A competitive advantage by neonatally engrafted human glial progenitors yields mice whose brains are chimeric for human glia

Journal of Neuroscience

Volumn 34, Issue 48, 2014, Pages 16153-16161

  Windrem, Martha S ^a   Schanz, Steven J ^a   Morrow, Carolyn ^a   Munir, Jared ^a   Chandler Militello, Devin ^a   Wang, Su ^a   Goldman, Steven A ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell transplant; Chimera; Demyelinating disease; Glial progenitor; Neural stem cell; Oligodendrocytic progenitor

Indexed keywords

BROXURIDINE; ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; TRANSFERRIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRDU ASSAY; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL FATE; CELL ISOLATION; CELL LINEAGE; CELL MATURATION; CELL SELECTION; CELL TRANSPLANTATION; CONTROLLED STUDY; DEMYELINATING DISEASE; DOMINANCE BEHAVIOR; ENGRAFTMENT; FETUS; FOREBRAIN; GLIA CELL; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN GLIAL PROGENITOR CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MACROGLIA; MITOSIS INDEX; MOUSE; NONHUMAN; OLIGODENDROGLIA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TISSUE DISTRIBUTION; XENOGRAFT; ANIMAL; CHIMERA; CYTOLOGY; FEMALE; FETAL STEM CELL; GLIA; MALE; NEWBORN; PHYSIOLOGY; PROCEDURES; STEM CELL TRANSPLANTATION; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; CHIMERA; FEMALE; FETAL STEM CELLS; HUMANS; MALE; MICE; MICE, TRANSGENIC; NEUROGLIA; PROSENCEPHALON; STEM CELL TRANSPLANTATION;

EID: 84911888756     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1510-14.2014     Document Type: Article

References (30)

1. Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory syn apses via GluA1 AMPA receptors. Nature 486:410–414.
2. Amoyel M, Bach EA (2014) Cell competition: how to eliminate your neighbours. Development 141:988–1000.
3. Amoyel M, Simons BD, Bach EA (2014) Neutral competition of stem cells is skewed by proliferative changes downstream of Hh and Hpo. EMBO J 33:2295–2313.
4. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–215.
5. Bu J, Banki A, Wu Q, Nishiyama A (2004) Increased NG2(+) glial cell proliferation and oligodendrocyte generation in the hypomyelinating mutant shiverer. Glia 48:51–63.
6. Clavería C, Giovinazzo G, Sierra R, Torres M (2013) Myc-driven endogenous cell competition in the early mammalian embryo. Nature 500:39–44.
7. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376–380.
8. Goldman SA, Schanz S, Windrem MS (2008) Stem cell-based strategies for treating pediatric disorders of myelin. Hum Mol Genet 17:R76–R83.
9. Goldman SA, Nedergaard M, Windrem MS (2012) Glial progenitor cell-based treatment and modeling of neurological disease. Science 338:491-495.
10. Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M (2013) Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12:342–353.
11. Horrobin DF (1998) Schizophrenia: the illness that made us human. Med Hypotheses 50:269–288.
12. Hughes EG, Kang SH, Fukaya M, Bergles DE (2013) Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16:668–676.
13. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683-692.
14. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE (2010) NG2+CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68:668–681.
15. Krencik R, Weick JP, Liu Y, Zhang ZJ, Zhang SC (2011) Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 29:528–534.
16. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9–22.
17. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G 2nd, Jiang L, Kang J, Nedergaard M, Goldman SA (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439–447.
18. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276–3287.
19. Oberheim N, Wang X, Goldman S, Nedergaard SA (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547–553.
20. Roy N, Wang S, Harrison-Restelli C, Benraiss A, Fraser R, Gravel M, Braun M, Goldman S (1999) Identification, isolation, and promoter-defined separation of mitotic oligodendrocyte progenitor cells from the adult human subcortical white matter. J Neurosci 19:9986–9995.
21. Roy N, Wang S, Jiang L, Kang J, Benraiss A, Restelli C, Fraser R, Couldwell W, Kawaguchi A, Okano H, Nedergaard M, Goldman S (2000) Invitroneurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6:271–277.
22. Sim FJ, Windrem MS, Goldman SA (2009) Fate determination of adult human glial progenitor cells. Neuron Glia Biol 5:45–55.
23. Sim FJ, McClain CR, Schanz SJ, Protack TL, Windrem MS, Goldman SA (2011) CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat Biotechnol 29:934–941.
24. Stellwagen D, Malenka RC (2006) Synaptic scaling mediated by glial TNF-alpha. Nature 440:1054–1059.
25. Tripathi RB, Rivers LE, Young KM, Jamen F, Richardson WD (2010) NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J Neurosci 30:16383–16390.
26. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657–661.
27. Wang S, Bates J, Li X, Schanz S, Chandler-Militello D, Levine C, Maherali N, Studer L, Hochedlinger K, Windrem M, Goldman SA (2013) Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 12:252–264.
28. West MJ (1998) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22: 51–61.
29. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann G 2nd, Roy NS, Goldman SA (2004) Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dys-myelinated brain. Nat Med 10:93–97.
30. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA (2008) Neonatal chimerization with human glial progenitor cells can both remy-elinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2:553–565.