 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, October 1, 1998, 18(19):7768-7778
Increased Neurogenesis in the Dentate Gyrus After Transient Global Ischemia in Gerbils
Jialing Liu1, Karen Solway1, Robert O. Messing2, and Frank R. Sharp1 1 Departments of Neurology and Neurosurgery, University of California at San Francisco and San Francisco Veterans Affairs Medical Center, San Francisco, California 94121, and 2 Department of Neurology, Ernest Gallo Clinic and Research Center and Graduate Programs in Neuroscience and Biomedical Sciences, University of California at San Francisco, San Francisco, California 94110
Neurogenesis in the dentate gyrus of adult rodents is regulated by NMDA receptors, adrenal steroids, environmental stimuli, and seizures. To determine whether ischemia affects neurogenesis, newly divided cells in the dentate gyrus were examined after transient global ischemia in adult gerbils. 5-Bromo-2'-deoxyuridine-5'-monophosphate (BrdU) immunohistochemistry demonstrated a 12-fold increase in cell birth in the dentate subgranular zone 1-2 weeks after 10 min bilateral common carotid artery occlusions. Two minutes of ischemia did not significantly increase BrdU incorporation. Confocal microscopy demonstrated that BrdU immunoreactive cells in the granule cell layer colocalized with neuron-specific markers for neuronal nuclear antigen, microtubule-associated protein-2, and calbindin D28k, indicating that the newly divided cells migrated from the subgranular zone into the granule cell layer and matured into neurons. Newborn cells with a neuronal phenotype were first seen 26 d after ischemia, survived for at least 7 months, were located only in the granule cell layer, and comprised ~60% of BrdU-labeled cells in the granule cell layer 6 weeks after ischemia. The increased neurogenesis was not attributable to entorhinal cortical lesions, because no cell loss was detected in this region. Ischemic preconditioning for 2 min, which protects CA1 neurons against subsequent ischemic damage, did not prevent increased neurogenesis in the granule cell layer after a subsequent severe ischemic challenge. Thus, ischemia-induced dentate neurogenesis is not attributable to CA1 neuronal loss. Enhanced neurogenesis in the dentate gyrus may be a compensatory adaptive response to ischemia-associated injury and could promote functional recovery after ischemic hippocampal injury.
Key words: neurogenesis; dentate gyrus; granule neuron; cerebral ischemia; hippocampus; CA1; NMDA receptor; entorhinal cortex; neural stem cells; BrdU; NeuN; GFAP; MAP-2; calbindin; spreading depression; subependyma; erythropoietin; FGF; BDNF
Copyright © 1998 Society for Neuroscience 0270-6474/98/18197768-11$05.00/0
This article has been cited by other articles:
T. D. Perera, S. Park, and Y. Nemirovskaya
Cognitive Role of Neurogenesis in Depression and Antidepressant Treatment
Neuroscientist, August 1, 2008; 14(4): 326 - 338.
[Abstract] [PDF]
M. Higashi, N. Maruta, A. Bernstein, K. Ikenaka, and S. Hitoshi
Mood Stabilizing Drugs Expand the Neural Stem Cell Pool in the Adult Brain Through Activation of Notch Signaling
Stem Cells, July 1, 2008; 26(7): 1758 - 1767.
[Abstract] [Full Text] [PDF]
F. V. Ermini, S. Grathwohl, R. Radde, M. Yamaguchi, M. Staufenbiel, T. D. Palmer, and M. Jucker
Neurogenesis and Alterations of Neural Stem Cells in Mouse Models of Cerebral Amyloidosis
Am. J. Pathol., June 1, 2008; 172(6): 1520 - 1528.
[Abstract] [Full Text] [PDF]
T. L. Walker, A. White, D. M. Black, R. H. Wallace, P. Sah, and P. F. Bartlett
Latent Stem and Progenitor Cells in the Hippocampus Are Activated by Neural Excitation
J. Neurosci., May 14, 2008; 28(20): 5240 - 5247.
[Abstract] [Full Text] [PDF]
T. P. Obrenovitch
Molecular Physiology of Preconditioning-Induced Brain Tolerance to Ischemia
Physiol Rev, January 1, 2008; 88(1): 211 - 247.
[Abstract] [Full Text] [PDF]
O. Hoffmann, C. Mahrhofer, N. Rueter, D. Freyer, B. Bert, H. Fink, and J. R. Weber
Pneumococcal Cell Wall-Induced Meningitis Impairs Adult Hippocampal Neurogenesis
Infect. Immun., September 1, 2007; 75(9): 4289 - 4297.
[Abstract] [Full Text] [PDF]
T. Sasaki, K. Kitagawa, E. Omura-Matsuoka, K. Todo, Y. Terasaki, S. Sugiura, J. Hatazawa, Y. Yagita, and M. Hori
The Phosphodiesterase Inhibitor Rolipram Promotes Survival of Newborn Hippocampal Neurons After Ischemia
Stroke, May 1, 2007; 38(5): 1597 - 1605.
[Abstract] [Full Text] [PDF]
K. Engelhard, U. Winkelheide, C. Werner, J. Kluge, E. Eberspacher, R. Hollweck, P. Hutzler, J. Winkler, and E. Kochs
Sevoflurane Affects Neurogenesis After Forebrain Ischemia in Rats
Anesth. Analg., April 1, 2007; 104(4): 898 - 903.
[Abstract] [Full Text] [PDF]
M. Chopp, Z. G. Zhang, and Q. Jiang
Neurogenesis, Angiogenesis, and MRI Indices of Functional Recovery From Stroke
Stroke, February 1, 2007; 38(2): 827 - 831.
[Abstract] [Full Text] [PDF]
S. Jomura, M. Uy, K. Mitchell, R. Dallasen, C. J. Bode, and Y. Xu
Potential Treatment of Cerebral Global Ischemia with Oct-4+ Umbilical Cord Matrix Cells
Stem Cells, January 1, 2007; 25(1): 98 - 106.
[Abstract] [Full Text] [PDF]
J. Macas, C. Nern, K. H. Plate, and S. Momma
Increased Generation of Neuronal Progenitors after Ischemic Injury in the Aged Adult Human Forebrain
J. Neurosci., December 13, 2006; 26(50): 13114 - 13119.
[Abstract] [Full Text] [PDF]
K. Jin, X. Wang, L. Xie, X. O. Mao, W. Zhu, Y. Wang, J. Shen, Y. Mao, S. Banwait, and D. A. Greenberg
Evidence for stroke-induced neurogenesis in the human brain
PNAS, August 29, 2006; 103(35): 13198 - 13202.
[Abstract] [Full Text] [PDF]
T. Yamashita, M. Ninomiya, P. Hernandez Acosta, J. M. Garcia-Verdugo, T. Sunabori, M. Sakaguchi, K. Adachi, T. Kojima, Y. Hirota, T. Kawase, et al.
Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum.
J. Neurosci., June 14, 2006; 26(24): 6627 - 6636.
[Abstract] [Full Text] [PDF]
M. D. Tran and J. T. Neary
Purinergic signaling induces thrombospondin-1 expression in astrocytes
PNAS, June 13, 2006; 103(24): 9321 - 9326.
[Abstract] [Full Text] [PDF]
K. Jin, M. LaFevre-Bernt, Y. Sun, S. Chen, J. Gafni, D. Crippen, A. Logvinova, C. A. Ross, D. A. Greenberg, and L. M. Ellerby
FGF-2 promotes neurogenesis and neuroprotection and prolongs survival in a transgenic mouse model of Huntington's disease
PNAS, December 13, 2005; 102(50): 18189 - 18194.
[Abstract] [Full Text] [PDF]
N. D. Bull and P. F. Bartlett
The Adult Mouse Hippocampal Progenitor Is Neurogenic But Not a Stem Cell
J. Neurosci., November 23, 2005; 25(47): 10815 - 10821.
[Abstract] [Full Text] [PDF]
T. Sasaki, S. Iwata, H. J. Okano, Y. Urasaki, J. Hamada, H. Tanaka, N. H. Dang, H. Okano, and C. Morimoto
Nedd9 Protein, a Cas-L Homologue, Is Upregulated After Transient Global Ischemia in Rats: Possible Involvement of Nedd9 in the Differentiation of Neurons After Ischemia
Stroke, November 1, 2005; 36(11): 2457 - 2462.
[Abstract] [Full Text] [PDF]
R. L. Zhang, Z. G. Zhang, and M. Chopp
Neurogenesis in the Adult Ischemic Brain: Generation, Migration, Survival, and Restorative Therapy
Neuroscientist, October 1, 2005; 11(5): 408 - 416.
[Abstract] [PDF]
C. Estrada and M. Murillo-Carretero
Nitric Oxide and Adult Neurogenesis in Health and Disease
Neuroscientist, August 1, 2005; 11(4): 294 - 307.
[Abstract] [PDF]
M. E. Gilbert, M. E. Kelly, T. E. Samsam, and J. H. Goodman
Chronic Developmental Lead Exposure Reduces Neurogenesis in Adult Rat Hippocampus but Does Not Impair Spatial Learning
Toxicol. Sci., August 1, 2005; 86(2): 365 - 374.
[Abstract] [Full Text] [PDF]
H. Yanamoto, S. Miyamoto, N. Tohnai, I. Nagata, J.-H. Xue, Y. Nakano, Y. Nakajo, and H. Kikuchi
Induced Spreading Depression Activates Persistent Neurogenesis in the Subventricular Zone, Generating Cells With Markers for Divided and Early Committed Neurons in the Caudate Putamen and Cortex
Stroke, July 1, 2005; 36(7): 1544 - 1550.
[Abstract] [Full Text] [PDF]
D. N. Abrous, M. Koehl, and M. Le Moal
Adult Neurogenesis: From Precursors to Network and Physiology
Physiol Rev, April 1, 2005; 85(2): 523 - 569.
[Abstract] [Full Text] [PDF]
S. W. Suh, Y. Fan, S. M. Hong, Z. Liu, Y. Matsumori, P. R. Weinstein, R. A. Swanson, and J. Liu
Hypoglycemia Induces Transient Neurogenesis and Subsequent Progenitor Cell Loss in the Rat Hippocampus
Diabetes, February 1, 2005; 54(2): 500 - 509.
[Abstract] [Full Text] [PDF]
T. L. Briones, E. Suh, H. Hattar, and M. Wadowska
Dentate Gyrus Neurogenesis after Cerebral Ischemia and Behavioral Training
Biol Res Nurs, January 1, 2005; 6(3): 167 - 179.
[Abstract] [PDF]
W. Sun, A. Winseck, S. Vinsant, O.-h. Park, H. Kim, and R. W. Oppenheim
Programmed Cell Death of Adult-Generated Hippocampal Neurons Is Mediated by the Proapoptotic Gene Bax
J. Neurosci., December 8, 2004; 24(49): 11205 - 11213.
[Abstract] [Full Text] [PDF]
C.-Y. Kuan, A. J. Schloemer, A. Lu, K. A. Burns, W.-L. Weng, M. T. Williams, K. I. Strauss, C. V. Vorhees, R. A. Flavell, R. J. Davis, et al.
Hypoxia-Ischemia Induces DNA Synthesis without Cell Proliferation in Dying Neurons in Adult Rodent Brain
J. Neurosci., November 24, 2004; 24(47): 10763 - 10772.
[Abstract] [Full Text] [PDF]
K. Nixon and F. T. Crews
Temporally Specific Burst in Cell Proliferation Increases Hippocampal Neurogenesis in Protracted Abstinence from Alcohol
J. Neurosci., October 27, 2004; 24(43): 9714 - 9722.
[Abstract] [Full Text] [PDF]
K. Jin, V. Galvan, L. Xie, X. O. Mao, O. F. Gorostiza, D. E. Bredesen, and D. A. Greenberg
Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice
PNAS, September 7, 2004; 101(36): 13363 - 13367.
[Abstract] [Full Text] [PDF]
T. Acker and H. Acker
Cellular oxygen sensing need in CNS function: physiological and pathological implications
J. Exp. Biol., August 15, 2004; 207(18): 3171 - 3188.
[Abstract] [Full Text] [PDF]
D. Y. Zhu, L. Lau, S. H. Liu, J. S. Wei, and Y. M. Lu
Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus
PNAS, June 22, 2004; 101(25): 9453 - 9457.
[Abstract] [Full Text] [PDF]
L. S. Overstreet, S. T. Hentges, V. F. Bumaschny, F. S. J. de Souza, J. L. Smart, A. M. Santangelo, M. J. Low, G. L. Westbrook, and M. Rubinstein
A Transgenic Marker for Newly Born Granule Cells in Dentate Gyrus
J. Neurosci., March 31, 2004; 24(13): 3251 - 3259.
[Abstract] [Full Text] [PDF]
K. Jin, A. L. Peel, X. O. Mao, L. Xie, B. A. Cottrell, D. C. Henshall, and D. A. Greenberg
Increased hippocampal neurogenesis in Alzheimer's disease
PNAS, January 6, 2004; 101(1): 343 - 347.
[Abstract] [Full Text] [PDF]
C. T. Ekdahl, J.-H. Claasen, S. Bonde, Z. Kokaia, and O. Lindvall
Inflammation is detrimental for neurogenesis in adult brain
PNAS, November 11, 2003; 100(23): 13632 - 13637.
[Abstract] [Full Text] [PDF]
E. Gustafsson, O. Lindvall, and Z. Kokaia
Intraventricular Infusion of TrkB-Fc Fusion Protein Promotes Ischemia-Induced Neurogenesis in Adult Rat Dentate Gyrus
Stroke, November 1, 2003; 34(11): 2710 - 2715.
[Abstract] [Full Text] [PDF]
K. Wada, H. Sugimori, P. G. Bhide, M. A. Moskowitz, and S. P. Finklestein
Effect of Basic Fibroblast Growth Factor Treatment on Brain Progenitor Cells After Permanent Focal Ischemia in Rats
Stroke, November 1, 2003; 34(11): 2722 - 2728.
[Abstract] [Full Text] [PDF]
H. E. Scharfman, A. L. Sollas, R. E. Berger, and J. H. Goodman
Electrophysiological Evidence of Monosynaptic Excitatory Transmission Between Granule Cells After Seizure-Induced Mossy Fiber Sprouting
J Neurophysiol, October 1, 2003; 90(4): 2536 - 2547.
[Abstract] [Full Text] [PDF]
H. Toda, M. Tsuji, I. Nakano, K. Kobuke, T. Hayashi, H. Kasahara, J. Takahashi, A. Mizoguchi, T. Houtani, T. Sugimoto, et al.
Stem Cell-derived Neural Stem/Progenitor Cell Supporting Factor Is an Autocrine/Paracrine Survival Factor for Adult Neural Stem/Progenitor Cells
J. Biol. Chem., September 12, 2003; 278(37): 35491 - 35500.
[Abstract] [Full Text] [PDF]
J. M. Parent
Injury-Induced Neurogenesis in the Adult Mammalian Brain
Neuroscientist, August 1, 2003; 9(4): 261 - 272.
[Abstract] [PDF]
Z. Nadareishvili and J. Hallenbeck
Neuronal Regeneration after Stroke
N. Engl. J. Med., June 5, 2003; 348(23): 2355 - 2356.
[Full Text] [PDF]
N. Matsuoka, K. Nozaki, Y. Takagi, M. Nishimura, J. Hayashi, S.-I. Miyatake, and N. Hashimoto
Adenovirus-Mediated Gene Transfer of Fibroblast Growth Factor-2 Increases BrdU-Positive Cells After Forebrain Ischemia in Gerbils
Stroke, June 1, 2003; 34(6): 1519 - 1525.
[Abstract] [Full Text] [PDF]
R. M. Friedlander
Apoptosis and Caspases in Neurodegenerative Diseases
N. Engl. J. Med., April 3, 2003; 348(14): 1365 - 1375.
[Full Text] [PDF]
R. Dono
Fibroblast growth factors as regulators of central nervous system development and function
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2003; 284(4): R867 - R881.
[Abstract] [Full Text] [PDF]
Y. ZHU, K. JIN, X. O. MAO, and D. A. GREENBERG
Vascular endothelial growth factor promotes proliferation of cortical neuron precursors by regulating E2F expression
FASEB J, February 1, 2003; 17(2): 186 - 193.
[Abstract] [Full Text] [PDF]
D. Y. Zhu, S. H. Liu, H. S. Sun, and Y. M. Lu
Expression of Inducible Nitric Oxide Synthase after Focal Cerebral Ischemia Stimulates Neurogenesis in the Adult Rodent Dentate Gyrus
J. Neurosci., January 1, 2003; 23(1): 223 - 229.
[Abstract] [Full Text] [PDF]
K. Jin, Y. Zhu, Y. Sun, X. O. Mao, L. Xie, and D. A. Greenberg
Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo
PNAS, September 3, 2002; 99(18): 11946 - 11950.
[Abstract] [Full Text] [PDF]
M. P. Mattson, S. L. Chan, and W. Duan
Modification of Brain Aging and Neurodegenerative Disorders by Genes, Diet, and Behavior
Physiol Rev, July 1, 2002; 82(3): 637 - 672.
[Abstract] [Full Text] [PDF]
K. Jin, X. O. Mao, Y. Sun, L. Xie, L. Jin, E. Nishi, M. Klagsbrun, and D. A. Greenberg
Heparin-Binding Epidermal Growth Factor-Like Growth Factor: Hypoxia-Inducible Expression In Vitro and Stimulation of Neurogenesis In Vitro and In Vivo
J. Neurosci., July 1, 2002; 22(13): 5365 - 5373.
[Abstract] [Full Text] [PDF]
J. M. Parent, V. V. Valentin, and D. H. Lowenstein
Prolonged Seizures Increase Proliferating Neuroblasts in the Adult Rat Subventricular Zone-Olfactory Bulb Pathway
J. Neurosci., April 15, 2002; 22(8): 3174 - 3188.
[Abstract] [Full Text] [PDF]
L. Vallieres, I. L. Campbell, F. H. Gage, and P. E. Sawchenko
Reduced Hippocampal Neurogenesis in Adult Transgenic Mice with Chronic Astrocytic Production of Interleukin-6
J. Neurosci., January 15, 2002; 22(2): 486 - 492.
[Abstract] [Full Text] [PDF]
Y. Yagita, K. Kitagawa, T. Ohtsuki, K.-i. Takasawa, T. Miyata, H. Okano, M. Hori, and M. Matsumoto
Neurogenesis by Progenitor Cells in the Ischemic Adult Rat Hippocampus
Stroke, August 1, 2001; 32(8): 1890 - 1896.
[Abstract] [Full Text] [PDF]
J. Katchanov, C. Harms, K. Gertz, L. Hauck, C. Waeber, L. Hirt, J. Priller, R. von Harsdorf, W. Bruck, H. Hortnagl, et al.
Mild Cerebral Ischemia Induces Loss of Cyclin-Dependent Kinase Inhibitors and Activation of Cell Cycle Machinery before Delayed Neuronal Cell Death
J. Neurosci., July 15, 2001; 21(14): 5045 - 5053.
[Abstract] [Full Text] [PDF]
W. Jiang, W. Gu, T. Brannstrom, R. Rosqvist, and P. Wester
Cortical Neurogenesis in Adult Rats After Transient Middle Cerebral Artery Occlusion
Stroke, May 1, 2001; 32(5): 1201 - 1207.
[Abstract] [Full Text] [PDF]
S. Yoshimura, Y. Takagi, J. Harada, T. Teramoto, S. S. Thomas, C. Waeber, J. C. Bakowska, X. O. Breakefield, and M. A. Moskowitz
FGF-2 regulation of neurogenesis in adult hippocampus after brain injury
PNAS, April 18, 2001; (2001) 101034998.
[Abstract] [Full Text]
K. Jin, M. Minami, J. Q. Lan, X. O. Mao, S. Batteur, R. P. Simon, and D. A. Greenberg
Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat
PNAS, April 10, 2001; 98(8): 4710 - 4715.
[Abstract] [Full Text] [PDF]
B. K. McCabe, D. C. Silveira, M. R. Cilio, B. H. Cha, X. Liu, Y. Sogawa, and G. L. Holmes
Reduced Neurogenesis after Neonatal Seizures
J. Neurosci., March 15, 2001; 21(6): 2094 - 2103.
[Abstract] [Full Text] [PDF]
S. J. Pleasure, A. E. Collins, and D. H. Lowenstein
Unique Expression Patterns of Cell Fate Molecules Delineate Sequential Stages of Dentate Gyrus Development
J. Neurosci., August 15, 2000; 20(16): 6095 - 6105.
[Abstract] [Full Text] [PDF]
H. E. Scharfman, J. H. Goodman, and A. L. Sollas
Granule-Like Neurons at the Hilar/CA3 Border after Status Epilepticus and Their Synchrony with Area CA3 Pyramidal Cells: Functional Implications of Seizure-Induced Neurogenesis
J. Neurosci., August 15, 2000; 20(16): 6144 - 6158.
[Abstract] [Full Text] [PDF]
M. A. I. Aberg, N. D. Aberg, H. Hedbacker, J. Oscarsson, and P. S. Eriksson
Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus
J. Neurosci., April 15, 2000; 20(8): 2896 - 2903.
[Abstract] [Full Text] [PDF]
J. T. Coyle and R. Schwarcz
Mind Glue: Implications of Glial Cell Biology for Psychiatry
Arch Gen Psychiatry, January 1, 2000; 57(1): 90 - 93.
