BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation

Brain Research Reviews

Volumn 53, Issue 1, 2007, Pages 198-214

  Taupin, Philippe ^a,b,c  

^a NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Abortive cell cycle reentry; Cell cycle; DNA synthesis; Gene duplication; Mutagen; Thymidine analog

Indexed keywords

BROXURIDINE; CELL MARKER; THYMIDINE DERIVATIVE;

BIOAVAILABILITY; BIRTH; CELL CYCLE S PHASE; CELL DEATH; CELL PROLIFERATION; DNA REPAIR; DNA SYNTHESIS; GENE CONTROL; GENE DUPLICATION; HUMAN; IMMUNOHISTOCHEMISTRY; MAMMAL; MOLECULAR STABILITY; MUTAGENESIS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROSCIENCE; NEUROTOXICITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; TERATOMA; VALIDATION PROCESS;

ANIMALS; ARTIFACTS; BROMODEOXYURIDINE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA; DNA DAMAGE; IMMUNOHISTOCHEMISTRY; NEURONAL PLASTICITY; STAINING AND LABELING;

EID: 33845209203     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2006.08.002     Document Type: Review

References (235)

1. Alexiades M.R., and Cepko C. Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev. Dyn. 205 (1996) 293-307
2. Altman J. Autoradiographic and histological studies of postnatal neurogenesis: IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137 (1969) 433-458
3. Altman J., and Bayer S.A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. Comp. Neurol. 301 (1990) 325-342
4. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124 (1965) 319-336
5. Alvarez-Buylla A., Garcia-Verdugo J.M., and Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev., Neurosci. 2 (2001) 287-293
6. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., Fike J.R., Lee H.O., Pfeffer K., Lois C., Morrison S.J., and Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003) 968-973
7. Anderson D.J., Gage F.H., and Weissman I.L. Can stem cells cross lineage boundaries?. Nat. Med. 7 (2001) 393-395
8. Angevine Jr. J.B. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. 11 (1965) 1-70
9. Arvidsson A., Kokaia Z., and Lindvall O. N-methyl-d-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur. J. Neurosci. 14 (2001) 10-18
10. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970
11. Ballabh P., Braun A., and Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16 (2004) 1-13
12. Bannigan J.G. The effects of 5-bromodeoxyuridine on fusion of the cranial neural folds in the mouse embryo. Teratology 32 (1985) 229-239
13. Bannigan J., and Langman J. The cellular effect of 5-bromodeoxyuridine on the mammalian embryo. J. Embryol. Exp. Morphol. 50 (1979) 123-135
14. Bannigan J.G., Cottel D.C., and Morris l.A. Study of the mechanisms of BUdR-induced cleft palate in the mouse. Teratology 42 (1990) 79-89
15. Bauer S., and Patterson P.H. The cell cycle-apoptosis connection revisited in the adult brain. J. Cell Biol. 171 (2005) 641-650
16. Bayer S.A., Yackel J.W., and Puri P.S. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216 (1982) 890-892
17. Bedard A., and Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res. Dev. Brain Res. 151 (2004) 159-168
18. Bedard A., Cossette M., Levesque M., and Parent A. Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci. Lett. 328 (2002) 213-216
19. Bedard A., Gravel C., and Parent A. Chemical characterization of newly generated neurons in the striatum of adult primates. Exp. Brain Res. 170 (2006) 501-512
20. Begg A.C., Hofland I., Van Der Pavert I., Van Der Schueren B., and Haustermans K. Use of thymidine analogues to indicate vascular perfusion in tumours. Br. J. Cancer 83 (2000) 899-905
21. Beisker W., and Hittelman W.N. Measurement of the kinetics of DNA repair synthesis after UV irradiation using immunochemical staining of incorporated 5-bromo-2′-deoxyuridine and flow cytometry. Exp. Cell Res. 174 (1988) 156-167
22. Belluzzi O., Benedusi M., Ackman J., and LoTurco J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Nuerosci. 23 (2003) 10411-10418
23. Bernhardt R., and Matus A. Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeletons. J. Comp. Neurol. 226 (1984) 203-221
24. Bernier P.J., Bedard A., Vinet J., Levesque M., and Parent A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 11464-11469
25. Blaschke A.J., Staley K., and Chun J. Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122 (1996) 1165-1174
26. Bonfanti L., and Theodosis D.T. Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62 (1994) 291-305
27. Brezun J.M., and Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 89 (1999) 999-1002
28. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
29. Bullwinkel J., Baron-Luhr B., Ludemann A., Wohlenberg C., Gerdes J., and Scholzen T. Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J. Cell. Physiol. 206 (2006) 624-635
30. Burns K.A., and Kuan C.Y. Low doses of bromo- and iododeoxyuridine produce near-saturation labeling of adult proliferative populations in the dentate gyrus. Eur. J. Neurosci. 21 (2005) 803-807
31. Burns T.C., Ortiz-Gonzalez X.R., Gutierrez-Perez M., Keene C.D., Sharda R., Demorest Z.L., Jiang Y., Nelson-Holte M., Soriano M., Nakagawa Y., Luquin M.R., Garcia-Verdugo J.M., Prosper F., Low W.C., and Verfaillie C.M. Thymidine Analogs are transferred from pre-labeled donor to host cells in the central nervous system after transplantation: a word of caution. Stem Cells 24 (2006) 1121-1127
32. Busser J., Geldmacher D.S., and Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18 (1998) 2801-2807
33. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001) 406-417
34. Cameron H.A., Woolley C.S., McEwen B.S., and Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56 (1993) 337-344
35. Carlen M., Cassidy R.M., Brismar H., Smith G.A., Enquist L.W., and Frisen J. Functional integration of adult-born neurons. Curr. Biol. 12 (2002) 606-608
36. Carpentier P., Delamanche I.S., Le Bert M., Blanchet G., and Bouchaud C. Seizure-related opening of the blood-brain barrier induced by soman: possible correlation with the acute neuropathology observed in poisoned rats. Neurotoxicology 11 (1990) 493-508
37. Charles P., Reynolds R., Seilhean D., Rougon G., Aigrot M.S., Niezgoda A., Zalc B., and Lubetzki C. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis?. Brain 125 (2002) 1972-1979
38. Chen Y., McPhie D.L., Hirschberg J., and Neve R.L. The amyloid precursor protein-binding protein APP-BP1 drives the cell cycle through the S-M checkpoint and causes apoptosis in neurons. J. Biol. Chem. 275 (2000) 8929-8935
39. Chen J., Magavi S.S., and Macklis J.D. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16357-16362
40. Cooper-Kuhn C.M., and Kuhn H.G. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res. Dev. Brain Res. 134 (2002) 13-21
41. Corotto F.S., Henegar J.A., and Maruniak J.A. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett. 149 (1993) 111-114
42. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., and van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16 (1996) 2649-2658
43. Crespo D., Stanfield B.B., and Cowan W.M. Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp. Brain Res. 62 (1986) 541-548
44. Curtis M.A., Penney E.B., Pearson A.G., van Roon-Mom W.M., Butterworth N.J., Dragunow M., Connor B., and Faull R.L. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9023-9027
45. D'Amour K.A., and Gage F.H. Are somatic stem cells pluripotent or lineage-restricted?. Nat. Med. 8 (2002) 213-214
46. Danilov A.I., Covacu R., Moe M.C., Langmoen I.A., Johansson C.B., Olsson T., and Brundin L. Neurogenesis in the adult spinal cord in an experimental model of multiple sclerosis. Eur. J. Neurosci. 23 (2006) 394-400
47. Dash P.K., Mach S.A., and Moore A.N. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J. Neurosci. Res. 63 (2001) 313-319
48. del Rio J.A., and Soriano E. Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Brain Res. Dev. Brain Res. 49 (1989) 311-317
49. Delp M.D., Armstrong R.B., Godfrey D.A., Laughlin M.H., Ross C.D., and Wilkerson M.K. Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine. J. Physiol. 533 (2001) 849-859
50. Doetsch F., and Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14895-14900
51. Doetsch F., Garcia-Verdugo J.M., and Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17 (1997) 5046-5061
52. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 (1999) 703-716
53. Eadie B.D., Redila V.A., and Christie B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol. 486 (2005) 39-47
54. Ekdahl C.T., Mohapel P., Elmer E., and Lindvall O. Caspase inhibitors increase short-term survival of progenitor-cell progeny in the adult rat dentate gyrus following status epilepticus. Eur. J. Neurosci. 14 (2001) 937-945
55. Endl E., and Gerdes J. The Ki-67 protein: fascinating forms and an unknown function. Exp. Cell Res. 257 (2000) 231-237
56. Endo Y., Nishimura J.I., Kobayashi S., and Kimura F. Long-term glucocorticoid treatments decrease local cerebral blood flow in the rat hippocampus, in association with histological damage. Neuroscience 79 (1997) 745-752
57. Engstrom Y., Eriksson S., Jildevik I., Skog S., Thelander L., and Tribukait B. Cell cycle-dependent expression of mammalian ribonucleotide reductase. Differential regulation of the two subunits. J. Biol. Chem. 260 (1985) 9114-9116
58. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
59. Fanarraga M.L., Avila J., and Zabala J.C. Expression of unphosphorylated class III beta-tubulin isotype in neuroepithelial cells demonstrates neuroblast commitment and differentiation. Eur. J. Neurosci. 11 (1999) 517-527
60. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., and Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23 (2003) 373-382
61. Florenes V.A., Holm R., Myklebost O., Lendahl U., and Fodstad O. Expression of the neuroectodermal intermediate filament nestin in human melanomas. Cancer Res. 54 (1994) 354-356
62. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., and Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23 (1999) 247-256
63. Freese A., O'Rourke D., Judy K., and O'Connor M.J. The application of 5-bromodeoxyuridine in the management of CNS tumors. J. Neuro-Oncol. 20 (1994) 81-95
64. Frielingsdorf H., Schwarz K., Brundin P., and Mohapel P. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 10177-10182
65. Frisen J., Johansson C.B., Torok C., Risling M., and Lendahl U. Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J. Cell Biol. 131 (1995) 453-464
66. Fukushima M., and Barka T. The effects of 5-bromodeoxyuridine and isoproterenol on the postnatal differentiation of rat submandibular gland. Am. J. Anat. 147 (1976) 159-182
67. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 (1992) 493-501
68. Gage F.H. Mammalian neural stem cells. Science 287 (2000) 1433-1438
69. Gage F.H., Coates P.W., Palmer T.D., Kuhn H.G., Fisher L.J., Suhonen J.O., Peterson D.A., Suhr S.T., and Ray J. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 11879-11883
70. Garcia-Verdugo J.M., Doetsch F., Wichterle H., Lim D.A., and Alvarez-Buylla. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J. Neurobiol. 36 (1998) 234-248
71. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
72. Gobbel G.T., Bellinzona M., Vogt A.R., Gupta N., Fike J.R., and Chan P.H. Response of postmitotic neurons to X-irradiation: implications for the role of DNA damage in neuronal apoptosis. J. Neurosci. 18 (1998) 147-155
73. Gould E., and Gross C.G. Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22 (2002) 619-623
74. Gould E., Tanapat P., McEwen B.S., Flugge G., and Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3168-3171
75. Gould E., Reeves A.J., Graziano M.S., and Gross C.G. Neurogenesis in the neocortex of adult primates. Science 286 (1999) 548-552
76. Gould E., Reeves A.J., Fallah M., Tanapat P., Gross C.G., and Fuchs E. Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5263-5267
77. Gould E., Vail N., Wagers M., and Gross C.G. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10910-10917
78. Graham V., Khudyakov J., Ellis P., and Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 39 (2003) 749-765
79. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218 (1982) 474-475
80. Hall P.A., McKee P.H., Menage H.D., Dover R., and Lane D.P. High levels of p53 protein in UV-irradiated normal human skin. Oncogene 8 (1993) 203-207
81. Hastings N.B., and Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 413 (1999) 146-154 (Erratum in: 1999. J. Comp. Neurol. 415, 144)
82. Haughey N.J., Nath A., Chan S.L., Borchard A.C., Rao M.S., and Mattson M.P. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J. Neurochem. 6 (2002) 1509-1524
83. Hayes N.L., and Nowakowski R.S. Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev. Neurosci. 22 (2000) 44-55
84. Hayes N.L., and Nowakowski R.S. Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res. 134 (2002) 77-85
85. Hendzel M.J., Wei Y., Mancini M.A., Van Hooser A., Ranalli T., Brinkley B.R., Bazett-Jones D.P., and Allis C.D. 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 106 (1997) 348-360
86. Herrup K., and Arendt T. Re-expression of cell cycle proteins induces neuronal cell death during Alzheimer's disease. J. Alzheimer's Dis. 4 (2002) 243-247
87. Herrup K., Neve R., Ackerman S.L., and Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J. Neurosci. 24 (2004) 9232-9239
88. Hoshino T., Nagashima T., Cho K.G., Davis R.L., Donegan J., Slusarz M., and Wilson C.B. Variability in the proliferative potential of human gliomas. J. Neuro-Oncol. 7 (1989) 137-143
89. Hume W.J., and Saffhill R. Iodo- and bromodeoxyuridine are excised at different rates from DNA of mouse tongue keratinocytes in vitro. Chem. Biol. Interact. 60 (1986) 227-232
90. Ide K., and Secher N.H. Cerebral blood flow and metabolism during exercise. Prog. Neurobiol. 61 (2000) 397-414
91. Ignatova T.N., Kukekov V.G., Laywell E.D., Suslov O.N., Vrionis F.D., and Steindler D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39 (2002) 193-206
92. Ino H., and Chiba T. Expression of proliferating cell nuclear antigen (PCNA) in the adult and developing mouse nervous system. Brain Res. Mol. Brain Res. 78 (2000) 163-174
93. Jin K., Sun Y., Xie L., Peel A., Mao X.O., Batteur S., and Greenberg D.A. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol. Cell. Neurosci. 24 (2003) 171-189
94. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., and Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 343-347
95. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., and Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13363-13367
96. Jin K., Xie L., Mao X.O., and Greenberg D.A. Alzheimer's disease drugs promote neurogenesis. Brain Res. 1085 (2006) 183-188
97. Kaneko Y., Sakakibara S., Imai T., Suzuki A., Nakamura Y., Sawamoto K., Ogawa Y., Toyama Y., Miyata T., and Okano H. Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev. Neurosci. 22 (2000) 139-153
98. Kanemura Y., Mori K., Sakakibara S., Fujikawa H., Hayashi H., Nakano A., Matsumoto T., Tamura K., Imai T., Ohnishi T., Fushiki S., Nakamura Y., Yamasaki M., Okano H., and Arita N. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 68 (2001) 141-152
99. Kaplan M.S. Proliferation of subependymal cells in the adult primate CNS: differential uptake of DNA labelled precursors. J. Hirnforsch. 24 (1983) 23-33
100. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
101. Katchanov J., Harms C., Gertz K., Hauck L., Waeber C., Hirt L., Priller J., von Harsdorf R., Bruck W., Hortnagl H., Dirnagl U., Bhide P.G., and Endres M. Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J. Neurosci. 21 (2001) 5045-5053
102. Kato T., Yokouchi K., Fukushima N., Kawagishi K., Li Z., and Moriizumi T. Continual replacement of newly-generated olfactory neurons in adult rats. Neurosci. Lett. 307 (2001) 17-20
103. Katsetos C.D., Del Valle L., Geddes J.F., Assimakopoulou M., Legido A., Boyd J.C., Balin B., Parikh N.A., Maraziotis T., de Chadarevian J.P., Varakis J.N., Matsas R., Spano A., Frankfurter A., Herman M.M., and Khalili K. Aberrant localization of the neuronal class III beta-tubulin in astrocytomas. Arch. Pathol. Lab. Med. 125 (2001) 613-624
104. Katsetos C.D., Herman M.M., and Mork S.J. Class III beta-tubulin in human development and cancer. Cell. Motil. Cytoskeleton 55 (2003) 77-96
105. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods 115 (2002) 97-105
106. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997) 493-495
107. Keoffler H.P., Yen J., and Carlson J. The study of human myeloid differentiation using bromodeoxyuridine (BrdU). J. Cell. Physiol. 116 (1983) 111-117
108. Klein J.A., and Ackerman S.L. Oxidative stress, cell cycle, and neurodegeneration. J. Clin. Invest. 111 (2003) 785-793
109. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., and Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419 (2002) 367-374
110. Koketsu D., Mikami A., Miyamoto Y., and Hisatsune T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J. Neurosci. 23 (2003) 937-942
111. Kokoeva M.V., Yin H., and Flier J.S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310 (2005) 679-683
112. Kolb B., Pedersen B., Ballermann M., Gibb R., and Whishaw I.Q. Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J. Neurosci. 19 (1999) 2337-2346
113. Komitova M., and Eriksson P.S. Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci. Lett. 369 (2004) 24-27
114. Kopen G.C., Prockop D.J., and Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10711-10716
115. Kornack D.R., and Rakic P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5768-5773
116. Kornack D.R., and Rakic P. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4752-4757
117. Kornack D.R., and Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 294 (2001) 2127-2130
118. Korr H., Koeser K., Oldenkott S., Schmidt H., and Schultze B. X-ray dose-effect relationship on unscheduled DNA synthesis and spontaneous unscheduled DNA synthesis in mouse brain cells studied in vivo. Radiat. Environ. Biophys. 28 (1989) 13-26
119. Kriss J.P., Maruyama Y., Tung L.A., Bond S.B., and Revesz L. The fate of 5-bromodeoxyuridine, 5-bromodeoxycytidine, and 5-iododeoxycytidine in man. Cancer Res. 23 (1963) 260-268
120. Kuan C.Y., Schloemer A.J., Lu A., Burns K.A., Weng W.L., Williams M.T., Strauss K.I., Vorhees C.V., Flavell R.A., Davis R.J., Sharp F.R., and Rakic P. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J. Neurosci. 24 (2004) 10763-10772
121. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16 (1996) 2027-2033
122. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., and Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17 (1997) 5820-5829
123. Kurki P., Vanderlaan M., Dolbeare F., Gray J., and Tan E.M. Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp. Cell Res. 166 (1986) 209-219
124. Kuwagata M., and Nagao T. Behavior and reproductive function of rat male offspring treated prenatally with 5-bromo-2′-deoxyuridine. Reprod. Toxicol. 12 (1998) 541-549
125. Langley B., and Ratan R.R. Oxidative stress-induced death in the nervous system: cell cycle dependent or independent?. J. Neurosci. Res. 77 (2004) 621-629
126. Lendahl U., Zimmerman L.B., and McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
127. Li L., Story M., and Legerski R.J. Cellular responses to ionizing radiation damage. Int. J. Radiat. Oncol. Biol. Phys. 49 (2001) 1157-1162
128. Li Y., Chen J., and Chopp M. Adult bone marrow transplantation after stroke in adult rats. Cell Transplant. 10 (2001) 31-40
129. Lie D.C., Dziewczapolski G., Willhoite A.R., Kaspar B.K., Shults C.W., and Gage F.H. The adult substantia nigra contains progenitor cells with neurogenic potential. J. Neurosci. 22 (2002) 6639-6649
130. Liu D.X., and Greene L.A. Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res. 305 (2001) 217-228
131. Liu J., Solway K., Messing R.O., and Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci. 18 (1998) 7768-7778
132. Lois C., and Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 264 (1994) 1145-1148
133. Lois C., Garcia-Verdugo J.M., and Alvarez-Buylla A. Chain migration of neuronal precursors. Science 271 (1996) 978-981
134. Lopez F., Belloc F., Lacombe F., Dumain P., Reiffers J., Bernard P., and Boisseau M.R. Modalities of synthesis of Ki-67 antigen during the stimulation of lymphocytes. Cytometry 12 (1991) 42-49
135. Lowndes N.F., and Murguia J.R. Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10 (2000) 17-25
136. Lynch T.P., Cass C.E., and Paterson A.R. Defective transport of thymidine by cultured cells resistant to 5-bromodeoxyuridine. J. Supramol. Struct. 6 (1977) 363-374
137. Magavi S.S., Leavitt B.R., and Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000) 951-955
138. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
139. Mann G.J., Musgrove E.A., Fox R.M., and Thelander L. Ribonucleotide reductase M1 subunit in cellular proliferation, quiescence, and differentiation. Cancer Res. 48 (1988) 5151-5156
140. Markakis E.A., and Gage F.H. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406 (1999) 449-460
141. Marusich M.F., Furneaux H.M., Henion P.D., and Weston J.A. Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol. 25 (1994) 143-155
142. Memo M. DNA damage and DNA repair in the nervous system. Neurobiol. Aging 20 (1999) 89-90
143. Mezey E. Commentary: on bone marrow stem cells and openmindedness. Stem Cells Dev. 13 (2004) 147-152
144. Miller M.W., and Nowakowski R.S. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res. 457 (1988) 44-52
145. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., and Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 63 (2003) 4021-4027
146. Moran R., Darzynkiewicz Z., Staiano-Coico L., and Melamed M.R. Detection of 5-bromodeoxyuridine (BrdUrd) incorporation by monoclonal antibodies: role of the DNA denaturation step. J. Histochem. Cytochem. 33 (1985) 821-827
147. Morris S.M. The genetic toxicology of 5-bromodeoxyuridine in mammalian cells. Mutat. Res. 258 (1991) 161-188
148. Morris S.M., Domon O.E., McGarrity L.J., Kodell R.L., and Casciano D.A. Effect of bromodeoxyuridine on the proliferation and growth of ethyl methanesulfonate-exposed P3 cells: relationship to the induction of sister-chromatid exchanges. Cell. Biol. Toxicol. 8 (1992) 75-87
149. Morshead C.M., and van der Kooy D. Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12 (1992) 249-256
150. Mullen R.J., Buck C.R., and Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116 (1992) 201-211
151. Nagai A., Matsumiya H., Yasui S., Aoshiba K., Ishihara Y., and Konno K. Administration of bromodeoxyuridine in early postnatal rats results in lung changes at maturity. Exp. Lung Res. 19 (1993) 203-219
152. Nagao T., Kuwagata M., and Saito Y. Effects of prenatal exposure to 5-fluoro-2′-deoxyuridine on developing central nervous system and reproductive function in male offspring of mice. Teratog., Carcinog., Mutagen. 18 (1998) 73-92
153. Nakashima K., Ninomiya H., and Fujiki Y. The effect of 5-bromodeoxyuridine on mouse embryos during neurulation in vitro. Experientia 40 (1984) 924-929
154. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K.J., Yuan J., and Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 18 (1998) 3659-3668
155. Nowakowski R.S., and Hayes N.L. New neurons: extraordinary evidence or extraordinary conclusion?. Science 288 (2000) 771
156. Nowakowski R.S., and Hayes N.L. Stem cells: the promises and pitfalls. Neuropsychopharmacology 25 (2001) 799-804
157. Nowakowski R.S., Lewin S.B., and Miller M.W. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol. 18 (1989) 311-318
158. Okuda T., Tagawa K., Qi M.L., Hoshio M., Ueda H., Kawano H., Kanazawa I., Muramatsu M., and Okazawa H. Oct-3/4 repression accelerates differentiation of neural progenitor cells in vitro and in vivo. Brain Res. Mol. Brain Res. 132 (2004) 18-30
159. Oltra S., and Martinez F. The doublecortin gene, a new molecular marker to detect minimal residual disease in neuroblastoma. Diagn. Mol. Pathol. 14 (2005) 53-57
160. Menzies R.A., and Skalko R.G. Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse. Differentiation 1 (1973) 397-404
161. Palmer T.D., Willhoite A.R., and Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425 (2000) 479-494
162. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
163. Parent J.M., Tada E., Fike J.R., and Lowenstein D.H. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci. 19 (1999) 4508-4519
164. Pencea V., Bingaman K.D., Freedman L.J., and Luskin M.B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 172 (2001) 1-16
165. Pompeiano M., Blaschke A.J., Flavell R.A., Srinivasan A., and Chun J. Decreased apoptosis in proliferative and postmitotic regions of the caspase 3-deficient embryonic central nervous system. J. Comp. Neurol. 423 (2000) 1-12
166. Pont F., Collet A., and Lallement G. Early and transient increase of rat hippocampal blood-brain barrier permeability to amino acids during kainic acid-induced seizures. Neurosci. Lett. 184 (1995) 52-54
167. Qu T.Y., Dong X.J., Sugaya I., Vaghani A., Pulido J., and Sugaya K. Bromodeoxyuridine increases multipotency of human bone marrow-derived stem cells. Restor. Neurol. Neurosci. 22 (2004) 459-468
168. Quinn C.C., Gray G.E., and Hockfield S. A family of proteins implicated in axon guidance and outgrowth. J. Neurobiol. 41 (1999) 158-164
169. Rakic P. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183 (1974) 425-427
170. Rakic P. Limits of neurogenesis in primates. Science 227 (1985) 1054-1056
171. Rakic P. Adult neurogenesis in mammals: an identity crisis. J. Neurosci. 22 (2002) 614-618
172. Rehen S.K., McConnell M.J., Kaushal D., Kingsbury M.A., Yang A.H., and Chun J. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13361-13366
173. Rehen S.K., Yung Y.C., McCreight M.P., Kaushal D., Yang A.H., Almeida B.S., Kingsbury M.A., Cabral K.M., McConnell M.J., Anliker B., Fontanoz M., and Chun J. Constitutional aneuploidy in the normal human brain. J. Neurosci. 25 (2005) 2176-2180
174. Rietze R., Poulin P., and Weiss S. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J. Comp. Neurol. 424 (2000) 397-408
175. Ribatti D., Nico B., Crivellato E., and Artico M. Development of the blood-brain barrier: a historical point of view. Anat. Rec. B New Anat. 289 (2006) 3-8
176. Rousselot P., Lois C., and Alvarez-Buylla A. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351 (1995) 51-61
177. Saffhill R., and Ockey C.H. Strand breaks arising from the repair of the 5-bromodeoxyuridine-substituted template and methyl methanesulphonate-induced lesions can explain the formation of sister chromatid exchanges. Chromosoma 92 (1985) 218-224
178. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Garcia-Verdugo J.M., Berger M.S., and Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004) 740-744
179. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
180. Schlessinger A.R., Cowan W.M., and Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 159 (1975) 149-175
181. Schmitz C., Axmacher B., Zunker U., and Korr H. Age-related changes of DNA repair and mitochondrial DNA synthesis in the mouse brain. Acta Neuropathol. (Berl) 97 (1999) 71-81
182. Scholzen T., and Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182 (2000) 311-322
183. Sekerkova G., Ilijic E., and Mugnaini E. Bromodeoxyuridine administered during neurogenesis of the projection neurons causes cerebellar defects in rat. J. Comp. Neurol. 470 (2004) 221-239
184. Seki T., and Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci. 13 (1993) 2351-2358
185. Seki T., and Arai Y. Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J. Comp. Neurol. 410 (1999) 503-513
186. Selden J.R., Dolbeare F., Clair J.H., Nichols W.W., Miller J.E., Kleemeyer K.M., Hyland R.J., and DeLuca J.G. Statistical confirmation that immunofluorescent detection of DNA repair in human fibroblasts by measurement of bromodeoxyuridine incorporation is stoichiometric and sensitive. Cytometry 14 (1993) 154-167
187. Selden J.R., Dolbeare F., Clair J.H., Miller J.E., McGettigan K., DiJohn J.A., Dysart G.R., and DeLuca J.G. Validation of a flow cytometric in vitro DNA repair (UDS) assay in rat hepatocytes. Mutat. Res. 315 (1994) 147-167
188. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
189. Sharma H.S., Cervos-Navarro J., and Dey P.K. Increased blood-brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats. Neurosci. Res. 10 (1991) 211-221
190. Shihabuddin L.S., Horner P.J., Ray J., and Gage F.H. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci. 20 (2000) 8727-8735
191. Shinohara C., Gobbel G.T., Lamborn K.R., Tada E., and Fike J.R. Apoptosis in the subependyma of young adult rats after single and fractionated doses of X-rays. Cancer Res. 57 (1997) 2694-2702
192. Sidman R.L. Autoradiographic methods and principles for study of the nervous system with thymidine-H3. In: Nauta W.J.H., and Ebbesson S.O.E. (Eds). Contemporary Research Methods in Neuroanatomy (1970), Springer, New York 252-274
193. Sidman R.L., Miale I.L., and Feder N. Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp. Neurol. 1 (1959) 322-333
194. Sloviter R.S. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. Comp. Neurol. 280 (1989) 183-196
195. Snider B.J., Gottron F.J., and Choi D.W. Apoptosis and necrosis in cerebrovascular disease. Ann. N. Y. Acad. Sci. 893 (1999) 243-253
196. Spalding K.L., Bhardwaj R.D., Buchholz B.A., Druid H., and Frisen J. Retrospective birth dating of cells in humans. Cell 122 (2005) 133-143
197. Spector R., and Berlinger W.G. Localization and mechanism of thymidine transport in the central nervous system. J. Neurochem. 39 (1982) 837-841
198. Stanfield B.B., and Trice J.E. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res. 72 (1988) 399-406
199. Struikmans H., Rutgers D.H., Jansen G.H., Tulleken C.A., van der Tweel I., and Batterman J.J. S-phase fraction, 5-bromo-2′-deoxy-uridine labelling index, duration of S-phase, potential doubling time, and DNA index in benign and malignant brain tumors. Radiat. Oncol. Investig. 5 (1997) 170-179
200. Suhonen J.O., Peterson D.A., Ray J., and Gage F.H. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383 (1996) 624-627
201. Sun W., Winseck A., Vinsant S., Park O.H., Kim H., and Oppenheim R.W. Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J. Neurosci. 24 (2004) 11205-11213
202. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Engberg K., Lauterbur P.C., and Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117 (2003) 1037-1046
203. Tada E., Yang C., Gobbel G.T., Lamborn K.R., and Fike J.R. Long-term impairment of subependymal repopulation following damage by ionizing irradiation. Exp. Neurol. 160 (1999) 66-77
204. Tada E., Parent J.M., Lowenstein D.H., and Fike J.R. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99 (2000) 33-41
205. Tai M.H., Chang C.C., Kiupel M., Webster J.D., Olson L.K., and Trosko J.E. Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26 (2005) 495-502 (Erratum in: 2005. Carcinogenesis 26, 1316)
206. Takahashi T., and Caviness Jr. V.S. PCNA-binding to DNA at the G1/S transition in proliferating cells of the developing cerebral wall. J. Neurocytol. 22 (1993) 1096-1102
207. Takahashi T., Nowakowski R.S., and Caviness Jr. V.S. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15 (1995) 6046-6057
208. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999) 5792-5801
209. Tattersfield A.S., Croon R.J., Liu Y.W., Kells A.P., Faull R.L., and Connor B. Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience 127 (2004) 319-332
210. Taupin P. Adult neurogenesis in the mammalian central nervous system: functionality and potential clinical interest. Med. Sci. Monit. 11 (2005) RA247-RA252
211. Taupin P. Neurogenesis in the adult central nervous system. C. R. Biol. 329 (2006) 465-475
212. Taupin P., and Gage F.H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69 (2002) 745-749
213. Taupin P., Ray J., Fischer W.H., Suhr S.T., Hakansson K., Grubb A., and Gage F.H. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28 (2000) 385-397
214. Thomas nee Williams S.A., and Segal M.B. Identification of a saturable uptake system for deoxyribonucleosides at the blood-brain and blood-cerebrospinal fluid barriers. Brain Res. 741 (1996) 230-239
215. Thomas S.A., and Segal M.B. Saturation kinetics, specificity and NBMPR sensitivity of thymidine entry into the central nervous system. Brain Res. 760 (1997) 59-67
216. Thomas S.A., Davson H., and Segal M.B. Quantification of efflux into the blood and brain of intraventricularly perfused [3H]-thymidine in the anaesthetized rabbit. Exp. Physiol. 82 (1997) 139-148
217. Tillfors M., Furmark T., Marteinsdottir I., Fischer H., Pissiota A., Langstrom B., and Fredrikson M. Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. Am. J. Psychiatry 158 (2001) 1220-1226
218. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2 (1999) 266-270
219. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nat. Rev., Neurosci. 1 (2000) 191-198
220. Van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
221. Vincent I., Rosado M., and Davies P. Mitotic mechanisms in Alzheimer's disease?. J. Cell Biol. 132 (1996) 413-425
222. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
223. Wichterle H., Garcia-Verdugo J.M., and Alvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18 (1997) 779-791
224. Wilt F.H., and Anderson M. The action of 5-bromodeoxyuridine on differentiation. Dev. Biol. 28 (1972) 443-447
225. Yamada M., Onodera M., Mizuno Y., and Mochizuki H. Neurogenesis in olfactory bulb identified by retroviral labeling in normal and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated adult mice. Neuroscience 124 (2004) 173-181
226. Yamaguchi M., Saito H., Suzuki M., and Mori K. Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. NeuroReport 11 (2000) 1991-1996
227. Yang Y., Geldmacher D.S., and Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J. Neurosci. 21 (2001) 2661-2668
228. Yang Y., Mufson E.J., and Herrup K. Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23 (2003) 2557-2563
229. Yu W.H. The effect of 5-bromodeoxyuridine on the postnatal development of the rat cerebellum: a biochemical study. Brain Res. 118 (1976) 281-291
230. Younkin L., and Silberberg D. Myelination in developing cultured newborn rat cerebellum inhibited by 5-bromodeoxyuridine. Exp. Cell Res. 76 (1973) 455-458
231. Younkin L.H., and Silberberg D.H. Delay of oligodendrocyte differentiation by 5-bromodeoxyuridine (BUdR). Brain Res. 101 (1976) 600-605
232. Zacchetti A., van Garderen E., Teske E., Nederbragt H., Dierendonck J.H., and Rutteman G.R. Validation of the use of proliferation markers in canine neoplastic and non-neoplastic tissues: comparison of KI-67 and proliferating cell nuclear antigen (PCNA) expression versus in vivo bromodeoxyuridine labelling by immunohistochemistry. APMIS 111 (2003) 430-438
233. Zhao M., Momma S., Delfani K., Carlen M., Cassidy R.M., Johansson C.B., Brismar H., Shupliakov O., Frisen J., and Janson A.M. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7925-7930
234. Zhu H., Wang Z.Y., and Hansson H.A. Visualization of proliferating cells in the adult mammalian brain with the aid of ribonucleotide reductase. Brain Res. 977 (2003) 180-189
235. Zhu H., Dahlstrom A., and Hansson H.A. Characterization of cell proliferation in the adult dentate under normal conditions and after kainate induced seizures using ribonucleotide reductase and BrdU. Brain Res. 1036 (2005) 7-17