Erratum: Protein S Protects Neurons from Excitotoxic Injury by Activating the TAM Receptor Tyro3–Phosphatidylinositol 3-Kinase–Akt Pathway through Its Sex Hormone-Binding Globulin-Like Region (Journal of Neuroscience DOI: 10.1523/JNEUROSCI.4437-10.2010);Protein S protects neurons from excitotoxic injury by activating the TAM receptor tyro3-phosphatidylinositol 3-kinase-Akt pathway through its sex hormone-binding globulin-like region

Journal of Neuroscience

Volumn 30, Issue 46, 2010, Pages 15521-15534

  Zhong, Zhihui ^a   Wang, Yaoming ^a   Guo, Huang ^a   Sagare, Abhay ^a   Fernández, José A ^b   Bell, Robert D ^a   Barrett, Theresa M ^a   Griffin, John H ^b   Freeman, Robert S ^a   Zlokovic, Berislav V ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; N METHYL DEXTRO ASPARTIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BAX; PROTEIN MDM2; PROTEIN MER; PROTEIN P53; PROTEIN S; PROTEIN TAM; SEX HORMONE BINDING GLOBULIN; TYROSINE; TYROSINE 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRAL GENE DELIVERY SYSTEM;

EID: 78449263958     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0435-24.2024     Document Type: Erratum

References (103)

1. Anderson HA, Maylock CA, Williams JA, Paweletz CP, Shu H, Shacter E (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 4:87-91. (Pubitemid 36113217)
2. Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC (2002) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923-929.
3. Arundine M, Tymianski M (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 61:657-668.
4. Ayata C, Ayata G, Hara H, Matthews RT, Beal MF, Ferrante RJ, Endres M, Kim A, Christie RH, Waeber C, Huang PL, Hyman BT, Moskowitz MA (1997) Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J Neurosci 17:6908-6917. (Pubitemid 27427869)
5. Benzakour O, Formstone C, Rahman S, Kanthou C, Dennehy U, Scully MF, Kakkar VV, Cooper DN (1995) 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 308:481-485.
6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 92:7162-7166.
7. Boutahar N, Reynaud E, Lassabliere F, Borg J (2008) Timing differences of signaling response in neuron cultures activated by glutamate analogue or free radicals. Brain Res 1191:20-29.
8. Budd SL, Tenneti L, Lishnak T, Lipton SA (2000) Mitochondrial and extra-mitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc Natl Acad Sci U S A 97:6161-6166.
9. Burstyn-Cohen T, Heeb MJ, Lemke G (2009) Lack of protein S in mice causes embryonic lethal coagulopathy and vascular dysgenesis. J Clin Invest 119:2942-2953.
10. Chen Q, He S, Hu XL, Yu J, Zhou Y, Zheng J, Zhang S, Zhang C, Duan WH, Xiong ZQ (2007) Differential roles of NR2A- and NR2B-containing NMDA receptors in activity-dependent brain-derived neurotrophic factor gene regulation and limbic epileptogenesis. J Neurosci 27:542-552.
11. Crowder RJ, Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18:2933-2943.
12. Dahlbäck B (2007) The tale of protein S and C4b-binding protein, a story of affection. Thromb Haemost 98:90-96.
13. Dasari VR, Veeravalli KK, Saving KL, Gujrati M, Fassett D, Klopfenstein JD, Dinh DH, Rao JS (2008) Neuroprotection by cord blood stem cells against glutamate-induced apoptosis is mediated by Akt pathway. Neurobiol Dis 32:486-498.
14. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
15. Datta SR, Ranger AM, Lin MZ, Sturgill JF, Ma YC, Cowan CW, Dikkes P, Korsmeyer SJ, Greenberg ME (2002) Survival factor-mediated BAD phosphorylation raises the mitochondrial threshold for apoptosis. Dev Cell 3:631-643.
16. del Peso L, González-García M, Page C, Herrera R, Nuñez G (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
17. Djebaïli M, Rondouin G, Baille V, Bockaert J (2000) p53 and Bax implication in NMDA induced-apoptosis in mouse hippocampus. Neuroreport 11:2973-2976.
18. Dömötör E, Benzakour O, Griffin JH, Yule D, Fukudome K, Zlokovic BV (2003) Activated protein C alters cytosolic calcium flux in human brain endothelium val binding to endothelial protein C receptor and activation of protease activated receptor-1. Blood 101:4797-4801.
19. Du Y, Bales KR, Dodel RC, Hamilton-Byrd E, Horn JW, Czilli DL, Simmons LK, Ni B, Paul SM (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc Natl Acad Sci U S A 94:11657-11662. (Pubitemid 27451054)
20. Evenäs P, Dahlbäck B, García de Frutos P (2000) The first laminin G-type domain in the SHBG-like region of protein S contains residues essential for activation of the receptor tyrosine kinase sky. Biol Chem 381:199-209.
21. Fernández JA, Heeb MJ, Xu X, Singh I, Zlokovic BV, Griffin JH (2009) Species-specific anticoagulant and mitogenic activities of murine protein S. Haematologica 94:1721-1731.
22. Fuentealba RA, Liu Q, Kanekiyo T, Zhang J, Bu G (2009) Low density lipoprotein receptor-related protein 1 promotes anti-apoptotic signaling in neurons by activating Akt survival pathway. J Biol Chem 284:34045-34053.
23. Gabriel B, Sureau F, Casselyn M, Teissié J, Petit PX (2003) Retroactive pathway involving mitochondria in electroloaded cytochrome c-induced apoptosis. Protective properties of Bcl-2 and Bcl-XL. Exp Cell Res 289:195-210.
24. Gasic GP, Arenas CP, Gasic TB, Gasic GJ (1992) Coagulation factors X, Xa, and protein S as potent mitogens of cultured aortic smooth muscle cells. Proc Natl Acad Sci U S A 89:2317-2320.
25. Goruppi S, Ruaro E, Schneider C (1996) Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 12:471-480. (Pubitemid 26059640)
26. Gottlieb TM, Leal JF, Seger R, Taya Y, Oren M (2002) Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene 21:1299-1303. (Pubitemid 34185247)
27. Guo H, Liu D, Gelbard H, Cheng T, Insalaco R, Fernández JA, Griffin JH, Zlokovic BV (2004) Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 41:563-572.
28. Guo H, Singh I, Wang Y, Deane R, Barrett T, Fernández JA, Chow N, Griffin JH, Zlokovic BV (2009a) Neuroprotective activities of activated protein C mutant with reduced anticoagulant activity. Eur J Neurosci 29:1119-1130.
29. Guo H, Wang Y, Singh I, Liu D, Fernández JA, Griffin JH, Chow N, Zlokovic BV (2009b) Species-dependent neuroprotection by activated protein C mutants with reduced anticoagulant activity. J Neurochem 109:116-124.
30. Guo W, Ahmed KM, Hui Y, Guo G, Li JJ (2007) siRNA-mediated Mdm2 inhibition sensitizes human lung cancer A549 cells to radiation. Int J Oncol 30:1447-1452.
31. Hackeng TM, Fernández JA, Dawson PE, Kent SB, Griffin JH (2000) Chemical synthesis and spontaneous folding of a multidomain protein: anticoagulant microprotein S. Proc Natl Acad Sci U S A 97:14074-14078.
32. Hafizi S, Dahlbäck B (2006) Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 273:5231-5244.
33. Hall MO, Obin MS, Heeb MJ, Burgess BL, Abrams TA (2005) Both protein S and Gas6 stimulate outer segment phagocytosis by cultured rat retinal pigment epithelial cells. Exp Eye Res 81:581-591.
34. Hardingham GE (2009) Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem Soc Trans 37:1147-1160.
35. Heeb MJ, Griffin JH (2002) Activated protein C-dependent and -independent anticoagulant activities of protein S have different structural requirements. Blood Cells Mol Dis 29:190-199.
36. Hori N, Carpenter DO (1994) Functional and morphological changes induced by transient in vivo ischemia. Exp Neurol 129:279-289.
37. Hsuan SL, Klintworth HM, Xia Z (2006) Basic fibroblast growth factor protects against rotenone-induced dopaminergic cell death through activation of extracellular signal-regulated kinases 1/2 and phosphatidylinositol-3 kinase pathways. J Neurosci 26:4481-4491.
38. Jamison CS, McDowell SA, Marlar RA, Degen SJ (1995) Developmental expression of protein C and protein S in the rat. Thromb Res 78:407-419.
39. Jordán J, Galindo MF, González-García C, Ceña V (2003) Role and regulation of p53 in depolarization-induced neuronal death. Neuroscience 122:707-715. (Pubitemid 37410292)
40. Jover-Mengual T, Miyawaki T, Latuszek A, Alborch E, Zukin RS, Etgen AM (2010) Acute estradiol protects CA1 neurons from ischemia-induced apoptotic cell death via the PI3K/Akt pathway. Brain Res 1321:1-12.
41. Kajimoto T, Okada T, Yu H, Goparaju SK, Jahangeer S, Nakamura S (2007) Involvement of sphingosine-1-phosphate in glutamate secretion in hippocampal neurons. Mol Cell Biol 27:3429-3440.
42. Kakee A, Terasaki T, Sugiyama Y (1996) Brain efflux index as a novel method of analyzing efflux transport at the blood-brain barrier. J Pharmacol Exp Ther 277:1550-1559. (Pubitemid 27167171)
43. Kim NH, Kim K, Park WS, Son HS, Bae Y (2007) PKB/Akt inhibits ceramide-induced apoptosis in neuroblastoma cells by blocking apoptosis-inducing factor (AIF) translocation. J Cell Biochem 102:1160-1170.
44. Konishi A, Aizawa T, Mohan A, Korshunov VA, Berk BC (2004) Hydrogen peroxide activates the Gas6-Axl pathway in vascular smooth muscle cells. J Biol Chem 279:28766-28770. (Pubitemid 38900161)
45. Lemke G, Lu Q (2003) Macrophage regulation by Tyro 3 family receptors. Curr Opin Immunol 15:31-36.
46. Lemke G, Rothlin CV (2008) Immunobiology of the TAM receptors. Nat Rev Immunol 8:327-336.
47. Lesuisse C, Martin LJ (2002a) Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J Neurobiol 51:9-23.
48. Lesuisse C, Martin LJ (2002b) Immature and mature cortical neurons engage different apoptotic mechanisms involving caspase-3 and the mitogen-activated protein kinase pathway. J Cereb Blood Flow Metab 22:935-950. (Pubitemid 34831600)
49. Lipton SA (2006) NMDA receptors, glial cells, and clinical medicine. Neuron 50:9-11.
50. Lipton SA, Nakanishi N (1999) Shakespeare in love - with NMDA receptors? Nat Med 5:270-271.
51. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613-622.
52. Liu D, Guo H, Griffin JH, Fernández JA, Zlokovic BV (2003) Protein S confers neuronal protection during ischemic/hypoxic injury in mice. Circulation 107:1791-1796.
53. Liu D, Cheng T, Guo H, Fernández JA, Griffin JH, Song X, Zlokovic BV (2004) Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C. Nat Med 10:1379-1383.
54. Lu Q, Lemke G (2001) Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306-311. (Pubitemid 32694748)
55. Lu Q, Gore M, Zhang Q, Camenisch T, Boast S, Casagranda F, Lai C, Skinner MK, Klein R, Matsushima GK, Earp HS, Goff SP, Lemke G (1999) Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398:723-728.
56. Luo HR, Hattori H, Hossain MA, Hester L, Huang Y, Lee-Kwon W, Donowitz M, Nagata E, Snyder SH (2003) Akt as a mediator of cell death. Proc Natl Acad Sci U S A 100:11712-11717.
57. Madhavan L, Freed WJ, Anantharam V, Kanthasamy AG (2003) 5-Hydroxytryptamine 1A receptor activation protects against N-methyl-D- aspartate-induced apoptotic cell death in striatal and mesencephalic cultures. J Pharmacol Exp Ther 304:913-923.
58. Mayo LD, Donner DB (2001) A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci U S A 98:11598-11603.
59. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, Schwartzkroin PA (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16:1337-1345. (Pubitemid 126500803)
60. Nakatsu Y, Kotake Y, Komasaka K, Hakozaki H, Taguchi R, Kume T, Akaike A, Ohta S (2006) Glutamate excitotoxicity is involved in cell death caused by tributyltin in cultured rat cortical neurons. Toxicol Sci 89:235-242. (Pubitemid 43013771)
61. Ohi N, Nishikawa Y, Tokairin T, Yamamoto Y, Doi Y, Omori Y, Enomoto K (2006) Maintenance of Bad phosphorylation prevents apoptosis of rat hepatic sinusoidal endothelial cells in vitro and in vivo. Am J Pathol 168:1097-1106.
62. Okamoto S, Li Z, Ju C, Scholzke MN, Mathews E, Cui J, Salvesen GS, Bossy-Wetzel E, Lipton SA (2002) Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis. Proc Natl Acad Sci U S A 99:3974-3979.
63. Okayasu R, Takakura K, Poole S, Bedford JS (2003) Radiosensitization of normal human cells by LY294002: cell killing and the rejoining of DNA and interphase chromosome breaks. J Radiat Res (Tokyo) 44:329-333.
64. Papadia S, Hardingham GE (2007) The dichotomy of NMDA receptor signaling. Neuroscientist 13:572-579.
65. Patneau DK, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10:2385-2399.
66. Penninger JM, Kroemer G (2003) Mitochondria, AIF and caspases - rivaling for cell death execution. Nat Cell Biol 5:97-99.
67. Phillips DJ, Greengard JS, Fernández JA, Ribeiro M, Evatt BL, Griffin JH, Hooper WC (1993) Protein S, an antithrombotic factor, is synthesized and released by neural tumor cells. J Neurochem 61:344-347. (Pubitemid 23175920)
68. Pierce A, Bliesner B, Xu M, Nielsen-Preiss S, Lemke G, Tobet S, Wierman ME (2008) Axl and Tyro3 modulate female reproduction by influencing gonadotropin-releasing hormone neuron survival and migration. Mol Endocrinol 22:2481-2495.
69. Prasad D, Rothlin CV, Burrola P, Burstyn-Cohen T, Lu Q, Garcia de Frutos P, Lemke G (2006) TAM receptor function in the retinal pigment epithelium. Mol Cell Neurosci 33:96-108. (Pubitemid 44291594)
70. Prieto AL, Weber JL, Lai C (2000) Expression of the receptor protein-tyrosine kinases Tyro-3, Axl, and mer in the developing rat central nervous system. J Comp Neurol 425:295-314.
71. Prieto AL, O'Dell S, Varnum B, Lai C (2007) Localization and signaling of the receptor protein tyrosine kinase Tyro3 in cortical and hippocampal neurons. Neuroscience 150:319-334.
72. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G (2007) TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131:1124-1136.
73. Sakhi S, Sun N, Wing LL, Mehta P, Schreiber SS (1996) Nuclear accumulation of p53 protein following kainic acid-induced seizures. Neuroreport 7:493-496. (Pubitemid 26105025)
74. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS (1997) Induction of tumor suppressor p53 and DNA fragmentation in organotypic hippocampal cultures following excitotoxin treatment. Exp Neurol 145:81-88.
75. Saller F, Villoutreix BO, Amelot A, Kaabache T, Le Bonniec BF, Aiach M, Gandrille S, Borgel D (2005) The gamma-carboxyglutamic acid domain of anticoagulant protein S is involved in activated protein C cofactor activity, independently of phospholipid binding. Blood 105:122-130.
76. Saller F, Brisset AC, Tchaikovski SN, Azevedo M, Chrast R, Fernández JA, Schapira M, Hackeng TM, Griffin JH, Angelillo-Scherrer A (2009) Generation and phenotypic analysis of protein S-deficient mice. Blood 114:2307-2314.
77. Saposnik B, Borgel D, Aiach M, Gandrille S (2003) Functional properties of the sex-hormone-binding globulin (SHBG)-like domain of the anticoagulant protein S. Eur J Biochem 270:545-555. (Pubitemid 36177321)
78. Shankar SL, O'Guin K, Kim M, Varnum B, Lemke G, Brosnan CF, Shafit-Zagardo B (2006) Gas6/Axl signaling activates the phosphatidylinositol 3-kinase/Akt1 survival pathway to protect oligodendrocytes from tumor necrosis factor α-induced apoptosis. J Neurosci 26:5638-5648.
79. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matsuda H, Tsujimoto Y (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13:21-29.
80. Stanika RI, Pivovarova NB, Brantner CA, Watts CA, Winters CA, Andrews SB (2009) Coupling diverse routes of calcium entry to mitochondrial dysfunction and glutamate excitotoxicity. Proc Natl Acad Sci U S A 106:9854-9859.
81. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C, Mattsson K, Fisher J, Gies DR, Jones PF (1995) The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 80:661-670.
82. + channels, glutamate release, and NMDA receptors mediates delayed neurodegeneration through nitric oxide formation. J Neurosci 16:5004-5013.
83. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446. (Pubitemid 29078912)
84. Takeuchi H, Mizuno T, Zhang G, Wang J, Kawanokuchi J, Kuno R, Suzumura A (2005) Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport. J Biol Chem 280:10444-10454.
85. Tan Z, Sun X, Hou FS, Oh HW, Hilgenberg LG, Hol EM, van Leeuwen FW, Smith MA, O'Dowd DK, Schreiber SS (2007) Mutant ubiquitin found in Alzheimer's disease causes neuritic beading of mitochondria in association with neuronal degeneration. Cell Death Differ 14:1721-1732.
86. Tenneti L, Lipton SA (2000) Involvement of activated caspase-3-like proteases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem 74:134-142.
87. Tenneti L, D'Emilia DM, Troy CM, Lipton SA (1998) Role of caspases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem 71:946-959.
88. Trinh E, Boutillier AL, Loeffler JP (2001) Regulation of the retinoblastoma-dependent Mdm2 and E2F-1 signaling pathways during neuronal apoptosis. Mol Cell Neurosci 17:342-353. (Pubitemid 32176490)
89. Uberti D, Belloni M, Grilli M, Spano P, Memo M (1998) Induction of tumour-suppressor phosphoprotein p53 in the apoptosis of cultured rat cerebellar neurones triggered by excitatory amino acids. Eur J Neurosci 10:246-254.
90. Uehara H, Shacter E (2008) 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 180:2522-2530.
91. Valverde P, Obin MS, Taylor A (2004) Role of Gas6/Axl signaling in lens epithelial cell proliferation and survival. Exp Eye Res 78:27-37.
92. Wang H, Yu SW, Koh DW, Lew J, Coombs C, Bowers W, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 24:10963-10973. (Pubitemid 39602407)
93. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922-2933.
94. Wang Y, Dong XX, Cao Y, Liang ZQ, Han R, Wu JC, Gu ZL, Qin ZH (2009) p53 induction contributes to excitotoxic neuronal death in rat striatum through apoptotic and autophagic mechanisms. Eur J Neurosci 30:2258-2270.
95. Webb JH, Blom AM, Dahlbäck B (2002) Vitamin K-dependent protein S localizing complement regulator C4b-binding protein to the surface of apoptotic cells. J Immunol 169:2580-2586.
96. Weinger JG, Gohari P, Yan Y, Backer JM, Varnum B, Shafit-Zagardo B (2008) In brain, Axl recruits Grb2 and the p85 regulatory subunit of PI3 kinase; in vitro mutagenesis defines the requisite binding sites for downstream Akt activation. J Neurochem 106:134-146.
97. Woodhouse A, Vickers JC, Adlard PA, Dickson TC (2009) Dystrophic neurites in TgCRND8 and Tg2576 mice mimic human pathological brain aging. Neurobiol Aging 30:864-874.
98. Xiang H, Hochman DW, Saya H, Fujiwara T, Schwartzkroin PA, Morrison RS (1996) Evidence for p53-mediated modulation of neuronal viability. J Neurosci 16:6753-6765.
99. Yang X, Fraser M, Abedini MR, Bai T, Tsang BK (2008) Regulation of apoptosis-inducing factor-mediated, cisplatin-induced apoptosis by Akt. Br J Cancer 98:803-808.
100. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259-263. (Pubitemid 34761289)
101. Zhong J, Russell SL, Pritchett DB, Molinoff PB, Williams K (1994) Expression of mRNAs encoding subunits of the N-methyl-D-aspartate receptor in cultured cortical neurons. Mol Pharmacol 45:846-853.
102. Zhu D, Wang Y, Singh I, Bell RD, Deane R, Zhong Z, Sagare A, Winkler EA, Zlokovic BV (2010) Protein S controls hypoxic/ischemic blood-brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor. Blood 115:4963-4972.
103. Zuckerman V, Wolyniec K, Sionov RV, Haupt S, Haupt Y (2009) Tumour suppression by p53: the importance of apoptosis and cellular senescence. J Pathol 219:3-15.