The role of polymorphonuclear leukocyte trafficking in the perpetuation of inflammation during inflammatory bowel disease

Inflammatory Bowel Diseases

Volumn 19, Issue 7, 2013, Pages 1556-1565

  Brazil, Jennifer C ^a   Louis, Nancy A ^a   Parkos, Charles A ^b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

IBD; Intestinal inflammation; PMN trafficking

Indexed keywords

CELL TRANSPORT; ENTERITIS; HUMAN; INFLAMMATION; INTESTINE CRYPT; INTESTINE MUCOSA; MEDIATOR RELEASE; NEUTROPHIL; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SYMPTOMATOLOGY;

ANIMALS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; NEUTROPHILS; PROGNOSIS;

EID: 84879068635     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e318281f54e     Document Type: Review

References (101)

1. Shanahan F. Crohn's disease. Lancet. 2002;359:62-69.
2. Farrell RJ, Peppercorn MA. Ulcerative colitis. Lancet. 2002;359:331-340.
3. Hanauer SB. 2006. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis. 12(suppl 1):S3-S9.
4. Neurath MF, Finotto S. The many roads to inflammatory bowel diseases. Immunity. 2006;25:189-191.
5. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-429.
6. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117:514-521.
7. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-434.
8. Saverymuttu SH, Peters AM, Lavender JP, et al. In vivo assessment of granulocyte migration to diseased bowel in Crohn's disease. Gut. 1985;26:378-383.
9. Saverymuttu SH, Peters AM, Crofton ME, et al. 111Indium autologous granulocytes in the detection of inflammatory bowel disease. Gut. 1985;26:955-960.
10. Saverymuttu SH, Chadwick VS, Hodgson HJ. Granulocyte migration in ulcerative colitis. Eur J Clin Invest. 1985;15:60-63.
11. Scholmerich J, Schmidt E, Schumichen C, et al. Scintigraphic assessment of bowel involvement and disease activity in Crohn's disease using technetium 99m-hexamethyl propylene amine oxine as leukocyte label. Gastroenterology. 1988;95:1287-1293.
12. Kucharzik T, Walsh SV, Chen J, et al. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol. 2001;159:2001-2009.
13. Zelensky AN, Gready JE. The C-type lectin-like domain superfamily. FEBS J. 2005;272:6179-6217.
14. Sperandio M. Selectins and glycosyltransferases in leukocyte rolling in vivo. FEBS J. 2006;273:4377-4389.
15. Vestweber D, Blanks JE. Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev. 1999;79:181-213.
16. McEver RP, Cummings RD. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest. 1997;100:S97-S103.
17. Smith ML, Olson TS, Ley K. CXCR2-and E-selectin-induced neutrophil arrest during inflammation in vivo. J Exp Med. 2004;200:935-939.
18. Rot A, Von Andrian UH. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol. 2004;22:891-928.
19. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol. 2010;11:366-378.
20. Ibbotson GC, Doig C, Kaur J, et al. Functional alpha4-integrin: a newly identified pathway of neutrophil recruitment in critically ill septic patients. Nat Med. 2001;7:465-470.
21. Phillipson M, Heit B, Colarusso P, et al. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J Exp Med. 2006;203:2569-2575.
22. Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol. 2004;167:377-388.
23. Wang S, Voisin MB, Larbi KY, et al. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med. 2006;203:1519-1532.
24. Sumagin R, Sarelius IH. Intercellular adhesion molecule-1 enrichment near tricellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J Immunol. 2010;184:5242-5252.
25. Hyun YM, Sumagin R, Sarangi PP, et al. Uropod elongation is a common final step in leukocyte extravasation through inflamed vessels. J Exp Med. 2012;209:1349-1362.
26. Arndt H, Palitzsch KD, Grisham MB, et al. Metronidazole inhibits leukocyte-endothelial cell adhesion in rat mesenteric venules. Gastroenterology. 1994;106:1271-1276.
27. Bernstein LH, Frank MS, Brandt LJ, et al. Healing of perineal Crohn's disease with metronidazole. Gastroenterology. 1980;79:357-365.
28. Jakobovits J, Schuster MM. Metronidazole therapy for Crohn's disease and associated fistulae. Am J Gastroenterol. 1984;79:533-540.
29. Glover JM, Leeds JM, Mant TG, et al. 1997. Phase I safety and pharmacokinetic profile of an intercellular adhesion molecule-1 antisense oligodeoxynucleotide (ISIS 2302). J Pharmacol Exp Ther. 282:1173-1180.
30. Yacyshyn BR, Chey WY, Goff J, et al. Double blind, placebo controlled trial of the remission inducing and steroid sparing properties of an ICAM-1 antisense oligodeoxynucleotide, alicaforsen (ISIS 2302), in active steroid dependent Crohn's disease. Gut. 2002;51:30-36.
31. Thomas S, Baumgart DC. Targeting leukocyte migration and adhesion in Crohn's disease and ulcerative colitis. Inflammopharmacology. 2012;20:1-18.
32. Targan SR, Feagan BG, Fedorak RN, et al. 2007. Natalizumab for the treatment of active Crohn's disease: results of the ENCORE Trial. Gastroenterology. 132:1672-1683.
33. Parkos CA, Delp C, Arnaout MA, et al. Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J Clin Invest. 1991;88:1605-1612.
34. Blake KM, Carrigan SO, Issekutz AC, et al. Neutrophils migrate across intestinal epithelium using beta2 integrin (CD11b/CD18)-independent mechanisms. Clin Exp Immunol. 2004;136:262-268.
35. Zen K, Liu Y, Cairo D, et al. CD11b/CD18-dependent interactions of neutrophils with intestinal epithelium are mediated by fucosylated proteoglycans. J Immunol. 2002;169:5270-5278.
36. Parkos CA, Colgan SP, Liang TW, et al. CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J Cell Biol. 1996;132:437-450.
37. Liu Y, Merlin D, Burst SL, et al. The role of CD47 in neutrophil transmigration. Increased rate of migration correlates with increased cell surface expression of CD47. J Biol Chem. 2001;276:40156-40166.
38. Zen K, Liu Y, McCall IC, et al. Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol Biol Cell. 2005;16:2694-2703.
39. Lawrence DW, Bruyninckx WJ, Louis NA, et al. Antiadhesive role of apical decay-accelerating factor (CD55) in human neutrophil transmigration across mucosal epithelia. J Exp Med. 2003;198:999-1010.
40. Campbell EL, Louis NA, Tomassetti SE, et al. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J. 2007;21:3162-3170.
41. Brazil JC, Lee WY, Kolegraff KN, et al. Neutrophil migration across intestinal epithelium: evidence for a role of CD44 in regulating detachment of migrating cells from the luminal surface. J Immunol. 2010;185:7026-7036.
42. Wittig B, Seiter S, Schmidt DS, et al. CD44 variant isoforms on blood leukocytes in chronic inflammatory bowel disease and other systemic autoimmune diseases. Lab Invest. 1999;79:747-759.
43. Nusrat A, Parkos CA, Liang TW, et al. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology. 1997;113:1489-1500.
44. Nash S, Stafford J, Madara JL. Effects of polymorphonuclear leukocyte transmigration on the barrier function of cultured intestinal epithelial monolayers. J Clin Invest. 1987;80:1104-1113.
45. Grisham MB. Oxidants and free radicals in inflammatory bowel disease. Lancet. 1994;344:859-861.
46. Halliwell B, Gutteridge JM. The definition and measurement of antioxidants in biological systems. Free Radic Biol Med. 1995;18:125-126.
47. Pavlick KP, Laroux FS, Fuseler J, et al. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic Biol Med. 2002;33:311-322.
48. Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol. 2007;5:577-582.
49. Yipp BG, Petri B, Salina D, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med. 2012;18:1386-1393.
50. Naito Y, Takagi T, Yoshikawa T. Neutrophil-dependent oxidative stress in ulcerative colitis. J Clin Biochem Nutr. 2007;41:18-26.
51. Pravda J. Radical induction theory of ulcerative colitis. World J Gastroenterol. 2005;11:2371-2384.
52. Kruidenier L, Kuiper I, Lamers CB, et al. Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol. 2003;201:28-36.
53. Shiratora Y, Aoki S, Takada H, et al. Oxygen-derived free radical generating capacity of polymorphonuclear cells in patients with ulcerative colitis. Digestion. 1989;44:163-171.
54. *-production in neutrophils of Crohn's disease patients. Exp Biol Med. 2006;231:186-195.
55. Hayee B, Rahman FZ, Tempero J, et al. The neutrophil respiratory burst and bacterial digestion in Crohn's disease. Dig Dis Sci. 2011;56:1482-1488.
56. Simmonds NJ, Allen RE, Stevens TR, et al. Chemiluminescence assay of mucosal reactive oxygen metabolites in inflammatory bowel disease. Gastroenterology 1992;103:186-196.
57. Oshitani N, Kitano A, Okabe H, et al. Location of superoxide anion generation in human colonic mucosa obtained by biopsy. Gut. 1993;34:936-938.
58. Ahnfelt-Ronne I, Nielsen OH, Christensen A, et al. Clinical evidence supporting the radical scavenger mechanism of 5-aminosalicylic acid. Gastroenterology. 1990;98:1162-1169.
59. D'Inca R, Cardin R, Benazzato L, et al. Oxidative DNA damage in the mucosa of ulcerative colitis increases with disease duration and dysplasia. Inflamm Bowel Dis. 2004;10:23-27.
60. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med. 1989;320:365-376.
61. Gaginella TS, Kachur JF, Tamai H, et al. Reactive oxygen and nitrogen metabolites as mediators of secretory diarrhea. Gastroenterology. 1995;109:2019-2028.
62. Weitzman SA, Gordon LI. Inflammation and cancer: role of phagocytegenerated oxidants in carcinogenesis. Blood. 1990;76:655-663.
63. Oz HS, Chen TS, McClain CJ, et al. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 2005;16:297-304.
64. Araki Y, Sugihara H, Hattori T. The free radical scavengers edaravone and tempol suppress experimental dextran sulfate sodium-induced colitis in mice. Int J Mol Med. 2006;17:331-334.
65. Segui J, Gironella M, Sans M, et al. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. J Leukoc Biol. 2004;76:537-544.
66. Kruidenier L, Van Meeteren ME, Kuiper I, et al. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic Biol Med. 2003;34:753-765.
67. Oku T, Iyama S, Sato T, et al. Amelioration of murine dextran sulfate sodium-induced colitis by ex vivo extracellular superoxide dismutase gene transfer. Inflamm Bowel Dis. 2006;12:630-640.
68. Watterlot L, Rochat T, Sokol H, et al. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int J Food Microbiol. 2010;144:35-41.
69. Anderson ME, Naganuma A, Meister A. Protection against cisplatin toxicity by administration of glutathione ester. FASEB J. 1990;4:3251-3255.
70. Esworthy RS, Aranda R, Martin MG, et al. Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G848-G855.
71. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol. 2012;5:354-366.
72. Sylvia CJ. The role of neutrophil apoptosis in influencing tissue repair. J Wound Care. 2003;12:13-16.
73. Stevens C, Walz G, Singaram C, et al. Tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-6 expression in inflammatory bowel disease. Dig Dis Sci. 1992;37:818-826.
74. Cassatella MA. Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol. 1999;73:369-509.
75. Mantovani A, Cassatella MA, Costantini C, et al. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11:519-531.
76. Oppenheim J. J., Zachariae C. O., Mukaida N., et al. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617-648.
77. Mazzucchelli L, Hauser C, Zgraggen K, et al. Expression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation. Am J Pathol. 1994;144:997-1007.
78. Kasama T, Strieter RM, Standiford TJ, et al. Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1 alpha. J Exp Med. 1993;178:63-72.
79. Mantovani A. The interplay between primary and secondary cytokines. Cytokines involved in the regulation of monocyte recruitment. Drugs. 1997;54(Suppl 1):15-23.
80. Beil WJ, Weller PF, Peppercorn MA, et al. Ultrastructural immunogold localization of subcellular sites of TNF-alpha in colonic Crohn's disease. J Leukoc Biol. 1995;58:284-298.
81. Tracey KJ, Cerami A. Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu Rev Med. 1994;45:491-503.
82. Chertov O, Yang D, Howard OM, et al. Leukocyte granule proteins mobilize innate host defenses and adaptive immune responses. Immunol Rev. 2000;177:68-78.
83. Yamaguchi N, Isomoto H, Mukae H, et al. Concentrations of alpha-and beta-defensins in plasma of patients with inflammatory bowel disease. Inflamm Res. 2009;58:192-197.
84. Cunliffe RN, Kamal M, Rose FR, et al. Expression of antimicrobial neutrophil defensins in epithelial cells of active inflammatory bowel disease mucosa. J Clin Pathol. 2002;55:298-304.
85. Yang D, Chen Q, Chertov O, et al. Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J Leukoc Biol. 2000;68:9-14.
86. Grigat J, Soruri A, Forssmann U, et al. Chemoattraction of macrophages, T lymphocytes, and mast cells is evolutionarily conserved within the human alpha-defensin family. J Immunol. 2007;179:3958-3965.
87. Van Wetering S, Mannesse-Lazeroms SP, Van Sterkenburg MA, et al. Effect of defensins on interleukin-8 synthesis in airway epithelial cells. Am J Physiol. 1997;272:L888-L896.
88. Yui S, Nakatani Y, Mikami M. Calprotectin (S100A8/S100A9), an inflammatory protein complex from neutrophils with a broad apoptosisinducing activity. Biol Pharm Bull. 2003;26:753-760.
89. Cornish CJ, Devery JM, Poronnik P, et al. S100 protein CP-10 stimulates myeloid cell chemotaxis without activation. J Cell Physiol. 1996;166:427-437.
90. Lackmann M, Cornish CJ, Simpson RJ, et al. Purification and structural analysis of a murine chemotactic cytokine (CP-10) with sequence homology to S100 proteins. J Biol Chem. 1992;267:7499-7504.
91. Newton RA, Hogg N. The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. J Immunol. 1998;160:1427-1435.
92. Ginzberg HH, Cherapanov V, Dong Q, et al. Neutrophil-mediated epithelial injury during transmigration: role of elastase. Am J Physiol Gastrointest Liver Physiol. 2001;281:G705-G717.
93. Saitoh O, Sugi K, Matsuse R, et al. The forms and the levels of fecal PMN-elastase in patients with colorectal diseases. Am J Gastroenterol. 1995;90:388-393.
94. Zemans RL, Briones N, Campbell M, et al. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc Natl Acad Sci U S A. 2011;108:15990-15995.
95. Adeyemi EO, Hodgson HJ. Faecal elastase reflects disease activity in active ulcerative colitis. Scand J Gastroenterol. 1992;27:139-142.
96. Nagao Y, Miyata H, Mizuguchi K, et al. [Effects of ulinastatin on experimental ulcerative colitis in rats]. Nihon Yakurigaku Zasshi. 1997;109:41-52.
97. Rasmussen PB, Bjorn S, Hastrup S, et al. Characterization of recombinant human HBP/CAP37/azurocidin, a pleiotropic mediator of inflammation-enhancing LPS-induced cytokine release from monocytes. FEBS Lett. 1996;390:109-112.
98. Tschesche H, Zolzer V, Triebel S, et al. The human neutrophil lipocalin supports the allosteric activation of matrix metalloproteinases. Eur J Biochem. 2001;268:1918-1928.
99. Ravi A, Garg P, Sitaraman SV. Matrix metalloproteinases in inflammatory bowel disease: boon or a bane? Inflamm Bowel Dis. 2007;13:97-107.
100. Castaneda FE, Walia B, Vijay-Kumar M, et al. Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP. Gastroenterology. 2005;129:1991-2008.
101. Alexander JS, Elrod JW. Extracellular matrix, junctional integrity and matrix metalloproteinase interactions in endothelial permeability regulation. J Anat. 2002;200:561-574.