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Blockade of cannabinoid receptors reduces inflammation, leukocyte accumulation and neovascularization in a model of sponge-induced inflammatory angiogenesis

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Abstract

Objective

Angiogenesis depends on a complex interaction between cellular networks and mediators. The endocannabinoid system and its receptors have been shown to play a role in models of inflammation. Here, we investigated whether blockade of cannabinoid receptors may interfere with inflammatory angiogenesis.

Materials and methods

Polyester-polyurethane sponges were implanted in C57Bl/6j mice. Animals received doses (3 and 10 mg/kg/daily, s.c.) of the cannabinoid receptor antagonists SR141716A (CB1) or SR144528 (CB2). Implants were collected at days 7 and 14 for cytokines, hemoglobin, myeloperoxidase, and N-acetylglucosaminidase measurements, as indices of inflammation, angiogenesis, neutrophil and macrophage accumulation, respectively. Histological and morphometric analysis were also performed.

Results

Cannabinoid receptors expression in implants was detected from day 4 after implantation. Treatment with CB1 or CB2 receptor antagonists reduced cellular influx into sponges at days 7 and 14 after implantation, although CB1 receptor antagonist were more effective at blocking leukocyte accumulation. There was a reduction in TNF-α, VEGF, CXCL1/KC, CCL2/JE, and CCL3/MIP-1α levels, with increase in CCL5/RANTES. Both treatments reduced neovascularization. Dual blockade of cannabinoid receptors resulted in maximum inhibition of inflammatory angiogenesis.

Conclusions

Blockade of cannabinoid receptors reduced leukocyte accumulation, inflammation and neovascularization, suggesting an important role of endocannabinoids in sponge-induced inflammatory angiogenesis both via CB1 and CB2 receptors.

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References

  1. Bussolino F, Mantovani A, Persico G. Molecular mechanisms of blood vessel formation. Trends Biochem Sci. 1997;22:251–6.

    Article  PubMed  CAS  Google Scholar 

  2. Klagsbrun M, Moses MA. Molecular angiogenesis. Chem Biol. 1999;6:R217–24.

    Article  PubMed  CAS  Google Scholar 

  3. Brooks PC, Clark RA, Cheresh DA. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science. 1994;264:569–71.

    Article  PubMed  CAS  Google Scholar 

  4. Odedra R, Weiss JB. Low molecular weight angiogenesis factors. Pharmacol Ther. 1991;49:111–24.

    Article  PubMed  CAS  Google Scholar 

  5. Wang H, Keiser JA. Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ Res. 1998;83:832–40.

    Article  PubMed  CAS  Google Scholar 

  6. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–57.

    Article  PubMed  CAS  Google Scholar 

  7. Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy. 2005;4:3–8.

    Article  PubMed  CAS  Google Scholar 

  8. Lage AP, Andrade SP. Assessment of angiogenesis and tumor growth in conscious mice by a fluorimetric method. Microvasc Res. 2000;59:278–85.

    Article  PubMed  CAS  Google Scholar 

  9. Ford HR, Hoffman RA, Wing EJ, Magee DM, McIntyre L, Simmons RL. Characterization of wound cytokines in the sponge matrix model. Arch Surg. 1989;124:1422–8.

    Article  PubMed  CAS  Google Scholar 

  10. Andrade SP, Bakhle YS, Hart I, Piper PJ. Effects of tumour cells on angiogenesis and vasoconstrictor responses in sponge implants in mice. Br J Cancer. 1992;66:821–6.

    Article  PubMed  CAS  Google Scholar 

  11. Barcelos LS, Coelho AM, Russo RC, Guabiraba R, Souza AL, Bruno-Lima G Jr. et al. Role of the chemokines CCL3/MIP-1alpha and CCL5/RANTES in sponge-induced inflammatory angiogenesis in mice. Microvasc Res. 2009;78(2):148–54.

    Article  PubMed  CAS  Google Scholar 

  12. Barcelos LS, Talvani A, Teixeira AS, Cassali GD, Andrade SP, Teixeira MM. Production and in vivo effects of chemokines CXCL1-3/KC and CCL2/JE in a model of inflammatory angiogenesis in mice. Inflamm Res. 2004;53:576–84.

    Article  PubMed  CAS  Google Scholar 

  13. Barcelos LS, Talvani A, Teixeira AS, Vieira LQ, Cassali GD, Andrade SP, et al. Impaired inflammatory angiogenesis, but not leukocyte influx, in mice lacking TNFR1. J Leukoc Biol. 2005;78:352–8.

    Article  PubMed  CAS  Google Scholar 

  14. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 1990;346:561–4.

    Article  PubMed  CAS  Google Scholar 

  15. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 1993;365:61–5.

    Article  PubMed  CAS  Google Scholar 

  16. Mechoulam R, Fride E, Di Marzo V. Endocannabinoids. Eur J Pharmacol. 1998;359:1–18.

    Article  PubMed  CAS  Google Scholar 

  17. Guindon J, Hohmann AG. The endocannabinoid system and cancer: therapeutic implication. Br J Pharmacol. 2011;163:1447–63.

    Article  PubMed  CAS  Google Scholar 

  18. Smith TH, Sim-Selley LJ, Selley DE. Cannabinoid CB1 receptor-interacting proteins: novel targets for central nervous system drug discovery? Br J Pharmacol. 2010;160:454–66.

    Article  PubMed  CAS  Google Scholar 

  19. Cristino L, de Petrocellis L, Pryce G, Baker D, Guglielmotti V, Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience. 2006;139:1405–15.

    Article  PubMed  CAS  Google Scholar 

  20. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriere D, Carayon P, et al. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem. 1995;232:54–61.

    Article  PubMed  CAS  Google Scholar 

  21. Kishimoto S, Gokoh M, Oka S, Muramatsu M, Kajiwara T, Waku K, et al. 2-arachidonoylglycerol induces the migration of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes through the cannabinoid CB2 receptor-dependent mechanism. J Biol Chem. 2003;278:24469–75.

    Article  PubMed  CAS  Google Scholar 

  22. Jorda MA, Verbakel SE, Valk PJ, Vankan-Berkhoudt YV, Maccarrone M, Finazzi-Agro A, et al. Hematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol. Blood. 2002;99:2786–93.

    Article  PubMed  CAS  Google Scholar 

  23. Kishimoto S, Kobayashi Y, Oka S, Gokoh M, Waku K, Sugiura T. 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces accelerated production of chemokines in HL-60 cells. J Biochem. 2004;135:517–24.

    Article  PubMed  CAS  Google Scholar 

  24. Gokoh M, Kishimoto S, Oka S, Mori M, Waku K, Ishima Y, et al. 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces rapid actin polymerization in HL-60 cells differentiated into macrophage-like cells. Biochem J. 2005;386:583–9.

    Article  PubMed  CAS  Google Scholar 

  25. Oka S, Wakui J, Ikeda S, Yanagimoto S, Kishimoto S, Gokoh M, et al. Involvement of the cannabinoid CB2 receptor and its endogenous ligand 2-arachidonoylglycerol in oxazolone-induced contact dermatitis in mice. J Immunol. 2006;177:8796–805.

    PubMed  CAS  Google Scholar 

  26. Zoratti C, Kipmen-Korgun D, Osibow K, Malli R, Graier WF. Anandamide initiates Ca(2 +) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br J Pharmacol. 2003;140:1351–62.

    Article  PubMed  CAS  Google Scholar 

  27. Zhang X, Maor Y, Wang JF, Kunos G, Groopman JE. Endocannabinoid-like N-arachidonoyl serine is a novel pro-angiogenic mediator. Br J Pharmacol. 2010;160:1583–94.

    Article  PubMed  CAS  Google Scholar 

  28. Bifulco M, Di Marzo V. Targeting the endocannabinoid system in cancer therapy: a call for further research. Nat Med. 2002;8:547–50.

    Article  PubMed  CAS  Google Scholar 

  29. Bouaboula M, Perrachon S, Milligan L, Canat X, Rinaldi-Carmona M, Portier M, et al. A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. Evidence for a new model of receptor/ligand interactions. J Biol Chem. 1997;272:22330–9.

    Article  PubMed  CAS  Google Scholar 

  30. Shire D, Calandra B, Bouaboula M, Barth F, Rinaldi-Carmona M, Casellas P, et al. Cannabinoid receptor interactions with the antagonists SR 141716A and SR 144528. Life Sci. 1999;65:627–35.

    Article  PubMed  CAS  Google Scholar 

  31. Bouaboula M, Dussossoy D, Casellas P. Regulation of peripheral cannabinoid receptor CB2 phosphorylation by the inverse agonist SR 144528. Implications for receptor biological responses. J Biol Chem. 1999;274:20397–405.

    Article  PubMed  CAS  Google Scholar 

  32. Rhee MH, Kim SK. SR144528 as inverse agonist of CB2 cannabinoid receptor. J Vet Sci. 2002;3:179–84.

    PubMed  Google Scholar 

  33. Gelderblom H, Verweij J, Nooter K, Sparreboom A, Cremophor EL, The drawbacks and advantages of vehicle selection for drug formulation. Eur J Cancer. 2001;37:1590–8.

    Article  PubMed  CAS  Google Scholar 

  34. Costa B, Trovato AE, Colleoni M, Giagnoni G, Zarini E, Croci T. Effect of the cannabinoid CB1 receptor antagonist, SR141716, on nociceptive response and nerve demyelination in rodents with chronic constriction injury of the sciatic nerve. Pain. 2005;116:52–61.

    Article  PubMed  CAS  Google Scholar 

  35. Lim SY, Davidson SM, Yellon DM, Smith CCT. The cannabinoid CB1 receptor antagonist, rimonabant, protects against acute myocardial infarction. Basic Res Cardiol. 2009;104:781–92.

    Article  PubMed  CAS  Google Scholar 

  36. Smith SR, Terminelli C, Denhardt G. Effects of cannabinoid receptor agonist and antagonist ligands on production of inflammatory cytokines and anti-inflammatory interleukin-10 in endotoxemic mice. J pharmacol Exp Ther. 2000;293:136–50.

    PubMed  CAS  Google Scholar 

  37. Sugamura K, Sugiyama S, Fujiwara Y, Matsubara J, Akiyama E, Maeda H, et al. Cannabinoid 1 receptor blockade reduces atherosclerosis with enhances reverse cholesterol transport. J Atheroscler Thromb. 2010;17:141–7.

    Article  PubMed  CAS  Google Scholar 

  38. Conti S, Costa B, Colleoni M, Parolaro D, Giagnoni G. Antiinflammatory action of endocannabinoid palmitoylethanolamide and the synthetic cannabinoid nabilone in a model of acute inflammation in the rat. Br J Pharmacol. 2002;135:181–7.

    Article  PubMed  CAS  Google Scholar 

  39. Croci T, Landi M, Galzin A-M, Marini P. Role of cannabinoid CB1 receptors and tumor necrosis factor-alpha in the gut and systemic anti-inflammatory activity of SR 141716 (rimonabant) in rodents. Br J Pharmacol. 2003;140:115–22.

    Article  PubMed  CAS  Google Scholar 

  40. Hu DE, Hiley CR, Smither RL, Gresham GA, Fan TP. Correlation of 133Xe clearance, blood flow and histology in the rat sponge model for angiogenesis. Further studies with angiogenic modifiers. Lab Invest. 1995;72:601–10.

    PubMed  CAS  Google Scholar 

  41. Machado RD, Santos RA, Andrade SP. Opposing actions of angiotensins on angiogenesis. Life Sci. 2000;66:67–76.

    Article  PubMed  CAS  Google Scholar 

  42. Ferreira MA, Barcelos LS, Campos PP, Vasconcelos AC, Teixeira MM, Andrade SP. Sponge-induced angiogenesis and inflammation in PAF receptor-deficient mice (PAFR-KO). Br J Pharmacol. 2004;141:1185–92.

    Article  PubMed  CAS  Google Scholar 

  43. Bertini R, Barcelos LS, Beccari AR, Cavalieri B, Moriconi A, Bizzarri C, et al. Receptor binding mode and pharmacological characterization of a potent and selective dual CXCR1/CXCR2 non-competitive allosteric inhibitor. Br J Pharmacol. 2012;165:436–54.

    Article  PubMed  CAS  Google Scholar 

  44. Smith SR, Terminelli C, Denhardt G. Modulation of cytokine responses in Corynebacterium parvum-primed endotoxemic mice by centrally administered cannabinoid ligands. Eur J Pharmacol. 2001;425:73–83.

    Article  PubMed  CAS  Google Scholar 

  45. Smith SR, Denhardt G, Terminelli C. The anti-inflammatory activities of cannabinoid receptor ligands in mouse peritonitis models. Eur J Pharmacol. 2001;432:107–19.

    Article  PubMed  CAS  Google Scholar 

  46. Sacerdote P, Massi P, Panerai AE, Parolaro D. In vivo and in vitro treatment with the synthetic cannabinoid CP55, 940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J Neuroimmunol. 2000;109:155–63.

    Article  PubMed  CAS  Google Scholar 

  47. Massi P, Fuzio D, Vigano D, Sacerdote P, Parolaro D. Relative involvement of cannabinoid CB(1) and CB(2) receptors in the Delta(9)-tetrahydrocannabinol-induced inhibition of natural killer activity. Eur J Pharmacol. 2000;387:343–7.

    Article  PubMed  CAS  Google Scholar 

  48. Sugamura K, Sugiyama S, Nozaki T, Matsuzawa Y, Izumiya Y, Miyata K, et al. Activated endocannabinoid system in coronary artery disease and antiinflammatory effects of cannabinoid 1 receptor blockade on macrophages. Circulation. 2009;119:28–36.

    Article  PubMed  CAS  Google Scholar 

  49. Schafer A, Pfrang J, Neumuller J, Fiedler S, Ertl G, Bauersachs J. The cannabinoid receptor-1 antagonist rimonabant inhibits platelet activation and reduces pro-inflammatory chemokines and leukocytes in Zucker rats. Br J Pharmacol. 2008;154:1047–54.

    Article  PubMed  CAS  Google Scholar 

  50. Strieter RM, Burdick MD, Gomperts BN, Belperio JA, Keane MP. CXC chemokines in angiogenesis. Cytokine Growth Factor Rev. 2005;16:593–609.

    Article  PubMed  CAS  Google Scholar 

  51. Russo RC, Guabiraba R, Garcia CC, Barcelos LS, Roffe E, Souza AL, et al. Role of the chemokine receptor CXCR2 in bleomycin-induced pulmonary inflammation and fibrosis. Am J Respir Cell Mol Biol. 2009;40:410–21.

    Article  PubMed  CAS  Google Scholar 

  52. Li A, Varney ML, Valasek J, Godfrey M, Dave BJ, Singh RK. Autocrine role of interleukin-8 in induction of endothelial cell proliferation, survival, migration and MMP-2 production and angiogenesis. Angiogenesis. 2005;8:63–71.

    Article  PubMed  CAS  Google Scholar 

  53. Scapini P, Calzetti F, Cassatella MA. On the detection of neutrophil-derived vascular endothelial growth factor (VEGF). J Immunol Methods. 1999;232:121–9.

    Article  PubMed  CAS  Google Scholar 

  54. Robertson M, Liversidge J, Forrester JV, Dick AD. Neutralizing tumor necrosis factor-alpha activity suppresses activation of infiltrating macrophages in experimental autoimmune uveoretinitis. Invest Ophthalmol Vis Sci. 2003;44:3034–41.

    Article  PubMed  Google Scholar 

  55. Belo AV, Leles F, Barcelos LS, Ferreira MA, Bakhle YS, Teixeira MM, et al. Murine chemokine CXCL2/KC is a surrogate marker for angiogenic activity in the inflammatory granulation tissue. Microcirculation. 2005;12:597–606.

    Article  PubMed  CAS  Google Scholar 

  56. Vallien G, Langley R, Jennings S, Specian R, Granger DN. Expression of endothelial cell adhesion molecules in neovascularized tissue. Microcirculation. 2000;7:249–58.

    PubMed  CAS  Google Scholar 

  57. Pisanti S, Bifulco M. Endocannabinoid system modulation in cancer biology and therapy. Pharmacol Res. 2009;60:107–16.

    Article  PubMed  CAS  Google Scholar 

  58. Oka S, Ikeda S, Kishimoto S, Gokoh M, Yanagimoto S, Waku K, et al. 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces the migration of EoL-1 human eosinophilic leukemia cells and human peripheral blood eosinophils. J Leukoc Biol. 2004;76:1002–9.

    Article  PubMed  CAS  Google Scholar 

  59. Deusch E, Kraft B, Nahlik G, Weigl L, Hohenegger M, Kress HG. No evidence for direct modulatory effects of delta 9-tetrahydrocannabinol on human polymorphonuclear leukocytes. J Neuroimmunol. 2003;141:99–103.

    Article  PubMed  CAS  Google Scholar 

  60. Kurihara R, Tohyama Y, Matsusaka S, Naruse H, Kinoshita E, Tsujioka T, et al. Effects of peripheral cannabinoid receptor ligands on motility and polarization in neutrophil-like HL60 cells and human neutrophils. J Biol Chem. 2006;281:12908–18.

    Article  PubMed  CAS  Google Scholar 

  61. McCourt M, Wang JH, Sookhai S, Redmond HP. Proinflammatory mediators stimulate neutrophil-directed angiogenesis. Arch Surg. 1999;134:1325–31.

    Article  PubMed  CAS  Google Scholar 

  62. Kasama T, Shiozawa F, Kobayashi K, Yajima N, Hanyuda M, Takeuchi HT, et al. Vascular endothelial growth factor expression by activated synovial leukocytes in rheumatoid arthritis: critical involvement of the interaction with synovial fibroblasts. Arthritis Rheum. 2001;44:2512–24.

    Article  PubMed  CAS  Google Scholar 

  63. Malinowska B, Baranowska-Kuczko M, Schlicker E. Triphasic blood pressure responses to cannabinoids: do we understand the mechanism? Br J Pharmacol. 2012;165:2073–88.

    Article  PubMed  CAS  Google Scholar 

  64. De Filippis D, Russo A, De Stefano D, Maiuri MC, Esposito G, Cinelli MP, et al. Local administration of WIN 55,212–2 reduces chronic granuloma-associated angiogenesis in rat by inhibiting NF-kappaB activation. J Mol Med (Berl). 2007;85:635–45.

    Article  Google Scholar 

  65. Solinas M, Massi P, Cantelmo AR, Cattaneo MG, Cammarota R, Bartolini D, et al. Cannabidiol inhibits angiogenesis by multiple mechanisms. Br J Pharmacol. 2012;167:1218–31.

    Article  PubMed  CAS  Google Scholar 

  66. Wu DF, Yang LQ, Goschke A, Stumm R, Brandenburg LO, Liang YJ, et al. Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J Neurochem. 2008;104:1132–43.

    Article  PubMed  CAS  Google Scholar 

  67. Romero J, Berrendero F, Garcia-Gil L, Ramos JA, Fernandez-Ruiz JJ. Cannabinoid receptor and WIN-55,212–2-stimulated [35S]GTP gamma S binding and cannabinoid receptor mRNA levels in the basal ganglia and the cerebellum of adult male rats chronically exposed to delta 9-tetrahydrocannabinol. J Mol Neurosci. 1998;11:109–19.

    Article  PubMed  CAS  Google Scholar 

  68. Romero J, Berrendero F, Garcia-Gil L, de la Cruz P, Ramos JA, Fernandez-Ruiz JJ. Loss of cannabinoid receptor binding and messenger RNA levels and cannabinoid agonist-stimulated [35S]guanylyl-5′O-(thio)-triphosphate binding in the basal ganglia of aged rats. Neuroscience. 1998;84:1075–83.

    Article  PubMed  CAS  Google Scholar 

  69. Barcelos LS, Coelho AM, Russo RC, Guabiraba R, Souza AL, Bruno-Lima G Jr, et al. Role of the chemokines CCL3/MIP-1 alpha and CCL5/RANTES in sponge-induced inflammatory angiogenesis in mice. Microvasc Res. 2009;78:148–54.

    Article  PubMed  CAS  Google Scholar 

  70. Ahuja SK, Gao JL, Murphy PM. Chemokine receptors and molecular mimicry. Immunol Today. 1994;15:281–7.

    Article  PubMed  CAS  Google Scholar 

  71. Boshoff C, Endo Y, Collins PD, Takeuchi Y, Reeves JD, Schweickart VL, et al. Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science. 1997;278:290–4.

    Article  PubMed  CAS  Google Scholar 

  72. Jensen KK, Lira SA. Chemokines and Kaposi’s sarcoma. Semin Cancer Biol. 2004;14:187–94.

    Article  PubMed  CAS  Google Scholar 

  73. Chen S, Bacon KB, Li L, Garcia GE, Xia Y, Lo D, et al. In vivo inhibition of CC and CX3C chemokine-induced leukocyte infiltration and attenuation of glomerulonephritis in Wistar-Kyoto (WKY) rats by vMIP-II. J Exp Med. 1998;188:193–8.

    Article  PubMed  CAS  Google Scholar 

  74. Raborn ES, Marciano-Cabral F, Buckley NE, Martin BR, Cabral GA. The cannabinoid delta-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: linkage to the CB2 receptor. J Neuroimmune Pharmacol. 2008;3:117–29.

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by research grants of Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq, Brazil) and Fundacao do Amparo a Pesquisas do Estado de Minas Gerais (FAPEMIG, Brazil). We are grateful to Prof. Frederico M. Soriani (UFMG) for his helpful technical assistance.

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Authors and Affiliations

  1. Departamento de Bioquímica e Imunologia-ICB, Universidade Federal de Minas Gerais (UFMG), Av. Antônio Carlos, 6627. Pampulha, 31270-901, Belo Horizonte, MG, Brazil

    Rodrigo Guabiraba, Remo C. Russo, Amanda M. Coelho, Luciola S. Barcelos & Mauro M. Teixeira

  2. Departamento de Fisiologia e Biofísica-ICB, Universidade Federal de Minas Gerais (UFMG), Av. Antônio Carlos, 6627. Pampulha, 31270-901, Belo Horizonte, MG, Brazil

    Remo C. Russo, Amanda M. Coelho, Gabriel A. O. Lopes, Ariane K. C. Gomes, Silvia P. Andrade & Luciola S. Barcelos

  3. Departamento de Patologia Geral-ICB, Universidade Federal de Minas Gerais (UFMG), Av. Antônio Carlos, 6627. Pampulha, 31270-901, Belo Horizonte, MG, Brazil

    Mônica A. N. D. Ferreira

  4. Institute of Infection, Immunity and Inflammation, Glasgow Biomedical Research Centre, University of Glasgow, 120 University Place, Glasgow, G12 8TA, UK

    Rodrigo Guabiraba

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  1. Rodrigo Guabiraba
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Correspondence to Rodrigo Guabiraba or Mauro M. Teixeira.

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Guabiraba, R., Russo, R.C., Coelho, A.M. et al. Blockade of cannabinoid receptors reduces inflammation, leukocyte accumulation and neovascularization in a model of sponge-induced inflammatory angiogenesis. Inflamm. Res. 62, 811–821 (2013). https://doi.org/10.1007/s00011-013-0638-8

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