyk CD Dollard AC Issekutz (2000) ArticleTitleNeutrophil migration stimulates rat intestinal epithelial cell cytokine expression during helminth infection J Leukoc Biol 68 821–7 Occurrence Handle11129649 Occurrence Handle1:CAS:528:DC%2BD3cXptVKns7Y%3D

    PubMed  CAS  Google Scholar 

  70. G Le'Negrate E Selva P Auberger B Rossi P Hofman (2000) ArticleTitleSustained polymorphonuclear leukocyte transmigration induces apoptosis in T84 intestinal epithelial cells J Cell Biol 150 1479–88 Occurrence Handle10995451 Occurrence Handle10.1083/jcb.150.6.1479

    Article  PubMed  Google Scholar 

  71. JL Madara C Parkos S Colgan RJ MacLeod S Nash J Matthews et al. (1992) ArticleTitleCl-secretion in a model intestinal epithelium induced by a neutrophil-derived secretagogue J Clin Invest 89 1938–44 Occurrence Handle1602001 Occurrence Handle1:CAS:528:DyaK38XksVGrsbw%3D Occurrence Handle10.1172/JCI115800

    Article  PubMed  CAS  Google Scholar 

  72. AR Saniabadi H Hanai K Takeuchi K Umemura M Nakashima T Adachi et al. (2003) ArticleTitleAdacolumn, an adsorptive carrier based granulocyte and monocyte apheresis device for the treatment of inflammatory and refractory diseases associated with leukocytes Ther Apher Dial 7 48–59 Occurrence Handle12921115 Occurrence Handle10.1046/j.1526-0968.2003.00012.x

    Article  PubMed  Google Scholar 

  73. T Kanai T Hibi M Watanabe (2006) ArticleTitleThe logics of leukocytapheresis as a natural biological therapy for inflammatory bowel disease Expert Opin Biol Ther 6 453–66 Occurrence Handle16610976 Occurrence Handle10.1517/14712598.6.5.453 Occurrence Handle1:CAS:528:DC%2BD28Xkt12gs7s%3D

    Article  PubMed  CAS  Google Scholar 

  74. H Hanai T Iida M Yamada Y Sato K Takeuchi T Tanaka et al. (2006) ArticleTitleEffects of Adacolumn selective leukocytapheresis on plasma cytokines during active disease in patients with active ulcerative colitis World J Gastroenterol 12 3393–9 Occurrence Handle16733857 Occurrence Handle1:CAS:528:DC%2BD28XnsFWktb8%3D

    PubMed  CAS  Google Scholar 

  75. H Hanai F Watanabe M Yamada Y Sato K Takeuchi T Iida et al. (2004) ArticleTitleCorrelation of serum soluble TNF-alpha receptors I and II levels with disease activity in patients with ulcerative colitis Am J Gastroenterol 99 1532–8 Occurrence Handle15307873 Occurrence Handle10.1111/j.1572-0241.2004.30432.x Occurrence Handle1:CAS:528:DC%2BD2cXotVKjur8%3D

    Article  PubMed  CAS  Google Scholar 

  76. Y Takeda N Shiobara AR Saniabadi M Adachi K Hiraishi (2004) ArticleTitleAdhesion dependent release of hepatocyte growth factor and interleukin-1 receptor antagonist from human blood granulocytes and monocytes: evidence for the involvement of plasma IgG, complement C3 and beta2 integrin Inflamm Res 53 277–83 Occurrence Handle15241561 Occurrence Handle10.1007/s00011-004-1253-5 Occurrence Handle1:CAS:528:DC%2BD2cXms1eiu7o%3D

    Article  PubMed  CAS  Google Scholar 

  77. K Hiraishi Y Takeda N Shiobara H Shibusawa F Jimma N Kashiwagi et al. (2003) ArticleTitleStudies on the mechanisms of leukocyte adhesion to cellulose acetate beads: an in vitro model to assess the efficacy of cellulose acetate carrier-based granulocyte and monocyte adsorptive apheresis Ther Apher Dial 7 334–40 Occurrence Handle12924609 Occurrence Handle10.1046/j.1526-0968.2003.00049.x

    Article  PubMed  Google Scholar 

  78. N Kashiwagi K Sugimura H Koiwai H Yamamoto T Yoshikawa AR Saniabadi et al. (2002) ArticleTitleImmunomodulatory effects of granulocyte and monocyte adsorption apheresis as a treatment for patients with ulcerative colitis Dig Dis Sci 47 1334–41 Occurrence Handle12064810 Occurrence Handle10.1023/A:1015330816364 Occurrence Handle1:CAS:528:DC%2BD38XltFakurw%3D

    Article  PubMed  CAS  Google Scholar 

  79. T Shimoyama K Sawada N Hiwatashi T Sawada K Matsueda A Munakata et al. (2001) ArticleTitleSafety and efficacy of granulocyte and monocyte adsorption apheresis in patients with active ulcerative colitis: a multicenter study J Clin Apher 16 1–9 Occurrence Handle11309823 Occurrence Handle10.1002/jca.1000 Occurrence Handle1:STN:280:DC%2BD3M3hvFaitg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  80. H Hanai F Watanabe K Takeuchi T Iida M Yamada Y Iwaoka et al. (2003) ArticleTitleLeukocyte adsorptive apheresis for the treatment of active ulcerative colitis: a prospective, uncontrolled, pilot study Clin Gastroenterol Hepatol 1 28–35 Occurrence Handle15017514 Occurrence Handle10.1053/jcgh.2003.50005

    Article  PubMed  Google Scholar 

  81. Y Suzuki N Yoshimura AR Saniabadi Y Saito (2004) ArticleTitleSelective granulocyte and monocyte adsorptive apheresis as a first-line treatment for steroid naive patients with active ulcerative colitis: a prospective uncontrolled study Dig Dis Sci 49 565–71 Occurrence Handle15185858 Occurrence Handle10.1023/B:DDAS.0000026299.43792.ae Occurrence Handle1:CAS:528:DC%2BD2cXjs1WqurY%3D

    Article  PubMed  CAS  Google Scholar 

  82. Y Fukuda T Matsui Y Suzuki K Kanke T Matsumoto M Takazoe et al. (2004) ArticleTitleAdsorptive granulocyte and monocyte apheresis for refractory Crohn's disease: an open multicenter prospective study J Gastroenterol 39 1158–64 Occurrence Handle15622479 Occurrence Handle10.1007/s00535-004-1465-z

    Article  PubMed  Google Scholar 

  83. T Ljung OO Thomsen M Vatn P Karlen LN Karlsen C Tysk et al. (2007) ArticleTitleGranulocyte, monocyte/macrophage apheresis for inflammatory bowel disease: the first 100 patients treated in Scandinavia Scand J Gastroenterol 42 221–7 Occurrence Handle17327942 Occurrence Handle10.1080/00365520600979369

    Article  PubMed  Google Scholar 

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Naito, Y., Takagi, T. & Yoshikawa, T. Molecular fingerprints of neutrophil-dependent oxidative stress in inflammatory bowel disease. J Gastroenterol 42, 787–798 (2007). https://doi.org/10.1007/s00535-007-2096-y

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