Front Cell Neurosci. 2016 Jan 19;9:501. doi: 10.3389/fncel.2015.00501. eCollection 2015.
Exosomes as Novel Regulators of Adult Neurogenic Niches.
Frontiers in cellular neuroscience
Luis Federico Bátiz, Maite A Castro, Patricia V Burgos, Zahady D Velásquez, Rosa I Muñoz, Carlos A Lafourcade, Paulina Troncoso-Escudero, Ursula Wyneken
Affiliations
Affiliations
- Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de ChileValdivia, Chile; Program for Cell Biology and Microscopy, Universidad Austral de ChileValdivia, Chile; Instituto de Anatomía, Histología y Patología, Facultad de Medicina, Universidad Austral de ChileValdivia, Chile.
- Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de ChileValdivia, Chile; Program for Cell Biology and Microscopy, Universidad Austral de ChileValdivia, Chile; Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de ChileValdivia, Chile.
- Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de ChileValdivia, Chile; Program for Cell Biology and Microscopy, Universidad Austral de ChileValdivia, Chile; Instituto de Fisiología, Facultad de Medicina, Universidad Austral de ChileValdivia, Chile.
- Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de ChileValdivia, Chile; Instituto de Anatomía, Histología y Patología, Facultad de Medicina, Universidad Austral de ChileValdivia, Chile.
- Laboratorio de Neurociencias, Facultad de Medicina, Universidad de Los Andes Santiago, Chile.
- Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de ChileValdivia, Chile; Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de ChileValdivia, Chile.
PMID: 26834560
PMCID: PMC4717294 DOI: 10.3389/fncel.2015.00501
Abstract
Adult neurogenesis has been convincingly demonstrated in two regions of the mammalian brain: the sub-granular zone (SGZ) of the dentate gyrus (DG) in the hippocampus, and the sub-ventricular zone (SVZ) of the lateral ventricles (LV). SGZ newborn neurons are destined to the granular cell layer (GCL) of the DG, while new neurons from the SVZ neurons migrate rostrally into the olfactory bulb (OB). The process of adult neurogenesis persists throughout life and is supported by a pool of neural stem cells (NSCs), which reside in a unique and specialized microenvironment known as "neurogenic niche". Neurogenic niches are structured by a complex organization of different cell types, including the NSC-neuron lineage, glial cells and vascular cells. Thus, cell-to-cell communication plays a key role in the dynamic modulation of homeostasis and plasticity of the adult neurogenic process. Specific cell-cell contacts and extracellular signals originated locally provide the necessary support and regulate the balance between self-renewal and differentiation of NSCs. Furthermore, extracellular signals originated at distant locations, including other brain regions or systemic organs, may reach the niche through the cerebrospinal fluid (CSF) or the vasculature and influence its nature. The role of several secreted molecules, such as cytokines, growth factors, neurotransmitters, and hormones, in the biology of adult NSCs, has been systematically addressed. Interestingly, in addition to these well-recognized signals, a novel type of intercellular messengers has been identified recently: the extracellular vesicles (EVs). EVs, and particularly exosomes, are implicated in the transfer of mRNAs, microRNAs (miRNAs), proteins and lipids between cells and thus are able to modify the function of recipient cells. Exosomes appear to play a significant role in different stem cell niches such as the mesenchymal stem cell niche, cancer stem cell niche and pre-metastatic niche; however, their roles in adult neurogenic niches remain virtually unexplored. This review focuses on the current knowledge regarding the functional relationship between cellular and extracellular components of the adult SVZ and SGZ neurogenic niches, and the growing evidence that supports the potential role of exosomes in the physiology and pathology of adult neurogenesis.
Keywords: adult neurogenesis; biomarkers; exosomes; extracellular vesicles; neurological disorders; niche; psychiatric disorders; stem cells
References
- Front Neurosci. 2013 Aug 20;7:145 - PubMed
- J Neuropathol Exp Neurol. 2003 Oct;62(10 ):1019-40 - PubMed
- Nature. 2006 Feb 2;439(7076):589-93 - PubMed
- Cell Commun Signal. 2015 Feb 03;13:8 - PubMed
- Glia. 2005 Aug 15;51(3):173-86 - PubMed
- Eur Rev Med Pharmacol Sci. 2015 May;19(10):1821-8 - PubMed
- Science. 2014 Oct 3;346(6205):89-93 - PubMed
- Front Cell Neurosci. 2013 Jan 30;7:6 - PubMed
- J Neurosci. 2012 Jun 27;32(26):8879-89 - PubMed
- Science. 2006 Feb 3;311(5761):629-32 - PubMed
- Annu Rev Neurosci. 2008;31:535-61 - PubMed
- Front Integr Neurosci. 2013 Jan 04;6:126 - PubMed
- Mol Immunol. 2012 Apr;50(4):278-86 - PubMed
- J Biol Chem. 2003 Jul 4;278(27):24438-48 - PubMed
- Brain Res. 2015 Aug 18;1617:63-71 - PubMed
- Nat Cell Biol. 2012 Jun 29;14(7):654-5 - PubMed
- J Biol Chem. 2004 Aug 6;279(32):33538-46 - PubMed
- J Biol Chem. 2012 Jun 15;287(25):21384-95 - PubMed
- Transl Neurodegener. 2012 Apr 24;1(1):9 - PubMed
- J Neurosci. 2003 Dec 17;23(37):11732-40 - PubMed
- Nat Commun. 2013;4:2712 - PubMed
- J Comp Neurol. 2000 Oct 2;425(4):479-94 - PubMed
- Brain. 2002 Aug;125(Pt 8):1859-74 - PubMed
- Brain. 2003 Mar;126(Pt 3):623-31 - PubMed
- J Biol Chem. 1987 Jul 5;262(19):9412-20 - PubMed
- Glia. 2013 Jul;61(7):1003-17 - PubMed
- Science. 2014 May 9;344(6184):630-4 - PubMed
- Acta Neuropathol. 2011 Jun;121(6):721-35 - PubMed
- J Neurosci. 2008 Apr 2;28(14):3804-13 - PubMed
- Nature. 2005 Oct 27;437(7063):1370-5 - PubMed
- Neurobiol Aging. 2014 Aug;35(8):1792-800 - PubMed
- Blood. 2013 May 9;121(19):3997-4006, S1-15 - PubMed
- Annu Rev Neurosci. 2009;32:149-84 - PubMed
- Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11784-9 - PubMed
- Glia. 2015 Apr;63(4):626-34 - PubMed
- J Physiol. 1974 Nov;243(1):63-78 - PubMed
- Curr Top Dev Biol. 2005;71:1-52 - PubMed
- Nat Genet. 2004 Aug;36(8):827-35 - PubMed
- Regen Med. 2006 Jan;1(1):15-28 - PubMed
- Front Cell Neurosci. 2013 Oct 30;7:182 - PubMed
- Drug Discov Today. 2013 May;18(9-10):456-63 - PubMed
- J Cell Sci. 2011 Feb 1;124(Pt 3):447-58 - PubMed
- Nat Cell Biol. 2012 Jun 03;14(7):677-85 - PubMed
- Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13427-31 - PubMed
- Nat Neurosci. 1999 Mar;2(3):266-70 - PubMed
- Development. 2005 Feb;132(3):565-78 - PubMed
- Mol Cell Neurosci. 2006 Apr;31(4):642-8 - PubMed
- Science. 2004 Jan 23;303(5657):531-4 - PubMed
- Prog Neurobiol. 2011 Mar;93(3):313-40 - PubMed
- Physiol Rev. 2009 Apr;89(2):607-48 - PubMed
- Mol Brain. 2013 Nov 13;6:47 - PubMed
- Regen Med. 2011 Jul;6(4):481-92 - PubMed
- Biol Direct. 2007 Nov 30;2:35 - PubMed
- Mol Neurobiol. 2014 Feb;49(1):590-600 - PubMed
- J Extracell Vesicles. 2014 Aug 04;3:null - PubMed
- Neurobiol Aging. 2012 Jan;33(1):195.e1-12 - PubMed
- Nat Rev Neurosci. 2015 Apr;16(4):189-200 - PubMed
- Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1317-22 - PubMed
- J Extracell Vesicles. 2012 Apr 16;1:null - PubMed
- Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9683-8 - PubMed
- Nat Med. 2012 Jun;18(6):883-91 - PubMed
- Cell Mol Life Sci. 2015 Feb;72 (4):773-97 - PubMed
- J Transl Med. 2012 Jan 05;10:5 - PubMed
- Stem Cells. 2016 Jan;34(1):220-32 - PubMed
- Neuron. 2014 Aug 6;83(3):572-85 - PubMed
- Front Physiol. 2012 May 03;3:124 - PubMed
- Nucleic Acids Res. 2012 Jan;40(Database issue):D1241-4 - PubMed
- Stem Cells. 2013 Dec;31(12):2737-46 - PubMed
- Annu Rev Pharmacol Toxicol. 2015;55:439-64 - PubMed
- Biol Psychiatry. 2008 Apr 1;63(7):650-5 - PubMed
- J Biol Chem. 2013 Mar 8;288(10 ):7105-16 - PubMed
- Nature. 2012 Sep 6;489(7414):150-4 - PubMed
- Nature. 1965 Aug 28;207(5000):953-6 - PubMed
- Curr Opin Neurobiol. 2013 Dec;23(6):928-34 - PubMed
- Cell Stem Cell. 2008 Sep 11;3(3):279-88 - PubMed
- Semin Cell Dev Biol. 2015 Apr;40:82-8 - PubMed
- Fluids Barriers CNS. 2011 Jan 18;8(1):10 - PubMed
- Nat Genet. 2009 Feb;41(2):149-55 - PubMed
- Brain Pathol. 2011 Mar;21(2):163-79 - PubMed
- Local Reg Anesth. 2011;4:21-4 - PubMed
- Neural Plast. 2012;2012:854285 - PubMed
- Clin Ther. 2014 Jun 1;36(6):882-8 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2008 Jan 12;363(1489):123-37 - PubMed
- Annu Rev Cell Dev Biol. 2005;21:605-31 - PubMed
- J Biol Chem. 2012 Feb 3;287(6):3842-9 - PubMed
- Cell Mol Life Sci. 2012 Sep;69(17):2863-78 - PubMed
- Pediatr Neurol. 1992 May-Jun;8(3):163-78 - PubMed
- J Neurosci. 2010 May 19;30(20):6838-51 - PubMed
- Glia. 2009 Aug 1;57(10):1046-61 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2014 Sep 26;369(1652):null - PubMed
- EMBO J. 2009 Apr 22;28(8):1043-54 - PubMed
- J Biol Chem. 2013 Apr 5;288(14):10093-9 - PubMed
- Nat Neurosci. 2009 Mar;12(3):259-67 - PubMed
- Cell Stem Cell. 2014 Apr 3;14(4):500-11 - PubMed
- Mol Cancer. 2014 Apr 26;13:88 - PubMed
- Mol Cell Neurosci. 2011 Feb;46(2):409-18 - PubMed
- J Extracell Vesicles. 2013 Sep 24;2:null - PubMed
- Science. 2008 Feb 29;319(5867):1244-7 - PubMed
- J Cell Sci. 2005 Jul 1;118(Pt 13):2849-58 - PubMed
- J Neurosci Res. 2005 Aug 1;81(3):302-13 - PubMed
- Eur J Neurosci. 2006 Jan;23(1):83-93 - PubMed
- Stem Cells Dev. 2006 Jun;15(3):407-21 - PubMed
- Blood Cells. 1978;4(1-2):7-25 - PubMed
- Neurosci Res. 2011 Apr;69(4):337-42 - PubMed
- Science. 1999 Oct 15;286(5439):548-52 - PubMed
- J Neurosci. 2001 Sep 15;21(18):7153-60 - PubMed
- Nat Rev Neurosci. 2014 Apr;15(4):233-49 - PubMed
- Neuron. 2009 Jul 30;63(2):154-70 - PubMed
- Nat Rev Mol Cell Biol. 2009 Apr;10 (4):287-92 - PubMed
- Brain Res. 2015 Dec 2;1628(Pt B):327-42 - PubMed
- Allergy. 2008 Apr;63(4):404-8 - PubMed
- PLoS One. 2011;6(8):e23461 - PubMed
- Semin Cell Dev Biol. 2015 Apr;40:60-71 - PubMed
- Front Physiol. 2012 May 22;3:149 - PubMed
- J Biol Chem. 2013 Sep 27;288(39):28058-67 - PubMed
- J Biol Chem. 2010 Nov 26;285(48):37405-14 - PubMed
- J Exp Med. 1996 Mar 1;183(3):1161-72 - PubMed
- Nucleic Acids Res. 2012 Nov;40(21):10937-49 - PubMed
- Cell. 1983 Jul;33(3):967-78 - PubMed
- Nat Rev Mol Cell Biol. 2014 Mar;15(3):197-210 - PubMed
- Curr Opin Cell Biol. 2006 Dec;18(6):704-9 - PubMed
- Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):2853-8 - PubMed
- Biochem Soc Trans. 2013 Feb 1;41(1):241-4 - PubMed
- World J Gastroenterol. 2014 Apr 7;20(13):3552-63 - PubMed
- Aging Dis. 2010 Dec 1;1(3):232-244 - PubMed
- Neuroscience. 2008 Aug 26;155(3):751-9 - PubMed
- Gynecol Obstet (Sunnyvale). 2013 Apr 29;Suppl 4:3 - PubMed
- Front Oncol. 2014 May 27;4:127 - PubMed
- J Nat Sci Biol Med. 2011 Jan;2(1):26-37 - PubMed
- Cancer Sci. 2014 Nov;105(11):1384-92 - PubMed
- Science. 2000 Feb 25;287(5457):1433-8 - PubMed
- Cell Stem Cell. 2010 Aug 6;7(2):163-73 - PubMed
- Dev Cell. 2011 Aug 16;21(2):193-215 - PubMed
- Prog Brain Res. 2007;163:63-84 - PubMed
- J Clin Invest. 2015 Mar 2;125(3):978-80 - PubMed
- Science. 2005 Oct 28;310(5748):679-83 - PubMed
- Science. 2004 May 28;304(5675):1338-40 - PubMed
- PLoS Genet. 2015 Apr 15;11(4):e1005175 - PubMed
- Front Mol Neurosci. 2015 Feb 23;8:4 - PubMed
- Proteomics Clin Appl. 2007 Nov;1(11):1446-61 - PubMed
- Cell Death Dis. 2015 Jan 29;6:e1622 - PubMed
- Annu Rev Pharmacol Toxicol. 2004;44:399-421 - PubMed
- Science. 2007 Mar 2;315 (5816):1243-9 - PubMed
- Neurosci Lett. 2010 May 26;476(1):18-22 - PubMed
- J Neurosci. 2004 Sep 1;24(35):7623-31 - PubMed
- J Proteome Res. 2008 Aug;7(8):3475-80 - PubMed
- Nat Neurosci. 2006 Mar;9(3):331-9 - PubMed
- Curr Biol. 2011 May 10;21(9):779-86 - PubMed
- J Pathol. 2007 Apr;211(5):582-90 - PubMed
- BMC Neurosci. 2012 Nov 23;13:144 - PubMed
- FASEB J. 2010 Jun;24(6):1925-34 - PubMed
- J Virol. 2010 Aug;84(16):8181-92 - PubMed
- PLoS One. 2014 Feb 12;9(2):e88810 - PubMed
- Pharmacol Ther. 2013 Sep;139(3):313-26 - PubMed
- Nature. 2011 Aug 03;476(7361):458-61 - PubMed
- Neural Plast. 2014;2014:454696 - PubMed
- J Occup Environ Med. 2003 Dec;45(12):1257-66 - PubMed
- J Neurosci. 2012 Feb 1;32(5):1687-704 - PubMed
- Brain Res Bull. 1999 Aug;49(6):377-91 - PubMed
- Sci Rep. 2015 Aug 19;5:13243 - PubMed
- Glia. 1995 May;14(1):1-13 - PubMed
- Cell Stem Cell. 2008 Sep 11;3(3):289-300 - PubMed
- Neuron. 2000 Dec;28(3):713-26 - PubMed
- Sci Rep. 2014 Feb 07;4:4031 - PubMed
- Mol Neurodegener. 2011 Dec 22;6:85 - PubMed
- Cell Stem Cell. 2015 Mar 5;16(3):225-38 - PubMed
- Dev Neurobiol. 2007 Nov;67(13):1815-29 - PubMed
- Biol Psychiatry. 2005 Aug 1;58(3):175-89 - PubMed
- J Cereb Blood Flow Metab. 2013 Nov;33(11):1711-5 - PubMed
- Stem Cells. 2012 Oct;30(10 ):2320-9 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2014 Sep 26;369(1652):null - PubMed
- Front Cell Neurosci. 2015 May 20;9:193 - PubMed
- Nat Med. 2012 Dec;18(12):1835-40 - PubMed
- Front Cell Neurosci. 2014 May 22;8:117 - PubMed
- Nat Cell Biol. 2015 Jun;17(6):816-26 - PubMed
- J Neurosci. 1997 Jul 1;17(13):5046-61 - PubMed
- BMC Genomics. 2013 May 10;14:319 - PubMed
- J Cardiovasc Transl Res. 2013 Aug;6(4):458-70 - PubMed
- Semin Cancer Biol. 2014 Oct;28:3-13 - PubMed
- Expert Opin Biol Ther. 2010 Sep;10(9):1315-29 - PubMed
- J Neurosci. 2008 Feb 27;28(9):2231-41 - PubMed
- Can J Psychiatry. 2008 Jun;53(6):346-53 - PubMed
- Science. 2005 May 27;308(5726):1314-8 - PubMed
- Neural Plast. 2014;2014:610343 - PubMed
- J Cell Biol. 2010 Apr 19;189(2):223-32 - PubMed
- Cancer Cell. 2008 Nov 4;14(5):382-93 - PubMed
- Front Physiol. 2012 Apr 30;3:119 - PubMed
- Nat Neurosci. 2004 Jul;7(7):726-35 - PubMed
- Mol Cell Proteomics. 2010 Feb;9(2):197-208 - PubMed
- Nat Neurosci. 2002 May;5(5):438-45 - PubMed
- Cell Stem Cell. 2010 Oct 8;7(4):483-95 - PubMed
- Development. 2005 Dec;132(23):5329-39 - PubMed
- Trends Genet. 2006 Feb;22(2):65-6 - PubMed
- Nat Rev Neurosci. 2000 Oct;1(1):67-73 - PubMed
- J Biol Chem. 2015 Mar 13;290(11):7141-50 - PubMed
- Semin Immunopathol. 2009 Nov;31(4):497-511 - PubMed
- J Neurosurg. 2015 Apr;122(4):856-67 - PubMed
- J Neurosci. 2015 Mar 18;35(11):4528-39 - PubMed
- Proc Natl Acad Sci U S A. 2006 Jul 25;103(30):11172-7 - PubMed
- Science. 2003 Aug 8;301(5634):805-9 - PubMed
- J Neuropathol Exp Neurol. 2007 Dec;66(12):1082-92 - PubMed
- Neuron. 2004 Mar 4;41(5):683-6 - PubMed
- Front Immunol. 2014 Apr 10;5:160 - PubMed
- Annu Rev Cell Dev Biol. 2012;28:337-62 - PubMed
- J Biol Chem. 2009 Dec 4;284(49):34211-22 - PubMed
- Brain Res. 2005 Mar 21;1038(2):208-15 - PubMed
- Mech Dev. 2015 Nov;138 Pt 1:56-62 - PubMed
- Nat Neurosci. 2005 Sep;8(9):1179-87 - PubMed
- Nat Biotechnol. 2011 Apr;29(4):341-5 - PubMed
- J Cell Biol. 2002 Nov 25;159(4):625-35 - PubMed
- Mol Neurobiol. 2016 Mar;53(2):818-34 - PubMed
- Brain Res Bull. 2014 Oct;109:32-8 - PubMed
- Curr Opin Cell Biol. 2014 Aug;29:116-25 - PubMed
- J Neuroinflammation. 2014 Apr 03;11:68 - PubMed
- Neuroscientist. 2014 Jun;20(3):235-42 - PubMed
- Front Cell Neurosci. 2013 Apr 17;7:45 - PubMed
- Radiographics. 2006 Oct;26 Suppl 1:S97-110 - PubMed
- Physiol Rev. 2005 Apr;85(2):523-69 - PubMed
- Sci Rep. 2015 Jan 23;5:7989 - PubMed
- Neuron. 2009 Oct 15;64(1):79-92 - PubMed
- Circulation. 2005 May 10;111(18):2299-305 - PubMed
- Annu Rev Neurosci. 2005;28:223-50 - PubMed
- Front Cell Neurosci. 2014 Mar 28;8:100 - PubMed
- Nat Rev Neurosci. 2006 Mar;7(3):179-93 - PubMed
- Sci Rep. 2015 Feb 17;5:8505 - PubMed
- Anticancer Agents Med Chem. 2016;16(1):38-58 - PubMed
- Neurotoxicology. 2015 Sep;50:46-55 - PubMed
- J Immunol. 2014 Aug 1;193(3):1006-11 - PubMed
- J Neuropathol Exp Neurol. 2001 Nov;60(11):1105-19 - PubMed
- Trends Neurosci. 2001 Oct;24(10):617-20 - PubMed
- Nat Commun. 2013;4:2123 - PubMed
- Physiol Rev. 2014 Oct;94(4):991-1026 - PubMed
- Science. 2003 Jan 3;299(5603):117-20 - PubMed
- Mol Neurodegener. 2012 Aug 24;7:42 - PubMed
- Int J Mol Med. 2008 Jan;21(1):63-7 - PubMed
- Neuron. 2014 May 7;82(3):545-59 - PubMed
- Mol Cell. 2014 Oct 23;56(2):193-204 - PubMed
- J Neurosci. 2008 Jan 9;28(2):434-46 - PubMed
- CNS Neurol Disord Drug Targets. 2007 Oct;6(5):336-41 - PubMed
- Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):1876-81 - PubMed
- J Comp Neurol. 1969 Dec;137(4):433-57 - PubMed
- J Extracell Vesicles. 2015 May 29;4:26760 - PubMed
- Curr Opin Neurobiol. 2005 Oct;15(5):514-20 - PubMed
- Semin Immunopathol. 2011 Sep;33(5):419-40 - PubMed
- Mol Neurobiol. 2016 Apr;53(3):2016-28 - PubMed
- Gastroenterology. 2013 Jan;144(1):36-49 - PubMed
- J Neurosci. 2008 Nov 12;28(46):11785-91 - PubMed
- Brain Res. 2005 Apr 8;1040(1-2):81-91 - PubMed
- Biochem Biophys Res Commun. 1983 Jun 15;113(2):650-8 - PubMed
- Front Cell Neurosci. 2013 May 16;7:71 - PubMed
- Am J Obstet Gynecol. 2014 Oct;211(4):380.e1-13 - PubMed
- J Immunol. 2001 Jun 15;166(12):7309-18 - PubMed
- J Cereb Blood Flow Metab. 2006 May;26(5):613-24 - PubMed
- J Neurosci. 2008 Dec 31;28(53):14522-36 - PubMed
- Neuroscientist. 2015 Apr;21(2):169-84 - PubMed
- Acta Neuropathol. 2012 Oct;124(4):531-46 - PubMed
- Genomics Proteomics Bioinformatics. 2015 Feb;13(1):17-24 - PubMed
- Microvasc Res. 2012 May;83(3):352-9 - PubMed
- Cold Spring Harb Perspect Biol. 2015 Jul 01;7(7):a018994 - PubMed
- J Neurosci. 2006 Jul 26;26(30):7907-18 - PubMed
- Proc Natl Acad Sci U S A. 2015 May 12;112(19):E2497-506 - PubMed
- Nat Neurosci. 2009 Dec;12 (12 ):1514-23 - PubMed
- Fluids Barriers CNS. 2013 Jan 10;10(1):4 - PubMed
- BMC Neurosci. 2015 Sep 19;16:60 - PubMed
- Mov Disord. 2014 Oct;29(12):1476-85 - PubMed
- Dev Cell. 2015 Feb 23;32(4):435-46 - PubMed
- J Cell Sci. 2014 May 1;127(Pt 9):1966-79 - PubMed
- Neurobiology (Bp). 1996;4(3):185-201 - PubMed
- Cold Spring Harb Perspect Biol. 2015 Apr 01;7(4):a021287 - PubMed
- FASEB J. 2015 Feb;29(2):589-96 - PubMed
- Nat Rev Immunol. 2009 Aug;9(8):581-93 - PubMed
- Front Cell Neurosci. 2014 Jan 28;8:10 - PubMed
- Clin Immunol. 2015 Sep;160(1):46-58 - PubMed
- Eur J Neurosci. 2004 Jul;20(2):575-9 - PubMed
- J Neurosci. 2004 Feb 11;24(6):1497-506 - PubMed
- Cold Spring Harb Perspect Biol. 2014 May 22;6(10):a016857 - PubMed
- J Neurosci. 2000 Dec 15;20(24):9104-10 - PubMed
- J Neural Transm (Vienna). 2010 Jan;117(1):1-4 - PubMed
- J Immunol. 2008 Jul 15;181(2):1519-25 - PubMed
- PLoS Biol. 2013 Jul;11(7):e1001604 - PubMed
- Biochimie. 2013 Dec;95(12):2271-85 - PubMed
- Pediatr Res. 2005 Jul;58(1):89-93 - PubMed
- Traffic. 2011 Dec;12(12):1659-68 - PubMed
- FASEB J. 2009 May;23(5):1541-57 - PubMed
- PLoS One. 2012;7(3):e33554 - PubMed
- Immunology. 2014 Mar;141(3):302-13 - PubMed
- Proc Natl Acad Sci U S A. 2015 Aug 4;112(31):9745-50 - PubMed
- Cold Spring Harb Symp Quant Biol. 2008;73:357-65 - PubMed
- Nat Cell Biol. 2008 Dec;10(12):1470-6 - PubMed
- J Neuropathol Exp Neurol. 2009 Sep;68(9):1006-20 - PubMed
- Biol Res. 2013;46(1):5-11 - PubMed
- Neuron. 2013 Mar 20;77(6):1039-46 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2014 Sep 26;369(1652):null - PubMed
- J Extracell Vesicles. 2014 Nov 13;3:24722 - PubMed
- J Neurosci. 2012 May 9;32(19):6435-43 - PubMed
- J Neurosci. 2001 Oct 1;21(19):7642-53 - PubMed
- J Immunol. 2005 Aug 15;175(4):2237-43 - PubMed
- Clin Exp Pharmacol Physiol. 2007 May-Jun;34(5-6):533-45 - PubMed
- Blood. 2010 Sep 30;116(13):2385-94 - PubMed
- J Immunol. 2005 Jun 1;174(11):7268-77 - PubMed
- Mol Ther. 2011 Oct;19(10):1769-79 - PubMed
- Mol Brain. 2009 Jun 08;2:16 - PubMed
- Trends Cell Biol. 2015 Jun;25(6):364-72 - PubMed
- Cancer Res. 2010 Feb 15;70(4):1668-78 - PubMed
- Cell Tissue Res. 2008 Jan;331(1):211-24 - PubMed
- Stem Cells. 2013 Aug;31(8):1633-43 - PubMed
- J Neurosci. 2005 Jan 5;25(1):10-8 - PubMed
- Biochem Biophys Res Commun. 2007 Aug 3;359(3):649-54 - PubMed
- Oncoimmunology. 2015 Mar 2;4(6):e1008347 - PubMed
- Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11336-41 - PubMed
- Cold Spring Harb Perspect Biol. 2015 Sep 01;7(9):a018812 - PubMed
- Eur J Neurosci. 2003 Nov;18(10):2803-12 - PubMed
- Nat Rev Neurosci. 2009 Feb;10(2):153-63 - PubMed
- Neurobiol Aging. 2011 Aug;32(8):1435-42 - PubMed
- Can J Physiol Pharmacol. 2003 Apr;81(4):317-28 - PubMed
- Neurobiol Dis. 2011 Jun;42(3):360-7 - PubMed
- Nat Rev Neurosci. 2007 Jun;8(6):481-8 - PubMed
- Apoptosis. 2010 Nov;15(11):1415-21 - PubMed
- J Neurosci. 2015 Jul 1;35(26):9764-81 - PubMed
- Nat Neurosci. 2009 Apr;12(4):399-408 - PubMed
- J Thromb Haemost. 2006 Jun;4(6):1296-302 - PubMed
- PLoS Biol. 2014 Jun 03;12(6):e1001874 - PubMed
- J Neuropathol Exp Neurol. 2013 Sep;72(9):846-60 - PubMed
- J Neurosci. 2011 May 18;31(20):7275-90 - PubMed
- Mol Cell Neurosci. 2014 Jul;61:176-86 - PubMed
- Methods Mol Biol. 2011;686:49-68 - PubMed
- Am J Med. 2008 Nov;121(11 Suppl 2):S8-15 - PubMed
- Development. 2013 Jun;140(12):2548-61 - PubMed
- J Comp Neurol. 1966 Mar;126(3):337-89 - PubMed
- Eur J Neurosci. 2011 Mar;33(6):1139-51 - PubMed
- Nature. 2001 Nov 1;414(6859):98-104 - PubMed
- Nat Neurosci. 2014 Jul;17 (7):934-42 - PubMed
- PLoS One. 2013;8(1):e48814 - PubMed
- Science. 2003 Dec 5;302(5651):1760-5 - PubMed
- J Neurosci. 2009 Dec 2;29(48):15063-72 - PubMed
- Nature. 2006 Jun 29;441(7097):1075-9 - PubMed
- Eur Cell Mater. 2014 Sep 22;28:137-51; discussion 151 - PubMed
- Hum Mol Genet. 2004 Sep 15;13(18):2133-41 - PubMed
- Nature. 2006 Aug 24;442(7105):929-33 - PubMed
- Nephrol Dial Transplant. 2015 Sep;30(9):1488-96 - PubMed
- Annu Rev Cell Dev Biol. 2014;30:255-89 - PubMed
- Inflamm Allergy Drug Targets. 2013 Feb;12(1):29-37 - PubMed
- Nat Struct Mol Biol. 2009 Apr;16(4):365-71 - PubMed
- Nat Neurosci. 2012 Oct;15(10):1399-406 - PubMed
- J Neurosci. 2005 Jun 15;25(24):5815-23 - PubMed
- J Gen Intern Med. 2008 Oct;23(10):1571-5 - PubMed
- Nat Med. 1998 Nov;4(11):1313-7 - PubMed
- J Cell Biol. 1969 Mar;40(3):648-77 - PubMed
- Ann Neurol. 2009 Aug;66(2):191-9 - PubMed
- Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3620-5 - PubMed
- J Biol Chem. 2008 Nov 21;283(47):32621-7 - PubMed
- Int J Neuropsychopharmacol. 2015 Mar 26;18(10):pyv038 - PubMed
- Cell Stem Cell. 2010 May 7;6(5):445-56 - PubMed
- Front Physiol. 2012 May 28;3:145 - PubMed
- Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3168-71 - PubMed
- Front Immunol. 2014 Aug 20;5:403 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2015 Jul 5;370(1672):null - PubMed
- Cell Stem Cell. 2008 Sep 11;3(3):265-78 - PubMed
- J Neuropathol Exp Neurol. 2005 Jul;64(7):595-604 - PubMed
- J Gen Virol. 2015 Jul;96(Pt 7):1969-74 - PubMed
- Proc Natl Acad Sci U S A. 2015 Mar 31;112(13):4128-33 - PubMed
- Int J Nanomedicine. 2014 Oct 21;9:4893-7 - PubMed
- J Extracell Vesicles. 2014 Mar 26;3:null - PubMed
- Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11946-50 - PubMed
- Alzheimers Dement. 2015 Jun;11(6):600-7.e1 - PubMed
- Glia. 2006 Dec;54(8):815-25 - PubMed
- Nat Protoc. 2012 Dec;7(12):2112-26 - PubMed
- J Neurosci Res. 2001 Nov 1;66(3):317-26 - PubMed
- Stem Cells. 2008 Mar;26(3):698-705 - PubMed
- Brain Res. 2013 Jul 3;1520:1-14 - PubMed
- J Proteomics. 2014 Jun 25;106:191-204 - PubMed
- Nat Rev Mol Cell Biol. 2012 Apr 18;13(5):328-35 - PubMed
- Acta Neuropathol. 2014 Nov;128(5):639-50 - PubMed
- Mol Psychiatry. 2000 May;5(3):262-9 - PubMed
- Hum Mol Genet. 2009 Feb 1;18(3):497-516 - PubMed
Publication Types