Culturing conditions remarkably affect viability and organization of mouse subventricular zone in ex vivo cultured forebrain slices

Journal of Neuroscience Methods

Volumn 197, Issue 1, 2011, Pages 65-81

  Armentano, Maria ^a   Canalia, Nadia ^a   Crociara, Paola ^a   Bonfanti, Luca ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Brain plasticity; Electron microscopy; Neural stem cells; Postnatal neurogenesis; Subventricular zone

Indexed keywords

BALANCED SALT SOLUTION; BROXURIDINE; CASPASE 3; CD11B ANTIGEN; CD31 ANTIGEN; CELL MARKER; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLUTAMINE; HISTONE H3; ISOLECTIN B4; KI 67 ANTIGEN; PARAFORMALDEHYDE; PENICILLIN G; PHOSPHATE BUFFERED SALINE; STREPTOMYCIN; TRYPAN BLUE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL ACTIVATION; CELL COUNT; CELL DEATH; CELL PROLIFERATION; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EX VIVO STUDY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MICROGLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; TISSUE CULTURE;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL DEATH; CELL SURVIVAL; LATERAL VENTRICLES; MICE; MICE, INBRED ICR; MICROGLIA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NEURAL STEM CELLS; ORGAN CULTURE TECHNIQUES; PROSENCEPHALON;

EID: 79953047460     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2011.01.031     Document Type: Article

References (81)

1. Ajami B., Bennett J.L., Krieger C., Tetzlaff W., Rossi F.M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 2007, 10:1538-1543.
2. Baldwin H.S., Shen H.M., Yan H.C., DeLisser H.M., Chung A., Mickanin C., et al. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 1994, 120:2539-2553.
3. Bernaudin M., Nouvelot A., MacKenzie E.T., Petit E. Selective neuronal vulnerability and specific glial reactions in hippocampal and neocortical organotypic cultures submitted to ischemia. Exp Neurol 1998, 150:30-39.
4. Bolteus A.J., Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 2004, 24:7623-7631.
5. Bonfanti L., Peretto P. Radial glial origin of the adult neural stem cells in the subventricular zone. Prog Neurobiol 2007, 83:24-36.
6. Bonfanti L., Ponti G. Adult mammalian neurogenesis and the New Zealand white rabbit. Vet J 2008, 175:310-331.
7. Brunne B., Zhao S., Derouiche A., Herz J., May P., Frotscher M., et al. Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Glia 2010, 58:1553-1569.
8. Cavaliere F., Dinkel K., Reymann K. Microglia response and P2 receptor participation in oxygen/glucose deprivation-induced cortical damage. Neuroscience 2005, 136:615-623.
9. Cavaliere F., Dinkel K., Reymann K. The subventricular zone releases factors which can be protective in oxygen/glucose deprivation-induced cortical damage: an organotypic study. Exp Neurol 2006, 201:66-74.
10. Cavaliere F., Vicente E.S., Matute C. An organotypic culture model to study nigro-striatal degeneration. J Neurosci Methods 2010, 188:205-212.
11. Chang C.Y., Chien H.F., Jiangshieh Y.F., Wu C.H. Microglia in the olfactory bulb of rats during postnatal development and olfactory nerve injury with zinc sulfate: a lectin labeling and ultrastrucutural study. Neurosci Res 2003, 45:325-333.
12. Cho S., Liu D., Fairman D., Li P., Jenkins L., McGonigle P., et al. Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures. Neurochem Int 2004, 45:117-127.
13. Crosio C., Fimia G.M., Loury R., Kimura M., Okano Y., Zhou H., et al. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002, 22:874-885.
14. Dailey M.E., Waite M. Confocal imaging of microglial cell dynamics in hippocampal slice cultures. Methods 1999, 18:222-230. 177.
15. Davies J.D., Cobbold S.P., Waldmann H. Strain variation in susceptibility to monoclonal antibody-induced transplantation tolerance. Transplantation 1997, 63:1570-1573.
16. Dayer A.G., Jenny B., Potter G., Sauvain M.O., Szabo G., Vutskits L., et al. Recruiting new neurons from the subventricular zone to the rat postnatal cortex: an organotypic slice culture model. Eur J Neurosci 2008, 27:1051-1060.
17. De Marchis S., Fasolo A., Shipley M., Puche A. Unique neuronal tracers show migration and differentiation of SVZ progenitors in organotypic slices. J Neurobiol 2001, 49:326-338.
18. Di Cunto F., Imarisio S., Hirsch E., Broccoli V., Bulfone A., Migheli A., et al. Defective neurogenesis in citron kinase knockout mice by altered cytokinesis and massive apoptosis. Neuron 2000, 28:115-127.
19. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997, 17:5046-5061.
20. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev 2003, 13:543-550.
21. Eckenhoff M.F., Rakic P. Radial organization of the hippocampal dentate gyrus: a golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 1984, 223:1-21.
22. Emsley J.G., Mitchell B.D., Kempermann G., Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 2005, 75:321-341.
23. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
24. Gahwiler B.H. Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 1981, 4:329-342.
25. Gerdes J., Lemke H., Baisch H., Wacker H.H., Schwab U., Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 1984, 133:1710-1715.
26. Ghoumari A.M., Wehrle R., Bernard O., Sotelo C., Dusart I. Implication of Bcl-2 and caspase-3 in age-related Purkinje cell death in murine organotypic culture: an in vitro model to study apoptosis. Eur J Neurosci 2000, 12:2935-2949.
27. Goings G.E., Kozlowski D.A., Szele F.G. Differential activation of microglia in neurogenic versus non-neurogenic regions of the forebrain. Glia 2006, 54:329-342.
28. Gould E., Gross C.G. Neurogenesis in adult mammals: some progress and problems. J Neurosci 2002, 22:619-623.
29. Graeber M.B., Streit W.J. Microglia: biology and pathology. Acta Neuropathol 2010, 119:89-105.
30. Gritti A., Bonfanti L. Neuronal-glial interactions in central nervous system neurogenesis: the neural stem cell perspective. Neuron Glia Biol 2007, 3:309-323.
31. Gritti A., Dal Molin M., Foroni C., Bonfanti L. Effects of developmental age, brain region, and time in culture on long-term proliferation and multipotency of neural stem cell populations. J Comp Neurol 2009, 517:333-349.
32. Hendzel M.J., Wei Y., Mancini M.A., Van Hooser A., Ranalli T., Brinkley B.R., et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106:348-360.
33. House S.B., Thomas A., Kusano K., Gainer H. Stationary organotypic cultures of oxytocin and vasopressin magnocellular neurones from rat and mouse hypothalamus. J Neuroendocrinol 1998, 10:849-861.
34. Hu B.R., Liu C.L., Ouyang Y., Blomgren K., Siesjo B.K. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 2000, 20:1294-1300.
35. Ikegami K., Koike T. Non-apoptotic neurite degeneration in apoptotic neuronal death: pivotal role of mitochondrial function in neurites. Neuroscience 2003, 122:617-626.
36. Imai Y., Ibata I., Ito D., Ohsawa K., Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 1996, 224:855-862.
37. Kamada M., Li R.Y., Hashimoto M., Kakuda M., Okada H., Koyanagi Y., et al. Intrinsic and spontaneous neurogenesis in the postnatal slice culture of rat hippocampus. Eur J Neurosci 2004, 20:2499-2508.
38. Kee N., Sivalingam S., Boonstra R., Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 2002, 115:97-105.
39. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009, 32:149-184.
40. Laskowski A., Schmidt W., Dinkel K., Martinez-Sanchez M., Reymann K.G. bFGF and EGF modulate trauma-induced proliferation and neurogenesis in juvenile organotypic hippocampal slice cultures. Brain Res 2005, 1037:78-89.
41. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., Steindler D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci U S A 2000, 97:13883-13888.
42. Lushnikova I.V., Voronin K.Y., Malyarevskyy P.Y., Skibo G.G. Morphological and functional changes in rat hippocampal slice cultures after short-term oxygen-glucose deprivation. J Cell Mol Med 2004, 8:241-248.
43. Marshall G.P., Demir M., Steindler D.A., Laywell E.D. Subventricular zone microglia possess a unique capacity for massive in vitro expansion. Glia 2008, 56:1799-1808.
44. McIlroy D., Sakahira H., Talanian R.V., Nagata S. Involvement of caspase 3-activated DNase in internucleosomal DNA cleavage induced by diverse apoptotic stimuli. Oncogene 1999, 18:4401-4408.
45. Menezes J.R., Luskin M.B. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 1994, 14:5399-5416.
46. Morrison S.J., Spradling A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132:598-611.
47. Nam S.C., Kim Y., Dryanovski D., Walker A., Goings G., Woolfrey K., et al. Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol 2007, 505:190-208.
48. Namba T., Mochizuki H., Onodera M., Namiki H., Seki T. Postnatal neurogenesis in hippocampal slice cultures: early in vitro labeling of neural precursor cells leads to efficient neuronal production. J Neurosci Res 2007, 85:1704-1712.
49. Newell D.W., Barth A., Papermaster V., Malouf A.T. Glutamate and non-glutamate receptor mediated toxicity caused by oxygen and glucose deprivation in organotypic hippocampal cultures. J Neurosci 1995, 15:7702-7711.
50. Noraberg J., Kristensen B.W., Zimmer J. Markers for neuronal degeneration in organotypic slice cultures. Brain Res Brain Res Protoc 1999, 3:278-290.
51. Noyan-Ashraf M.H., Brandizzi F., Juurlink B.H. Constitutive nuclear localization of activated caspase 3 in subpopulations of the astroglial family of cells. Glia 2005, 49:588-593.
52. Ohira K., Furuta T., Hioki H., Nakamura K.C., Kuramoto E., Tanaka Y., et al. Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci 2009, 13:173-179.
53. Peretto P., Giachino C., Aimar P., Fasolo A., Bonfanti L. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 2005, 487:407-427.
54. Platel J.C., Gordon V., Heintz T., Bordey A. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 2009, 57:66-78.
55. Plenz D., Kitai S.T. Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures. J Neurophysiol 1996, 76:4180-4184.
56. Ponti G., Aimar P., Bonfanti L. Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J Comp Neurol 2006, 498:491-507.
57. Ponti G., Peretto P., Bonfanti L. A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 2006, 294:168-180.
58. Ponti G., Crociara P., Armentano M., Bonfanti L. Adult neurogenesis without germinal layers: the " atypical" cerebellum of rabbits. Arch Ital Biol 2010, 148:147-158.
59. Raineteau O., Rietschin L., Gradwohl G., Guillemot F., Gahwiler B.H. Neurogenesis in hippocampal slice cultures. Mol Cell Neurosci 2004, 26:241-250.
60. Rakic P. Adult neurogenesis in mammals: an identity crisis. J Neurosci 2002, 22:614-618.
61. Reynolds B.A., Rietze R.L. Neural stem cells and neurospheres - re-evaluating the relationship. Nat Methods 2005, 2:333-336.
62. Rosenzweig S., Luu P. Adult neurogenesis workshop report. Front Neurosci 2010, 4.
63. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
64. Sedgwick J.D., Schwender S., Imrich H., Dorries R., Butcher G.W., ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci U S A 1991, 88:7438-7442.
65. Soares S., Sotelo C. Adult neural stem cells from the mouse subventricular zone are limited in migratory ability compared to progenitor cells of similar origin. Neuroscience 2004, 128:807-817.
66. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009, 32:638-647.
67. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol 2009, 119:7-35.
68. Stoppini L., Buchs P.A., Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991, 37:173-182.
69. Streit W.J., Kreutzberg G.W. Lectin binding by resting and reactive microglia. J Neurocytol 1987, 16:249-260.
70. Tanvig M., Blaabjerg M., Andersen R.K., Villa A., Rosager A.M., Poulsen F.R., et al. A brain slice culture model for studies of endogenous and exogenous precursor cell migration in the rostral migratory stream. Brain Res 2009, 1295:1-12.
71. Tramontin A.D., Garcia-Verdugo J.M., Lim D.A., Alvarez-Buylla A. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 2003, 13:580-587.
72. Van Cruchten S., Van Den Broeck W. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol 2002, 31:214-223.
73. Vergni D., Castiglione F., Briani M., Middei S., Alberdi E., Reymann K.G., et al. A model of ischemia-induced neuroblast activation in the adult subventricular zone. PLoS One 2009, 4:e5278.
74. Weissman T., Noctor S.C., Clinton B.K., Honig L.S., Kriegstein A.R. Neurogenic radial glial cells in reptile, rodent and human: from mitosis to migration. Cereb Cortex 2003, 13:550-559.
75. Wichterle H., Garcia-Verdugo J.M., Alvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 1997, 18:779-791.
76. Wood C., Kabat E.A., Murphy L.A., Goldstein I.J. Immunochemical studies of the combining sites of the two isolectins, A4 and B4, isolated from Bandeiraea simplicifolia. Arch Biochem Biophys 1979, 198:1-11.
77. Wu C.H., Chien H.F., Chang C.Y., Chen S.H., Huang Y.S. Response of amoeboid and differentiating ramified microglia to glucocorticoids in postnatal rats: a lectin histochemical and ultrastructural study. Neurosci Res 2001, 40:235-244.
78. Yan X.X., Najbauer J., Woo C.C., Dashtipour K., Ribak C.E., Leon M. Expression of active caspase-3 in mitotic and postmitotic cells of the rat forebrain. J Comp Neurol 2001, 433:4-22.
79. Ye Y., Fortini M.E. Proteolysis and developmental signal transduction. Semin Cell Dev Biol 2000, 11:211-221.
80. Zhang Y., Allodi S., Sandeman D.C., Beltz B.S. Adult neurogenesis in the crayfish brain: proliferation, migration, and possible origin of precursor cells. Dev Neurobiol 2009, 69:415-436.
81. Zupanc G.K. Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2006, 192:649-670.