Autacoid 14S,21R-dihydroxy-docosahexaenoic acid counteracts diabetic impairment of macrophage prohealing functions

American Journal of Pathology

Volumn 179, Issue 4, 2011, Pages 1780-1791

  Tian, Haibin ^a   Lu, Yan ^a   Shah, Shraddha P ^a   Hong, Song ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

14,21 DIHYDROXYDOCOSA 4,7,10,12,16,19 HEXAENOIC ACID; AUTACOID; DOCOSAHEXAENOIC ACID; INTERLEUKIN 10; PLATELET DERIVED GROWTH FACTOR BB; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH INHIBITOR; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DIABETES MELLITUS; DRUG MECHANISM; EPITHELIZATION; FEMALE; GRANULATION TISSUE; HYPERGLYCEMIA; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MACROPHAGE; MACROPHAGE FUNCTION; MASS SPECTROMETRY; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; VASCULARIZATION; WOUND HEALING;

ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONATE 15-LIPOXYGENASE; AUTACOIDS; CELL LINE; DIABETES MELLITUS; DOCOSAHEXAENOIC ACIDS; FEMALE; HUMANS; INTERLEUKIN-10; MACROPHAGES; MICE; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; REACTIVE OXYGEN SPECIES; SKIN; WOUND HEALING;

EID: 80053275279     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.06.026     Document Type: Article

References (49)

1. V. Falanga Wound healing and its impairment in the diabetic foot Lancet 366 2005 1736 1743 (Pubitemid 41587454)
2. G. Broughton 2nd, J.E. Janis, and C.E. Attinger The basic science of wound healing Plast Reconstr Surg 117 2006 12S 34S (Pubitemid 44317769)
3. D. Danon, M.A. Kowatch, and G.S. Roth Promotion of wound repair in old mice by local injection of macrophages Proc Natl Acad Sci USA 86 1989 2018 2020 (Pubitemid 19087059)
4. K. Maruyama, J. Asai, M. Ii, T. Thorne, D.W. Losordo, and P.A. D'Amore Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing Am J Pathol 170 2007 1178 1191 (Pubitemid 47339326)
5. T. Lucas, A. Waisman, R. Ranjan, J. Roes, T. Krieg, W. Mller, A. Roers, and S.A. Eming Differential roles of macrophages in diverse phases of skin repair J Immunol 184 2010 3964 3977
6. R. Mirza, L.A. DiPietro, and T.J. Koh Selective and specific macrophage ablation is detrimental to wound healing in mice Am J Pathol 175 2009 2454 2462
7. S. Khanna, S. Biswas, Y. Shang, E. Collard, A. Azad, C. Kauh, V. Bhasker, G.M. Gordillo, C.K. Sen, and S. Roy Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice PLoS One 5 2010 e9539
8. Y. Lu, H. Tian, and S. Hong Novel 14,21-dihydroxy-docosahexaenoic acids: structures, formation pathways, and enhancement of wound healing J Lipid Res 51 2010 923 932
9. A.M. Abbatecola, W. Evans, and G. Paolisso PUFA supplements and type 2 diabetes in the elderly Curr Pharm Des 15 2009 4126 4134
10. J.A. Nettleton, and R. Katz n-3 Long-chain polyunsaturated fatty acids in type 2 diabetes: a review J Am Diet Assoc 105 2005 428 440 (Pubitemid 40326734)
11. V.M. Montori, A. Farmer, P.C. Wollan, and S.F. Dinneen Fish oil supplementation in type 2 diabetes: a quantitative systematic review Diabetes Care 23 2000 1407 1415
12. K.I. Shingel, M.P. Faure, L. Azoulay, C. Roberge, and R.J. Deckelbaum Solid emulsion gel as a vehicle for delivery of polyunsaturated fatty acids: implications for tissue repair, dermal angiogenesis and wound healing J Tissue Eng Regen Med 2 2008 383 393
13. C.N. Serhan, R. Yang, K. Martinod, K. Kasuga, P.S. Pillai, T.F. Porter, S.F. Oh, and M. Spite Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions J Exp Med 206 2009 15 23
14. S. Hong, K. Gronert, P.R. Devchand, R.L. Moussignac, and C.N. Serhan Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells Autacoids in anti-inflammation J Biol Chem 278 2003 14677 14687 (Pubitemid 36799790)
15. K. Gronert, N. Maheshwari, N. Khan, I.R. Hassan, M. Dunn, and M. Laniado Schwartzman A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense J Biol Chem 280 2005 15267 15278 (Pubitemid 40562883)
16. H. Tian, Y. Lu, S.P. Shah, and S. Hong 14S,21R-Dihydroxydocosahexaenoic acid remedies impaired healing and mesenchymal stem cell functions in diabetic wounds J Biol Chem 286 2011 4443 4453
17. M. Brownlee Biochemistry and molecular cell biology of diabetic complications Nature 414 2001 813 820 (Pubitemid 34000785)
18. W. Ptak, M. Klimek, K. Bryniarski, M. Ptak, and P. Majcher Macrophage function in alloxan diabetic mice: expression of adhesion molecules, generation of monokines and oxygen and NO radicals Clin Exp Immunol 114 1998 13 18 (Pubitemid 28442808)
19. K. Haskins, B. Bradley, K. Powers, V. Fadok, S. Flores, X. Ling, S. Pugazhenthi, J. Reusch, and J. Kench Oxidative stress in type 1 diabetes Ann NY Acad Sci 1005 2003 43 54 (Pubitemid 38507733)
20. H. Tian, Y. Lu, A.M. Sherwood, D. Hongqian, and S. Hong Resolvins E1 and D1 in choroid-retinal endothelial cells and leukocytes: biosynthesis and mechanisms of anti-inflammatory actions Invest Ophthalmol Vis Sci 50 2009 3613 3620
21. M. Dona, G. Fredman, J.M. Schwab, N. Chiang, M. Arita, A. Goodarzi, G. Cheng, U.H. von Andrian, and C.N. Serhan Resolvin E1, an EPA-derived mediator in whole blood, selectively counterregulates leukocytes and platelets Blood 112 2008 848 855
22. C.N. Serhan, K. Gotlinger, S. Hong, Y. Lu, J. Siegelman, T. Baer, R. Yang, S.P. Colgan, and N.A. Petasis Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes [Erratum appeared in J Immunol 2006, 176:3843] J Immunol 176 2006 1848 1859 (Pubitemid 43134330)
23. V.L. Marcheselli, S. Hong, W.J. Lukiw, X.H. Tian, K. Gronert, A. Musto, M. Hardy, J.M. Gimenez, N. Chiang, C.N. Serhan, and N.G. Bazan Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression [Erratum appeared in J Biol Chem 2003, 278:51974] J Biol Chem 278 2003 43807 43817 (Pubitemid 37346009)
24. M. Basselin, H.W. Kim, M. Chen, K. Ma, S.I. Rapoport, R.C. Murphy, and S.E. Farias Lithium modifies brain arachidonic and docosahexaenoic metabolism in rat lipopolysaccharide model of neuroinflammation J Lipid Res 51 2010 1049 1056
25. P. Yang, D. Chan, E. Felix, T. Madden, R.D. Klein, I. Shureiqi, X. Chen, A.J. Dannenberg, and R.A. Newman Determination of endogenous tissue inflammation profiles by LC/MS/MS: COX- and LOX-derived bioactive lipids Prostaglandins Leukot Essent Fatty Acids 75 2006 385 395 (Pubitemid 44648734)
26. K. Gronert, C.B. Clish, M. Romano, and C.N. Serhan Transcellular regulation of eicosanoid biosynthesis Methods Mol Biol 120 1999 119 144
27. N.G. Bazan, V.L. Marcheselli, Y. Lu, S. Hong, and F. Jackson Lipidomic approaches to neuroprotection signaling in the retinal pigment epithelium S.J. Fliesler, O.G. Kisselev, Signal Transduction in the Retina 2008 CRC Press Boca Raton, FL 349 374
28. L.M. Hall, and R.C. Murphy Electrospray mass spectrometric analysis of 5-hydroperoxy and 5-hydroxyeicosatetraenoic acids generated by lipid peroxidation of red blood cell ghost phospholipids J Am Soc Mass Spectrom 9 1998 527 532
29. K.A. Barsness, D.D. Bensard, D.A. Partrick, C.M. Calkins, R.J. Hendrickson, and R.C. McIntyre Jr Endotoxin induces an exaggerated interleukin-10 response in peritoneal macrophages of children compared with adults J Pediatr Surg 39 2004 912 915 discussion 912915 (Pubitemid 38833781)
30. R.D. Galiano, J. Michaels 5th, M. Dobryansky, J.P. Levine, and G.C. Gurtner Quantitative and reproducible murine model of excisional wound healing Wound Repair Regen 12 2004 485 492 (Pubitemid 39007049)
31. J. Michaels 5th, S.S. Churgin, K.M. Blechman, M.R. Greives, S. Aarabi, R.D. Galiano, and G.C. Gurtner db/db mice exhibit severe wound-healing impairments compared with other murine diabetic strains in a silicone-splinted excisional wound model Wound Repair Regen 15 2007 665 670 (Pubitemid 47493885)
32. H. Tian, Y. Lu, S.P. Shah, and S. Hong Novel 14S,21-dihydroxy- docosahexaenoic acid rescues wound healing and associated angiogenesis impaired by acute ethanol intoxication/exposure J Cell Biochem 111 2010 266 273
33. V. Stepanovic, O. Awad, C. Jiao, M. Dunnwald, and G.C. Schatteman Leprdb diabetic mouse bone marrow cells inhibit skin wound vascularization but promote wound healing Circ Res 92 2003 1247 1253 (Pubitemid 36723653)
34. E. Gee, M. Milkiewicz, and T.L. Haas p38 MAPK activity is stimulated by vascular endothelial growth factor receptor 2 activation and is essential for shear stress-induced angiogenesis J Cell Physiol 222 2010 120 126
35. G.D. Sharma, J. HE, and H.E. Bazan p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades J Biol Chem 278 2003 21989 21997 (Pubitemid 36792607)
36. C.A. Louis, V. Mody, W.L. Henry Jr, J.S. Reichner, and J.E. Albina Regulation of arginase isoforms I and II by IL-4 in cultured murine peritoneal macrophages Am J Physiol 276 1999 R237 R242
37. M.H. Ali, S.A. Schlidt, N.S. Chandel, K.L. Hynes, P.T. Schumacker, and B.L. Gewertz Endothelial permeability and IL-6 production during hypoxia: role of ROS in signal transduction Am J Physiol 277 1999 L1057 L1065
38. C. Pang, Z. Gao, J. Yin, J. Zhang, W. Jia, and J. Ye Macrophage infiltration into adipose tissue may promote angiogenesis for adipose tissue remodeling in obesity Am J Physiol Endocrinol Metab 295 2008 E313 E322
39. M. Siebert, P. Krieg, W.D. Lehmann, F. Marks, and G. Frstenberger Enzymic characterization of epidermis-derived 12-lipoxygenase isoenzymes Biochem J 355 2001 97 104 (Pubitemid 32304239)
40. R.D. Stout, and J. Suttles Functional plasticity of macrophages: reversible adaptation to changing microenvironments J Leukoc Biol 76 2004 509 513 (Pubitemid 39129080)
41. M. VanRollins, R.C. Baker, H.W. Sprecher, and R.C. Murphy Oxidation of docosahexaenoic acid by rat liver microsomes J Biol Chem 259 1984 5776 5783 (Pubitemid 14145045)
42. P. Christmas, K. Tolentino, V. Primo, K.Z. Berry, R.C. Murphy, M. Chen, D.M. Lee, and R.J. Soberman Cytochrome P-450 4F18 is the leukotriene B4 omega-1/omega-2 hydroxylase in mouse polymorphonuclear leukocytes: identification as the functional orthologue of human polymorphonuclear leukocyte CYP4F3A in the down-regulation of responses to LTB4 J Biol Chem 281 2006 7189 7196 (Pubitemid 43847485)
43. C.N. Serhan, N. Chiang, and T.E. Van Dyke Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators Nat Rev Immunol 8 2008 349 361 (Pubitemid 351595216)
44. S.E. Farias, S. Zarini, T. Precht, R.C. Murphy, and K.A. Heidenreich Transcellular biosynthesis of cysteinyl leukotrienes in rat neuronal and glial cells J Neurochem 103 2007 1310 1318 (Pubitemid 47631801)
45. M. Kapoor, F. Kojima, I. Appleton, S. Kawai, and L.J. Crofford Major enzymatic pathways in dermal wound healing: current understanding and future therapeutic targets Curr Opin Investig Drugs 7 2006 418 422 (Pubitemid 43772980)
46. H. Kmpfer, R. Schmidt, G. Geisslinger, J. Pfeilschifter, and S. Frank Wound inflammation in diabetic ob/ob mice: functional coupling of prostaglandin biosynthesis to cyclooxygenase-1 activity in diabetes-impaired wound healing Diabetes 54 2005 1543 1551 (Pubitemid 40586688)
47. E. Wright Jr, J.L. Scism-Bacon, and L.C. Glass Oxidative stress in type 2 diabetes: the role of fasting and postprandial glycaemia Int J Clin Pract 60 2006 308 314 (Pubitemid 43337611)
48. S.D. Cederbaum, H. Yu, W.W. Grody, R.M. Kern, P. Yoo, and R.K. Iyer Arginases I and II: do their functions overlap? Mol Genet Metab 81 Suppl 1 2004 S38 S44
49. S.L. Li, M.A. Reddy, Q. Cai, L. Meng, H. Yuan, L. Lanting, and R. Natarajan Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice Diabetes 55 2006 2611 2619 (Pubitemid 44871163)