Antimicrobial aspects of inflammatory resolution in the mucosa: A role for proresolving mediators

Journal of Immunology

Volumn 187, Issue 7, 2011, Pages 3475-3481

  Campbell, Eric L ^a   Serhan, Charles N ^b   Colgan, Sean P ^a  

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

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE ISOENZYME; ARACHIDONIC ACID; AUTACOID; BACTERIAL ANTIGEN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; BETA DEFENSIN 2; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CYCLOOXYGENASE 2; DEFENSIN; LECTIN; LIPOXYGENASE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PHOSPHOLIPASE A2; POLYPEPTIDE ANTIBIOTIC AGENT; PROSTAGLANDIN; PROTECTIN D1; RESOLVIN E1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UVOMORULIN;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; CELL JUNCTION; CELL MIGRATION; CELL PROLIFERATION; EPITHELIUM CELL; GRAM NEGATIVE BACTERIUM; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INFECTION RESISTANCE; MUCOSA INFLAMMATION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; SHORT SURVEY; WOUND HEALING;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; AUTACOIDS; HUMANS; IMMUNITY, MUCOSAL; INFLAMMATION;

EID: 80053468941     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100150     Document Type: Short Survey

References (88)

1. Majno, G., and I. Joris. 1996. Cells, Tissues and Disease: Principles of General Pathology. Blackwell Science, Cambridge, MA.
2. Serhan, C. N., and N. Chiang. 2008. Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus. Br. J. Pharmacol. 153 (Suppl. 1): S200-S215. (Pubitemid 351340979)
3. Serhan, C. N., N. Chiang, and T. E. Van Dyke. 2008. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8: 349-361. (Pubitemid 351595216)
4. Serhan, C. N., C. B. Clish, J. Brannon, S. P. Colgan, N. Chiang, and K. Gronert. 2000. 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. 192: 1197-1204.
5. Bik, E. M. 2009. Composition and function of the human-associated microbiota. Nutr. Rev. 67(Suppl. 2): S164-S171.
6. Gilroy, D. W., P. R. Colville-Nash, D. Willis, J. Chivers, M. J. Paul-Clark, and D. A. Willoughby. 1999. Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. 5: 698-701.
7. Spite, M., and C. N. Serhan. 2010. Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins. Circ. Res. 107: 1170-1184.
8. Schwab, J. M., N. Chiang, M. Arita, and C. N. Serhan. 2007. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447: 869-874. (Pubitemid 46920139)
9. Serhan, C. N., S. D. Brain, C. D. Buckley, D. W. Gilroy, C. Haslett, L. A. O'Neill, M. Perretti, A. G. Rossi, and J. L. Wallace. 2007. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21: 325-332. (Pubitemid 46213480)
10. Clària, J., and C. N. Serhan. 1995. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc. Natl. Acad. Sci. USA 92: 9475-9479.
11. Serhan, C. N., J. F. Maddox, N. A. Petasis, I. Akritopoulou-Zanze, A. Papayianni, H. R. Brady, S. P. Colgan, and J. L. Madara. 1995. Design of lipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 34: 14609-14615. (Pubitemid 3000720)
12. Bannenberg, G., and C. N. Serhan. 2010. Specialized pro-resolving lipid mediators in the inflammatory response: an update. Biochim. Biophys. Acta 1801: 1260-1273.
13. Campbell, E. L., C. F. MacManus, D. J. Kominsky, S. Keely, L. E. Glover, B. E. Bowers, M. Scully, W. J. Bruyninckx, and S. P. Colgan. 2010. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc. Natl. Acad. Sci. USA 107: 14298-14303.
14. Canny, G., O. Levy, G. T. Furuta, S. Narravula-Alipati, R. B. Sisson, C. N. Serhan, and S. P. Colgan. 2002. Lipid mediator-induced expression of bactericidal/permeability-increasing protein (BPI) in human mucosal epithelia. Proc. Natl. Acad. Sci. USA 99: 3902-3907. (Pubitemid 34252203)
15. Rajasagi, N. K., P. B. Reddy, A. Suryawanshi, S. Mulik, P. Gjorstrup, and B. T. Rouse. 2011. Controlling herpes simplex virus-induced ocular inflammatory lesions with the lipid-derived mediator resolvin E1. J. Immunol. 186: 1735-1746.
16. Gronert, K., N. Maheshwari, N. Khan, I. R. Hassan, M. Dunn, and M. Laniado Schwartzman. 2005. A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense. J. Biol. Chem. 280: 15267-15278. (Pubitemid 40562883)
17. Aoki, H., T. Hisada, T. Ishizuka, M. Utsugi, T. Kawata, Y. Shimizu, F. Okajima, K. Dobashi, and M. Mori. 2008. Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem. Biophys. Res. Commun. 367: 509-515.
18. Haworth, O., M. Cernadas, R. Yang, C. N. Serhan, and B. D. Levy. 2008. Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9: 873-879.
19. Levy, B. D., P. Kohli, K. Gotlinger, O. Haworth, S. Hong, S. Kazani, E. Israel, K. J. Haley, and C. N. Serhan. 2007. Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness. J. Immunol. 178: 496-502. (Pubitemid 46039663)
20. Wang, B., X. Gong, J. Y. Wan, L. Zhang, Z. Zhang, H. Z. Li, and S. Min. 2011. Resolvin D1 protects mice from LPS-induced acute lung injury. Pulm. Pharmacol. Ther. 24: 434-441.
21. Hasturk,H., A.Kantarci, E.Goguet-Surmenian, A.Blackwood, C.Andry,C. N. Serhan, and T. E. Van Dyke. 2007. Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179: 7021-7029.
22. Campbell, E. L., N. A. Louis, S. E. Tomassetti, G. O. Canny, M. Arita, C. N. Serhan, and S. P. Colgan. 2007. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J. 21: 3162-3170. (Pubitemid 47565535)
23. Hasturk, H., A. Kantarci, T. Ohira, M. Arita, N. Ebrahimi, N. Chiang, N. A. Petasis, B. D. Levy, C. N. Serhan, and T. E. Van Dyke. 2006. RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 20: 401-403. (Pubitemid 46671185)
24. Arita, M., M. Yoshida, S. Hong, E. Tjonahen, J. N. Glickman, N. A. Petasis, R. S. Blumberg, and C. N. Serhan. 2005. Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc. Natl. Acad. Sci. USA 102: 7671-7676. (Pubitemid 40741029)
25. Bento, A. F., R. F. Claudino, R. C. Dutra, R. Marcon, and J. B. Calixto. 2011. Omega-3 fatty acid-derived mediators 17(R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J. Immunol. 187: 1957-1969.
26. Lima-Garcia, J., R. Dutra, K. Da Silva, E. Motta, M. Campos, and J. Calixto. The precursor of resolvin D series and aspirin-triggered resolvin D1 display antihyperalgesic properties in adjuvant-induced arthritis in rats. Br. J. Pharmacol. In press.
27. Xu, Z. Z., L. Zhang, T. Liu, J. Y. Park, T. Berta, R. Yang, C. N. Serhan, and R. R. Ji. 2010. Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat. Med. 16: 592-597, 1p following 597.
28. Takano, T., S. Fiore, J. F. Maddox, H. R. Brady, N. A. Petasis, and C. N. Serhan. 1997. Aspirin-triggered 15-epi-lipoxin A4 (LXA4) and LXA4 stable analogues are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J. Exp. Med. 185: 1693-1704. (Pubitemid 27203265)
29. Ohira, T., M. Arita, K. Omori, A. Recchiuti, T. E. Van Dyke, and C. N. Serhan. 2010. Resolvin E1 receptor activation signals phosphorylation and phagocytosis. J. Biol. Chem. 285: 3451-3461.
30. Arita, M., T. Ohira, Y. P. Sun, S. Elangovan, N. Chiang, and C. N. Serhan. 2007. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J. Immunol. 178: 3912-3917. (Pubitemid 46417661)
31. Ariel, A., G. Fredman, Y. P. Sun, A. Kantarci, T. E. Van Dyke, A. D. Luster, and C. N. Serhan. 2006. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat. Immunol. 7: 1209-1216. (Pubitemid 44594317)
32. Serhan, C. N., S. Hong, K. Gronert, S. P. Colgan, P. R. Devchand, G. Mirick, and R. L. Moussignac. 2002. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 196: 1025-1037. (Pubitemid 35231761)
33. Sun, Y. P., S. F. Oh, J. Uddin, R. Yang, K. Gotlinger, E. Campbell, S. P. Colgan, N. A. Petasis, and C. N. Serhan. 2007. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282: 9323-9334. (Pubitemid 47104612)
34. Spite, M., L. V. Norling, L. Summers, R. Yang, D. Cooper, N. A. Petasis, R. J. Flower, M. Perretti, and C. N. Serhan. 2009. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461: 1287-1291.
35. Palmer, C. D., C. J. Mancuso, J. P. Weiss, C. N. Serhan, E. C. Guinan, and O. Levy. 17(R)-Resolvin D1 differentially regulates TLR4-mediated responses of primary human macrophages to purified LPS and live E. coli. J. Leukoc. Biol. In press.
36. Beagley, K. W., and A. J. Husband. 1998. Intraepithelial lymphocytes: origins, distribution, and function. Crit. Rev. Immunol. 18: 237-254. (Pubitemid 128670069)
37. Laukoetter, M. G., P. Nava, and A. Nusrat. 2008. Role of the intestinal barrier in inflammatory bowel disease. World J. Gastroenterol. 14: 401-407. (Pubitemid 351320848)
38. McCole, D. F., and K. E. Barrett. 2007. Varied role of the gut epithelium in mucosal homeostasis. Curr. Opin. Gastroenterol. 23: 647-654. (Pubitemid 47508795)
39. Kim, Y. S., and S. B. Ho. 2010. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr. Gastroenterol. Rep. 12: 319-330.
40. Singh, P. K., H. P. Jia, K. Wiles, J. Hesselberth, L. Liu, B. A. Conway, E. P. Greenberg, E. V. Valore, M. J. Welsh, T. Ganz, et al. 1998. Production of beta-defensins by human airway epithelia. Proc. Natl. Acad. Sci. USA 95: 14961-14966. (Pubitemid 29003739)
41. Gordon, Y. J., L. C. Huang, E. G. Romanowski, K. A. Yates, R. J. Proske, and A. M. McDermott. 2005. Human cathelicidin (LL-37), a multifunctional peptide, is expressed by ocular surface epithelia and has potent antibacterial and antiviral activity. Curr. Eye Res. 30: 385-394. (Pubitemid 40910819)
42. Sahasrabudhe, K. S., J. R. Kimball, T. H. Morton, A. Weinberg, and B. A. Dale. 2000. Expression of the antimicrobial peptide, human beta-defensin 1, in duct cells of minor salivary glands and detection in saliva. J. Dent. Res. 79: 1669-1674. (Pubitemid 32489432)
43. Abiko, Y., M. Nishimura, and T. Kaku. 2003. Defensins in saliva and the salivary glands. Med. Electron Microsc. 36: 247-252. (Pubitemid 38145543)
44. Shale, M., and S. Ghosh. 2009. How intestinal epithelial cells tolerise dendritic cells and its relevance to inflammatory bowel disease. Gut 58: 1291-1299.
45. Wan, M., C. Godson, P. J. Guiry, B. Agerberth, and J. Z. Haeggström. 2011. Leukotriene B4/antimicrobial peptide LL-37 proinflammatory circuits are mediated by BLT1 and FPR2/ALX and are counterregulated by lipoxin A4 and resolvin E1. FASEB J. 25: 1697-1705.
46. Cole, A. M., J. Shi, A. Ceccarelli, Y. H. Kim, A. Park, and T. Ganz. 2001. Inhibition of neutrophil elastase prevents cathelicidin activation and impairs clearance of bacteria from wounds. Blood 97: 297-304. (Pubitemid 32061273)
47. Yamasaki, K., J. Schauber, A. Coda, H. Lin, R. A. Dorschner, N. M. Schechter, C. Bonnart, P. Descargues, A. Hovnanian, and R. L. Gallo. 2006. Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 20: 2068-2080. (Pubitemid 44953906)
48. Sørensen, O., K. Arnljots, J. B. Cowland,D. F. Bainton, and N. Borregaard. 1997. The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and meta-myelocytes and localized to specific granules in neutrophils. Blood 90: 2796-2803. (Pubitemid 27413490)
49. Rosenfeld, Y., N. Papo, and Y. Shai. 2006. Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem. 281: 1636-1643.
50. Mookherjee, N., K. L. Brown, D. M. Bowdish, S. Doria, R. Falsafi, K. Hokamp, F. M. Roche, R. Mu, G. H. Doho, J. Pistolic, et al. 2006. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol. 176: 2455-2464. (Pubitemid 43201696)
51. Iimura, M., R. L. Gallo, K. Hase, Y. Miyamoto, L. Eckmann, and M. F. Kagnoff. 2005. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J. Immunol. 174: 4901-4907.
52. Van Wetering, S., P. J. Sterk, K. F. Rabe, and P. S. Hiemstra. 1999. Defensins: key players or bystanders in infection, injury, and repair in the lung? J. Allergy Clin. Immunol. 104: 1131-1138.
53. Wilson, C. L., A. J. Ouellette, D. P. Satchell, T. Ayabe, Y. S. López-Boado, J. L. Stratman, S. J. Hultgren, L. M. Matrisian, and W. C. Parks. 1999. Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286: 113-117. (Pubitemid 29484488)
54. Salzman, N. H., M. A. Underwood, and C. L. Bevins. 2007. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin. Immunol. 19:70-83. Epub 20May 07, 2007.
55. Schaefer, A. S., G. M. Richter, M. Nothnagel, M. L. Laine, A. Rühling, C. Schäfer, N. Cordes, B. Noack, M. Folwaczny, J. Glas, et al. 2010. A 3′ UTR transition within DEFB1 is associated with chronic and aggressive periodontitis. Genes Immun. 11: 45-54.
56. De Yang, Q. Chen, A. P. Schmidt, G. M. Anderson, J. M. Wang, J. Wooters, J. J. Oppenheim, and O. Chertov. 2000. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192: 1069-1074.
57. Niyonsaba, F., M. Hirata, H. Ogawa, and I. Nagaoka. 2003. Epithelial cell-derived antibacterial peptides human beta-defensins and cathelicidin: multifunctional activities on mast cells. Curr. Drug Targets Inflamm. Allergy 2: 224-231.
58. Niyonsaba, F., K. Iwabuchi, H. Matsuda, H. Ogawa, and I. Nagaoka. 2002. Epithelial cell-derived human beta-defensin-2 acts as a chemotaxin for mast cells through a pertussis toxin-sensitive and phospholipase C-dependent pathway. Int. Immunol. 14: 421-426. (Pubitemid 34257769)
59. Chotjumlong, P., S. Khongkhunthian, S. Ongchai, V. Reutrakul, and S. Krisanaprakornkit. 2010. Human beta-defensin-3 up-regulates cyclooxygenase-2 expression and prostaglandin E2 synthesis in human gingival fibroblasts. J. Periodontal Res. 45: 464-470.
60. Feng, Z., G. R. Dubyak, M. M. Lederman, and A. Weinberg. 2006. Cutting edge: human beta defensin 3 - a novel antagonist of the HIV-1 coreceptor CXCR4. J. Immunol. 177: 782-786. (Pubitemid 44036577)
61. Ghannam, S., C. Dejou, N. Pedretti, J. P. Giot, K. Dorgham, H. Boukhaddaoui, V. Deleuze, F. X. Bernard, C. Jorgensen, H. Yssel, and J. Pène. 2011. CCL20 and b-defensin-2 induce arrest of human Th17 cells on inflamed endothelium in vitro under flow conditions. J. Immunol. 186: 1411-1420.
62. Oppenheim, J. J., and D. Yang. 2005. Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol. 17: 359-365. (Pubitemid 40848537)
63. Otte, J. M., A. E. Zdebik, S. Brand, A. M. Chromik, S. Strauss, F. Schmitz, L. Steinstraesser, and W. E. Schmidt. 2009. Effects of the cathelicidin LL-37 on intestinal epithelial barrier integrity. Regul. Pept. 156: 104-117.
64. Carretero, M., M. J. Escámez, M. García, B. Duarte, A. Holguín, L. Retamosa, J. L. Jorcano, M. D. Río, and F. Larcher. 2008. In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J. Invest. Dermatol. 128: 223-236. (Pubitemid 350249392)
65. Otte, J. M., I. Werner, S. Brand, A. M. Chromik, F. Schmitz, M. Kleine, and W. E. Schmidt. 2008. Human beta defensin 2 promotes intestinal wound healing in vitro. J. Cell. Biochem. 104: 2286-2297.
66. Baroni, A., G. Donnarumma, I. Paoletti, I. Longanesi-Cattani, K. Bifulco, M. A. Tufano, and M. V. Carriero. 2009. Antimicrobial human beta-defensin-2 stimulates migration, proliferation and tube formation of human umbilical vein endothelial cells. Peptides 30: 267-272.
67. Canny, G., and O. Levy. 2008. Bactericidal/permeability-increasing protein (BPI) and BPI homologs at mucosal sites. Trends Immunol. 29: 541-547.
68. Canny, G., E. Cario, A. Lennartsson, U. Gullberg, C. Brennan, O. Levy, and S. P. Colgan. 2006. Functional and biochemical characterization of epithelial bactericidal/permeability-increasing protein. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G557-G567.
69. Canny, G. O., R. T. Trifonova, D. W. Kindelberger, S. P. Colgan, and R. N. Fichorova. 2006. Expression and function of bactericidal/permeability- increasing protein in human genital tract epithelial cells. J. Infect. Dis. 194: 498-502. (Pubitemid 44162662)
70. Elsbach, P., and J. Weiss. 1998. Role of the bactericidal/permeability- increasing protein in host defence. Curr. Opin. Immunol. 10: 45-49. (Pubitemid 28112078)
71. Levy, O. 2000. A neutrophil-derived anti-infective molecule: bactericidal/permeability-increasing protein. Antimicrob. Agents Chemother. 44: 2925-2931.
72. Gazzano-Santoro, H., J. B. Parent, L. Grinna, A. Horwitz, T. Parsons, G. Theofan, P. Elsbach, J. Weiss, and P. J. Conlon. 1992. High-affinity binding of the bactericidal/permeability-increasing protein and a recombinant amino-terminal fragment to the lipid A region of lipopolysaccharide. Infect. Immun. 60: 4754-4761.
73. Mannion, B. A., J. Weiss, and P. Elsbach. 1990. Separation of sublethal and lethal effects of the bactericidal/permeability increasing protein on Escherichia coli. J. Clin. Invest. 85: 853-860. (Pubitemid 20087489)
74. Levy, O., C. E. Ooi, P. Elsbach, M. E. Doerfler, R. I. Lehrer, and J. Weiss. 1995. Antibacterial proteins of granulocytes differ in interaction with endotoxin. Comparison of bactericidal/permeability-increasing protein, p15s, and defensins. J. Immunol. 154: 5403-5410.
75. Ulevitch, R. J., and P. S. Tobias. 1999. Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11: 19-22. (Pubitemid 29082331)
76. Gazzano-Santoro, H., K. Mészáros, C. Birr, S. F. Carroll, G. Theofan, A. H. Horwitz, E. Lim, S. Aberle, H. Kasler, and J. B. Parent. 1994. Competition between rBPI23, a recombinant fragment of bactericidal/ permeability-increasing protein, and lipopolysaccharide (LPS)-binding protein for binding to LPS and gram-negative bacteria. Infect. Immun. 62: 1185-1191.
77. Weiss, J., P. Elsbach, I. Olsson, and H. Odeberg. 1978. Purification and characterization of a potent bactericidal and membrane active protein from the granules of human polymorphonuclear leukocytes. J. Biol. Chem. 253: 2664-2672. (Pubitemid 8328425)
78. Evans, T. J., A. Carpenter, D. Moyes, R. Martin, and J. Cohen. 1995. Protective effects of a recombinant amino-terminal fragment of human bactericidal/permeability-increasing protein in an animal model of gram-negative sepsis. J. Infect. Dis. 171: 153-160.
79. Lin, Y., W. J. Leach, and W. S. Ammons. 1996. Synergistic effect of a recombinant N-terminal fragment of bactericidal/permeability-increasing protein and cefamandole in treatment of rabbit gram-negative sepsis. Antimicrob. Agents Chemother. 40: 65-69. (Pubitemid 26019679)
80. Vaishnava, S., and L. V. Hooper. 2007. Alkaline phosphatase: keeping the peace at the gut epithelial surface. Cell Host Microbe 2: 365-367. (Pubitemid 350215328)
81. Goldberg, R. F., W. G. Austen, Jr., X. Zhang, G. Munene, G. Mostafa, S. Biswas, M. McCormack, K. R. Eberlin, J. T. Nguyen, H. S. Tatlidede, et al. 2008. Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc. Natl. Acad. Sci. USA 105: 3551-3556. (Pubitemid 351723590)
82. Mata-Haro, V., C. Cekic, M. Martin, P. M. Chilton, C. R. Casella, and T. C. Mitchell. 2007. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316: 1628-1632. (Pubitemid 46982038)
83. Moyle, P. M., and I. Toth. 2008. Self-adjuvanting lipopeptide vaccines. Curr. Med. Chem. 15: 506-516. (Pubitemid 351472417)
84. Wozniak, M., J. R. Keefer, C. Saunders, and L. E. Limbird. 1997. Differential targeting and retention of G protein-coupled receptors in polarized epithelial cells. J. Recept. Signal Transduct. Res. 17: 373-383. (Pubitemid 27057373)
85. Lawrence, D. W., W. J. Bruyninckx, N. A. Louis, D. M. Lublin, G. L. Stahl, C. A. Parkos, and S. P. Colgan. 2003. Antiadhesive role of apical decay-accelerating factor (CD55) in human neutrophil transmigration across mucosal epithelia. J. Exp. Med. 198: 999-1010. (Pubitemid 37248616)
86. Louis, N. A., K. E. Hamilton, T. Kong, and S. P. Colgan. 2005. HIF-dependent induction of apical CD55 coordinates epithelial clearance of neutrophils. FASEB J. 19: 950-959. (Pubitemid 40827716)
87. Serhan, C. N. 2007. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu. Rev. Immunol. 25: 101-137. (Pubitemid 46697904)
88. Oh, S. F., P. S. Pillai, A. Recchiuti, R. Yang, and C. N. Serhan. 2011. Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J. Clin. Invest. 121: 569-581.