Protective effects of angiopoietin-like 4 on cerebrovascular and functional damages in ischaemic stroke

European Heart Journal

Volumn 34, Issue 47, 2013, Pages 3657-3668

  Bouleti, Claire ^a,b,c,d,e   Mathivet, Thomas ^a,b,c,d   Coqueran, Berard ^f   Serfaty, Jean Michel ^g   Lesage, Mathieu ^a,b,c,d   Berland, Elodie ^a,b,c,d   Ardidie Robouant, Corinne ^a,b,c,d   Kauffenstein, Gilles ^h   Henrion, Daniel ^h   Lapergue, Bertrand ^g   Mazighi, Mikael ^g   Duyckaerts, Charles ⁱ   Thurston, Gavin ^j   Valenzuela, David M ^j   Murphy, Andrew J ^j   Yancopoulos, George D ^j   Monnot, Catherine ^a,b,c,d,k   Margaill, Isabelle ^f   Germain, Stephane ^a,b,c,d,k,l  

^a l'alimentation et l'Environnement   (France)

^b CNRS   (France)

^c INSERM   (France)

^d Laboratory of Excellence and Paris Science Lettre   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g BICHAT HOSPITAL   (France)

^h UNIVERSITÉ D'ANGERS   (France)

ⁱ PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^j REGENERON PHARMACEUTICALS INC   (United States)

^k Cartes d'Identité des Tumeurs Program   (France)

^l SAINT LOUIS HOSPITAL   (France)

more..

Author keywords

Acute cerebral infarction; Angiogenesis; Endothelium; Hypoxia; Ischaemia; Vascular biology

Indexed keywords

ANGIOPOIETIN; CLAUDIN 5; PROTEIN KINASE P60; RECOMBINANT ANGIOPOIETIN LIKE 4 PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL INJURY; BRAIN CIRCULATION; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PROTECTION; BRAIN TISSUE; CELL DENSITY; CELL JUNCTION; CELL LOSS; CEREBROVASCULAR DISEASE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; ENDOTHELIUM CELL; INJURY SEVERITY; MALE; MOUSE; MURINE MODEL; NERVE CELL; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

ACUTE CEREBRAL INFARCTION; ANGIOGENESIS; ENDOTHELIUM; HYPOXIA; ISCHAEMIA; VASCULAR BIOLOGY;

ANGIOPOIETINS; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; BRAIN ISCHEMIA; CADHERINS; CELL MEMBRANE PERMEABILITY; ENCEPHALITIS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MALE; MICE; MICE, INBRED C57BL; NOOTROPIC AGENTS; SRC-FAMILY KINASES; STROKE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84891365313     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/eht153     Document Type: Article

References (35)

1. Kinlay S. Changes in stroke epidemiology, prevention, and treatment. Circulation 2011;124:e494-e496.
2. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010;67:181-198.
3. delZoppo GJ.Inflammation and the neurovascular unit in the setting of focal cerebral ischemia. Neuroscience 2009;158:972-982.
4. Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, Leybaert L, Molnar Z, O'Donnell ME, Povlishock JT, Saunders NR, Sharp F, Stanimirovic D, Watts RJ, Drewes LR. Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 2011;12:169-182.
5. Bates DO, Curry FE. Vascular endothelial growth factor increases hydraulic conductivity of isolated perfused microvessels. Am J Physiol 1996;271(6 Pt 2): H2520-H2528.
6. Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 2002;125(Pt 11):2549-2557.
7. Zhang ZG, Zhang L, Jiang Q, Zhang R, Davies K, Powers C, Bruggen N, Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 2000;106:829-838.
8. Weis SM, ChereshDA. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 2005;437:497-504.
9. van Bruggen N, Thibodeaux H, Palmer JT, Lee WP, Fu L, Cairns B, Tumas D, Gerlai R, Williams SP, van Lookeren Campagne M, Ferrara N. VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J Clin Invest 1999;104:1613-1620.
10. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999;4:915-924.
11. Paul R, Zhang ZG, Eliceiri BP, Jiang Q, Boccia AD, Zhang RL, Chopp M, Cheresh DA. Src deficiency or blockade of Src activity in mice provides cerebral protection following stroke. Nat Med 2001;7:222-227.
12. Roodhart JM, Langenberg MH, Witteveen E, Voest EE. The molecular basis of class side effects due to treatment with inhibitors of the VEGF/VEGFR pathway. Curr Clin Pharmacol 2008;3:132-143.
13. Le Jan S, Amy C, Cazes A, Monnot C, Lamande N, Favier J, Philippe J, Sibony M, Gasc JM, Corvol P, Germain S. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol 2003; 162:1521-1528.
14. Galaup A, Gomez E, Souktani R, Durand M, Cazes A, Monnot C, Teillon J, Le Jan S, Bouleti C, Briois G, Philippe J, Pons S, Martin V, Assaly R, Bonnin P, Ratajczak P, Janin A, Thurston G, Valenzuela DM, Murphy AJ, Yancopoulos GD, Tissier R, Berdeaux A, Ghaleh B, Germain S. Protection against myocardial infarction and no-reflow through preservation of vascular integrity by angiopoietin-like 4. Circulation 2012;125:140-149.
15. ValenzuelaDM,Murphy AJ, Frendewey D, GaleNW, EconomidesAN, AuerbachW, Poueymirou WT, Adams NC, Rojas J, Yasenchak J, Chernomorsky R, Boucher M, Elsasser AL, Esau L, Zheng J, Griffiths JA, Wang X, Su H, Xue Y, Dominguez MG, Noguera I, Torres R, Macdonald LE, Stewart AF, DeChiara TM, Yancopoulos GD. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol 2003;21:652-659.
16. Perdiguero EG, Galaup A, Durand M, Teillon J, Philippe J, Valenzuela DM, Murphy AJ, Yancopoulos GD, Thurston G, Germain S. Alteration of developmental and pathological retinal angiogenesis in angptl4-deficient mice. J Biol Chem 2011;286: 36841-36851.
17. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994; 265:1883-1885.
18. Chomel C, Cazes A, Faye C, Bignon M, Gomez E, Ardidie-Robouant C, Barret A, Ricard-Blum S, Muller L, Germain S, Monnot C. Interaction of the coiled-coil domain with glycosaminoglycans protects angiopoietin-like 4 from proteolysis and regulates its antiangiogenic activity. FASEB J 2009;23:940-949.
19. Wiesner G, Brown RE, Robertson GS, Imran SA, Ur E, Wilkinson M. Increased expression of the adipokine genes resistin and fasting-induced adipose factor in hypoxic/ischaemic mouse brain. Neuroreport 2006;17:1195-1198.
20. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006;8: 1223-1234.
21. Rabiet MJ, Plantier JL, Rival Y, Genoux Y, Lampugnani MG, Dejana E. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler Thromb Vasc Biol 1996;16:488-496.
22. Weis S, Shintani S, Weber A, Kirchmair R, Wood M, Cravens A, McSharry H, Iwakura A, Yoon YS, Himes N, Burstein D, Doukas J, Soll R, Losordo D, Cheresh D. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest 2004;113:885-894.
23. Ito Y, Oike Y, Yasunaga K, Hamada K, Miyata K, Matsumoto S, Sugano S, Tanihara H, Masuho Y, Suda T. Inhibition of angiogenesis and vascular leakiness by angiopoietinrelated protein 4. Cancer Res 2003;63:6651-6657.
24. KochAW, MathivetT, Larrivee B, Tong RK,Kowalski J, Pibouin-Fragner L, Bouvree K, Stawicki S, Nicholes K, Rathore N, Scales SJ, Luis E, del Toro R, Freitas C, Breant C, Michaud A, Corvol P, Thomas JL,WuY, Peale F,Watts RJ,Tessier-Lavigne M, Bagri A, EichmannA. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell 2011;20:33-46.
25. Lindsberg PJ, Carpen O, Paetau A, Karjalainen-Lindsberg ML, Kaste M. Endothelial ICAM-1 expression associated with inflammatory cell response in human ischemic stroke. Circulation 1996;94:939-945.
26. Turowski P, Adamson P, Greenwood J. Pharmacological targeting of ICAM-1 signaling in brain endothelial cells: potential for treating neuroinflammation. Cell Mol Neurobiol 2005;25:153-170.
27. Lapergue B,MorenoJA, DangBQ, Coutard M, Delbosc S, Raphaeli G, AugeN, Klein I, Mazighi M, Michel JB, Amarenco P, Meilhac O. Protective effect of high-density lipoprotein-based therapy in a model of embolic stroke. Stroke 2010;41:1536-1542.
28. Bell RD, Winkler EA, Singh I, Sagare AP, Deane R,WuZ, Holtzman DM, Betsholtz C, Armulik A, SallstromJ, Berk BC, ZlokovicBV. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature 2012;485:512-516.
29. Hariri RJ. Cerebral edema. Neurosurg Clin N Am 1994;5:687-706.
30. Xu F, Severinghaus JW. Rat brain VEGF expression in alveolar hypoxia: possible role in high-altitude cerebral edema. J Appl Physiol 1998;85:53-57.
31. Dejana E, Giampietro C. Vascular endothelial-cadherin and vascular stability. Curr Opin Hematol 2012;19:218-223.
32. Dijkhuizen RM, Asahi M,WuO, Rosen BR, Lo EH. Rapid breakdown of microvascular barriers and subsequent hemorrhagic transformation after delayed recombinant tissue plasminogen activator treatment in a rat embolic stroke model. Stroke 2002; 33:2100-2104.
33. Sligh JE Jr, Ballantyne CM, Rich SS, Hawkins HK, Smith CW, Bradley A, Beaudet AL. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc Natl Acad Sci USA 1993;90: 8529-8533.
34. Whalen MJ, Carlos TM, Dixon CE, Robichaud P, Clark RS, Marion DW, Kochanek PM. Reduced brain edema after traumatic brain injury in mice deficient in P-selectin and intercellular adhesion molecule-1. J Leukoc Biol 2000;67: 160-168.
35. Davis SM,Donnan GA. Clinical practice. Secondary prevention after ischemic stroke or transient ischemic attack. N Engl J Med 2012;366:1914-1922.