Targeting mannose-binding lectin confers long-lasting protection with a surprisingly wide therapeutic window in cerebral ischemia

Circulation

Volumn 126, Issue 12, 2012, Pages 1484-1494

  Orsini, Franca ^a   Villa, Pia ^a,e   Parrella, Sara ^a   Zangari, Rosalia ^a,f   Zanier, Elisa R ^a   Gesuete, Raffaella ^a,j   Stravalaci, Matteo ^b   Fumagalli, Stefano ^a   Ottria, Roberta ^c,d   Reina, José J ^k   Paladini, Alessandra ^a   Micotti, Edoardo ^a   Ribeiro Viana, Renato ^g   Rojo, Javier ^c,d,g   Pavlov, Vasile I ^h,i   Stahl, Gregory L ^h,i   Bernardi, Anna ^c,d   Gobbi, Marco ^b   De Simoni, Maria Grazia ^a,c  

^a Neuroscience Department   (Italy)

^b Molecular Biochemistry and Pharmacology Department   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e CNR   (Italy)

^f UNIVERSITY OF SIENA   (Italy)

^g CSIC   (Spain)

^h Center for Experimental Therapeutics and Reperfusion Injury   (United States)

ⁱ BRIGHAM AND WOMEN S HOSPITAL   (United States)

^j OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^k Mario Negri Institute ^*

more..

Author keywords

cerebral ischemia; complement system; endothelium; inflammation; stroke

Indexed keywords

MANNOSE BINDING LECTIN; MANNOSE BINDING LECTIN 2; POLYMAN 2; POLYSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CHEMICAL REACTION; CONTROLLED STUDY; MALE; MANNOSYLATION; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SURFACE PLASMON RESONANCE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN EDEMA; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MANNANS; MANNOSE-BINDING LECTIN; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; RATS; RATS, INBRED STRAINS;

EID: 84866491168     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.103051     Document Type: Article

References (46)

1. Lo EH. A new penumbra: transitioning from injury into repair after stroke. Nat Med. 2008;14:497-500. (Pubitemid 351655209)
2. Lees JS, Mishra NK, Saini M, Lyden PD, Shuaib A. Low body temperature does not compromise the treatment effect of alteplase. Stroke. 2011;42:2618-2621.
3. Fonarow GC, Smith EE, Saver JL, Reeves MJ, Bhatt DL, Grau-Sepulveda MV, Olson DM, Hernandez AF, Peterson ED, Schwamm LH. Timeliness of tissue-type plasminogen activator therapy in acute ischemic stroke: patient characteristics, hospital factors, and outcomes associated with door-to-needle times within 60 minutes. Circulation. 2011;123:750-758.
4. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med. 2011;17:796-808.
5. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010; 11:785-797.
6. Mocco J, Mack WJ, Ducruet AF, Sosunov SA, Sughrue ME, Hassid BG, Nair MN, Laufer I, Komotar RJ, Claire M, Holland H, Pinsky DJ, Connolly ES Jr. Complement component C3 mediates inflammatory injury following focal cerebral ischemia. Circ Res. 2006;99:209-217. (Pubitemid 44297045)
7. Veerhuis R, Nielsen HM, Tenner AJ. Complement in the brain. Mol Immunol. 2011;48:1592-1603.
8. Yanamadala V, Friedlander RM. Complement in neuroprotection and neurodegeneration. Trends Mol Med. 2010;16:69-76.
9. De Simoni MG, Rossi E, Storini C, Pizzimenti S, Echart C, Bergamaschini L. The powerful neuroprotective action of C1-inhibitor on brain ischemia-reperfusion injury does not require C1q. Am J Pathol. 2004; 164:1857-1863. (Pubitemid 38529788)
10. Storini C, Rossi E, Marrella V, Distaso M, Veerhuis R, Vergani C, Bergamaschini L, De Simoni MG. C1 inhibitor protects against brain ischemia-reperfusion injury via inhibition of cell recruitment and inflammation. Neurobiol Dis. 2005;19:10-17. (Pubitemid 40544719)
11. Longhi L, Perego C, Ortolano F, Zanier ER, Bianchi P, Stocchetti N, McIntosh TK, De Simoni MG. C1-inhibitor attenuates neurobehavioral deficits and reduces contusion volume after controlled cortical impact brain injury in mice. Crit Care Med. 2009;37:659-665.
12. Gesuete R, Storini C, Fantin A, Stravalaci M, Zanier ER, Orsini F, Vietsch H, Mannesse ML, Ziere B, Gobbi M, De Simoni MG. Recombinant C1 inhibitor in brain ischemic injury. Ann Neurol. 2009;66: 332-342.
13. Heydenreich N, Nolte MW, Gob E, Langhauser F, Hofmeister M, Kraft P, Albert-Weissenberger C, Brede M, Varallyay C, Gobel K, Meuth SG, Nieswandt B, Dickneite G, Stoll G, Kleinschnitz C. C1-Inhibitor protects from brain ischemia-reperfusion injury by combined antiinflammatory and antithrombotic mechanisms. Stroke. June 28, 2012. doi: 10.1161/STROKEAHA.112.660340. http://stroke.ahajournals.org. Accessed August 1, 2012.
14. Ip WK, Takahashi K, Ezekowitz RA, Stuart LM. Mannose-binding lectin and innate immunity. Immunol Rev. 2009;230:9-21.
15. Caplan LR, Arenillas J, Cramer SC, Joutel A, Lo EH, Meschia J, Savitz S, Tournier-Lasserve E. Stroke-related translational research. Arch Neurol. 2011;68:1110-1123.
16. La Bonte LR, Dokken B, Davis-Gorman G, Stahl GL, McDonagh PF. The mannose-binding lectin pathway is a significant contributor to reperfusion injury in the type 2 diabetic heart. Diab Vasc Dis Res. 2009;6:172-180.
17. Villa P, van Beek J, Larsen AK, Gerwien J, Christensen S, Cerami A, Brines M, Leist M, Ghezzi P, Torup L. Reduced functional deficits, neuroinflammation, and secondary tissue damage after treatment of stroke by nonerythropoietic erythropoietin derivatives. J Cereb Blood Flow Metab. 2007;27:552-563.
18. Jordan JE, Montalto MC, Stahl GL. Inhibition of mannose-binding lectin reduces postischemic myocardial reperfusion injury. Circulation. 2001; 104:1413-1418. (Pubitemid 32880155)
19. De Simoni MG, Storini C, Barba M, Catapano L, Arabia AM, Rossi E, Bergamaschini L. Neuroprotection by complement (C1) inhibitor in mouse transient brain ischemia. J Cereb Blood Flow Met. 2003;23: 232-239. (Pubitemid 36188461)
20. Storini C, Bergamaschini L, Gesuete R, Rossi E, Maiocchi D, De Simoni MG. Selective inhibition of plasma kallikrein protects brain from reperfusion injury. J Pharmacol Exp Ther. 2006;318:849-854. (Pubitemid 44061260)
21. Perego C, Fumagalli S, De Simoni MG. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation. 2011;8:174.
22. Chen ST, Hsu CY, Hogan EL, Maricq H, Balentine JD. A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke. 1986;17:738-743. (Pubitemid 16066549)
23. Cipriani R, Villa P, Chece G, Lauro C, Paladini A, Micotti E, Perego C, De Simoni MG, Fredholm BB, Eusebi F, Limatola C. CX3CL1 is neuroprotective in permanent focal cerebral ischemia in rodents. J Neurosci. 2011;31:16327-16335.
24. Lin YC, Ko TL, Shih YH, Lin MY, Fu TW, Hsiao HS, Hsu JY, Fu YS. Human umbilical mesenchymal stem cells promote recovery after ischemic stroke. Stroke. 2011;42:2045-2053.
25. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 5th ed. New York, NY: Academic Press; 2005.
26. Vakeva AP, Agah A, Rollins SA, Matis LA, Li L, Stahl GL. Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: role of the terminal complement components and inhibition by anti-C5 therapy. Circulation. 1998;97:2259-2267. (Pubitemid 28265388)
27. Hansen S, Thiel S, Willis A, Holmskov U, Jensenius JC. Purification and characterization of two mannan-binding lectins from mouse serum. J Immunol. 2000;164:2610-2618. (Pubitemid 30115492)
28. Cervera A, Planas AM, Justicia C, Urra X, Jensenius JC, Torres F, Lozano F, Chamorro A. Genetically-defined deficiency of mannosebinding lectin is associated with protection after experimental stroke in mice and outcome in human stroke. PLoS One. 2010;5:e8433.
29. Ducruet AF, Sosunov SA, Zacharia BE, Gorski J, Yeh ML, Derosa P, Cohen G, Gigante PR, Connolly ES Jr. The neuroprotective effect of genetic mannose-binding lectin deficiency is not sustained in the sub-acute phase of stroke. Transl Stroke Res. 2011;2:588-599.
30. Sattin S, Daghetti A, Thepaut M, Berzi A, Sanchez-Navarro M, Tabarani G, Rojo J, Fieschi F, Clerici M, Bernardi A. Inhibition of DC-SIGNmediated HIV infection by a linear trimannoside mimic in a tetravalent presentation. ACS Chem Biol. 2010;5:301-312.
31. Walsh MC, Bourcier T, Takahashi K, Shi L, Busche MN, Rother RP, Solomon SD, Ezekowitz RA, Stahl GL. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J Immunol. 2005;175:541-546. (Pubitemid 40884360)
32. Hart ML, Ceonzo KA, Shaffer LA, Takahashi K, Rother RP, Reenstra WR, Buras JA, Stahl GL. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J Immunol. 2005;174:6373-6380. (Pubitemid 40663830)
33. Castellano G, Melchiorre R, Loverre A, Ditonno P, Montinaro V, Rossini M, Divella C, Battaglia M, Lucarelli G, Annunziata G, Palazzo S, Selvaggi FP, Staffieri F, Crovace A, Daha MR, Mannesse M, van Wetering S, Paolo Schena F, Grandaliano G. Therapeutic targeting of classical and lectin pathways of complement protects from ischemiareperfusion-induced renal damage. Am J Pathol. 2010;176:1648-1659.
34. Trendelenburg M, Theroux P, Stebbins A, Granger C, Armstrong P, Pfisterer M. Influence of functional deficiency of complement mannosebinding lectin on outcome of patients with acute ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention. Eur Heart J. 2010;31:1181-1187.
35. Matthijsen RA, Derikx JP, Steffensen R, van Dam RM, Dejong CH, Buurman WA. Mannose-binding lectin null alleles are associated with preserved epithelial cell integrity following intestinal ischemia reperfusion in man. Mol Immunol. 2009;46:2244-2248.
36. Schwaeble WJ, Lynch NJ, Clark JE, Marber M, Samani NJ, Ali YM, Dudler T, Parent B, Lhotta K, Wallis R, Farrar CA, Sacks S, Lee H, Zhang M, Iwaki D, Takahashi M, Fujita T, Tedford CE, Stover CM. Targeting of mannan-binding lectin-associated serine protease-2 confers protection from myocardial and gastrointestinal ischemia/reperfusion injury. Proc Natl Acad Sci USA. 2011;108:7523-7528.
37. Yongqing T, Drentin N, Duncan RC, Wijeyewickrema LC, Pike RN. Mannose-binding lectin serine proteases and associated proteins of the lectin pathway of complement: two genes, five proteins and many functions? Biochim Biophys Acta. 2011;1824:253-262.
38. Holmskov U, Thiel S, Jensenius JC. Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol. 2003;21: 547-578. (Pubitemid 37174541)
39. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805-820.
40. van der Pol P, Schlagwein N, van Gijlswijk DJ, Berger SP, Roos A, Bajema IM, de Boer HC, de Fijter JW, Stahl GL, Daha MR, van Kooten C. Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am J Transplant. 2012;12: 877-887.
41. Wagner S, Lynch NJ, Walter W, Schwaeble WJ, Loos M. Differential expression of the murine mannose-binding lectins A and C in lymphoid and nonlymphoid organs and tissues. J Immunol. 2003;170:1462-1465. (Pubitemid 36139515)
42. Worthley DL, Bardy PG, Mullighan CG. Mannose-binding lectin: biology and clinical implications. Intern Med J. 2005;35:548-555. (Pubitemid 41291384)
43. Seyfarth J, Garred P, Madsen HO. The 'involution' of mannose-binding lectin. Hum Mol Genet. 2005;14:2859-2869. (Pubitemid 41418791)
44. Osthoff M, Katan M, Fluri F, Schuetz P, Bingisser R, Kappos L, Steck AJ, Engelter ST, Mueller B, Christ-Crain M, Trendelenburg M. Mannosebinding lectin deficiency is associated with smaller infarction size and favorable outcome in ischemic stroke patients. PLoS One. 2011;6:e21338.
45. Osthoff M, Trendelenburg G, Eisen DP, Trendelenburg M. Mannosebinding lectin-the forgotten molecule? Nat Med. 2011;17:1547-1548.
46. Fust G, Munthe-Fog L, Illes Z, Szeplaki G, Molnar T, Pusch G, Hirschberg K, Szegedi R, Szeplaki Z, Prohaszka Z, Skjoedt MO, Garred P. Low ficolin-3 levels in early follow-up serum samples are associated with the severity and unfavorable outcome of acute ischemic stroke. J Neuroinflammation. 2011;8:185.