Targeting formyl peptide receptor 2 reduces leukocyteendothelial interactions in a murine model of stroke

FASEB Journal

Volumn 29, Issue 5, 2015, Pages 2161-2171

  Smith, Helen K ^a,b   Gil, Cristiane Damas ^c   Oliani, Sonia M ^c   Gavins, Felicity N E ^a,b  

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

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Annexin A1; FPR2 ALX; Inflammation; Ischemia reperfusion

Indexed keywords

15 EPIMER LIPOXIN A 4; ANNEXIN A1 [AC2-26]; ANTIINFLAMMATORY AGENT; LIPOXIN RECEPTOR; PEPTIDE; UNCLASSIFIED DRUG; ANNEXIN A1, MOUSE; FORMYL PEPTIDE RECEPTOR 2, MOUSE; FORMYLPEPTIDE RECEPTOR; HSH2 PROTEIN, MOUSE; LIPOCORTIN 1; PEPTIDE FRAGMENT; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN MICROCIRCULATION; CELL INTERACTION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DRUG EFFICACY; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; LEUKOCYTE ADHERENCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; STEREOCHEMISTRY; ANIMAL; C57BL MOUSE; CAROTID ARTERY DISEASES; CELL ADHESION; CELL CULTURE; CYTOLOGY; DISEASE MODEL; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; MICROVASCULATURE; NEUTROPHIL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ANIMALIA; MURINAE; MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANNEXIN A1; BLOTTING, WESTERN; CAROTID ARTERY DISEASES; CELL ADHESION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; INFLAMMATION; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MICROVESSELS; NEUTROPHILS; PEPTIDE FRAGMENTS; RECEPTORS, FORMYL PEPTIDE; REPERFUSION INJURY; STROKE;

EID: 84932606300     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-263160     Document Type: Article

References (49)

1. Yenari, M. A., Kauppinen, T. M., and Swanson, R. A. (2010) Microglial activation in stroke: therapeutic targets. Neurotherapeutics 7, 378-391
2. Van Lookeren Campagne, M., Thomas, G. R., Thibodeaux, H., Palmer, J. T., Williams, S. P., Lowe, D. G., and Van Bruggen, N. (1999) Secondary reduction in the apparent diffusion coefficient of water, increase in cerebral blood volume, and delayed neuronal death after middle cerebral artery occlusion and early reperfusion in the rat. J. Cereb. Blood Flow Metab. 19, 1354-1364
3. Matsuo, Y., Onodera, H., Shiga, Y., Shozuhara, H., Ninomiya, M., Kihara, T., Tamatani, T., Miyasaka, M., and Kogure, K. (1994) Role of cell adhesion molecules in brain injury after transient middle cerebral artery occlusion in the rat. Brain Res. 656, 344-352
4. Zhang, R. L., Chopp, M., Zaloga, C., Zhang, Z. G., Jiang, N., Gautam, S. C., Tang, W. X., Tsang, W., Anderson, D. C., and Manning, A. M. (1995) The temporal profiles of ICAM-1 protein and mRNA expression after transient MCA occlusion in the rat. Brain Res. 682, 182-188
5. Prestigiacomo, C. J., Kim, S. C., Connolly, Jr., E. S., Liao, H., Yan, S. F., and Pinsky, D. J. (1999) CD18-mediated neutrophil recruitment contributes to the pathogenesis of reperfused but not nonreperfused stroke. Stroke 30, 1110-1117
6. Okada, Y., Copeland, B. R., Mori, E., Tung, M. M., Thomas, W. S., and Del Zoppo, G. J. (1994) P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 25, 202-211
7. Liesz, A., Hagmann, S., Zschoche, C., Adamek, J., Zhou, W., Sun, L., Hug, A., Zorn, M., Dalpke, A., Nawroth, P., and Veltkamp, R. (2009) The spectrum of systemic immune alterations after murine focal ischemia: immunodepression versus immunomodulation. Stroke 40, 2849-2858
8. Gavins, F. N., Dalli, J., Flower, R. J., Granger, D. N., and Perretti, M. (2007) Activation of the annexin 1 counter-regulatory circuit affords protection in the mouse brain microcirculation. FASEB J. 21, 1751-1758
9. Le, Y., Murphy, P. M., and Wang, J. M. (2002) Formyl-peptide receptors revisited. Trends Immunol. 23, 541-548
10. Maderna, P., Cottell, D. C., Toivonen, T., Dufton, N., Dalli, J., Perretti, M., and Godson, C. (2010) FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J. 24, 4240-4249
11. Devosse, T., Guillabert, A., D'Haene, N., Berton, A., De Nadai, P., Noel, S., Brait, M., Franssen, J. D., Sozzani, S., Salmon, I., and Parmentier, M. (2009) Formyl peptide receptor-like 2 is expressed and functional in plasmacytoid dendritic cells, tissue-specific macrophage subpopulations, and eosinophils. J. Immunol. 182, 4974-4984
12. Cooray, S. N., Gobbetti, T., Montero-Melendez, T., McArthur, S., Thompson, D., Clark, A. J., Flower, R. J., and Perretti, M. (2013) Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses. Proc. Natl. Acad. Sci. USA 110, 18232-18237
13. Dufton, N., Hannon, R., Brancaleone, V., Dalli, J., Patel, H. B., Gray, M., D'Acquisto, F., Buckingham, J. C., Perretti, M., and Flower, R. J. (2010) Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J. Immunol. 184, 2611-2619
14. Yan, B. Y., Pan, C. S., Mao, X. W., Yang, L., Liu, Y. Y., Yan, L., Mu, H. N., Wang, C. S., Sun, K., Liao, F. L., Fan, J. Y., Wang, X. M., and Han, J. Y. (2014) Icariside II improves cerebral microcirculatory disturbance and alleviates hippocampal injury in gerbils after ischemia-reperfusion. Brain Res. 1573, 63-73
15. Patel, F. J., Volkmann, D. T., Taylor, G. W., Hansson, M. A., Anderson, J. F., Zhou, Y., Scoazec, L. M., Hartford, C. V., and Hainz, D. L. (2014) IL-37 reduces inflammatory response after cerebral ischemia and reperfusion injury through down-regulation of pro-inflammatory cytokines. Cytokine 69, 234-239
16. Yang, G., Kitagawa, K., Matsushita, K., Mabuchi, T., Yagita, Y., Yanagihara, T., and Matsumoto, M. (1997) C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Res. 752, 209-218
17. Murakami, K., Kondo, T., Kawase, M., and Chan, P. H. (1998) The development of a new mouse model of global ischemia: focus on the relationships between ischemia duration, anesthesia, cerebral vasculature, and neuronal injury following global ischemia in mice. Brain Res. 780, 304-310
18. Pascual, J. L., Murcy, M. A., Li, S., Gong, W., Eisenstadt, R., Kumasaka, K., Sims, C., Smith, D. H., Browne, K., Allen, S., and Baren, J. (2013) Neuroprotective effects of progesterone in traumatic brain injury: blunted in vivo neutrophil activation at the blood-brain barrier. Am. J. Surg. 206, 840-845, discussion 845-846
19. Gavins, F. N., Hughes, E. L., Buss, N. A., Holloway, P. M., Getting, S. J., and Buckingham, J. C. (2012) Leukocyte recruitment in the brain in sepsis: involvement of the annexin 1-FPR2/ALX antiinflammatory system. FASEB J. 26, 4977-4989
20. Todd, N. V., Picozzi, P., Crockard, H. A., and Russell, R. R. (1986) Reperfusion after cerebral ischemia: influence of duration of ischemia. Stroke 17, 460-466
21. Rezkalla, S. H., and Kloner, R. A. (2002) No-reflow phenomenon. Circulation 105, 656-662
22. Abbott, N. J. (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J. Anat. 200, 629-638
23. Tikka, T. M., and Koistinaho, J. E. (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 166, 7527-7533
24. Hoyte, L. C., Brooks, K. J., Nagel, S., Akhtar, A., Chen, R., Mardiguian, S., McAteer, M. A., Anthony, D. C., Choudhury, R. P., Buchan, A. M., and Sibson, N. R. (2010) Molecular magnetic resonance imaging of acute vascular cell adhesion molecule-1 expression in a mouse model of cerebral ischemia. J. Cereb. Blood Flow Metab. 30, 1178-1187
25. Ishikawa, M., Cooper, D., Russell, J., Salter, J. W., Zhang, J. H., Nanda, A., and Granger, D. N. (2003) Molecular determinants of the prothrombogenic and inflammatory phenotype assumed by the postischemic cerebral microcirculation. Stroke 34, 1777-1782
26. Ishikawa, M., Sekizuka, E., Yamaguchi, N., Nakadate, H., Terao, S., Granger, D. N., and Minamitani, H. (2007) Angiotensin II type 1 receptor signaling contributes to platelet-leukocyteendothelial cell interactions in the cerebral microvasculature. Am. J. Physiol. Heart Circ. Physiol. 292, H2306-H2315
27. Wellons III, J. C., Sheng, H., Laskowitz, D. T., Mackensen, G. B., Pearlstein, R. D., and Warner, D. S. (2000) A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Res. 868, 14-21
28. Kitagawa, K., Matsumoto, M., Yang, G., Mabuchi, T., Yagita, Y., Hori, M., and Yanagihara, T. (1998) Cerebral ischemia after bilateral carotid artery occlusion and intraluminal suture occlusion in mice: evaluation of the patency of the posterior communicating artery. J. Cereb. Blood Flow Metab. 18, 570-579
29. Yrjanheikki, J., Keinanen, R., Pellikka, M., Hokfelt, T., and Koistinaho, J. (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. USA 95, 15769-15774
30. Yenari, M. A., Xu, L., Tang, X. N., Qiao, Y., and Giffard, R G. (2006) Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 37, 1087-1093
31. Riazi, K., Galic, M. A., Kuzmiski, J. B., Ho, W., Sharkey, K. A., and Pittman, Q. J. (2008) Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation. Proc. Natl. Acad. Sci. USA 105, 17151-17156
32. Biscaro, B., Lindvall, O., Tesco, G., Ekdahl, C. T., and Nitsch, R. M. (2012) Inhibition of microglial activation protects hippocampal neurogenesis and improves cognitive deficits in a transgenic mouse model for Alzheimer's disease. Neurodegener. Dis. 9, 187-198
33. Zhang, L., and Zhao, J. (2014) Profile of minocycline and its potential in the treatment of schizophrenia. Neuropsychiatr. Dis. Treat. 10, 1103-1111
34. De Coupade, C., Solito, E., and Levine, J. D. (2003) Dexamethasone enhances interaction of endogenous annexin 1 with L-selectin and triggers shedding of L-selectin in the monocytic cell line U-937. Br. J. Pharmacol. 140, 133-145
35. Strausbaugh, H. J., and Rosen, S. D. (2001) Apotential role for annexin 1 as a physiologic mediator of glucocorticoid-induced L-selectin shedding from myeloid cells. J. Immunol. 166, 6294-6300
36. Fierro, I. M., Colgan, S. P., Bernasconi, G., Petasis, N. A., Clish, C. B., Arita, M., and Serhan, C. N. (2003) Lipoxin A4 and aspirintriggered 15-epi-lipoxin A4 inhibit human neutrophil migration: comparisons between synthetic 15 epimers in chemotaxis and transmigration with microvessel endothelial cells and epithelial cells. J. Immunol. 170, 2688-2694
37. Gavins, F. N., Kamal, A. M., D'Amico, M., Oliani, S. M., and Perretti, M. (2005) Formyl-peptide receptor is not involved in the protection afforded by annexin 1 in murine acute myocardial infarct. FASEB J. 19, 100-102
38. Folco, G., and Murphy, R. C. (2006) Eicosanoid transcellular biosynthesis: from cell-cell interactions to in vivo tissue responses. Pharmacol. Rev. 58, 375-388
39. Norris, P. C., Gosselin, D., Reichart, D., Glass, C. K., and Dennis, E. A. (2014) Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc. Natl. Acad. Sci. USA 111, 12746-12751
40. Dalli, J., and Serhan, C. N. (2012) Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 120, e60-e72
41. Levy, B. D., Lukacs, N. W., Berlin, A. A., Schmidt, B., Guilford, W. J., Serhan, C. N., and Parkinson, J. F. (2007) Lipoxin A4 stable analogs reduce allergic airway responses via mechanisms distinct from CysLT1 receptor antagonism. FASEB J. 21, 3877-3884
42. Guilford, W. J., Bauman, J. G., Skuballa, W., Bauer, S., Wei, G. P., Davey, D., Schaefer, C., Mallari, C., Terkelsen, J., Tseng, J. L., Shen, J., Subramanyam, B., Schottelius, A. J., and Parkinson, J. F. (2004) Novel 3-oxa lipoxin A4 analogues with enhanced chemical and metabolic stability have anti-inflammatory activity in vivo. J. Med. Cheem. 47, 2157-2165
43. Yoshioka, H., Niizuma, K., Katsu, M., Sakata, H., Okami, N., and Chan, P. H. (2011) Consistent injury to medium spiny neurons and white matter in the mouse striatum after prolonged transient global cerebral ischemia. J. Neurotrauma 28, 649-660
44. Bena, S., D'Amico, M., Flower, R. J., Reutelingsperger, C., and Perretti, M. (2012) The impact of FPRs on Annexin A1 cardioprotection in vivo. pA2 Online: E-journal of the British Society of Pharmacology
45. Lambertsen, K. L., Biber, K., and Finsen, B. (2012) Inflammatory cytokines in experimental and human stroke. J. Cereb. Blood Flow Metab. 32, 1677-1698
46. Murray, P. J. (2005) The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. USA 102, 8686-8691
47. Shouval, D. S., Biswas, A., Goettel, J. A., McCann, K., Conaway, E., Redhu, N. S., Mascanfroni, I. D., Al Adham, Z., Lavoie, S., Ibourk, M., Nguyen, D. D., Samsom, J. N., Escher, J. C., Somech, R., Weiss, B., Beier, R., Conklin, L. S., Ebens, C. L., Santos, F. G., Ferreira, A. R., Sherlock, M., Bhan, A. K., Muller, W., Mora, J. R., Quintana, F. J., Klein, C., Muise, A. M., Horwitz, B. H., and Snapper, S. B. (2014) Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and antiinflammatory macrophage function. Immunity 40, 706-719
48. Ye, X. H., Wu, Y., Guo, P. P., Wang, J., Yuan, S. Y., Shang, Y., and Yao, S. L. (2010) Lipoxin A4 analogue protects brain and reduces inflammation in a rat model of focal cerebral ischemia reperfusion. Brain Res. 1323, 174-183
49. El Kebir, D., Joozsef, L., Pan, W., Wang, L., Petasis, N. A., Serhan, C. N., and Filep, J. G. (2009) 15-epi-lipoxin A4 inhibits myeloperoxidase signaling and enhances resolution of acute lung injury. Am. J. Respir. Crit. Care Med. 180, 311-319