Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation

Immunity

Volumn 40, Issue 1, 2014, Pages 66-77

  Campbell, Eric L ^a   Bruyninckx, Walter J ^b   Kelly, Caleb J ^a   Glover, Louise E ^a   McNamee, Eóin N ^a   Bowers, Brittelle E ^a   Bayless, Amanda J ^a   Scully, Melanie ^a   Saeedi, Bejan J ^a   Golden Mason, Lucy ^a   Ehrentraut, Stefan F ^a   Curtis, Valerie F ^a   Burgess, Adrianne ^a   Garvey, John F ^c   Sorensen, Amber ^a   Nemenoff, Raphael ^a   Jedlicka, Paul ^a   Taylor, Cormac T ^c   Kominsky, Douglas J ^a   Colgan, Sean P ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b HANOVER COLLEGE   (United States)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL HYPOXIA; CHRONIC INFLAMMATION; COLITIS; CONTROLLED STUDY; GOBLET CELL; INTESTINE EPITHELIUM CELL; MOLECULAR STABILITY; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY BURST; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANIMALS; ANOXIA; CELL COMMUNICATION; CELL MOVEMENT; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COLITIS; COLON; DISEASE MODELS, ANIMAL; HYPOXIA-INDUCIBLE FACTOR 1; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MUCOUS MEMBRANE; NADPH OXIDASE; NEUTROPHILS; OXIDATIVE STRESS; OXYGEN; PROTEIN STABILITY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84892447705     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.11.020     Document Type: Article

References (42)

1. Amulic B., Cazalet C., Hayes G.L., Metzler K.D., Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol. 2012, 30:459-489.
2. Beck P.L., Ihara E., Hirota S.A., MacDonald J.A., Meng D., Nanthakumar N.N., Podolsky D.K., Xavier R.J. Exploring the interplay of barrier function and leukocyte recruitment in intestinal inflammation by targeting fucosyltransferase VII and trefoil factor 3. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G43-G53.
3. Bobrie A., Krumeich S., Reyal F., Recchi C., Moita L.F., Seabra M.C., Ostrowski M., Théry C. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 2012, 72:4920-4930.
4. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
5. Campbell E.L., MacManus C.F., Kominsky D.J., Keely S., Glover L.E., Bowers B.E., Scully M., Bruyninckx W.J., Colgan S.P. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc. Natl. Acad. Sci. USA 2010, 107:14298-14303.
6. Chen L.W., Egan L., Li Z.W., Greten F.R., Kagnoff M.F., Karin M. The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med. 2003, 9:575-581.
7. Colgan S.P., Taylor C.T. Hypoxia: an alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol 2010, 7:281-287.
8. Colgan S.P., Curtis V.F., Campbell E.L. The inflammatory tissue microenvironment in IBD. Inflamm. Bowel Dis. 2013, 19:2238-2244.
9. Colgan S.P., Ehrentraut S.F., Glover L.E., Kominsky D.J., Campbell E.L. Contributions of neutrophils to resolution of mucosal inflammation. Immunol. Res. 2013, 55:75-82.
10. Cox G., Crossley J., Xing Z. Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation invivo. Am. J. Respir. Cell Mol. Biol. 1995, 12:232-237.
11. Cross A.R., Jones O.T. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem. J. 1986, 237:111-116.
12. Cross A.R., Segal A.W. The NADPH oxidase of professional phagocytes-prototype of the NOX electron transport chain systems. Biochim. Biophys. Acta 2004, 1657:1-22.
13. Cummins E.P., Seeballuck F., Keely S.J., Mangan N.E., Callanan J.J., Fallon P.G., Taylor C.T. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 2008, 134:156-165.
14. Dalli J., Serhan C.N. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 2012, 120:e60-e72.
15. Dinauer M.C., Orkin S.H., Brown R., Jesaitis A.J., Parkos C.A. The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex. Nature 1987, 327:717-720.
16. Ehrentraut S.F., Kominsky D.J., Glover L.E., Campbell E.L., Kelly C.J., Bowers B.E., Bayless A.J., Colgan S.P. Central role for endothelial human deneddylase-1/SENP8 in fine-tuning the vascular inflammatory response. J.Immunol. 2013, 190:392-400.
17. Furuta G.T., Turner J.R., Taylor C.T., Hershberg R.M., Comerford K., Narravula S., Podolsky D.K., Colgan S.P. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J.Exp. Med. 2001, 193:1027-1034.
18. Huang J.S., Noack D., Rae J., Ellis B.A., Newbury R., Pong A.L., Lavine J.E., Curnutte J.T., Bastian J. Chronic granulomatous disease caused by a deficiency in p47(phox) mimicking Crohn's disease. Clin. Gastroenterol. Hepatol. 2004, 2:690-695.
19. Johansson M.E., Larsson J.M., Hansson G.C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. USA 2011, 108(Suppl 1):4659-4665.
20. Karhausen J., Furuta G.T., Tomaszewski J.E., Johnson R.S., Colgan S.P., Haase V.H. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J.Clin. Invest. 2004, 114:1098-1106.
21. Khor B., Gardet A., Xavier R.J. Genetics and pathogenesis of inflammatory bowel disease. Nature 2011, 474:307-317.
22. Kominsky D.J., Campbell E.L., Colgan S.P. Metabolic shifts in immunity and inflammation. J.Immunol. 2010, 184:4062-4068.
23. Kühl A.A., Kakirman H., Janotta M., Dreher S., Cremer P., Pawlowski N.N., Loddenkemper C., Heimesaat M.M., Grollich K., Zeitz M., et al. Aggravation of different types of experimental colitis by depletion or adhesion blockade of neutrophils. Gastroenterology 2007, 133:1882-1892.
24. Lim K., Sumagin R., Hyun Y.M. Extravasating neutrophil-derived microparticles preserve vascular barrier function in inflamed tissue. Immune Netw. 2013, 13:102-106.
25. Louis N.A., Hamilton K.E., Canny G., Shekels L.L., Ho S.B., Colgan S.P. Selective induction of mucin-3 by hypoxia in intestinal epithelia. J.Cell. Biochem. 2006, 99:1616-1627.
26. Mashimo H., Wu D.C., Podolsky D.K., Fishman M.C. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 1996, 274:262-265.
27. Mittelbrunn M., Sánchez-Madrid F. Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell Biol. 2012, 13:328-335.
28. Nauseef W.M. Biological roles for the NOX family NADPH oxidases. J.Biol. Chem. 2008, 283:16961-16965.
29. Okumura C.Y., Hollands A., Tran D.N., Olson J., Dahesh S., von Köckritz-Blickwede M., Thienphrapa W., Corle C., Jeung S.N., Kotsakis A., et al. A new pharmacological agent (AKB-4924) stabilizes hypoxia inducible factor-1 (HIF-1) and increases skin innate defenses against bacterial infection. J.Mol. Med. 2012, 90:1079-1089.
30. Polosukhin V.V., Cates J.M., Lawson W.E., Milstone A.P., Matafonov A.G., Massion P.P., Lee J.W., Randell S.H., Blackwell T.S. Hypoxia-inducible factor-1 signalling promotes goblet cell hyperplasia in airway epithelium. J.Pathol. 2011, 224:203-211.
31. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J.Biol. Chem. 1991, 266:4244-4250.
32. Robinson A., Keely S., Karhausen J., Gerich M.E., Furuta G.T., Colgan S.P. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology 2008, 134:145-155.
33. Safran M., Kim W.Y., O'Connell F., Flippin L., Günzler V., Horner J.W., Depinho R.A., Kaelin W.G. Mouse model for noninvasive imaging of HIF prolyl hydroxylase activity: assessment of an oral agent that stimulates erythropoietin production. Proc. Natl. Acad. Sci. USA 2006, 103:105-110.
34. Sanmun D., Witasp E., Jitkaew S., Tyurina Y.Y., Kagan V.E., Ahlin A., Palmblad J., Fadeel B. Involvement of a functional NADPH oxidase in neutrophils and macrophages during programmed cell clearance: implications for chronic granulomatous disease. Am. J. Physiol. Cell Physiol. 2009, 297:C621-C631.
35. Savill J.S., Wyllie A.H., Henson J.E., Walport M.J., Henson P.M., Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J.Clin. Invest. 1989, 83:865-875.
36. Serhan C.N., Chiang N. Resolution phase lipid mediators of inflammation: agonists of resolution. Curr. Opin. Pharmacol. 2013, 13:632-640.
37. Stie J., Jesaitis A.J. Reorganization of the human neutrophil plasma membrane is associated with functional priming: implications for neutrophil preparations. J.Leukoc. Biol. 2007, 81:672-685.
38. Taupin D., Podolsky D.K. Trefoil factors: initiators of mucosal healing. Nat. Rev. Mol. Cell Biol. 2003, 4:721-732.
39. Taupin D.R., Kinoshita K., Podolsky D.K. Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc. Natl. Acad. Sci. USA 2000, 97:799-804.
40. Van der Sluis M., De Koning B.A., De Bruijn A.C., Velcich A., Meijerink J.P., Van Goudoever J.B., Büller H.A., Dekker J., Van Seuningen I., Renes I.B., Einerhand A.W. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 2006, 131:117-129.
41. Van Rees E.P., Palmen M.J., Van De Goot F.R., Macher B.A., Dieleman L.A. Leukocyte migration in experimental inflammatory bowel disease. Mediators Inflamm. 1997, 6:85-93.
42. Zen K., Parkos C.A. Leukocyte-epithelial interactions. Curr. Opin. Cell Biol. 2003, 15:557-564.