Home LiteratureArticle Details
PMID: 18651636 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

ERM proteins regulate growth cone responses to Sema3A.

The Journal of comparative neurology ·Vol. 510 ·No. 4 ·2008-10-01 ·Pages 351-66

Mintz CD, Carcea I, McNickle DG, Dickson TC, Ge Y, Salton SR, Benson DL

Abstract

Axonal growth cones initiate and sustain directed growth in response to cues in their environment. A variety of events such as receptor internalization, kinase activation, and actin rearrangement can be stimulated by guidance cues and are essential for mediating targeted growth cone behavior. Surprisingly little is known about how such disparate actions are coordinated. Our data suggest that ezrin, radixin, and moesin (ERMs), a family of highly homologous, multifunctional proteins may be able to coordinate growth cone responses to the guidance cue Semaphorin 3A (Sema3A). We show that active ERMs concentrate asymmetrically in neocortical growth cones, are rapidly and transiently inactivated by Sema3A, and are required for Sema3A-mediated growth cone collapse and guidance. The FERM domain of active ERMs regulates internalization of the Sema3A receptor, Npn1, and its coreceptor, L1CAM, while the ERM C-terminal domain binds and caps F-actin. Our data support a model in which ERMs can coordinate membrane and actin dynamics in response to Sema3A.

MeSH Terms
Actins/physiology Animals Axons/physiology Chickens Cytoskeletal Proteins/genetics DNA-Binding Proteins/genetics,metabolism Growth Cones/physiology Mice Mutation Plasmids Rabbits Receptors, Cell Surface/physiology Semaphorin-3A/genetics,metabolism Transcription Factors/genetics,metabolism
Chemicals
Actins Cytoskeletal Proteins DNA-Binding Proteins Etv5 protein, mouse Receptors, Cell Surface Sema3a protein, mouse Semaphorin-3A Transcription Factors ezrin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Mintz C David
Fishberg Department of Neuroscience, Mount Sinai School of Medicine, New York, NY 10029, USA.
Carcea Ioana
McNickle Daniel G
Dickson Tracey C
Ge Yongchao
Salton Stephen R J
Benson Deanna L
References (117)
117 references, click to expand
  1. Recycling of the cell adhesion molecule L1 in axonal growth cones.
    J Neurosci. 2000 May 15;20(10):3676-86 PMID: 10804209
  2. The mechanism of axon growth: what we have learned from the cell adhesion molecule L1.
    Mol Neurobiol. 2003 Dec;28(3):219-28 PMID: 14709786
  3. Ezrin NH2-terminal domain inhibits the cell extension activity of the COOH-terminal domain.
    J Cell Biol. 1995 Mar;128(6):1081-93 PMID: 7896873
  4. Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain.
    Neuron. 1993 Aug;11(2):237-51 PMID: 8352941
  5. Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling.
    J Neurosci. 2006 Mar 15;26(11):2971-80 PMID: 16540575
  6. The two poles of the lymphocyte: specialized cell compartments for migration and recruitment.
    Cell Adhes Commun. 1998;6(2-3):125-33 PMID: 9823463
  7. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1.
    Nat Neurosci. 2006 Oct;9(10):1247-56 PMID: 16980963
  8. Looking into growth cones.
    Trends Neurosci. 1989 Dec;12(12):503-6 PMID: 2480665
  9. Adaptation in the chemotactic guidance of nerve growth cones.
    Nature. 2002 May 23;417(6887):411-8 PMID: 11986620
  10. Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton.
    J Neurosci. 2004 Mar 24;24(12):3002-12 PMID: 15044539
  11. Orientation of chemotactic cells and growth cones: models and mechanisms.
    J Cell Sci. 1999 Sep;112 ( Pt 17):2867-74 PMID: 10444381
  12. Interaction of radixin with Rho small G protein GDP/GTP exchange protein Dbl.
    Oncogene. 1998 Jun 25;16(25):3279-84 PMID: 9681826
  13. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment.
    Nature. 1986 Oct 23-29;323(6090):712-5 PMID: 3773996
  14. Molecular dissection of radixin: distinct and interdependent functions of the amino- and carboxy-terminal domains.
    J Cell Biol. 1995 May;129(4):1007-22 PMID: 7744951
  15. A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer's disease.
    J Neurochem. 2004 Nov;91(3):716-36 PMID: 15485501
  16. Surface expression of the netrin receptor UNC5H1 is regulated through a protein kinase C-interacting protein/protein kinase-dependent mechanism.
    J Neurosci. 2003 Dec 10;23(36):11279-88 PMID: 14672991
  17. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family.
    J Cell Biol. 1994 Sep;126(6):1445-53 PMID: 8089177
  18. CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS.
    Proc Natl Acad Sci U S A. 1963 Oct;50:703-10 PMID: 14077501
  19. Dual regulation of actin rearrangement through lysophosphatidic acid receptor in neuroblast cell lines: actin depolymerization by Ca(2+)-alpha-actinin and polymerization by rho.
    Mol Biol Cell. 2002 Aug;13(8):2692-705 PMID: 12181339
  20. Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane.
    J Cell Biol. 2000 Jul 10;150(1):193-203 PMID: 10893267
  21. Signalling and crosstalk of Rho GTPases in mediating axon guidance.
    Nat Cell Biol. 2003 Jan;5(1):38-45 PMID: 12510192
  22. Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation.
    J Cell Biol. 2004 Oct 25;167(2):327-37 PMID: 15504914
  23. When a diffusible axon guidance cue stops diffusing: roles for netrins in adhesion and morphogenesis.
    Curr Opin Neurobiol. 2006 Oct;16(5):529-34 PMID: 16935486
  24. Endocytosis-dependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation.
    Nat Neurosci. 2005 Feb;8(2):179-86 PMID: 15643427
  25. ERMs colocalize transiently with L1 during neocortical axon outgrowth.
    J Comp Neurol. 2003 Sep 29;464(4):438-48 PMID: 12900915
  26. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones.
    Neuron. 2003 Mar 27;37(6):939-52 PMID: 12670423
  27. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III.
    Cell. 1997 Aug 22;90(4):739-51 PMID: 9288753
  28. Ethanol inhibits L1 cell adhesion molecule activation of mitogen-activated protein kinases.
    J Neurochem. 2006 Mar;96(5):1480-90 PMID: 16478533
  29. Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins.
    Neuron. 2005 Feb 17;45(4):513-23 PMID: 15721238
  30. Vav family GEFs link activated Ephs to endocytosis and axon guidance.
    Neuron. 2005 Apr 21;46(2):205-17 PMID: 15848800
  31. Mechanism of action of cytochalasin B on actin.
    Cell. 1980 Jun;20(2):329-41 PMID: 6893016
  32. Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization.
    Blood. 2003 Dec 1;102(12):3890-9 PMID: 12907449
  33. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker.
    J Cell Biol. 1993 Jan;120(1):129-39 PMID: 8416983
  34. Identification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor: In vivo expression and antitumor activity.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2573-8 PMID: 10688880
  35. cAMP-dependent protein kinase phosphorylation of EVL, a Mena/VASP relative, regulates its interaction with actin and SH3 domains.
    J Biol Chem. 2000 Nov 17;275(46):36143-51 PMID: 10945997
  36. Size, shape, and solubility of a class of releasable cell surface proteins of sympathetic neurons.
    J Neurosci. 1983 Dec;3(12):2518-24 PMID: 6655497
  37. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin.
    J Cell Biol. 2004 Mar 1;164(5):653-9 PMID: 14993232
  38. Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse.
    J Cell Biol. 2000 Apr 17;149(2):411-22 PMID: 10769032
  39. Radixin is a novel member of the band 4.1 family.
    J Cell Biol. 1991 Nov;115(4):1039-48 PMID: 1955455
  40. Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization.
    J Biol Chem. 1999 Dec 31;274(53):37965-73 PMID: 10608864
  41. The role of cytoskeleton in organizing growth cones: a microfilament-associated growth cone component depends upon microtubules for its localization.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1621-31 PMID: 2677024
  42. Normal development of mice and unimpaired cell adhesion/cell motility/actin-based cytoskeleton without compensatory up-regulation of ezrin or radixin in moesin gene knockout.
    J Biol Chem. 1999 Jan 22;274(4):2315-21 PMID: 9890997
  43. A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis.
    J Neurosci. 2000 Jun 1;20(11):4177-88 PMID: 10818153
  44. Guiding neuronal growth cones using Ca2+ signals.
    Trends Cell Biol. 2004 Jun;14(6):320-30 PMID: 15183189
  45. Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics.
    J Cell Biol. 2002 Sep 2;158(5):855-62 PMID: 12213833
  46. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane.
    Trends Biochem Sci. 1998 Aug;23(8):281-2 PMID: 9757824
  47. Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction.
    J Cell Biol. 1999 Sep 6;146(5):1097-106 PMID: 10477762
  48. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides.
    Science. 1998 Sep 4;281(5382):1515-8 PMID: 9727979
  49. Ezrin is an effector of hepatocyte growth factor-mediated migration and morphogenesis in epithelial cells.
    J Cell Biol. 1997 Jul 28;138(2):423-34 PMID: 9230083
  50. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain.
    Cell. 2000 Apr 28;101(3):259-70 PMID: 10847681
  51. Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM.
    Mol Cell Neurosci. 2004 May;26(1):89-100 PMID: 15121181
  52. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse.
    Nat Neurosci. 2001 Apr;4(4):367-73 PMID: 11276226
  53. Numb is an endocytic protein.
    J Cell Biol. 2000 Dec 11;151(6):1345-52 PMID: 11121447
  54. Growth cone advance is inversely proportional to retrograde F-actin flow.
    Neuron. 1995 Apr;14(4):763-71 PMID: 7536426
  55. Cellular motility driven by assembly and disassembly of actin filaments.
    Cell. 2003 Feb 21;112(4):453-65 PMID: 12600310
  56. The gradient-sensing mechanism in bacterial chemotaxis.
    Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509-12 PMID: 4560688
  57. The molecular basis for calcium-dependent axon pathfinding.
    Nat Rev Neurosci. 2006 Feb;7(2):115-25 PMID: 16429121
  58. Lipid rafts as organizing platforms for cell chemotaxis and axon guidance.
    Neuron. 2004 Apr 8;42(1):3-5 PMID: 15066259
  59. Specific expression of ezrin, a cytoskeletal-membrane linker protein, in a subset of chick retinotectal and sensory projections.
    Eur J Neurosci. 1999 Feb;11(2):545-58 PMID: 10051754
  60. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho.
    J Cell Biol. 1994 Aug;126(3):801-10 PMID: 8045941
  61. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin.
    Nature. 2002 Nov 7;420(6911):85-9 PMID: 12422219
  62. Regulation of growth cone actin filaments by guidance cues.
    J Neurobiol. 2004 Jan;58(1):92-102 PMID: 14598373
  63. Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins.
    J Cell Biol. 1999 Jun 28;145(7):1497-509 PMID: 10385528
  64. Response of radixin to perturbations of growth cone morphology and motility in chick sympathetic neurons in vitro.
    Cell Motil Cytoskeleton. 1996;34(2):122-36 PMID: 8769724
  65. AL-1-induced growth cone collapse of rat cortical neurons is correlated with REK7 expression and rearrangement of the actin cytoskeleton.
    Eur J Neurosci. 1997 Jan;9(1):177-88 PMID: 9042581
  66. Effect of basic compounds on the polymerization of clathrin.
    Biochemistry. 1981 Nov 10;20(23):6706-10 PMID: 7306530
  67. Involvement of phosphatidylinositol 3-kinase in stromal cell-derived factor-1 alpha-induced lymphocyte polarization and chemotaxis.
    J Immunol. 1999 Oct 1;163(7):4001-12 PMID: 10491003
  68. Filopodial calcium transients promote substrate-dependent growth cone turning.
    Science. 2001 Mar 9;291(5510):1983-7 PMID: 11239161
  69. Disruption of dynamic cell surface architecture of NIH3T3 fibroblasts by the N-terminal domains of moesin and ezrin: in vivo imaging with GFP fusion proteins.
    J Cell Sci. 1999 Jan;112 ( Pt 1):111-25 PMID: 9841908
  70. Structure and activity of the axon guidance protein MICAL.
    Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16830-5 PMID: 16275926
  71. CHL1 promotes Sema3A-induced growth cone collapse and neurite elaboration through a motif required for recruitment of ERM proteins to the plasma membrane.
    J Neurochem. 2008 Feb;104(3):731-44 PMID: 17995939
  72. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor.
    Nature. 1999 Sep 16;401(6750):286-90 PMID: 10499588
  73. Effects of cytochalasin and phalloidin on actin.
    J Cell Biol. 1987 Oct;105(4):1473-8 PMID: 3312229
  74. RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction.
    J Cell Sci. 2006 Aug 15;119(Pt 16):3413-23 PMID: 16899819
  75. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient.
    J Neurosci. 1996 Feb 1;16(3):1140-9 PMID: 8558243
  76. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site.
    J Cell Sci. 1996 Nov;109 ( Pt 11):2715-26 PMID: 8937989
  77. Regulation of F-actin binding to platelet moesin in vitro by both phosphorylation of threonine 558 and polyphosphatidylinositides.
    Mol Biol Cell. 1999 Aug;10(8):2669-85 PMID: 10436021
  78. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion.
    Cell. 2002 Jun 28;109(7):887-900 PMID: 12110185
  79. Post-translational modification and evoked release of two large surface proteins of sympathetic neurons.
    J Neurosci. 1983 Dec;3(12):2504-17 PMID: 6361221
  80. Antigenic expression of neuron-associated class III beta-tubulin isotype (h beta 4) and microtubule-associated protein 2 (MAP2) by the human retinoblastoma cell line WERI-Rb1. A comparative immunoblot and immunocytochemical study.
    Ophthalmic Res. 1990;22(1):57-66 PMID: 2188187
  81. Rho kinase activates ezrin-radixin-moesin (ERM) proteins and mediates their function in cortical neuron growth, morphology and motility in vitro.
    J Neurosci Res. 2007 Jan;85(1):34-46 PMID: 17075902
  82. Expression of L1 decreases during postnatal development of rat spinal cord.
    J Comp Neurol. 2003 Dec 15;467(3):375-88 PMID: 14608600
  83. Mechanisms and molecules that control growth cone guidance.
    Annu Rev Neurosci. 1996;19:341-77 PMID: 8833447
  84. Interdomain interactions of radixin in vitro.
    J Biol Chem. 1995 Oct 27;270(43):25324-7 PMID: 7592691
  85. The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway.
    J Neurosci. 1998 Jul 15;18(14):5311-21 PMID: 9651214
  86. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance.
    Neuron. 2000 Aug;27(2):237-49 PMID: 10985345
  87. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family.
    J Cell Biol. 2002 Jun 24;157(7):1105-12 PMID: 12070130
  88. Moesin: a member of the protein 4.1-talin-ezrin family of proteins.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8297-301 PMID: 1924289
  89. A new 82-kD barbed end-capping protein (radixin) localized in the cell-to-cell adherens junction: purification and characterization.
    J Cell Biol. 1989 Jun;108(6):2369-82 PMID: 2500445
  90. cAMP-induced switching in turning direction of nerve growth cones.
    Nature. 1997 Jul 17;388(6639):275-9 PMID: 9230436
  91. Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance.
    J Neurobiol. 2000 Aug;44(2):97-113 PMID: 10934315
  92. Patterning of cortical efferent projections by semaphorin-neuropilin interactions.
    Science. 1998 Dec 4;282(5395):1904-6 PMID: 9836643
  93. Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility.
    EMBO J. 2001 Jun 1;20(11):2723-41 PMID: 11387207
  94. Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites.
    Traffic. 2006 Aug;7(8):1060-77 PMID: 16734664
  95. The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors.
    Proc Natl Acad Sci U S A. 2006 Sep 5;103(36):13391-6 PMID: 16938849
  96. Suppression of radixin and moesin alters growth cone morphology, motility, and process formation in primary cultured neurons.
    J Cell Biol. 1998 Oct 19;143(2):443-55 PMID: 9786954
  97. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance.
    Annu Rev Neurosci. 2003;26:509-63 PMID: 12677003
  98. Protein interacting with C-kinase 1/protein kinase Calpha-mediated endocytosis converts netrin-1-mediated repulsion to attraction.
    J Neurosci. 2006 Mar 22;26(12):3192-205 PMID: 16554470
  99. Protein kinase A activation promotes plasma membrane insertion of DCC from an intracellular pool: A novel mechanism regulating commissural axon extension.
    J Neurosci. 2004 Mar 24;24(12):3040-50 PMID: 15044543
  100. Phosphorylated ERM is responsible for increased T cell polarization, adhesion, and migration in patients with systemic lupus erythematosus.
    J Immunol. 2007 Feb 1;178(3):1938-47 PMID: 17237445
  101. Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling.
    J Biol Chem. 1999 Apr 9;274(15):10203-12 PMID: 10187805
  102. Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site.
    Mol Biol Cell. 1995 Aug;6(8):1061-75 PMID: 7579708
  103. Maturation of glutamatergic and GABAergic synapse composition in hippocampal neurons.
    Neuropharmacology. 2004 Oct;47(5):694-705 PMID: 15458841
  104. Cytoskeletal dynamics and transport in growth cone motility and axon guidance.
    Neuron. 2003 Oct 9;40(2):209-27 PMID: 14556705
  105. Negative regulation of fibroblast motility by Ena/VASP proteins.
    Cell. 2000 Jun 23;101(7):717-28 PMID: 10892743
  106. Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases.
    J Neurobiol. 2000 Aug;44(2):126-44 PMID: 10934317
  107. Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity.
    Nature. 2003 Jan 2;421(6918):83-7 PMID: 12511959
  108. ERM proteins: head-to-tail regulation of actin-plasma membrane interaction.
    Trends Biochem Sci. 1997 Feb;22(2):53-8 PMID: 9048483
  109. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association.
    J Cell Biol. 1998 Feb 9;140(3):647-57 PMID: 9456324
  110. Semaphorin III is needed for normal patterning and growth of nerves, bones and heart.
    Nature. 1996 Oct 10;383(6600):525-8 PMID: 8849723
  111. L1-mediated branching is regulated by two ezrin-radixin-moesin (ERM)-binding sites, the RSLE region and a novel juxtamembrane ERM-binding region.
    J Neurosci. 2005 Jan 12;25(2):395-403 PMID: 15647482
  112. Growth cone turning induced by direct local modification of microtubule dynamics.
    J Neurosci. 2002 Nov 1;22(21):9358-67 PMID: 12417661
  113. The detection and quantification of growth cone collapsing activities.
    Nat Protoc. 2007;2(8):2005-11 PMID: 17703212
  114. Binding partners L1 cell adhesion molecule and the ezrin-radixin-moesin (ERM) proteins are involved in development and the regenerative response to injury of hippocampal and cortical neurons.
    Eur J Neurosci. 2004 Sep;20(6):1436-44 PMID: 15355311
  115. FARP2 triggers signals for Sema3A-mediated axonal repulsion.
    Nat Neurosci. 2005 Dec;8(12):1712-9 PMID: 16286926
  116. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance.
    Nat Neurosci. 2006 Oct;9(10):1265-73 PMID: 16980965
  117. Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth.
    Nature. 1997 Oct 23;389(6653):852-6 PMID: 9349817
Article Info
Journal
The Journal of comparative neurology
Abbr.
J Comp Neurol
ISSN
1096-9861
DOI
10.1002/cne.21799
Published
2008-10-01
Pages
351-66
Language
English
Region
United States
NLM ID
0406041
PMCID
PMC2691689
Subset
IM
Grants
NIAAA NIH HHS · R01 AA014898-05 · United States
NINDS NIH HHS · R01 NS037731 · United States
NINDS NIH HHS · NS046142 · United States
NIAAA NIH HHS · R01 AA014898 · United States
NINDS NIH HHS · R01 NS050634 · United States
NINDS NIH HHS · R01 NS050634-03 · United States
NINDS NIH HHS · R01 NS045305 · United States
NIAAA NIH HHS · AA014898 · United States
NINDS NIH HHS · NS037731 · United States
NINDS NIH HHS · R01 NS050634-01A2 · United States
NINDS NIH HHS · NS050634 · United States
NIAAA NIH HHS · R01 AA014898-04S1 · United States
NIAAA NIH HHS · R01 AA014898-03 · United States
NINDS NIH HHS · F30 NS046142 · United States
NINDS NIH HHS · NS045305 · United States
External Links
PubMed source DOI: 10.1002/cne.21799 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2