Protein S controls hypoxic/ischemic blood-brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor

Blood

Volumn 115, Issue 23, 2010, Pages 4963-4972

  Zhu, Donghui ^a   Wang, Yaoming ^a   Singh, Itender ^a   Bell, Robert D ^a   Deane, Rashid ^a   Zhong, Zhihui ^a   Sagare, Abhay ^a   Winkler, Ethan A ^a   Zlokovic, Berislav V ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; DEXTRAN; F ACTIN; PROTEIN S; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; RECOMBINANT PROTEIN; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TAM RECEPTOR TYROSINE KINASE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; AXL RECEPTOR TYROSINE KINASE; MERTK PROTEIN, HUMAN; MERTK PROTEIN, MOUSE; NEUROPEPTIDE; ONCOPROTEIN; RAC PROTEIN; RAC1 PROTEIN, HUMAN; RAC1 PROTEIN, MOUSE; S1PR1 PROTEIN, HUMAN; TYRO3 PROTEIN, HUMAN; TYRO3 PROTEIN, MOUSE;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CELL; BRAIN CORTEX; BRAIN DAMAGE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN PROTECTION; CELL MEMBRANE PERMEABILITY; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; DOSE RESPONSE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LIPID MONOLAYER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; TRANSIENT ISCHEMIC ATTACK; ANIMAL; BIOLOGICAL MODEL; BRAIN; GENETICS; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN ISCHEMIA; ENDOTHELIAL CELLS; HUMANS; MICE; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; NEUROPEPTIDES; PHOSPHORYLATION; PROTEIN S; PROTO-ONCOGENE PROTEINS; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, LYSOSPHINGOLIPID; YOUNG ADULT;

EID: 77954747250     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-01-262386     Document Type: Article

References (44)

1. Dahlbäck B. The tale of protein S and C4b-binding protein, a story of affection. Thromb Haemost. 2007;98(1):90-96. (Pubitemid 47074183)
2. Saller F, Villoutreix BO, Amelot A, et al. The gamma-carboxyglutamic acid domain of anticoagulant protein S is involved in activated protein C cofactor activity, independently of phospholipid binding. Blood. 2005;105(1):122-130.
3. Saller F, Brisset AC, Tchaikovski SN, et al. Generation and phenotypic analysis of protein S-deficient mice. Blood. 2009;114(11):2307-2314.
4. Burstyn-Cohen T, Heeb MJ, Lemke G. Lack of Protein S in mice causes embryonic lethal coagulopathy and vascular dysgenesis. J Clin Invest. 2009;119(10):2942-2953.
5. Marlar RA, Neumann A. Neonatal purpura fulminans due to homozygous protein C or protein S deficiencies. Semin Thromb Hemost. 1990;16(4):299-309.
6. Ten Kate MK, van der Meer J. Protein S deficiency: a clinical perspective. Haemophilia. 2008;14(6):1222-1228.
7. Miyata T, Sato Y, Ishikawa J, et al. Prevalence of genetic mutations in protein S, protein C and anti-thrombin genes in Japanese patients with deep vein thrombosis. Thromb Res. 2009;124(1):14-18.
8. Webb JH, Blom AM, Dahlback B. Vitamin K-dependent protein S localizing complement regulator C4b-binding protein to the surface of apoptotic cells. J Immunol. 2002;169(5):2580-2586.
9. Anderson HA, Maylock CA, Williams JA, et al. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol. 2003;4(1):87-91.
10. Uehara H, Shacter E. Auto-oxidation and oligomerization of protein S on the apoptotic cell surface is required for Mer tyrosine kinase-mediated phagocytosis of apoptotic cells. J Immunol. 2008;180(4):2522-2530.
11. Gasic GP, Arenas CP, Gasic TB, et al. Coagulation factors X, Xa, and protein S as potent mitogens of cultured aortic smooth muscle cells. Proc Natl Acad Sci U S A. 1992;89(6):2317-2320.
12. Benzakour O, Formstone C, Rahman S, et al. Evidence for a protein S receptor(s) on human vascular smooth muscle cells: analysis of the binding characteristics and mitogenic properties of protein S on human vascular smooth muscle cells. Biochem J. 1995;308(pt 2):481-485.
13. Fernández JA, Heeb MJ, Xu X, et al. Species specific anticoagulant and mitogenic activities of murine protein S. Haematologica. 2009;94(12):1721-1731.
14. Liu D, Guo H, Griffin JH, et al. Protein S confers neuronal protection during ischemic/hypoxic injury in mice. Circulation. 2003;107(13):1791-1796. (Pubitemid 36418361)
15. Prieto AL, O'Dell S, Varnum B, et al. Localization and signaling of the receptor protein tyrosine kinase Tyro3 in cortical and hippocampal neurons. Neuroscience. 2007;150(2):319-334.
16. Shankar SL, O'Guin K, Kim M, et al. Gas6/Axl signaling activates the phosphatidylinositol 3-kinase/Akt1 survival pathway to protect oligodendrocytes from tumor necrosis factor alpha-induced apoptosis. J Neurosci. 2006;26(21):5638-5648.
17. Stitt TN, Conn G, Gore M, et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell. 1995;80(4):661-670.
18. Hall MO, Obin MS, Heeb MJ, et al. Both protein S and Gas6 stimulate outer segment phagocytosis by cultured rat retinal pigment epithelial cells. Exp Eye Res. 2005;81(5):581-591.
19. Prasad D, Rothlin CV, Burrola P, et al. TAM receptor function in the retinal pigment epithelium. Mol Cell Neurosci. 2006;33(1):96-108. (Pubitemid 44291594)
20. Lu Q, Gore M, Zhang Q, et al. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature. 1999;398(6729):723-728.
21. Lu Q, Lemke G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science. 2001;293(5528):306-311.
22. Lemke G, Lu Q. Macrophage regulation by Tyro 3 family receptors. Curr Opin Immunol. 2003;15(1):31-36. (Pubitemid 35454189)
23. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol. 2008;8(5):327-336.
24. Prieto AL, Weber JL, Lai C. Expression of the receptor protein-tyrosine kinases Tyro-3, Axl, and Mer in the developing rat central nervous system. J Comp Neurol. 2000;425(2):295-314.
25. Fair DS, Marlar RA, Levin EG. Human endothelial cells synthesize protein S. Blood. 1986;67(4):1168-1171.
26. Stern D, Brett J, Harris K, et al. Participation of endothelial cells in the protein C-protein S anticoagulant pathway: the synthesis and release of protein S. J Cell Biol. 1986;102(5):1971-1978. (Pubitemid 16078781)
27. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron. 2008;57(2):178-201.
28. Mackic JB, Stins M, McComb JG, et al. Human blood-brain barrier receptors for Alzheimer's amyloid-beta 1-40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer. J Clin Invest. 1998;102(4):734-743.
29. Garcia JG, Liu F, Verin AD, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001;108(5):689-701.
30. Benchenane K, Berezowski V, Fernandez-Monreal M, et al. Oxygen glucose deprivation switches the transport of tPA across the blood-brain barrier from an LRP-dependent to an increased LRP-independent process. Stroke. 2005;36(5):1065-1070.
31. Wojciak-Stothard B, Torondel B, Zhao L, et al. Modulation of Rac1 activity by ADMA/DDAH regulates pulmonary endothelial barrier function. Mol Biol Cell. 2009;20(1):33-42.
32. Liu D, Cheng T, Guo H, et al. Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C. Nat Med. 2004;10(12):1379-1383. (Pubitemid 40022721)
33. Finigan JH, Dudek SM, Singleton PA, et al. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem. 2005;280(17):17286-17293.
34. Weksler BB, Subileau EA, Perriere N, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005;19(13):1872-1874.
35. Wu Z, Hofman FM, Zlokovic BV. A simple method for isolation and characterization of mouse brain microvascular endothelial cells. J Neurosci Methods. 2003;130(1):53-63. (Pubitemid 37315929)
36. Wang L, Kittaka M, Sun N, et al. Chronic nicotine treatment enhances focal ischemic brain injury and depletes free pool of brain microvascular tissue plasminogen activator in rats. J Cereb Blood Flow Metab. 1997;17(2):136-146.
37. Tanimoto T, Jin ZG, Berk BC. Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J Biol Chem. 2002;277(45):42997-43001.
38. Rosen H, Gonzalez-Cabrera P, Marsolais D, et al. Modulating tone: the overture of S1P receptor immunotherapeutics. Immunol Rev. 2008;223:221-235. (Pubitemid 351986190)
39. Deane R, Du Yan S, Submamaryan RK, et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med. 2003;9(7):907-913.
40. Niwa K, Kazama K, Younkin SG, et al. Alterations in cerebral blood flow and glucose utilization in mice overexpressing the amyloid precursor protein. Neurobiol Dis. 2002;9(1):61-68.
41. Paris D, Quadros A, Humphrey J, et al. Nilvadipine antagonizes both Abeta vasoactivity in isolated arteries, and the reduced cerebral blood flow in APPsw transgenic mice. Brain Res. 2004;999(1):53-61. (Pubitemid 38121450)
42. Oosthuyse B, Moons L, Storkebaum E, et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet. 2001;28(2):131-138.
43. Zhong Z, Deane R, Ali Z, et al. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci. 2008;11(4):420-422.
44. Henkel JS, Beers DR, Wen S, et al. Decreased mRNA expression of tight junction proteins in lumbar spinal cords of patients with ALS. Neurology. 2009;72(18):1614-1616.