Lipoxin A4 selectively programs the profile of M2 tumor-associated macrophages which favour control of tumor progression

International Journal of Cancer

Volumn 140, Issue 2, 2017, Pages 346-357

  Simoes R L ^a   De Brito, N M ^a   Cunha Costa, H ^a   Morandi, V ^a   Fierro, I M ^a   Roitt, I M ^b   Barja Fidalgo, C ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b MIDDLESEX UNIVERSITY   (United Kingdom)

Author keywords

inflammation; lipoxin; macrophage; tumor

Indexed keywords

ARGINASE; BIOLOGICAL MARKER; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOXIN; LIPOXIN A; NITROGEN OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL; APOPTOSIS; C57BL MOUSE; DISEASE COURSE; DOWN REGULATION; DRUG EFFECTS; HUMAN; MACROPHAGE; MELANOMA; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; APOPTOSIS; ARGINASE; BIOMARKERS; DISEASE PROGRESSION; DOWN-REGULATION; HUMANS; LIPOXINS; MACROPHAGES; MELANOMA; MICE; MICE, INBRED C57BL; NADPH OXIDASE; NITRIC OXIDE SYNTHASE TYPE II; NITROGEN OXIDES; REACTIVE OXYGEN SPECIES;

EID: 84995960006     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30424     Document Type: Article

References (48)

1. Mantovani A, Allavena P, Sica AF, et al. Cancer-related inflammation. Nature 2008; 454:436–44.
2. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007; 117:1155–66.
3. Mantovani A, Bottazzi B, Colotta FL, et al. The origin and function of tumor associated macrophages. Immunol Today 1992; 13:265–70.
4. Condeelis J, Pollard JW. Macrophages, obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006; 124:263–6.
5. Rőszer T. Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms. Mediators Inflamm 2015.
6. Murray PJ, Allen JE, Biswas SK, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014; 1741:14–20.
7. Mantovani A. Reflections on immunological nomenclature: in praise of imperfection. Nat Immunology 2016; 17:215–16.
8. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunology 2010; 11:889–96.
9. Mills CD. M1 and M2 Macrophages: oracles of health and disease. Crit Rev Immunol 2012; 32:463–88.
10. Sica A, Larghi P, Mancino A, et al. Macrophagepolarization in tumourprogression. Semin Cancer Biol 2008; 18:349–55.
11. Dinapoli MR, Calderon CL, Lopez DM. The altered tumoricidal capacity of macrophages isolated from tumor-bearing mice is related to reduced expression of the inducible nitric oxide synthase gene. J Exp Med 1996; 183:1323–29.
12. Lissbrant IF, Stattin P, Wikstrom P, et al. Tumor associated macrophages in human prostate cancer: relation to clinic pathological variables and survival. Int J Oncol 2000; 17:445–51.
13. Nishie A, Ono M, Shono T, et al. Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin Cancer Res 1999; 5:1107–13.
14. Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004; 351:2159–69.
15. Serhan CN, Hamberg M, Samuelsson B. Lipoxins, a novel series of biologically active compounds formed from arachidonic acid in human leukocytes. PNAS USA 1984; 81:5335–39.
16. Fierro IM, Serhan CN. Mechanisms in anti-inflammation and resolution, the role of lipoxins and aspirin-triggered lipoxins. Braz J Med Biol Res 2001; 34:555–66.
17. Claria J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. PNAS USA 1995; 92:9475–79.
18. 4 receptor. J Exp Med 1994; 180:253–60.
19. 4 synthetic analog. J Immunol 2005; 175:1843–50.
20. 4 inhibits human monocyte apoptosis, involvement of ERK-2 and PI3-kinase. Prostaglandins Other Lipid Mediat 2010; 91:10–17.
21. Godson C, Mitchell S, Harvey K, et al. Cutting edge, lipoxins rapidly stimulate non-phlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 2000; 15:1663–67.
22. Stenke L, Nasman-Glaser B, Edenius C, et al. Lipoxygenase products in myeloproliferative disorders, increased leukotriene C4 and decreased lipoxin formation in chronic myeloid leukemia. Adv Prostaglandin Thromboxane Leukot Res 1991; 21:883–86.
23. Stenke L, Edenius C, Samuelsson J, et al. Deficient lipoxin synthesis, a novel platelet dysfunction in myeloproliferative disorders with special reference to blastic crisis of chronic myelogenous leukemia. Blood 1991; 78:2989–995.
24. Citelli MM, Bittencourt LL, da Silva SV, et al. Vitamin A modulates the expression of genes involved in iron bioavailability. Bio. Trace Elem Res 2012; 149:64–70.
25. Silva SV, Garcia-Souza EP, Moura AS, et al. Maternal protein restriction during early lactation induces changes on neutrophil activation and TNF-alpha production of adult offspring. Inflammation 2010; 33:65–75.
26. 4 inhibits neutrophil apoptosis via NADPH oxidase activity: Redox control of NF-κB pathway and mitochondrial stability. BiochimBiophysActa 2012; 1823:1990–97.
27. Mhaidat NM, Wang YF, Kiejda KA, et al. Docetaxel-induced apoptosis in melanoma cells is dependent on activation of caspase-2. Mol Cancer Ther 2007; 6:752–61.
28. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–54.
29. Laoui D, MovahediK Van Overmeire E, et al. Tumor-associated macrophages in breast cancer, distinct subsets, distinct functions. Int J Dev Biol 2011; 55:861–7.
30. Odegaard JI, Chawla A. Mechanisms of macrophage activation in obesity-induced insulin resistance. Nat Clin Pract Endocrin Metab 2008; 11:619–26.
31. Laskin JD, Heck DE, Laskin DL. Nitric oxide pathways in toxic responses. In: Ballantyne R, Marrs T, Syversen T, General and Applied Toxicology. New Jersey: B. Hoboken 2009: pp. 425–38.
32. Li Y, Cai L, Wang H, et al. Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 2011; 30:3887–99.
33. Vasconcelos DP, Costa M, Amaral IF, et al. Modulation of the inflammatory response to chitosan through M2 macrophage polarization using pro-resolution mediators. Biomaterials 2014; 37:116–23.
34. Mertz PM, DeWitt DL, Stetler-Stevenson WG, et al. Interleukin 10 suppression of monocyte prostaglandin H synthase 2: Mechanism of inhibition of prostaglandin-dependent matrix metalloproteinase production. J Biol Chem 1994; 269:21322–29.
35. Cunha FQ, Moncada S, Liew FY. Interleukin-10 inhibits the induction of nitric oxide synthase by interferon gamma in murine macrophages. Biochem Biophys Res Commun 2003; 182:1155–59.
36. D'Andrea A, Aste-Amezaga M, Valiante NM, et al. Interleukin-10 inhibits human lymphocyte interferon gamma production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 2003; 178:1041–48.
37. 4 and annexin-1 for the production of IL-10 and inflammatory hyporesponsiveness in mice. J Immunol 2007; 179:8533–43.
38. 4 impairment of apoptotic signaling in macrophages: implication of the PI3K/Akt and the ERK/Nrf-2 defense pathways. Cell Death Differ 2010; 17:1179–88.
39. Lee HN, Surh YJ. Resolvin D1-mediated NOX2 inactivation rescues macrophages undertaking efferocytosis from oxidative stress-induced apoptosis. Biochem Pharmacol 2013; 86:759–69.
40. 4 inhibit peroxynitrite formation, NF-kB and AP-1 activation, and IL-8 gene expression in human leukocytes. PNAS USA 2002; 99:13266–71.
41. Okada H, Mak TW. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 2004; 4:592–603.
42. Vousden KH, Lu X. Live or let die, the cell's response to p53. Nat Rev Cancer 2002; 2:594–604.
43. Weis SM, Cheresh DA. Tumour angiogenesis: molecular pathways and therapeutic targets. Nat Med 2011; 17:1359–70.
44. 4. J Pharmacol Exp Ther 2002; 300:385–92.
45. 4, is a potent inhibitor of several steps in angiogenesis induced by vascular endothelial growth factor. Br J Pharmacol 2008; 153:956–65.
46. Abiru S, Nakao K, Ichikawa T, et al. Aspirin and NS-398 inhibit hepatocyte growth factor-induced invasiveness of human hepatoma cells. Hepatology 2002; 35:1117–24.
47. Tsujii M, Kawano S, DuBois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. PNAS USA 1997; 94:3336–40.
48. Clària J, Lee MH, Serhan CN. Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation. Mol Med 1996; 2:583–96.