In vivo targeting of adult neural stem cells in the dentate gyrus by a Split-Cre Approach

Stem Cell Reports

Volumn 2, Issue 2, 2014, Pages 153-162

  Beckervordersandforth, Ruth ^a,b   Deshpande, Aditi ^c   Schäffner, Iris ^a,b   Huttner, Hagen B ^b   Lepier, Alexandra ^c   Lie, Dieter Chichung ^b   Götz, Magdalena ^a,c,d  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d Germany 3 Munich Cluster for Systems Neurology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CRE RECOMBINASE; ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; PROMININ1; PROTEIN; UNCLASSIFIED DRUG; CD133 ANTIGEN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PROTEIN BINDING;

ADULT NEURAL STEM CELL; ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN REGION; CARBOXY TERMINAL SEQUENCE; CELL FATE; CELL LABELING; CELL LINEAGE; CELL RENEWAL; CONTROLLED STUDY; CYTOMETRY; DENTATE GYRUS; DEVELOPMENT; GENETIC FATE MAPPING; GLIA CELL; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROGENY; PROTEIN EXPRESSION; SUBGRANULAR ZONE; VERTEBRATE; ADULT STEM CELL; ANIMAL; CYTOLOGY; GENE EXPRESSION; GENE TARGETING; GENETICS; GLIA; HOMOLOGOUS RECOMBINATION; METABOLISM; PROTEIN TRANSPORT; REPORTER GENE;

MURINAE; VERTEBRATA;

ADULT STEM CELLS; ANIMALS; ANTIGENS, CD; DENTATE GYRUS; GENE EXPRESSION; GENE TARGETING; GENES, REPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEINS; HIPPOCAMPUS; HOMOLOGOUS RECOMBINATION; HUMANS; MICE; NEURAL STEM CELLS; NEUROGLIA; PEPTIDES; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84893733414     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.01.004     Document Type: Article

References (36)

1. R. Beckervordersandforth, P. Tripathi, J. Ninkovic, E. Bayam, A. Lepier, B. Stempfhuber, F. Kirchhoff, J. Hirrlinger, A. Haslinger, and D.C. Lie et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells Cell Stem Cell 7 2010 744 758
2. M.A. Bonaguidi, M.A. Wheeler, J.S. Shapiro, R.P. Stadel, G.J. Sun, G.L. Ming, and H. Song In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics Cell 145 2011 1142 1155
3. M.D. Brandt, A. Maass, G. Kempermann, and A. Storch Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis Eur. J. Neurosci. 32 2010 1256 1264
4. B. Bussolati, S. Bruno, C. Grange, S. Buttiglieri, M.C. Deregibus, D. Cantino, and G. Camussi Isolation of renal progenitor cells from adult human kidney Am. J. Pathol. 166 2005 545 555
5. D. Corbeil, A.M. Marzesco, M. Wilsch-Bräuninger, and W.B. Huttner The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation FEBS Lett. 584 2010 1659 1664
6. V. Coskun, H. Wu, B. Blanchi, S. Tsao, K. Kim, J. Zhao, J.C. Biancotti, L. Hutnick, R.C. Krueger Jr., and G. Fan et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain Proc. Natl. Acad. Sci. USA 105 2008 1026 1031
7. J.M. Encinas, T.V. Michurina, N. Peunova, J.H. Park, J. Tordo, D.A. Peterson, G. Fishell, A. Koulakov, and G. Enikolopov Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus Cell Stem Cell 8 2011 566 579
8. A.W. Ettinger, M. Wilsch-Brauninger, A.M. Marzesco, M. Bickle, A. Lohmann, Z. Maliga, J. Karbanova, D. Corbeil, A.A. Hyman, and W.B. Huttner Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour Nature communications 2 2011 503
9. M. Götz, and W.B. Huttner The cell biology of neurogenesis Nat. Rev. Mol. Cell Biol. 6 2005 777 788
10. P.G. Hirrlinger, A. Scheller, C. Braun, J. Hirrlinger, and F. Kirchhoff Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2 Glia 54 2006 11 20
11. J. Hirrlinger, A. Scheller, P.G. Hirrlinger, B. Kellert, W. Tang, M.C. Wehr, S. Goebbels, A. Reichenbach, R. Sprengel, M.J. Rossner, and F. Kirchhoff Split-cre complementation indicates coincident activity of different genes in vivo PLoS ONE 4 2009 e4286
12. R. Jagasia, K. Steib, E. Englberger, S. Herold, T. Faus-Kessler, M. Saxe, F.H. Gage, H. Song, and D.C. Lie GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus J. Neurosci. 29 2009 7966 7977
13. J. Jászai, S. Graupner, E.M. Tanaka, R.H. Funk, W.B. Huttner, M. Brand, and D. Corbeil Spatial distribution of prominin-1 (CD133)-positive cells within germinative zones of the vertebrate brain PLoS ONE 8 2013 e63457
14. J. Karbanova, E. Missol-Kolka, A.V. Fonseca, C. Lorra, P. Janich, H. Hollerova, J. Jaszai, J. Ehrmann, Z. Kolar, and C. Liebers et al. The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia J. Histochem. Cytochem 56 2008 977 993
15. G. Kempermann, E.J. Chesler, L. Lu, R.W. Williams, and F.H. Gage Natural variation and genetic covariance in adult hippocampal neurogenesis Proc. Natl. Acad. Sci. USA 103 2006 780 785
16. A. Kriegstein, and A. Alvarez-Buylla The glial nature of embryonic and adult neural stem cells Annu. Rev. Neurosci. 32 2009 149 184
17. D.C. Lagace, M.C. Whitman, M.A. Noonan, J.L. Ables, N.A. DeCarolis, A.A. Arguello, M.H. Donovan, S.J. Fischer, L.A. Farnbauch, and R.D. Beech et al. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis J. Neurosci. 27 2007 12623 12629
18. U. Lendahl, L.B. Zimmerman, and R.D. McKay CNS stem cells express a new class of intermediate filament protein Cell 60 1990 585 595
19. S. Lugert, O. Basak, P. Knuckles, U. Haussler, K. Fabel, M. Götz, C.A. Haas, G. Kempermann, V. Taylor, and C. Giachino Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging Cell Stem Cell 6 2010 445 456
20. C.M. Morshead, A.D. Garcia, M.V. Sofroniew, and D. van Der Kooy The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells Eur. J. Neurosci. 18 2003 76 84
21. T. Nakamura, M.C. Colbert, and J. Robbins Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system Circ. Res. 98 2006 1547 1554
22. J. Neuzil, M. Stantic, R. Zobalova, J. Chladova, X. Wang, L. Prochazka, L. Dong, L. Andera, and S.J. Ralph Tumour-initiating cells vs. cancer 'stem' cells and CD133: what's in the name? Biochem. Biophys. Res. Commun. 355 2007 855 859
23. J. Ninkovic, T. Mori, and M. Götz Distinct modes of neuron addition in adult mouse neurogenesis J. Neurosci. 27 2007 10906 10911
24. C. Nolte, M. Matyash, T. Pivneva, C.G. Schipke, C. Ohlemeyer, U.K. Hanisch, F. Kirchhoff, and H. Kettenmann GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue Glia 33 2001 72 86
25. L. Pinto, M.T. Mader, M. Irmler, M. Gentilini, F. Santoni, D. Drechsel, R. Blum, R. Stahl, A. Bulfone, and P. Malatesta et al. Prospective isolation of functionally distinct radial glial subtypes - lineage and transcriptome analysis Mol. Cell. Neurosci. 38 2008 15 42
26. E. Raponi, F. Agenes, C. Delphin, N. Assard, J. Baudier, C. Legraverend, and J.C. Deloulme S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage Glia 55 2007 165 177
27. N. Sanai, T. Nguyen, R.A. Ihrie, Z. Mirzadeh, H.H. Tsai, M. Wong, N. Gupta, M.S. Berger, E. Huang, and J.M. Garcia-Verdugo et al. Corridors of migrating neurons in the human brain and their decline during infancy Nature 478 2011 382 386
28. S.V. Shmelkov, R. St Clair, D. Lyden, and S. Rafii AC133/CD133/Prominin-1 Int. J. Biochem. Cell Biol. 37 2005 715 719
29. H.J. Snippert, J.H. van Es, M. van den Born, H. Begthel, D.E. Stange, N. Barker, and H. Clevers Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine Gastroenterology 136 2009 2187 2194.e1
30. K.L. Spalding, O. Bergmann, K. Alkass, S. Bernard, M. Salehpour, H.B. Huttner, E. Boström, I. Westerlund, C. Vial, and B.A. Buchholz et al. Dynamics of hippocampal neurogenesis in adult humans Cell 153 2013 1219 1227
31. B. Steiner, S. Zurborg, H. Hörster, K. Fabel, and G. Kempermann Differential 24 h responsiveness of Prox1-expressing precursor cells in adult hippocampal neurogenesis to physical activity, environmental enrichment, and kainic acid-induced seizures Neuroscience 154 2008 521 529
32. H. Suh, A. Consiglio, J. Ray, T. Sawai, K.A. D'Amour, and F.H. Gage In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus Cell Stem Cell 1 2007 515 528
33. T.L. Walker, A. Wierick, A.M. Sykes, B. Waldau, D. Corbeil, P. Carmeliet, and G. Kempermann Prominin-1 allows prospective isolation of neural stem cells from the adult murine hippocampus J. Neurosci. 33 2013 3010 3024
34. A. Weigmann, D. Corbeil, A. Hellwig, and W.B. Huttner Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells Proc. Natl. Acad. Sci. USA 94 1997 12425 12430
35. C. Zhao, E.M. Teng, R.G. Summers Jr., G.L. Ming, and F.H. Gage Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus J. Neurosci. 26 2006 3 11
36. L. Zhu, P. Gibson, D.S. Currle, Y. Tong, R.J. Richardson, I.T. Bayazitov, H. Poppleton, S. Zakharenko, D.W. Ellison, and R.J. Gilbertson Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation Nature 457 2009 603 607