Contributions of neutrophils to resolution of mucosal inflammation

Immunologic Research

Volumn 55, Issue 1-3, 2013, Pages 75-82

  Colgan, Sean P ^a   Ehrentraut, Stefan F ^a   Glover, Louise E ^a   Kominsky, Douglas J ^a   Campbell, Eric L ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Colitis; Endothelium; Epithelium; Hypoxia inducible factor; Inflammation; Metabolism; Mucosa; Murine model; Neutrophil; Nucleoside; Nucleotidase; Nucleotide

Indexed keywords

ADENOSINE; ADENOSINE KINASE;

ARTICLE; CELL INTERACTION; DIGESTIVE SYSTEM INFLAMMATION; DRUG INHIBITION; GASTROINTESTINAL MUCOSA; METABOLISM; NEUTROPHIL; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION;

ANIMALS; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; NEUTROPHILS; OXYGEN;

EID: 84876726276     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-012-8350-2     Document Type: Article

References (87)

1. Cohen IK. A brief history of wound healing. Yardley: Oxford Clinical Communications; 1998.
2. Majno G, Joris I. Cells, tissues and disease: principles of general pathology. Cambridge: Blackwell Science; 1996.
3. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol. 2008;8:349-61.
4. Serhan CN. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am J Pathol. 2010;177:1576-91.
5. Serhan CN, Brain SD, Buckley CD, et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007;21:325-32.
6. Laukoetter MG, Bruewer M, Nusrat A. Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr Opin Gastroenterol. 2006;22:85-9.
7. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9:799-809.
8. Colgan SP, Eltzschig HK, Eckle T, et al. Physiologic roles for ecto-5′-nucleotidase (CD73). Purinergic Signal. 2006;2:351-60.
9. Khoury J, Ibla JC, Neish AS, et al. Antiinflammatory adaptation to hypoxia through adenosine-mediated cullin-1 deneddylation. J Clin Invest. 2007;117:703-11.
10. Eltzschig HK, Macmanus CF, Colgan SP. Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc Med. 2008;18:103-7.
11. Taylor CT, Colgan SP. Hypoxia and gastrointestinal disease. J Mol Med. 2008;85:1295-300.
12. Bonnans C, Levy BD. Lipid mediators as agonists for the resolution of acute lung inflammation and injury. Am J Respir Cell Mol Biol. 2007;36:201-5.
13. Kuhl AA, Kakirman H, Janotta M, et al. Aggravation of different types of experimental colitis by depletion or adhesion blockade of neutrophils. Gastroenterology. 2007;133:1882-92.
14. Zemans RL, Colgan SP, Downey GP. Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol. 2009;40:519-35. Epub 2008 Oct 31.
15. Taylor CT, Colgan SP. Hypoxia and gastrointestinal disease. J Mol Med. 2007;85:1295-300.
16. Furuta GT, Turner JR, Taylor CT, et al. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J Exp Med. 2001;193:1027-34.
17. Colgan SP, Taylor CT. Hypoxia: an alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol. 2010;7:281-7.
18. Kominsky DJ, Campbell EL, Colgan SP. Metabolic shifts in immunity and inflammation. J Immunol. 2010;184:4062-8.
19. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 2003;112:453-65.
20. Borregaard N, Herlin T. Energy metabolism of human neutrophils during phagocytosis. J Clin Invest. 1982;70:550-7.
21. El-Benna J, Dang PM, Gougerot-Pocidalo MA. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol. 2008;30:279-89.
22. Gabig TG, Bearman SI, Babior BM. Effects of oxygen tension and pH on the respiratory burst of human neutrophils. Blood. 1979;53:1133-9.
23. Semenza GL. Oxygen sensing, homeostasis, and disease. NEJM. 2011;365:537-47.
24. Comerford KM, Wallace TJ, Karhausen J, et al. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 2002;62:3387-94.
25. Synnestvedt K, Furuta GT, Comerford KM, et al. Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 (HIF-1) mediates permeability changes in intestinal epithelia. J Clin Invest. 2002;110:993-1002.
26. 2B receptors. J Exp Med. 2003;198:783-96.
27. Cummins EP, Seeballuck F, Keely SJ, et al. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology. 2008;134:156-65. Epub 2007 Oct 10.
28. Han IO, Kim HS, Kim HC, et al. Synergistic expression of inducible nitric oxide synthase by phorbol ester and interferon-gamma is mediated through NF-kappaB and ERK in microglial cells. J Neurosci Res. 2003;73:659-69.
29. Karhausen JO, Furuta GT, Tomaszewski JE, et al. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest. 2004;114:1098-106.
30. Morote-Garcia JC, Rosenberger P, Nivillac NM, et al. Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology. 2009;136:607-18.
31. Robinson A, Keely S, Karhausen J, et al. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology. 2008;134:145-55.
32. Shah YM, Ito S, Morimura K, et al. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology. 2008;134:2036-48. 2048 e1-3.
33. Giatromanolaki A, Sivridis E, Maltezos E, et al. Hypoxia inducible factor 1alpha and 2alpha overexpression in inflammatory bowel disease. J Clin Pathol. 2003;56:209-13.
34. Mariani F, Sena P, Marzona L, et al. Cyclooxygenase-2 and Hypoxia-Inducible Factor-1alpha protein expression is related to inflammation, and up-regulated since the early steps of colorectal carcinogenesis. Cancer Lett. 2009;279:221-9.
35. Matthijsen RA, Derikx JP, Kuipers D, et al. Enterocyte shedding and epithelial lining repair following ischemia of the human small intestine attenuate inflammation. PLoS ONE. 2009;4:e7045.
36. Louis NA, Hamilton KE, Canny G, et al. Selective induction of mucin-3 by hypoxia in intestinal epithelia. J Cell Biochem. 2006;99:1616-27.
37. Blumberg RS, Saubermann LJ, Strober W. Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr Opin Immunol. 1999;11:648-56.
38. Linden J. Adenosine in tissue protection and tissue regeneration. Mol Pharmacol. 2005;67:1385-7. Epub 2005 Feb 9.
39. Jacobson KA, Gao ZG. Adenosine receptors as therapeutic targets. Nat Rev Drug Discov. 2006;5:247-64.
40. Kolachala VL, Bajaj R, Chalasani M, et al. Purinergic receptors in gastrointestinal inflammation. Am J Physiol Gastrointest Liver Physiol. 2008;294:G401-10. Epub 2007 Dec 6.
41. Decking UK, Schlieper G, Kroll K, et al. Hypoxia-induced inhibition of adenosine kinase potentiates cardiac adenosine release. Circ Res. 1997;81:154-64.
42. Linden J. Molecular approach to adenosine receptors: receptor-mediated mechanisms of tissue protection. Annu Rev Pharmacol Toxicol. 2001;41:775-87.
43. Aherne CM, Kewley EM, Eltzschig HK. The resurgence of A2B adenosine receptor signaling. Biochim Biophys Acta 2010.
44. Eckle T, Koeppen M, Eltzschig HK. Role of extracellular adenosine in acute lung injury. Physiology (Bethesda). 2009;24:298-306.
45. Eltzschig HK. Adenosine: an old drug newly discovered. Anesthesiology. 2009;111:904-15.
46. Chekeni FB, Elliott MR, Sandilos JK, et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature. 2010;467:863-7.
47. Elliott MR, Chekeni FB, Trampont PC, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature. 2009;461:282-6.
48. Eltzschig HK, Eckle T, Mager A, et al. ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ Res. 2006;99:1100-8. Epub 2006 Oct 12.
49. Eltzschig HK, Ibla JC, Furuta GT, et al. Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J Exp Med. 2003;198:783-96.
50. Chen Y, Corriden R, Inoue Y, et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science. 2006;314:1792-5.
51. Linden J. Purinergic chemotaxis. Science. 2006;314:1689-90.
52. Gordon JL. Extracellular ATP: effects, sources and fate. Biochem J. 1986;233:309-19.
53. Weissmuller T, Campbell EL, Rosenberger P, et al. PMNs facilitate translocation of platelets across human and mouse epithelium and together alter fluid homeostasis via epithelial cell-expressed ecto-NTPDases. J Clin Invest. 2008;118:3682-92.
54. Colgan SP, Eltzschig HK, Eckle T, et al. Physiological roles for ecto-5′-nucleotidase (CD73). Purinergic Signal. 2006;2:351-60.
55. Madara JL, Patapoff TW, Gillece-Castro B, 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.
56. Neish AS, Gewirtz AT, Zeng H, et al. Prokaryotic regulation of epithelial responses by inhibition of IkappaB- alpha ubiquitination. Science. 2000;289:1560-3.
57. Cope GA, Deshaies RJ. COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell. 2003;114:663-71.
58. Cardozo T, Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol. 2004;5:739-51.
59. Parry G, Estelle M. Regulation of cullin-based ubiquitin ligases by the Nedd8/RUB ubiquitin-like proteins. Semin Cell Dev Biol. 2004;15:221-9.
60. Mendoza HM, Shen LN, Botting C, et al. NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J Biol Chem. 2003;278:25637-43. Epub 2003 May 1.
61. Wu K, Yamoah K, Dolios G, et al. DEN1 is a dual function protease capable of processing the C terminus of Nedd8 and deconjugating hyper-neddylated CUL1. J Biol Chem. 2003;278:28882-91. Epub 2003 May 19.
62. Kumar A, Wu H, Collier-Hyams LS, et al. The bacterial fermentation product butyrate influences epithelial signaling via reactive oxygen species-mediated changes in cullin-1 neddylation. J Immunol. 2009;182:538-46.
63. Banerjee S, Zmijewski JW, Lorne E, et al. Modulation of SCF beta-TrCP-dependent I kappaB alpha ubiquitination by hydrogen peroxide. J Biol Chem. 2010;285:2665-75. Epub 2009 Nov 20.
64. Campbell EL, Serhan CN, Colgan SP. Antimicrobial aspects of inflammatory resolution in the mucosa: a role for proresolving mediators. J Immunol. 2011;187:3475-81.
65. Serhan CN, Yang R, Martinod K, et al. Maresins: novel macrophage mediators with potent anti-inflammatory and pro-resolving actions. J Exp Med. 2009;206:15-23.
66. Das UN, Ramos EJ, Meguid MM. Metabolic alterations during inflammation and its modulation by central actions of omega-3 fatty acids. Curr Opin Clin Nutr Metab Care. 2003;6:413-9.
67. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21:495-505.
68. Calder PC. Fatty acids and gene expression related to inflammation. Nestle Nutr Workshop Ser Clin Perform Programme. 2002;7:19-36. discussion 36-40.
69. Belluzzi A. N-3 fatty acids for the treatment of inflammatory bowel diseases. Proc Nutr Soc. 2002;61:391-5.
70. Nakazawa A, Hibi T. Is fish oil (n-3 fatty acids) effective for the maintenance of remission in Crohn's disease? J Gastroenterol. 2000;35:173-5.
71. Belluzzi A, Brignola C, Campieri M, et al. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med. 1996;334:1557-60.
72. Serhan CN, Hong S, Gronert K, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025-37.
73. Marcheselli VL, Hong S, Lukiw WJ, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem. 2003;278:43807-17.
74. Serhan CN, Clish CB, Brannon J, et al. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2- nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med. 2000;192:1197-204.
75. Levy BD, Clish CB, Schmidt B, et al. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol. 2001;2:612-9.
76. Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxin biosynthesis: an update and role in anti-inflammation and pro-resolution. Prostaglandins Other Lipid Mediat. 2002;68-69:433-55.
77. Arita M, Bianchini F, Aliberti J, et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med. 2005;201:713-22.
78. Arita M, Ohira T, Sun YP, et al. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol. 2007;178:3912-7.
79. Ariel A, Fredman G, Sun YP, et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol. 2006;7:1209-16.
80. Sun YP, Oh SF, Uddin J, et al. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem. 2007;282:9323-34.
81. 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;21:3162-70.
82. Spite M, Norling LV, Summers L, et al. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature. 2009;461:1287-91.
83. Palmer CD, Mancuso CJ, Weiss JP, et al. 17(R)-Resolvin D1 differentially regulates TLR4-mediated responses of primary human macrophages to purified LPS and live E. coli. J Leukoc Biol. 2011.
84. Campbell EL, MacManus CF, Kominsky DJ, et al. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc Natl Acad Sci USA. 2010;107:14298-303.
85. Mata-Haro V, Cekic C, Martin M, et al. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science. 2007;316:1628-32.
86. Moyle PM, Toth I. Self-adjuvanting lipopeptide vaccines. Curr Med Chem. 2008;15:506-16.
87. Canny G, Levy O, Furuta GT, et al. Lipid mediator-induced expression of bactericidal/permeability- increasing protein (BPI) in human mucosal epithelia. Proc Natl Acad Sci USA. 2002;99:3902-7.