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01-06-2015 | Review Article

TAM receptor deficiency affects adult hippocampal neurogenesis

Authors: Rui Ji, Lingbin Meng, Qiutang Li, Qingxian Lu

Published in: Metabolic Brain Disease | Issue 3/2015

Abstract

The Tyro3, Axl and Mertk (TAM) subfamily of receptor protein tyrosine kinases functions in cell growth, differentiation, survival, and most recently found, in the regulation of immune responses and phagocytosis. All three receptors and their ligands, Gas6 (growth arrest-specific gene 6) and protein S, are expressed in the central nervous system (CNS). TAM receptors play pivotal roles in adult hippocampal neurogenesis. Loss of these receptors causes a comprised neurogenesis in the dentate gyrus of adult hippocampus. TAM receptors have a negative regulatory effect on microglia and peripheral antigen-presenting cells, and play a critical role in preventing overproduction of pro-inflammatory cytokines detrimental to the proliferation, differentiation, and survival of adult neuronal stem cells (NSCs). Besides, these receptors also play an intrinsic trophic function in supporting NSC survival, proliferation, and differentiation into immature neurons. All these events collectively ensure a sustained neurogenesis in adult hippocampus.

Aimone JB, Deng W, Gage FH (2011) Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589–596PubMedCentralPubMed

Allen MP, Zeng C, Schneider K, Xiong X, Meintzer MK et al (1999) Growth arrest-specific gene 6 (Gas6)/adhesion related kinase (Ark) signaling promotes gonadotropin-releasing hormone neuronal survival via extracellular signal-regulated kinase (ERK) and Akt. Mol Endocrinol 13:191–201PubMed

Anderson HA, Maylock CA, Williams JA, Paweletz CP, Shu H et al (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 4:87–91PubMed

Anwar A, Keating AK, Joung D, Sather S, Kim GK et al (2009) Mer tyrosine kinase (MerTK) promotes macrophage survival following exposure to oxidative stress. J Leukoc Biol 86:73–79PubMedCentralPubMed

Bachstetter AD, Xing B, de Almeida L, Dimayuga ER, Watterson DM et al (2011) Microglial p38alpha MAPK is a key regulator of proinflammatory cytokine up-regulation induced by toll-like receptor (TLR) ligands or beta-amyloid (Abeta). J Neuroinflammation 8:79PubMedCentralPubMed

Bellosta P, Zhang Q, Goff SP, Basilico C (1997) Signaling through the ARK tyrosine kinase receptor protects from apoptosis in the absence of growth stimulation. Oncogene 15

Benzakour O, Formstone C, Rahman S, Kanthou C, Dennehy U et al (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 308:481–485PubMedCentralPubMed

Bernier PJ, Bédard A, Vinet J, Lévesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci 99:11464–11469PubMedCentralPubMed

Binder MD, Cate HS, Prieto AL, Kemper D, Butzkueven H et al (2008) Gas6 deficiency increases oligodendrocyte loss and microglial activation in response to cuprizone-induced demyelination. J Neurosci 28:5195–5206PubMedCentralPubMed

Braunger J, Schleithoff L, Schulz AS, Kessler H, Lammers R, et al. (1997) Intracellular signaling of the Ufo/Axl receptor tyrosine kinase is mediated mainly by a multi-substrate docking-site. Oncogene 14

Breitner JC, Baker LD, Montine TJ, Meinert CL, Lyketsos CG et al (2011) Extended results of the Alzheimer’s disease anti-inflammatory prevention trial. Alzheimers Dement 7:402–411PubMedCentralPubMed

Brown JE, Krodel M, Pazos M, Lai C, Prieto AL (2012) Cross-phosphorylation, signaling and proliferative functions of the Tyro3 and Axl receptors in Rat2 cells. PLoS One 7:e36800PubMedCentralPubMed

Butovsky O, Talpalar AE, Ben-Yaakov K, Schwartz M (2005) Activation of microglia by aggregated β-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-γ and IL-4 render them protective. Mol Cell Neurosci 29:381–393PubMed

Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE et al (2006) Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149–160PubMed

Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L (2008) In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 56:412–425PubMed

Carpentier PA, Palmer TD (2009) Immune influence on adult neural stem cell regulation and function. Neuron 64:79–92PubMedCentralPubMed

Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ et al (2005) Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49:360–374PubMed

Carrera Silva EA, Chan PY, Joannas L, Errasti AE, Gagliani N et al (2013) T cell-derived protein S engages TAM receptor signaling in dendritic cells to control the magnitude of the immune response. Immunity 39:160–170PubMedCentralPubMed

Carson MJ, Reilly CR, Sutcliffe JG, Lo D (1998) Mature microglia resemble immature antigen‐presenting cells. Glia 22:72–85PubMed

Chan MC, Mather JP, McCray G, Lee WM (2000) Identification and regulation of receptor tyrosine kinases Rse and Mer and their ligand Gas6 in testicular somatic cells. J Androl 21:291–302PubMed

Chen J, Magavi SS, Macklis JD (2004) Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci U S A 101:16357–16362PubMedCentralPubMed

Chen X, Ji R, Jiang X, Yang R, Liu F, et al. (2014) Iterative type I polyketide synthases involved in enediyne natural product biosynthesis. Iubmb Life

Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC et al (2002) Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 196:135–140PubMedCentralPubMed

Conover JC, Shook BA (2011) Aging of the subventricular zone neural stem cell niche. Aging Dis 2:49PubMedCentralPubMed

D’Arcangelo D, Gaetano C, Capogrossi MC (2002) Acidification prevents endothelial cell apoptosis by Axl activation. Circ Res 91:e4–e12PubMed

Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339–350PubMedCentralPubMed

Dickstein JB, Moldofsky H, Hay JB (2000) Brain–blood permeability: TNF-alpha promotes escape of protein tracer from CSF to blood. Am J Physiol Regul Integr Comp Physiol 279:R148–R151PubMed

Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100:13632–13637PubMedCentralPubMed

Ekdahl CT, Kokaia Z, Lindvall O (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158:1021–1029PubMed

Emsley JG, Mitchell BD, Kempermann G, Macklis JD (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75:321–341PubMed

Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138–145PubMed

Feng W, Yasumura D, Matthes MT, LaVail MM, Vollrath D (2002) Mertk triggers uptake of photoreceptor outer segments during phagocytosis by cultured retinal pigment epithelial cells. J Biol Chem 277:17016–17022PubMed

Finckh A, Aronson MD (2005) Cardiovascular risks of cyclooxygenase-2 inhibitors: where we stand now. Ann Intern Med 142:212–214PubMed

Fridell Y, Jin Y, Quilliam LA, Burchert A, McCloskey P et al (1996) Differential activation of the Ras/extracellular-signal-regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Mol Cell Biol 16:135–145PubMedCentralPubMed

Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438PubMed

Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ et al (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci 92:11879PubMedCentralPubMed

Gao X, Chen H, Schwarzschild MA, Ascherio A (2011) Use of ibuprofen and risk of Parkinson disease. Neurology 76:863–869PubMedCentralPubMed

Gely‐Pernot A, Coronas V, Harnois T, Prestoz L, Mandairon N et al (2012) An endogenous vitamin K‐dependent mechanism regulates cell proliferation in the brain subventricular stem cell niche. Stem Cells 30:719–731PubMedCentralPubMed

Ming G-l, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702PubMedCentralPubMed

Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918–934PubMedCentralPubMed

Gómez-Nicola D, Valle-Argos B, Pallas-Bazarra N, Nieto-Sampedro M (2011) Interleukin-15 regulates proliferation and self-renewal of adult neural stem cells. Mol Biol Cell 22:1960–1970PubMedCentralPubMed

Gorina R, Font-Nieves M, Marquez-Kisinousky L, Santalucia T, Planas AM (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59:242–255PubMed

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 12:471–480PubMed

Goruppi S, Ruaro E, Varnum B, Schneider C (1997) Requirement of phosphatidylinositol 3-kinase-dependent pathway and Src for Gas6-Axl mitogenic and survival activities in NIH 3 T3 fibroblasts. Mol Cell Biol 17:4442–4453PubMedCentralPubMed

Goruppi S, Ruaro E, Varnum B, Schneider C (1999) Gas6-mediated survival in NIH3T3 cells activates stress signalling cascade and is independent of Ras. Oncogene 18

Grommes C, Lee CD, Wilkinson BL, Jiang Q, Koenigsknecht-Talboo JL et al (2008) Regulation of microglial phagocytosis and inflammatory gene expression by Gas6 acting on the Axl/Mer family of tyrosine kinases. J Neuroimmune Pharm 3:130–140

Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140–155PubMed

Hasanbasic I, Cuerquis J, Varnum B, Blostein MD (2010) Intracellular signaling pathways involved in. J Immunol 185:5859–5868

Heiring C, Dahlback B, Muller YA (2004) Ligand recognition and homophilic interactions in Tyro3: structural insights into the Axl/Tyro3 receptor tyrosine kinase family. J Biol Chem 279:6952–6958PubMed

Hermann A, Maisel M, Wegner F, Liebau S, Kim DW et al (2006) Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 24:949–964PubMed

Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM et al (2005) Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 65:9294–9303PubMed

Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S et al (2006) Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26:9703–9712PubMed

Jacob A, Hack B, Chiang E, Garcia JG, Quigg RJ et al (2010) C5a alters blood–brain barrier integrity in experimental lupus. FASEB J 24:1682–1688PubMedCentralPubMed

James W, Hutchinson P, Bullard D, Hickey M (2006) Cerebral leucocyte infiltration in lupus‐prone MRL/MpJ‐faslpr mice − roles of intercellular adhesion molecule‐1 and P‐selectin. Clin Exp Immunol 144:299–308PubMedCentralPubMed

Janssen JW, Schulz AS, Steenvoorden AC, Schmidberger M, Strehl S et al (1991) A novel putative tyrosine kinase receptor with oncogenic potential. Oncogene 6:2113–2120PubMed

Jaturapatporn D, Isaac M, McCleery J, Tabet N (2012) Aspirin, steroidal and non-steroidal anti-inflammatory drugs for the treatment of Alzheimer’s disease. Cochrane Database Syst Rev 2

Ji R, Tian S, Lu HJ, Lu Q, Zheng Y et al (2013) TAM receptors affect adult brain neurogenesis by negative regulation of microglial cell activation. J Immunol 191:6165–6177PubMed

Ji R, Yan F, Yang R, Meng L, Ma X (2014) The preparation and evaluation of DNA microarray probes for detecting Bacillus anthracis. J Mıcrobıol Mıcrobıal Res 2:8–16

Jia R, Hanafusa H (1994) The proto-oncogene of v-eyk (v-ryk) is a novel receptor-type protein tyrosine kinase with extracellular Ig/GN-III domains. J Biol Chem 269:1839–1844PubMed

Kim MO, Kim S-H, Cho Y-Y, Nadas J, Jeong C-H et al (2012) ERK1 and ERK2 regulate embryonic stem cell self-renewal through phosphorylation of Klf4. Nat Struct Mol Biol 19:283–290PubMed

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 279:28766–28770PubMed

Korshunov VA, Mohan AM, Georger MA, Berk BC (2006) Axl, a receptor tyrosine kinase, mediates flow-induced vascular remodeling. Circ Res 98:1446–1452PubMed

Kuzumaki N, Ikegami D, Imai S, Narita M, Tamura R et al (2010) Enhanced IL-1beta production in response to the activation of hippocampal glial cells impairs neurogenesis in aged mice. Synapse 64:721–728PubMed

Lai C, Lemke G (1991) An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6:691–704PubMed

Lai C, Gore M, Lemke G (1994) Structure, expression, and activity of Tyro 3, a neural adhesion-related receptor tyrosine kinase. Oncogene 9:2567–2578PubMed

Lai K, Kaspar BK, Gage FH, Schaffer DV (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6:21–27PubMed

Laplagne DA, Kamienkowski JE, Espósito MS, Piatti VC, Zhao C et al (2007) Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25:2973–2981PubMed

Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R et al (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100:8514–8519PubMedCentralPubMed

Lemke G, Lu Q (2003) Macrophage regulation by Tyro 3 family receptors. Curr Opin Immunol 15:31–36PubMed

Lemke G, Rothlin CV (2008) Immunobiology of the TAM receptors. Nat Rev Immunol 8:327–336PubMedCentralPubMed

Leoutsakos JMS, Muthen BO, Breitner J, Lyketsos CG (2012) Effects of non‐steroidal anti‐inflammatory drug treatments on cognitive decline vary by phase of pre‐clinical Alzheimer disease: findings from the randomized controlled Alzheimer’s disease anti‐inflammatory prevention trial. Int J Geriatr Psychiatry 27:364–374PubMedCentralPubMed

Li Q, Lu Q, Lu H, Tian S, Lu Q (2013) Systemic autoimmunity in TAM triple knockout mice causes inflammatory brain damage and cell death. PLoS One 8:e64812PubMedCentralPubMed

Li R-h, Chen J, Hammonds G, Phillips H, Armanini M et al (1996) Identification of Gas6 as a growth factor for human Schwann cells. J Neurosci 16:2012–2019

Lie D-C, Colamarino SA, Song H-J, Désiré L, Mira H et al (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370–1375PubMed

Lillien L, Raphael H (2000) BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 127:4993–5005PubMed

Linger RM, Keating AK, Earp HS, Graham DK (2008) TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 100:35–83PubMedCentralPubMed

Liu YP, Lin HI, Tzeng SF (2005) Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res 1054:152–158PubMed

Lu Q, Lemke G (2001) Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306–311PubMed

Lu Q, Gore M, Zhang Q, Camenisch T, Boast S et al (1999) Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398:723–728PubMed

Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951–955PubMed

Mark MR, Scadden DT, Wang Z, Gu Q, Goddard A et al (1994) rse, a novel receptor-type tyrosine kinase with homology to Axl/Ufo, is expressed at high levels in the brain. J Biol Chem 269:10720–10728PubMed

Markakis EA, Gage FH (1999) Adult‐generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406:449–460PubMed

McHale JF, Harari OA, Marshall D, Haskard DO (1999) TNF-α and IL-1 sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice. J Immunol 163:3993–4000PubMed

Melaragno MG, Cavet ME, Yan C, Tai L-K, Jin Z-G et al (2004) Gas6 inhibits apoptosis in vascular smooth muscle: role of Axl kinase and Akt. J Mol Cell Cardiol 37:881–887PubMed

Meng L, Jiang X, Ji R (2014) Role of IL6 and TNFα in hippocampal neurogenesis of TAM triple knockout mice. Int J Adv Innovat Thoughts Ideas 3:109

Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760–1765PubMed

Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C et al (2000) Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499–510PubMed

Nakano T, Kawamoto K, Higashino K-I, Arita H (1996) Prevention of growth arrest-induced cell death of vascular smooth muscle cells by a product of growth arrest-specific gene,< i > gas6</i> FEBS Lett 387:78–80PubMed

Nakano T, Ishimoto Y, Kishino J, Umeda M, Inoue K et al (1997) Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J Biol Chem 272:29411–29414PubMed

Nandrot EF, Kim Y, Brodie SE, Huang X, Sheppard D et al (2004) Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J Exp Med 200:1539–1545PubMedCentralPubMed

Nishioku T, Matsumoto J, Dohgu S, Sumi N, Miyao K et al (2010) Tumor necrosis factor-α mediates the blood–brain barrier dysfunction induced by activated microglia in mouse brain microvascular endothelial cells. J Pharmacol Sci 112:251PubMed

O’Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B et al (1991) axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 11:5016–5031PubMedCentralPubMed

O’Donnell K, Harkes IC, Dougherty L, Wicks IP (1999) Expression of receptor tyrosine kinase Axl and its ligand Gas6 in rheumatoid arthritis: evidence for a novel endothelial cell survival pathway. Am J Pathol 154:1171–1180PubMedCentralPubMed

Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173:3916–3924PubMed

Ozaki H, Ishii K, Horiuchi H, Arai H, Kawamoto T et al (1999) Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol 163:553–557PubMed

Palmer TD, Takahashi J, Gage FH (1997) The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8:389–404PubMed

Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B et al (2002) Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci U S A 99:13211–13216PubMedCentralPubMed

Pierce A, Bliesner B, Xu M, Nielsen-Preiss S, Lemke G et al (2008) Axl and Tyro3 modulate female reproduction by influencing gonadotropin-releasing hormone neuron survival and migration. Mol Endocrinol 22:2481–2495PubMedCentralPubMed

Prasad D, Rothlin CV, Burrola P, Burstyn-Cohen T, Lu Q et al (2006) TAM receptor function in the retinal pigment epithelium. Mol Cell Neurosci 33:96–108PubMed

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 425:295–314PubMed

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 150:319–334PubMedCentralPubMed

Rees K, Stowe R, Patel S, Ives N, Breen K, et al. (2011) Non-steroidal anti-inflammatory drugs as disease-modifying agents for Parkinson’s disease: evidence from observational studies. Cochrane Database Syst Rev 11

Rescigno J, Mansukhani A, Basilico C (1991) A putative receptor tyrosine kinase with unique structural topology. Oncogene 6:1909–1913PubMed

Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707PubMed

Richards L, Kilpatrick T, Bartlett P (1992) De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci 89:8591PubMedCentralPubMed

Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9:429–439PubMed

Rolls A, Shechter R, London A, Ziv Y, Ronen A et al (2007) Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 9:1081–1088PubMed

Rothlin CV, Ghosh S, Zuniga EI, Oldstone M, Lemke G (2007) TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131:1124–1136PubMed

Saijo K, Winner B, Carson CT, Collier JG, Boyer L et al (2009) A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137:47–59PubMedCentralPubMed

Samii A, Etminan M, Wiens MO, Jafari S (2009) NSAID use and the risk of Parkinson’s DISEASE. Drugs Aging 26:769–779PubMed

Samuels IS, Karlo JC, Faruzzi AN, Pickering K, Herrup K et al (2008) Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function. J Neurosci 28:6983–6995PubMedCentralPubMed

Sasaki T, Knyazev PG, Clout NJ, Cheburkin Y, Gohring W et al (2006) Structural basis for Gas6-Axl signalling. EMBO J 25:80–87PubMedCentralPubMed

Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R et al (2001) Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411:207–211PubMed

Seitz HM, Camenisch TD, Lemke G, Earp HS, Matsushima GK (2007) Macrophages and dendritic cells use different Axl/Mertk/Tyro3 receptors in clearance of apoptotic cells. J Immunol 178:5635–5642PubMed

Shankar SL, O’Guin K, Cammer M, McMorris FA, Stitt TN et al (2003) The growth arrest-specific gene product Gas6 promotes the survival of human oligodendrocytes via a phosphatidylinositol 3-kinase-dependent pathway. J Neurosci 23:4208–4218PubMed

Shankar SL, O’Guin K, Kim M, Varnum B, Lemke G et al (2006) Gas6/Axl signaling activates the phosphatidylinositol 3-kinase/Akt1 survival pathway to protect oligodendrocytes from tumor necrosis factorα-induced apoptosis. J Neurosci 26:5638–5648PubMed

Sharif MN, Sosic D, Rothlin CV, Kelly E, Lemke G et al (2006) Twist mediates suppression of inflammation by type I IFNs and Axl. J Exp Med 203:1891–1901PubMedCentralPubMed

Shrikant P, Benveniste EN (1996) The central nervous system as an immunocompetent organ: role of glial cells in antigen presentation. J Immunol 157:1819–1822PubMed

Yamamoto S-I, Nagao M, Sugimori M, Kosako H, Nakatomi H et al (2001) Transcription factor expression and Notch-dependent regulation of neural progenitors in the adult rat spinal cord. J Neurosci 21:9814–9823PubMed

Son B-K, Kozaki K, Iijima K, Eto M, Kojima T et al (2006) Statins protect human aortic smooth muscle cells from inorganic phosphate-induced calcification by restoring Gas6-Axl survival pathway. Circ Res 98:1024–1031PubMed

Stenhoff J, Dahlbäck B, Hafizi S (2004) Vitamin K-dependent Gas6 activates ERK kinase and stimulates growth of cardiac fibroblasts. Biochem Biophys Res Commun 319:871–878PubMed

Stewart WF, Kawas C, Corrada M, Metter EJ (1997) Risk of Alzheimer’s disease and duration of NSAID use. Neurology 48:626–632PubMed

Stitt TN, Conn G, Goret M, Lai C, Bruno J et al (1995) The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 80:661–670PubMed

St-John WM (1998) Neurogenesis of patterns of automatic ventilatory activity. Prog Neurobiol 56:97–117PubMed

Suh H, Deng W, Gage FH (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev 25:253–275

Taylor IC, Roy S, Yaswen P, Stampfer MR, Varmus HE (1995) Mouse mammary tumors express elevated levels of RNA encoding the murine homology of SKY, a putative receptor tyrosine kinase. J Biol Chem 270:6872–6880PubMed

Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE et al (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901–907PubMedCentralPubMed

Tsao N, Hsu HP, Wu CM, Liu CC, Lei HY (2001) Tumour necrosis factor-alpha causes an increase in blood–brain barrier permeability during sepsis. J Med Microbiol 50:812–821PubMed

Tsou WI, Nguyen KQ, Calarese DA, Garforth SJ, Antes AL et al (2014) Receptor tyrosine kinases, TYRO3, AXL, and MER, demonstrate distinct patterns and complex regulation of Ligand-induced activation. J Biol Chem 289:25750–25763PubMed

Valverde P, Obin M, Taylor A (2004) Role of Gas6/Axl signaling in lens epithelial cell proliferation and survival. Exp Eye Res 78:27–37PubMed

Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM et al (2006) Microglia instruct subventricular zone neurogenesis. Glia 54:815–825PubMed

Wang J, Zhang H, Young AG, Qiu R, Argalian S et al (2011) Transcriptome analysis of neural progenitor cells by a genetic dual reporter strategy. Stem Cells 29:1589–1600PubMedCentralPubMed

Weinger JG, Gohari P, Yan Y, Backer JM, Varnum B et al (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 106:134–146PubMedCentralPubMed

Wexler EM, Paucer A, Kornblum HI, Palmer TD, Geschwind DH (2009) Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells 27:1130–1141PubMedCentralPubMed

Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C et al (2009) CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol 182:3979–3984PubMed

Wong D, Dorovini-Zis K (1992) Upregulation of intercellular adhesion molecule-1 (ICAM-1) expression in primary cultures of human brain microvessel endothelial cells by cytokines and lipopolysaccharide. J Neuroimmunol 39:11–21PubMed

Wu Y, Singh S, Georgescu M-M, Birge RB (2005) A role for Mer tyrosine kinase in αvβ5 integrin-mediated phagocytosis of apoptotic cells. J Cell Sci 118:539–553PubMed

Xiong W, Chen Y, Wang H, Wu H, Lu Q et al (2008) Gas6 and the Tyro 3 receptor tyrosine kinase subfamily regulate the phagocytic function of Sertoli cells. Reproduction 135:77–87PubMed

Yagami T, Ueda K, Asakura K, Sakaeda T, Nakazato H et al (2002) Gas6 rescues cortical neurons from amyloid β protein-induced apoptosis. Neuropharmacology 43:1289–1296PubMed

Yan X-B, Wang S-S, Hou H-L, Ji R, Zhou J-N (2007) Lithium improves the behavioral disorder in rats subjected to transient global cerebral ischemia. Behav Brain Res 177:282–289PubMed

Yanagita M, Ishii K, Ozaki H, Arai H, Nakano T et al (1999) Mechanism of inhibitory effect of warfarin on mesangial cell proliferation. J Am Soc Nephrol 10:2503–2509PubMed

Yang GY, Gong C, Qin Z, Liu XH, Lorris Betz A (1999) Tumor necrosis factor alpha expression produces increased blood–brain barrier permeability following temporary focal cerebral ischemia in mice. Brain Res Mol Brain Res 69:135–143PubMed

Ye F, Han L, Lu Q, Dong W, Chen Z et al (2011) Retinal self-antigen induces a predominantly Th1 effector response in Axl and Mertk double-knockout mice. J Immunol 187:4178–4186PubMedCentralPubMed

Yin JL, Pilmore HL, Yan YQ, McCaughan GW, Bishop GA et al (2002) Expression of growth arrest-specific gene 6 and its receptors in a rat model of chronic renal transplant rejection. Transplantation 73:657–660PubMed

Zagorska A, Traves PG, Lew ED, Dransfield I, Lemke G (2014) Diversification of TAM receptor tyrosine kinase function. Nat Immunol 15:920–928PubMedCentralPubMed

Zhao M, Momma S, Delfani K, Carlén M, Cassidy RM et al (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci 100:7925–7930PubMedCentralPubMed

Zheng Y, Zhang L, Lu Q, Wang X, Yu F et al (2009) NGF-induced Tyro3 and Axl function as survival factors for differentiating PC12 cells. Biochem Biophys Res Commun 378:371–375PubMed

Zhu D, Wang Y, Singh I, Bell RD, Deane R et al (2010) Protein S controls hypoxic/ischemic blood–brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor. Blood 115:4963–4972PubMedCentralPubMed

Title: TAM receptor deficiency affects adult hippocampal neurogenesis
Authors: Rui Ji
Lingbin Meng
Qiutang Li
Qingxian Lu
Publication date: 01-06-2015
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 3/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-014-9636-y

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TAM receptor deficiency affects adult hippocampal neurogenesis

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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