Resolvin D2 restores neutrophil directionality and improves survival after burns

FASEB Journal

Volumn 27, Issue 6, 2013, Pages 2270-2281

  Kurihara, Tomohiro ^a,b   Jones, Caroline N ^a,b   Yu, Yong Ming ^a,b   Fischman, Alan J ^a,b   Watada, Susumu ^a,b   Tompkins, Ronald G ^a,b   Fagan, Shawn P ^a,b   Irimia, Daniel ^a,b  

^a SHRINERS HOSPITALS FOR CHILDREN   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Chemotaxis; Inflammation; Innate immunity; Lipid mediators; Microfluidics

Indexed keywords

ANTIINFLAMMATORY AGENT; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; RESOLVIN D2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; LIGATION; MALE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROPHYLAXIS; RAT; SEPSIS; SURVIVAL RATE; TREATMENT DURATION;

CHEMOTAXIS; INFLAMMATION; INNATE IMMUNITY; LIPID MEDIATORS; MICROFLUIDICS;

ANIMALS; BURNS; CHEMOTAXIS, LEUKOCYTE; DOCOSAHEXAENOIC ACIDS; MALE; NEUTROPHILS; RATS; RATS, WISTAR; SEPSIS;

ANIMALIA; RATTUS;

EID: 84878767354     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-219519     Document Type: Article

References (44)

1. Centers for Disease Control and Prevention National Center for Injury Prevention and Control (2012) Web-based Injury Statistics Query and Reporting System (WISQARS) [Electronic version]. Retrieved Sept. 14, 2012, from http://www.cdc.gov/injury/wisqarss
2. MacKenzie, E. J., Rivara, F. P., Jurkovich, G. J., Nathens, A. B., Frey, K. P., Egleston, B. L., Salkever, D. S., and Scharfstein, D. O. (2006) A national evaluation of the effect of trauma-center care on mortality. N. Engl. J. Med. 354, 366-3788
3. Mann, E. A., Baun, M. M., Meininger, J. C., and Wade, C. E. (2012) Comparison of mortality associated with sepsis in the burn, trauma, and general intensive care unit patient: a systematic review of the literature. Shock 37, 4-166
4. Williams, F. N., Herndon, D. N., Hawkins, H. K., Lee, J. O., Cox, R. A., Kulp, G. A., Finnerty, C. C., Chinkes, D. L., and Jeschke, M. G. (2009) The leading causes of death after burn injury in a single pediatric burn center. Crit. Care 13, R1833
5. Chipp, E., Milner, C. S., and Blackburn, A. V. (2010) Sepsis in burns: a review of current practice and future therapies. Ann. Plast. Surg. 65, 228-2366
6. Greenhalgh, D. G., Saffle, J. R., Holmes, J. H. t., Gamelli, R. L., Palmieri, T. L., Horton, J. W., Tompkins, R. G., Traber, D. L., Mozingo, D. W., Deitch, E. A., Goodwin, C. W., Herndon, D. N., Gallagher, J. J., Sanford, A. P., Jeng, J. C., Ahrenholz, D. H., Neely, A. N., O'Mara, M. S., Wolf, S. E., Purdue, G. F., Garner, W. L., Yowler, C. J., and Latenser, B. A. (2007) American Burn Association consensus conference to define sepsis and infection in burns. J. Burn Care Res. 28, 776-7900
7. Branski, L. K., Al-Mousawi, A., Rivero, H., Jeschke, M. G., Sanford, A. P., and Herndon, D. N. (2009) Emerging infections in burns. Surg. Infect. (Larchmt.) 10, 389-3977
8. Calvano, S. E., Xiao, W., Richards, D. R., Felciano, R. M., Baker, H. V., Cho, R. J., Chen, R. O., Brownstein, B. H., Cobb, J. P., Tschoeke, S. K., Miller-Graziano, C., Moldawer, L. L., Mindrinos, M. N., Davis, R. W., Tompkins, R. G., and Lowry, S. F. (2005) A network-based analysis of systemic inflammation in humans. Nature 437, 1032-10377
9. Xiao, W., Mindrinos, M. N., Seok, J., Cuschieri, J., Cuenca, A. G., Gao, H., Hayden, D. L., Hennessy, L., Moore, E. E., Minei, J. P., Bankey, P. E., Johnson, J. L., Sperry, J., Nathens, A. B., Billiar, T. R., West, M. A., Brownstein, B. H., Mason, P. H., Baker, H. V., Finnerty, C. C., Jeschke, M. G., Lopez, M. C., Klein, M. B., Gamelli, R. L., Gibran, N. S., Arnoldo, B., Xu, W., Zhang, Y., Calvano, S. E., McDonald-Smith, G. P., Schoenfeld, D. A., Storey, J. D., Cobb, J. P., Warren, H. S., Moldawer, L. L., Herndon, D. N., Lowry, S. F., Maier, R. V., Davis, R. W., and Tompkins, R. G. (2011) A genomic storm in critically injured humans. J. Exp. Med. 208, 2581-25900
10. Kotz, K. T., Xiao, W., Miller-Graziano, C., Qian, W. J., Russom, A., Warner, E. A., Moldawer, L. L., De, A., Bankey, P. E., Petritis, B. O., Camp, D. G., 2nd, Rosenbach, A. E., Goverman, J., Fagan, S. P., Brownstein, B. H., Irimia, D., Xu, W., Wilhelmy, J., Mindrinos, M. N., Smith, R. D., Davis, R. W., Tompkins, R. G., and Toner, M. (2010) Clinical microfluidics for neutrophil genomics and proteomics. Nat. Med. 16, 1042-10477
11. Babcock, G. F., Alexander, J. W., and Warden, G. D. (1990) Flow cytometric analysis of neutrophil subsets in thermally injured patients developing infection. Clin. Immunol. Immunopathol. 54, 117-1255
12. Solomkin, J. S. (1990) Neutrophil disorders in burn injury: complement, cytokines, and organ injury. J. Trauma 30, S80-855
13. Butler, K. L., Ambravaneswaran, V., Agrawal, N., Bilodeau, M., Toner, M., Tompkins, R. G., Fagan, S., and Irimia, D. (2010) Burn injury reduces neutrophil directional migration speed in microfluidic devices. PLoS One 5, e119211
14. Weiss, S. J. (1989) Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-3766
15. Fazal, N., Shamim, M., Khan, S. S., Gamelli, R. L., and Sayeed, M. M. (2000) Neutrophil depletion in rats reduces burn-injury induced intestinal bacterial translocation. Crit. Care Med. 28, 1550-15555
16. Huber-Lang, M. S., Sarma, J. V., McGuire, S. R., Lu, K. T., Guo, R. F., Padgaonkar, V. A., Younkin, E. M., Laudes, I. J., Riedemann, N. C., Younger, J. G., and Ward, P. A. (2001) Protective effects of anti-C5a peptide antibodies in experimental sepsis. FASEB J. 15, 568-5700
17. Reutershan, J., Morris, M. A., Burcin, T. L., Smith, D. F., Chang, D., Saprito, M. S., and Ley, K. (2006) Critical role of endothelial CXCR2 in LPS-induced neutrophil migration into the lung. J. Clin. Invest. 116, 695-7022
18. Tsai, W. C., Strieter, R. M., Mehrad, B., Newstead, M. W., Zeng, X., and Standiford, T. J. (2000) CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect. Immun. 68, 4289-42966
19. Carter, E. A., Tompkins, R. G., Babich, J. W., Correia, J. A., and Fischman, A. J. (1996) Decreased cerebral glucose utilization in rats during the ebb phase of thermal injury. J. Trauma 40, 930-9355
20. Ambravaneswaran, V., Wong, I. Y., Aranyosi, A. J., Toner, M., and Irimia, D. (2010) Directional decisions during neutrophil chemotaxis inside bifurcating channels. Integr. Biol. (Camb.) 2, 639-6477
21. Serhan, C. N., Clish, C. B., Brannon, J., Colgan, S. P., Chiang, N., and Gronert, K. (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, 1197-12044
22. Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K., and Serhan, C. N. (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2, 612-6199
23. Wolf, K., Alexander, S., Schacht, V., Coussens, L. M., von Andrian, U. H., van Rheenen, J., Deryugina, E., and Friedl, P. (2009) Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol. 20, 931-9411
24. Tchervenkov, J. I., Epstein, M. D., Silberstein, E. B., and Alexander, J. W. (1988) Early burn wound excision and skin grafting postburn trauma restores in vivo neutrophil delivery to inflammatory lesions. Arch. Surg. 123, 1477-14811
25. Irimia, D. (2010) Microfluidic technologies for temporal perturbations of chemotaxis. Annu. Rev. Biomed. Eng. 12, 259-2844
26. Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P., Devchand, P. R., Mirick, G., and Moussignac, R. L. (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, 1025-10377
27. Sun, Y. P., Oh, S. F., Uddin, J., Yang, R., Gotlinger, K., Campbell, E., Colgan, S. P., Petasis, N. A., and Serhan, C. N. (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282, 9323-93344
28. Chiang, N., Fredman, G., Backhed, F., Oh, S. F., Vickery, T., Schmidt, B. A., and Serhan, C. N. (2012) Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484, 524-5288
29. Spite, M., Norling, L. V., Summers, L., Yang, R., Cooper, D., Petasis, N. A., Flower, R. J., Perretti, M., and Serhan, C. N. (2009) Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461, 1287-12911
30. Park, C. K., Xu, Z. Z., Liu, T., Lu, N., Serhan, C. N., and Ji, R. R. (2011) Resolvin D2 is a potent endogenous inhibitor for transient receptor potential subtype V1/A1, inflammatory pain, and spinal cord synaptic plasticity in mice: distinct roles of resolvin D1, D2, and E1. J. Neurosci. 31, 18433-184388
31. Kasuga, K., Yang, R., Porter, T. F., Agrawal, N., Petasis, N. A., Irimia, D., Toner, M., and Serhan, C. N. (2008) Rapid appearance of resolvin precursors in inflammatory exudates: novel mechanisms in resolution. J. Immunol. 181, 8677-86877
32. Norling, L. V., Dalli, J., Flower, R. J., Serhan, C. N., and Perretti, M. (2012) Resolvin D1 limits polymorphonuclear leukocytes recruitment to inflammatory loci: receptor-dependent actions. Arterioscler. Thromb. Vasc. Biol. 32, 1970-19788
33. Claria, J., Dalli, J., Yacoubian, S., Gao, F., and Serhan, C. N. (2012) Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J. Immunol. 189, 2597-26055
34. Krishnamoorthy, S., Recchiuti, A., Chiang, N., Fredman, G., and Serhan, C. N. (2012) Resolvin D1 receptor stereoselectivity and regulation of inflammation and proresolving microRNAs. Am. J. Pathol. 180, 2018-20277
35. Tsuda, Y., Takahashi, H., Kobayashi, M., Hanafusa, T., Herndon, D. N., and Suzuki, F. (2004) Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 21, 215-2266
36. Zhang, M. J., and Spite, M. (2012) Resolvins: anti-inflammatory and proresolving mediators derived from omega-3 polyunsaturated fatty acids. Annu. Rev. Nutr. 32, 203-2277
37. Bento, A. F., Claudino, R. F., Dutra, R. C., Marcon, R., and Calixto, J. B. (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, 1957-19699
38. Liu, T., Qian, W. J., Gritsenko, M. A., Xiao, W., Moldawer, L. L., Kaushal, A., Monroe, M. E., Varnum, S. M., Moore, R. J., Purvine, S. O., Maier, R. V., Davis, R. W., Tompkins, R. G., Camp, D. G., 2nd, and Smith, R. D. (2006) High dynamic range characterization of the trauma patient plasma proteome. Mol. Cell. Proteomics 5, 1899-19133
39. Noel, G., Wang, Q., Schwemberger, S., Hanson, C., Giacalone, N., Haar, L., and Ogle, C. K. (2011) Neutrophils, not monocyte/macrophages, are the major splenic source of postburn IL-10. Shock 36, 149-1555
40. Pillay, J., den Braber, I., Vrisekoop, N., Kwast, L. M., de Boer, R. J., Borghans, J. A., Tesselaar, K., and Koenderman, L. (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116, 625-6277
41. Hu, Z., and Sayeed, M. M. (2004) Suppression of mitochondriadependent neutrophil apoptosis with thermal injury. Am. J. Physiol. Cell Physiol. 286, C170-C1788
42. Bohr, S., Patel, S. J., Sarin, D., Irimia, D., Yarmush, M. L., and Berthiaume, F. (2013) Resolvin D2 prevents secondary thrombosis and necrosis in a mouse burn wound model. Wound Repair Regen. 21, 35-433
43. Jones, C. N., Dalli, J., Dimisko, L., Wong, E., Serhan, C. N., and Irimia, D. (2012) Microfluidic chambers for monitoring leukocyte trafficking and humanized nano-proresolving medicines interactions. Proc. Natl. Acad. Sci. U. S. A. 109, 20560-205655
44. Sheridan, R. L., Hinson, M., Nackel, A., Blaquiere, M., Daley, W., Querzoli, B., Spezzafaro, J., Lybarger, P., Martyn, J., Szyfelbein, S., and Tompkins, R. (1997) Development of a pediatric burn pain and anxiety management program. J. Burn Care Rehabil. 18, 455-4599