Maresin 1 induces a novel pro-resolving phenotype in human platelets

Journal of Thrombosis and Haemostasis

Volumn 15, Issue 4, 2017, Pages 802-813

  Lannan, K L ^a   Spinelli, S L ^a   Blumberg, N ^a   Phipps, R P ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

antiplatelet agents; hemostasis; inflammation; platelet activation; platelets

Indexed keywords

ANTITHROMBOCYTIC AGENT; CD40 LIGAND; FORMYLPEPTIDE RECEPTOR LIKE 1; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 32; LIPOXIN A; MARESIN 1; PADGEM PROTEIN; PROSTAGLANDIN E2; RESOLVIN D1; RESOLVIN D2; THROMBOCYTE FACTOR 4; THROMBOXANE B2; UNCLASSIFIED DRUG; 7,14-DIHYDROXYDOCOSA-4,8,10,12,16,19-HEXAENOIC ACID; DOCOSAHEXAENOIC ACID; GPR32 PROTEIN, HUMAN; HSH2D PROTEIN, HUMAN; LIPOXIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CELL SPREADING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; HEMOSTASIS; HUMAN; HUMAN CELL; MEDIATOR RELEASE; PROTEIN EXPRESSION; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; BLOOD; BLOOD CLOTTING PARAMETERS; CARDIOVASCULAR DISEASE; CYTOLOGY; DRUG EFFECTS; HEART INFARCTION; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHENOTYPE; THROMBOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BLOOD PLATELETS; CARDIOVASCULAR DISEASES; DOCOSAHEXAENOIC ACIDS; HEMOSTASIS; HUMANS; INFLAMMATION; LIPOXINS; MYOCARDIAL INFARCTION; PHENOTYPE; PLATELET ACTIVATION; PLATELET AGGREGATION INHIBITORS; PLATELET FUNCTION TESTS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 85014080377     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13620     Document Type: Article

References (39)

1. Morrell CN, Aggrey AA, Chapman LM, Modjeski KL. Emerging roles for platelets as immune and inflammatory cells. Blood 2014; 123: 2759–67.
2. Chapman LM, Aggrey AA, Field DJ, Srivastava K, Ture S, Yui K, Topham DJ, Baldwin WM, Morrell CN. Platelets present antigen in the context of MHC class I. J Immunol 2012; 189: 916–23.
3. Garraud O, Berthet J, Hamzeh-Cognasse H, Cognasse F. Pathogen sensing, subsequent signalling, and signalosome in human platelets. Thromb Res 2011; 127: 283–6.
4. Cognasse F, Hamzeh-Cognasse H, Garraud O. Platelets “Toll-like receptor” engagement stimulates the release of immunomodulating molecules. Transfus Clin Biol 2008; 15: 139–47.
5. Radomski MW, Palmer RM, Moncada S. Comparative pharmacology of endothelium-derived relaxing factor, nitric oxide and prostacyclin in platelets. Br J Pharmacol 1987; 92: 181–7.
6. Lannan KL, Phipps RP, White RJ. Thrombosis, platelets, microparticles and PAH: more than a clot. Drug Discov Today. 2014; 19: 1230–5.
7. Lannan KL, Refaai MA, Ture SK, Morrell CN, Blumberg N, Phipps RP, Spinelli SL. Resveratrol preserves the function of human platelets stored for transfusion. Br J Haematol 2016; 172: 794–806.
8. Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 2005; 6: 1191–7.
9. Serhan C, Brain S, Buckley C, Gilroy D, Haslett C, O'Neill L, Perretti M, Rossi A, Wallace J. Resolution of inflammation: state of the art, definitions and terms. FASEB J 2007; 21: 325–32.
10. Serhan CN. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 2007; 25: 101–37.
11. Serhan C, Chiang N, van Dyke T. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 2008; 8: 349–61.
12. Ariel A, Chiang N, Arita M, Petasis NA, Serhan CN. Aspirin-triggered lipoxin A4 and B4 analogs block extracellular signal-regulated kinase-dependent TNF-alpha secretion from human T cells. J Immunol 2003; 170: 6266–72.
13. Lee TH, Horton CE, Kyan-Aung U, Haskard D, Crea AE, Spur BW. Lipoxin A4 and lipoxin B4 inhibit chemotactic responses of human neutrophils stimulated by leukotriene B4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clin Sci (Lond) 1989; 77: 195–203.
14. Godson C, Mitchell S, Harvey K, Petasis N, Hogg N, Brady H. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 2000; 164: 1663–7.
15. Oh JY, Giles N, Landar A, Darley-Usmar V. Accumulation of 15-deoxy-delta(12,14)-prostaglandin J2 adduct formation with Keap1 over time: effects on potency for intracellular antioxidant defence induction. Biochem J. 2008; 411: 297–306.
16. Serhan CN, Clish CB, Brannon J, Colgan SP, Chiang N, Gronert K. 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.
17. Ramon S, Baker SF, Sahler JM, Kim N, Feldsott EA, Serhan CN, Martínez-Sobrido L, Topham DJ, Phipps RP. The specialized proresolving mediator 17-HDHA enhances the antibody-mediated immune response against influenza virus: a new class of adjuvant? J Immunol 2014; 193: 6031–40.
18. Croasdell A, Lacy SH, Thatcher TH, Sime PJ, Phipps RP. Resolvin D1 dampens pulmonary inflammation and promotes clearance of nontypeable haemophilus influenzae. J Immunol 2016; 196: 2742–52.
19. Kim N, Ramon S, Thatcher TH, Woeller CF, Sime PJ, Phipps RP. Specialized proresolving mediators (SPMs) inhibit human B-cell IgE production. Eur J Immunol 2016; 46: 81–91.
20. Fredman G, van Dyke TE, Serhan CN. Resolvin E1 regulates adenosine diphosphate activation of human platelets. Arterioscler Thromb Vasc Biol 2010; 30: 2005–13.
21. Serhan CN, Krishnamoorthy S, Recchiuti A, Chiang N. Novel anti-inflammatory–pro-resolving mediators and their receptors. Curr Top Med Chem 2011; 11: 629–47.
22. Chiang N, Dalli J, Colas RA, Serhan CN. Identification of resolvin D2 receptor mediating resolution of infections and organ protection. J Exp Med 2015; 212: 1203–17.
23. Arita M, Yoshida M, Hong S, Tjonahen E, Glickman JN, Petasis NA, Blumberg RS, Serhan CN. 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 U S A. 2005; 102: 7671–6.
24. Kaufman J, Spinelli SL, Schultz E, Blumberg N, Phipps RP. Release of biologically active CD154 during collection and storage of platelet concentrates prepared for transfusion. J Thromb Haemost 2007; 5: 788–96.
25. McEwen BJ. The influence of diet and nutrients on platelet function. Semin Thromb Hemost 2014; 40: 214–26.
26. Serhan C. A search for endogenous mechanisms of anti-inflammation uncovers novel chemical mediators: missing links to resolution. Histochem Cell Biol 2004; 122: 305–21.
27. Ariel A, Serhan C. Resolvins and protectins in the termination program of acute inflammation. Trends Immunol 2007; 28: 176–83.
28. Abdulnour RE, Dalli J, Colby JK, Krishnamoorthy N, Timmons JY, Tan SH, Colas RA, Petasis NA, Serhan CN, Levy BD. Maresin 1 biosynthesis during platelet-neutrophil interactions is organ-protective. Proc Natl Acad Sci U S A. 2014; 111: 16526–31.
29. Yeo EL, Sheppard JA, Feuerstein IA. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood 1994; 83: 2498–507.
30. Gawaz M, Vogel S. Platelets in tissue repair: control of apoptosis and interactions with regenerative cells. Blood 2013; 122: 2550–4.
31. Serhan CN, Dalli J, Karamnov S, Choi A, Park CK, Xu ZZ, Ji RR, Zhu M, Petasis NA. Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain. FASEB J 2012; 26: 1755–65.
32. Xian W, Wu Y, Xiong W, Li L, Li T, Pan S, Song L, Hu L, Pei L, Yao S, Shang Y. The pro-resolving lipid mediator Maresin 1 protects against cerebral ischemia/reperfusion injury by attenuating the pro-inflammatory response. Biochem Biophys Res Commun 2016; 472: 175–81.
33. Nordgren TM, Heires AJ, Wyatt TA, Poole JA, Levan TD, Cerutis DR, Romberger DJ. Maresin-1 reduces the pro-inflammatory response of bronchial epithelial cells to organic dust. Respir Res 2013; 14: 51.
34. Nordgren TM, Bauer CD, Heires AJ, Poole JA, Wyatt TA, West WW, Romberger DJ. Maresin-1 reduces airway inflammation associated with acute and repetitive exposures to organic dust. Transl Res 2015; 166: 57–69.
35. Dalli J, Zhu M, Vlasenko NA, Deng B, Haeggström JZ, Petasis NA, Serhan CN. The novel 13S,14S-epoxy-maresin is converted by human macrophages to maresin 1 (MaR1), inhibits leukotriene A4 hydrolase (LTA4H), and shifts macrophage phenotype. FASEB J 2013; 27: 2573–83.
36. Krishnamoorthy N, Burkett PR, Dalli J, Abdulnour RE, Colas R, Ramon S, Phipps RP, Petasis NA, Kuchroo VK, Serhan CN, Levy BD. Cutting edge: maresin-1 engages regulatory T cells to limit type 2 innate lymphoid cell activation and promote resolution of lung inflammation. J Immunol 2015; 194: 863–7.
37. Akagi D, Chen M, Toy R, Chatterjee A, Conte MS. Systemic delivery of proresolving lipid mediators resolvin D2 and maresin 1 attenuates intimal hyperplasia in mice. FASEB J 2015; 29: 2504–13.
38. Chatterjee A, Sharma A, Chen M, Toy R, Mottola G, Conte MS. The pro-resolving lipid mediator maresin 1 (MaR1) attenuates inflammatory signaling pathways in vascular smooth muscle and endothelial cells. PLoS ONE 2014; 9: e113480.
39. Battinelli EM, Markens BA, Italiano JE. Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood 2011; 118: 1359–69.