The DOI matches its Crossref record; 67 of the 67 references it cites were found in a registry or an index.
Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone
Abstract
The birth of cells with neurogenic potential in the adult brain is assessed commonly by detection of exogenous S phase markers, such as bromodeoxyuridine (BrdU). Analysis of other phases of the cell cycle, however, can provide insight into how external factors, such as opiates, influence the cycling of newly born cells. To this end, we examined the expression of two endogenous cell cycle markers in relation to BrdU: proliferating cell nuclear antigen (PCNA) and phosphorylated histone H3 (pHisH3). Two hours after one intraperitoneal BrdU injection, BrdU‐, PCNA‐, and pHisH3‐immunoreactive (IR) cells exhibited similar distribution in the adult mouse subgranular zone (SGZ). Quantitative analysis within the SGZ revealed a relative abundance of cells labeled for PCNA > BrdU >> pHisH3. Similar to our reports in rat SGZ, chronic morphine treatment decreased BrdU‐ and PCNA‐IR cells in mouse SGZ by 28 and 38%, respectively. We also show that pHisH3‐IR cells are influenced by chronic morphine to a greater extent (58% decrease) than are BrdU‐ or PCNA‐IR cells. Cell cycle phase analysis of SGZ BrdU‐IR cells using triple labeling for BrdU, PCNA, and pHisH3 revealed premature mitosis in chronic morphine‐treated mice. These results suggest that morphine‐treated mice have a shorter Gap2/mitosis (G 2/M) phase when compared to sham‐treated mice. These findings demonstrate the power of using a combination of exogenous and endogenous cell cycle markers and nuclear morphology to track proliferating cells through different phases of the cell cycle and to reveal the regulation of cell cycle phase by chronic morphine. © 2004 Wiley‐Liss, Inc.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Critically, not only do opioids interfere with memory acquisition and retrieval, but they also interfere with hippocampal neurogenesis, where chronic administration of morphine leads to reduced hippocampal neurogenesis and cell proliferation (Eisch et al., 2000;Kahn et al., 2005;Mandyam et al., 2004).”
From A review of the relation between dissociation, memory, executive functioning and social cognition in military members and civilians with neuropsychiatric conditions (2016) · cites this paper as Mandyam et al., 2004
In the citing paper
“Critically, not only do opioids interfere with memory acquisition and retrieval, but they also interfere with hippocampal neurogenesis, where chronic administration of morphine leads to reduced hippocampal neurogenesis and cell proliferation (Eisch et al., 2000;Kahn et al., 2005;Mandyam et al., 2004).”
From A review of the relation between dissociation, memory, executive functioning and social cognition in military members and civilians with neuropsychiatric conditions (2016) · cites this paper as Mandyam et al., 2004
Citations
Cites
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014
Hendzel, M. J., Wei, Y., Mancini, M. A., Hooser, A. A. V., Ranalli, T. A., Brinkley, B. R., Bazett‐Jones, D. P., & Allis, C. D. (1997) · Chromosoma · doi:10.1007/s004120050256 · Cited by 1,860
Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus
Cameron, H. A., & Mckay, R. D. G. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1040 · Cited by 1,585
Neurogenesis in the Adult Rat: Electron Microscopic Analysis of Light Radioautographs
Kaplan, M., & Hinds, J. W. (1977) · Science · doi:10.1126/science.887941 · Cited by 1,511
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496
Astrocytes give rise to new neurons in the adult mammalian hippocampus
Seri, B., Garcı́a-Verdugo, J. M., McEwen, B. S., & Alvarez-Buylla, A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07153.2001 · Cited by 1,495
Is a p53-Regulated Inhibitor of G2/M Progression
Hermeking, H., Lengauer, C., Polyak, K., He, T.-C., Zhang, L., Thiagalingam, S., Kinzler, K. W., & Vogelstein, B. (1997) · Molecular Cell · doi:10.1016/s1097-2765(00)80002-7 · Cited by 1,251
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat
Cameron, H. A., Woolley, C. S., McEwen, B. S., & Gould, E. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90335-d · Cited by 1,215
Jin, K., Minami, M., Lan, J. Q., Mao, X. O., Parmentier‐Batteur, S., Simon, R. P., & Greenberg, D. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.081011098 · Cited by 1,061
Altman, J., & Das, G. D. (1966) · The Journal of Comparative Neurology · doi:10.1002/cne.901260302 · Cited by 921
Autoantibody to a nuclear antigen in proliferating cells
Miyachi, K., Fritzler, M. J., & Tan, E. M. (1978) · The Journal of Immunology · doi:10.4049/jimmunol.121.6.2228 · Cited by 874
Hisano, S., Hoshi, K., Ikeda, Y., Maruyama, D., Kanemoto, M., Ichijo, H., Kojima, I., Takeda, J., & Nogami, H. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00194-7 · Cited by 806
The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis
Kee, N., Sivalingam, S., Boonstra, R., & Wojtowicz, J. M. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00007-9 · Cited by 785
Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance.
Sharma, S. K., Klee, W. A., & Nirenberg, M. W. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.8.3092 · Cited by 671
Mitotic Phosphorylation of Histone H3: Spatio-Temporal Regulation by Mammalian Aurora Kinases
Crosio, C., Fimia, G. M., Loury, R., Kimura, M., Okano, Y., Zhou, H., Sen, S., Allis, C. D., & Sassone‐Corsi, P. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.3.874-885.2002 · Cited by 668
S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex
Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., & Shirahige, K. (2003) · Nature · doi:10.1038/nature01900 · Cited by 649
Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessberger, S., Yamaguchi, M., & Kempermann, G. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10945 · Cited by 640 · cited 1×
“These include undifferentiated progenitors, neural and glial progenitors, as well as endothelial cells and pericytes (e.g., Palmer et al., 2000; Kronenberg et al., 2003).”
BackgroundCelis, J. E., & Celis, A. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.10.3262 · Cited by 636
Short‐term and long‐term survival of new neurons in the rat dentate gyrus
Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., & Cameron, H. A. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10675 · Cited by 628
Miller, M. W., & Nowakowski, R. S. (1988) · Brain Research · doi:10.1016/0006-8993(88)90055-8 · Cited by 613
Opiates inhibit neurogenesis in the adult rat hippocampus
Eisch, A. J., Barrot, M., Schad, C. A., Self, D. W., & Nestler, E. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120552597 · Cited by 599
Self-citationIncreased cell proliferation and neurogenesis in the adult human Huntington's disease brain
Curtis, M., Penney, E., Pearson, A. G., van Roon-Mom, W. V., Butterworth, N., Dragunow, M., Connor, B., & Faull, R. (2003) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1532244100 · Cited by 559
Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus
Kaplan, M., & Bell, D. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-06-01429.1984 · Cited by 455
Smart, I. H. M. (1961) · The Journal of Comparative Neurology · doi:10.1002/cne.901160306 · Cited by 449
Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections
Stanfield, B. B., & Trice, J. (1988) · Experimental Brain Research · doi:10.1007/bf00250261 · Cited by 431
Bayer, S. A., & Altman, J. (1974) · Journal of Comparative Neurology · doi:10.1002/cne.901580105 · Cited by 344
Yu, C. C. W., Woods, A. L., & Levison, D. A. (1992) · The Histochemical Journal · doi:10.1007/bf01047461 · Cited by 306
The time of origin of neurons in the hippocampal region of the rhesus monkey
RAKIC, P. T., & Nowakowski, R. S. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901960109 · Cited by 305
Changes in cell-cycle kinetics during the development and evolution of primate neocortex
Kornack, D. R., & RAKIC, P. T. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.1242 · Cited by 292
Mechanism by which caffeine potentiates lethality of nitrogen mustard.
Lau, C. C., & Pardee, A. B. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.9.2942 · Cited by 290
Galea, L. A. M., & McEwen, B. S. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00345-5 · Cited by 281
Multipotential stem cells and progenitors in the vertebrate retina
Reh, T. A., & Levine, E. M. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199808)36:2 · Cited by 231
Endogenous opioid systems regulate cell proliferation in the developing rat brain
Zagon, I. S., & MacLaughlin, P. J. (1987) · Brain Research · doi:10.1016/0006-8993(87)91440-5 · Cited by 222
Shaw-Lutchman, T. Z., Barrot, M., Wallace, T. L., Gilden, L., Zachariou, V., Impey, S., Duman, R. S., Storm, D. R., & Nestler, E. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03663.2002 · Cited by 205
Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice
Hayes, N. L., & Nowakowski, R. S. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00324-8 · Cited by 201
RB and Cdc2 expression in brain: correlations with 3H-thymidine incorporation and neurogenesis
Okano, H. J., Pfaff, D. W., & Gibbs, R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02930.1993 · Cited by 140
Cell cycle and cell fate in the nervous system
Ohnuma, S., Philpott, A., & Harris, W. A. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00175-6 · Cited by 127
Opiates, opioids and addiction.
Kreek, M. J. (1996) · PubMed · Cited by 126
Hauser, K. F., Stiene‐Martin, A., Mattson, M. P., Elde, R. P., Ryan, S., & Godleske, C. C. (1996) · Brain Research · doi:10.1016/0006-8993(96)00103-5 · Cited by 123
Expression Patterns of Retinoblastoma Protein in Parkinson Disease
Jordan-Sciutto, K. L., Dorsey, R., Chalovich, E. M., Hammond, R. R., & Achim, C. L. (2003) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/62.1.68 · Cited by 121
Cobb, J. A., Miyaike, M., Kikuchi, A., & Handel, M. A. (1999) · Chromosoma · doi:10.1007/s004120050393 · Cited by 121
Steinmann, K. E., Belinsky, G. S., Lee, D. H.-Y., & Schlegel, R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.15.6843 · Cited by 102
Adult neurogenesis: implications for psychiatry
Eisch, A. J. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38085-3 · Cited by 98
Self-citationNeuropsychological performance in opiate addicts after rapid detoxification
Guerra, D. (1987) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(87)90036-6 · Cited by 98
Effects of morphine on DNA synthesis in neonatal rat brain
Kornblum, H. I., Loughlin, S. E., & Leslie, F. M. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90081-2 · Cited by 94
Altered Distribution of Cell Cycle Transcriptional Regulators during Alzheimer Disease
Jordan‐Sciutto, K. L., Malaiyandi, L. M., & Bowser, R. P. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.4.358 · Cited by 94
A role for cadherins in cellular signaling and differentiation
Knudsen, K. A., Frankowski, C., Johnson, K. R., & Wheelock, M. J. (1998) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(1998)72:30/31+ · Cited by 88
Impulse control differences between abstinent heroin users and matched controls
Lee, T. M. C., & Pau, C. W. H. (2002) · Brain Injury · doi:10.1080/02699050210128915 · Cited by 86
Wildemann, B., Schmidmaier, G., Ordel, S., Stange, R., Haas, N. P., & Raschke, M. (2003) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.10512 · Cited by 79
The G2 DNA Damage Checkpoint Delays Expression of Genes Encoding Mitotic Regulators
Crawford, D. F., & Piwnica-Worms, H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103414200 · Cited by 79
PCNA-binding to DNA at the G1/S transition in proliferating cells of the developing cerebral wall
Takahashi, T., & Caviness, V. S. (1993) · Journal of Neurocytology · doi:10.1007/bf01235751 · Cited by 76
Wilson, M. T., & Snow, D. M. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000828)424:3 · Cited by 73
Cdc25C interacts with PCNA at G2/M transition
Kawabe, T., Suganuma, M., Ando, T., Kimura, M., Hori, H., & Okamoto, T. (2002) · Oncogene · doi:10.1038/sj.onc.1205229 · Cited by 65
Hippocampal Formation in the Mouse and Rat — Structural Organization and Development: A Review
Reznikov, K. Y. (1991) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-642-76447-9_1 · Cited by 63
Wierzba‐Bobrowicz, T., Gwiazda, E., Kosno-Kruszewska, E., Lewandowska, E., Lechowicz, W., Bertrand, E., Szpak, G. M., & Schmidt-Sidor, B. (2002) · PubMed · Cited by 53
Opioids modulate cell division in the germinal zone of the late embryonic neocortex
Reznikov, K. Y., Hauser, K. F., Nazarevskaja, G., Trunova, Y. A., Derjabin, V., & Bakalkin, G. Y. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00680.x · Cited by 45
Making scents of olfactory neurogenesis
Carleton, A., Rochefort, C., Morante, J., Desmaisons, D., Vincent, J., Gheusi, G., & Lledo, P. (2002) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(01)00087-0 · Cited by 44
Adult neurogenesis in natural populations
Boonstra, R., Galea, L. A. M., Matthews, S., & Wojtowicz, J. M. (2001) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y00-135 · Cited by 43
Schlegel, R., Croy, R. G., & Pardee, A. B. (1987) · Journal of Cellular Physiology · doi:10.1002/jcp.1041310113 · Cited by 39
The effects of morphine on cell proliferation
Glasel, J. A. (2000) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-8385-6_2 · Cited by 26
Johnson, F. A., Dawson, A. J., & Meyer, R. L. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990419)406:4 · Cited by 23
Miller, C. R. D., O’Steen, W. K., & Deadwyler, S. A. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902080209 · Cited by 20
Morphine induced increases in the incorporation of 3H-thymidine into brain striatal DNA
Messing, R. B., Miller, C. R. D., Waymire, J. C., LYNCH, G. S., & Deadwyler, S. A. (1979) · Brain Research Bulletin · doi:10.1016/0361-9230(79)90102-3 · Cited by 18
Premature expression of cyclin B sensitizes human HT1080 cells to caffeine‐induced premature mitosis
Tam, S. W., Belinsky, G. S., & Schlegel, R. (1995) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240590306 · Cited by 14
Day, H. E. W., Curran, E. J., Watson, S. J., & Akil, H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991011)413:1
Flagged first, then by citations
Research works printed but not linked: 3
- Eisch AJ, Use of endogenous cell cycle markers to examine adult mammalian neurogenesis: Basic and clinical implications, Nova Science
- 10.1002/(SICI)1097-4644(1998)72:30/31 <1::AID-JCB2>3.0.CO;2-E · DOI
- Norris RD, 2002, Use of endogenous cell cycle markers as a novel measure of cell proliferation in the adult hippocampus, Society for Neuroscience, 126, 2
Cited by
Sorted by citations
Dynamic Contribution of Nestin-Expressing Stem Cells to Adult Neurogenesis
Lagace, D. C., Whitman, M. C., Noonan, M. A., Ables, J. L., DeCarolis, N. A., Arguello, A. A., Donovan, M. H., Fischer, S. J., Farnbauch, L. A., Beech, R. D., et al. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3812-07.2007 · Cited by 502
Self-citationDecreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease
Donovan, M. H., Yazdani, U., Norris, R. D., Games, D., German, D. C., & Eisch, A. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20840 · Cited by 359
Self-citationNotch1 is required for maintenance of the reservoir of adult hippocampal stem cells
Ables, J. L., DeCarolis, N. A., Johnson, M. A., Rivera, P. D., Gao, Z., Cooper, D. C., Radtke, F., Hsieh, J., & Eisch, A. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4721-09.2010 · Cited by 292
Self-citationNeurogenesis in the adult hippocampus
Christie, B. R., & Cameron, H. A. (2006) · Hippocampus · doi:10.1002/hipo.20151 · Cited by 233
Mandyam, C. D., Harburg, G. C., & Eisch, A. J. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.12.064 · Cited by 206
Self-citation
Metadata
- Authors
- Mandyam, C. D., Norris, R. D., & Eisch, A. J.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Eisch, Amelia J.
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2004-05-03
- Volume
- 76
- Issue
- 6
- Pages
- 783-794
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2064038456
- Cited by
- 116
- References
- 67
- Citations by year
- 2026: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 5 · 2017: 3 · 2016: 6 · 2015: 2 · 2014: 13 · 2013: 5 · 2012: 6
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (P30AG012300, AG 12300)
- National Institute on Drug Abuse (DA-07290)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacological Receptor Mechanisms and Effects
- Keywords
- chronic morphine, subgranular zone, adult neurogenesis, premature mitosis, cell cycle phases, proliferating cell nuclear antigen, phosphorylated histone H3, bromodeoxyuridine, G2/M phase, opiates
- MeSH terms
- Animals, Bromodeoxyuridine, Cell Cycle, Cell Differentiation, Drug Administration Schedule, Hippocampus, Histones, Immunohistochemistry, Male, Mice, Inbred C57BL, Morphine, Neurons, Phosphorylation, Stem Cells, Biomarkers, Proliferating Cell Nuclear Antigen, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
