Control of neutrophil inflammation at mucosal surfaces by secreted epithelial products

Frontiers in Immunology

Volumn 4, Issue JUL, 2013, Pages

  Szabady, Rose L ^a   McCormick, Beth A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Eicosanoids; Hepoxilin; Intestinal inflammation; Lipid chemoattractant; Lipoxygenase; MRP2; Neutrophil migration; Salmonella

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GRANULOCYTE CHEMOTACTIC PROTEIN 2; HEPOXILIN A; INTERLEUKIN 10; INTERLEUKIN 8; LIPID; LIPOXIN A; LIPOXIN B; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; PATTERN RECOGNITION RECEPTOR;

CELL MIGRATION; DISEASE CONTROL; HUMAN; IMMUNOCOMPETENT CELL; INFECTION; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; NEUTROPHIL; NONHUMAN; RESPIRATORY TRACT MUCOSA; SHORT SURVEY;

EID: 84883679203     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00220     Document Type: Short Survey

References (63)

1. Urban CF, Lourido S, Zychlinsky A. How do microbes evade neutrophil killing? Cell Microbiol (2006) 8:1687-96. doi:10.1111/j.1462-5822.2006.00792.x
2. Dale DC, Liles WC, Llewellyn C, Price TH. Effects of granulocyte-macrophage colony-stimulating factor (GM-CSF) on neutrophil kinetics and function in normal human volunteers. Am J Hematol (1998) 57:7-15. doi:10.1002/(SICI)1096-8652(199801)57:1<7::AID-AJH2>3.0.CO;2-0
3. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol (2012) 5:354-66. doi:10.1038/mi.2012.24
4. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol (2013) 13:159-75. doi:10.1038/nri3399
5. Martire B, Rondelli R, Soresina A, Pignata C, Broccoletti T, Finocchi A, et al. Clinical features, long-term follow-up and outcome of a large cohort of patients with chronic granulomatous disease: an Italian multicenter study. Clin Immunol (2008) 126:155-64. doi:10.1016/j.clim.2007.09.008
6. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol (2006) 6:173-82. doi:10.1038/nri1785
7. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science (2004) 303:1532-5. doi:10.1126/science.1092385
8. Yipp BG, Petri B, Salina D, Jenne CN, Scott BNV, Zbytnuik LD, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med (2012) 18:1386-93. doi:10.1038/nm.2847
9. Mathias JR, Perrin BJ, Liu T, Kanki J, Look AT, Huttenlocher A. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J Leukoc Biol (2006) 80:1281-8. doi:10.1189/jlb.0506346
10. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science (1996) 272:60-6. doi:10.1126/science.272.5258.60
11. von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol (2003) 3:867-78. doi:10.1038/nri1222
12. Petri B, Phillipson M, Kubes P. The physiology of leukocyte recruitment: an in vivo perspective. Mian Yi Xue Za Zhi (2008) 180:6439-46.
13. Norgard KE, Moore KL, Diaz S, Stults NL, Ushiyama S, McEver RP, et al. Characterization of a specific ligand for P-selectin on myeloid cells. J Biol Chem (1993) 268:12764-74.
14. Hidalgo A, Peired AJ, Wild MK, Vestweber D, Frenette PS. Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1, and CD44. Immunity (2007) 26:477-89. doi:10.1016/j.immuni.2007.03.011
15. Sperandio M. Selectins and glycosyltransferases in leukocyte rolling in vivo. FEBS J (2006) 273:4377-89. doi:10.1111/j.1742-4658.2006.05437.x
16. Chin AC, Parkos C. Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury. Annu Rev Pathol (2007) 2:111-43. doi:10.1146/annurev.pathol.2.010506.091944
17. Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology (1997) 113:1489-500. doi:10.1053/gast.1997.v113.pm9352851
18. Nash S, Stafford J, Madara JL. Effects of polymorphonuclear leukocyte transmigration of cultured intestinal epithelial monolayers. J Clin Invest (1987) 80:1104-13. doi:10.1172/JCI113167
19. Kucharzik T, Hudson JT, Lügering A, Abbas JA, Bettini M, Lake JG, et al. Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut (2005) 54:1565-72. doi:10.1136/gut.2004.061168
20. Liu Y, O'Connor MB, Mandell KJ, Zen K, Ullrich A, Bühring H-J, et al. Peptide-mediated inhibition of neutrophil transmigration by blocking CD47 interactions with signal regulatory protein alpha. Mian Yi Xue Za Zhi (2004) 172:2578-85.
21. Parkos CA, Delp C, Arnaout MA, Madara JL. Neutrophil migration across a cultured intestinal epithelium. J Clin Invest (1991) 88:1605-12. doi:10.1172/JCI115473
22. Liu Y, Bühring H-J, Zen K, Burst SL, Schnell FJ, Williams IR, et al. Signal regulatory protein (SIRPalpha), a cellular ligand for CD47, regulates neutrophil transmigration. J Biol Chem (2002) 277:10028-36. doi:10.1074/jbc. M109720200
23. Parkos CA, Colgan SP, Liang TW, Nusrat A, Bacarra AE, Carnes DK, et al. CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J Cell Biol (1996) 132:437-50. doi:10.1083/jcb.132.3.437
24. Ginzberg HH, Cherapanov V, Dong Q, Cantin A, Christopher AG, Shannon PT, et al. Neutrophil-mediated epithelial injury during transmigration: role of elastase. Am J Physiol Gastrointest Liver Physiol (2001) 281:705-17.
25. Brazil JC, Lee WY, KolegraffKN, Nusrat A, Parkos CA, Louis NA. Neutrophil migration across intestinal epithelium: evidence for a role of CD44 in regulating detachment of migrating cells from the luminal surface. Mian Yi Xue Za Zhi (2010) 185:7026-36. doi:10.4049/jimmunol.1001293
26. Lawrence DW, Bruyninckx WJ, Louis NA, Lublin DM, Stahl GL, Parkos CA, et al. Antiadhesive role of apical decay-accelerating factor (CD55) in human neutrophil transmigration across mucosal epithelia. J Exp Med (2003) 198:999-1010. doi:10.1084/jem.20030380
27. Madara JL, PatapoffTW, Gillece-castro B, Colgan SP, Parkos CA, Delp C, et al. 5'-Adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J Clin Invest (1993) 91:2320-5. doi:10.1172/JCI116462
28. Reaves TA, Colgan SP, Selvaraj P, Pochet MM, Walsh S, Nusrat A, et al. Neutrophil transepithelial migration: regulation at the apical epithelial surface by Fcmediated events. Am J Physiol Gastrointest Liver Physiol (2001) 280:746-54.
29. Campbell EL, Louis NA, Tomassetti SE, Canny GO, Arita M, Serhan CN, et al. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J (2007) 21:3162-70. doi:10.1096/fj.07-8473com
30. Stillie R, Farooq SM, Gordon JR, Stadnyk AW. The functional significance behind expressing two IL-8 receptor types on PMN. J Leukoc Biol (2009) 86:529-43. doi:10.1189/jlb.0208125
31. Altstaedt J, Kirchner H, Rink L. Cytokine production of neutrophils is limited to interleukin-8. Immunology (1996) 89:563-8. doi:10.1046/j.1365-2567.1996.d01-784.x
32. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. Mian Yi Xue Za Zhi (2001) 167:1882-5.
33. Yu Y, Zeng H, Lyons S, Carlson A, Merlin D, Neish AS, et al. TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am J Physiol Gastrointest Liver Physiol (2003) 285:G282-90.
34. Casale TB, Abbas MK, Carolan EJ. Degree of neutrophil chemotaxis is dependent upon the chemoattractant and barrier. Am J Respir Cell Mol Biol (1992) 7:112-7. doi:10.1165/ajrcmb/7.1.112
35. Foxman EF, Campbell JJ, Butcher EC. Multistep navigation and the combinatorial control of leukocyte chemotaxis. J Cell Biol (1997) 139:1349-60. doi:10.1083/jcb.139.5.1349
36. Heit B, Tavener S, Raharjo E, Kubes P. An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients. J Cell Biol (2002) 159:91-102. doi:10.1083/jcb.200202114
37. Rabiet M-J, Huet E, Boulay F. Human mitochondria-derived N-formylated peptides are novel agonists equally active on FPR and FPRL1, while Listeria monocytogenes-derived peptides preferentially activate FPR. Eur J Immunol (2005) 35:2486-95. doi:10.1002/eji.200526338
38. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CCM, et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science (2010) 330:362-6. doi:10.1126/science.1195491
39. McCormick BA, Hofman ILPM, Kim J, Carnes DK, Miller SI, Madara JL. Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol (1995) 131:1599-608. doi:10.1083/jcb.131.6.1599
40. McCormick BA, Parkos CA, Colgan SP, Carnes DK, Madara JL. Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. Mian Yi Xue Za Zhi (1998) 160:455-66.
41. Mrsny RJ, Gewirtz AT, Siccardi D, Savidge T, Hurley BP, Madara JL, et al. Identification of hepoxilin A3 in inflammatory events: a required role in neutrophil migration across intestinal epithelia. Proc Natl Acad Sci U S A (2004) 101:7421-6. doi:10.1073/pnas.0400832101
42. Sadik CD, Luster AD. Lipid-cytokine-chemokine cascades orchestrate leukocyte recruitment in inflammation. J Leukoc Biol (2012) 91:207-15. doi:10.1189/jlb.0811402
43. Fabre J, Goulet JL, Riche E, Nguyen M, Coggins K, Offenbacher S, et al. Transcellular biosynthesis contributes to the production of leukotrienes during inflammatory responses in vivo. J Clin Invest (2002) 109:1373-80. doi:10.1172/JCI200214869
44. Chiang N, Arita M, Serhan CN. Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot Essent Fatty Acids (2005) 73:163-77. doi:10.1016/j.plefa.2005.05.003
45. Pace-Asciak CR. Hepoxilins: a review on their cellular actions. Biochim Biophys Acta (1994) 1215:1-8. doi:10.1016/0005-2760(94)90087-6
46. Pazos M, Siccardi D, Mumy KL, Bien JD, Louie S, Shi HN, et al. Multidrug resistance-associated transporter 2 regulates mucosal inflammation by facilitating the synthesis of hepoxilin A3. Mian Yi Xue Za Zhi (2008) 181:8044-52.
47. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, McCormick BA. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci U S A (2000) 97:12283-8. doi:10.1073/pnas.97.22.12283
48. Wall DM, Nadeau WJ, Pazos MA, Shi HN, Galyov EE, McCormick BA. Identification of the Salmonella enterica serotype typhimurium SipA domain responsible for inducing neutrophil recruitment across the intestinal epithelium. Cell Microbiol (2007) 9:2299-313. doi:10.1111/j.1462-5822.2007.00960.x
49. Silva M, Song C, Nadeau WJ, Matthews JB, McCormick BA. Salmonella typhimurium SipA-induced neutrophil transepithelial migration: involvement of a PKCalpha- dependent signal transduction pathway. Am J Physiol Gastrointest Liver Physiol (2004) 286:G1024-31. doi:10.1152/ajpgi.00299.2003
50. Srikanth CV, Wall DM, Maldonado-Contreras A, Shi HN, Zhou D, Demma Z, et al. Salmonella pathogenesis and processing of secreted effectors by caspase-3. Science (2010) 330:390-3. doi:10.1126/science.1194598
51. Agbor TA, Demma ZC, Mumy KL, Bien JD, McCormick BA. The ERM protein, ezrin, regulates neutrophil transmigration by modulating the apical localization of MRP2 in response to the SipA effector protein during Salmonella typhimurium infection. Cell Microbiol (2011) 13:2007-21. doi:10.1111/j.1462-5822.2011.01693.x
52. Dho S, Grinstein S, Corey EJ, Su W, Pace-Asciak CR. Hepoxilin A3 induced changes in cytosolic calcium, intracellular pH and membrane potential in human neutrophils. Biochem J (1990) 266:63-8.
53. Mumy KL, Bien JD, Pazos MA, Gronert K, Hurley BP, McCormick BA. Distinct isoforms of phospholipase A2 mediate the ability of Salmonella enterica serotype typhimurium and Shigella flexneri to induce the transepithelial migration of neutrophils. Infect Immun (2008) 76:3614-27. doi:10.1128/IAI.00407-08
54. Boll EJ, Struve C, Sander A, Demma Z, Krogfelt KA, McCormick BA. Enteroaggregative Escherichia coli promotes transepithelial migration of neutrophils through a conserved 12-lipoxygenase pathway. Cell Microbiol (2012) 14:120-32. doi:10.1111/j.1462-5822.2011.01706.x
55. Boll EJ, Struve C, Sander A, Demma Z, Nataro JP, McCormick BA, et al. The fimbriae of enteroaggregative Escherichia coli induce epithelial inflammation in vitro and in a human intestinal xenograft model. J Infect Dis (2012) 206:714-22. doi:10.1093/infdis/jis417
56. Hurley BP, Siccardi D, Mrsny RJ, McCormick BA. Polymorphonuclear cell transmigration induced by Pseudomonas aeruginosa requires the eicosanoid hepoxilin A 3. Mian Yi Xue Za Zhi (2004) 173:5712-20.
57. Hurley BP, Pirzai W, Mumy KL, Gronert K, McCormick BA. Selective eicosanoid-generating capacity of cytoplasmic phospholipase A2 in Pseudomonas aeruginosa-infected epithelial cells. Am J Physiol Lung Cell Mol Physiol (2011) 300:L286-94. doi:10.1152/ajplung.00147.2010
58. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol (2012) 10:717-25. doi:10.1038/nrmicro2873
59. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature (2011) 474:298-306. doi:10.1038/nature10208
60. Serhan CN, Petasis NA. Resolvins and protectins in inflammation resolution. Chem Rev (2011) 111:5922-43. doi:10.1021/cr100396c
61. Fierro IM, Colgan SP, Bernasconi G, Petasis NA, Clish CB, Arita M, et al. Lipoxin A4 and Aspiring-triggered 15-epi-lipoxin A4 inhibit human neutrophil migration: comparisons between synthetic 15 epimers in chemotaxis and transmigration with microvessel endothelial cells and epithelial cells. J Immunol (2003) 170:2688-94.
62. Norling LV, Dalli J, Flower RJ, Serhan CN, Perretti M. Resolvin D1 limits polymorphonuclear leukocytes recruitment to inflammatory loci: receptor-dependent actions. Arterioscler Thromb Vasc Biol (2012). Available from: http://www.ncbi.nlm.nih.gov/pubmed/22499990 doi:10.1161/ATVBAHA.112.249508
63. Campbell EL, MacManus CF, Kominsky DJ, Keely S, Glover LE, Bowers BE, et aal. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. PNAS (2010) 107(32):14298-303.