Prenatal cocaine exposure alters progenitor cell markers in the subventricular zone of the adult rat brain

International Journal of Developmental Neuroscience

Volumn 30, Issue 1, 2012, Pages 1-9

  Patel, Dhyanesh Arvind ^a   Booze, Rosemarie M ^a   Mactutus, Charles F ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Chronic administration; Cocaine; Drug abuse; Intravenous injection; Neural stem cells; Pregnancy; Progenitor cells; Rats; Subventricular zone; Vascular access port

Indexed keywords

CELL MARKER; COCAINE; GREEN FLUORESCENT PROTEIN; NESTIN; SODIUM CHLORIDE;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; MALE; NEURAL STEM CELL; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; FEMALE; MALE; NEUROGENESIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; STEM CELLS;

ANIMALIA; RATTUS;

EID: 83855161532     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.11.001     Document Type: Article

References (82)

1. Ackerman J.P., Riggins T., Black M.M. A review of the effects of prenatal cocaine exposure among school-aged children. Pediatrics 2010, 125:554-565.
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. 1969, 137:433-458.
3. Bateman D.A., Chiriboga C.A. Dose-response effect of cocaine on newborn head circumference. Pediatrics 2000, 106(3):E33.
4. Bauer L.O., Mott A.E. Differential effects of cocaine, alcohol, and nicotine dependence on olfactory evoked potentials. Drug Alcohol Depend. 1996, 42:21-26.
5. Bayer L.E., Kakumanu S., Mactutus C.F., Booze R.M., Strupp B.J. Prenatal cocaine exposure alters sensitivity to the effects of idazoxan in a distraction task. Behav. Brain Res. 2002, 133:185-196.
6. Bignami A., Dahl D. Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J. Comp. Neurol. 1974, 153:27-38.
7. Booze R.M., Lehner A.F., Wallace D.R., Welch M.A., Mactutus C.F. Dose-response cocaine pharmacokinetics and metabolite profile following intravenous administration and arterial sampling in unanesthesized, freely moving male rats. Neurotoxicol. Teratol. 1997, 19:7-15.
8. Booze R.M., Wallace D.R., Silvers J.M., Strupp B.J., Snow D.M., Mactutus C.F. Prenatal cocaine exposure alters alpha2 receptor expression in adolescent rats. BMC Neurosci. 2006, 7:33-40.
9. Borta A., Höglinger G.U. Dopamine and adult neurogenesis. J. Neurochem. 2007, 100:587-595.
10. Buxhoeveden D.P., Hasselrot U., Buxhoeveden N.E., Booze R.M., Mactutus C.F. Microanatomy in 21 day rat brains exposed prenatally to cocaine. Int. J. Dev. Neurosci. 2006, 24:335-341.
11. Chiriboga C.A., Starr D., Kuhn L., Wasserman G.A. Prenatal cocaine exposure and prolonged focus attention. Poor infant information processing ability or precocious maturation of attentional systems?. Dev. Neurosci. 2009, 31:149-158.
12. Curtis M.A., Kam M., Nannmark U., Anderson M.F., Axell M.Z., Wikkelso C., Holtås S., van Roon-Mom W.M., Björk-Eriksson T., Nordborg C., Frisén J., Dragunow M., Faull R.L., Eriksson P.S. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
13. Degenhardt L., Bucello C., Calabria B., Nelson P., Roberts A., Hall W., Lynskey M., Wiessing L. What data are available on the extent of illicit drug use and dependence globally? Results of four systematic reviews. Drug Alcohol Depend. 2011, the GBD Illicit Drug Use Writing Group, (Epub ahead of print).
14. Dey S., Mactutus C.F., Booze R.M., Snow D.M. Specificity of prenatal cocaine on inhibition of locus coeruleus neurite outgrowth. Neuroscience 2006, 139:899-907.
15. Dey S., Mactutus C.F., Booze R.M., Snow D.M. Cocaine exposure in vitro induces apoptosis in fetal locus coeruleus neurons by altering the Bax/Bcl-2 ratio and through caspase-3 apoptotic signaling. Neuroscience 2007, 144:509-521.
16. Dey S., Snow D.M. Cocaine exposure in vitro induces apoptosis in fetal locus coeruleus neurons through TNF-alpha-mediated induction of Bax and phosphorylated c-Jun NH(2)-terminal kinase. J. Neurochem. 2007, 103:542-556.
17. Doetsch F., García-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.
18. Dow-Edwards D. Sex differences in the effects of cocaine abuse across the life span. Physiol. Behav. 2010, 100:208-215.
19. Enwere E., Shingo T., Gregg C., Fujikawa H., Ohta S., Weiss S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 2004, 24:8354-8365.
20. Evans M., Cone E.J., Henningfeld J.E. Arterial and venous cocaine plasma concentrations in humans: relationship to route of administration, cardiovascular effects and subjective effects. J. Pharmacol. Exp. Ther. 1996, 279:1345-1356.
21. Eyler F.D., Warner T.D., Behnke M., Hou W., Wobie K., Garvan C.W. Executive functioning at ages 5 and 7 years in children with prenatal cocaine exposure. Dev. Neurosci. 2009, 31:121-136.
22. Ferris M.J., Mactutus C.F., Silvers J.M., Hasselrot U., Beaudin S.A., Strupp B.J., Booze R.M. Sex mediates dopamine and adrenergic receptor expression in adult rats exposed prenatally to cocaine. Int. J. Dev. Neurosci. 2007, 25:445-454.
23. Fischman M.W., Schuster C.R. Cocaine self-administration in humans. Fed. Proc. 1982, 41:241-246.
24. Foltz T.L., Snow D.M., Strupp B.J., Booze R.M., Mactutus C.F. Prenatal intravenous cocaine and the heart rate-orienting response: a dose-response study. Int. J. Dev. Neurosci. 2004, 22:285-296.
25. Frank D.A., Augustyn M., Knight W.G., Pell T., Zuckerman B. Growth, development, and behavior in early childhood following prenatal cocaine exposure: a systematic review. JAMA 2001, 285:1613-1625.
26. Gendle M.H., Strawderman M.S., Mactutus C.F., Booze R.M., Levitsky D.A., Strupp B.J. Impaired sustained attention and altered reactivity to errors in an animal model of prenatal cocaine exposure. Brain Res. Dev. Brain Res. 2003, 147:85-96.
27. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J.D., Lledo P.M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1823-1828.
28. Gordon A.S., Moran D.T., Jafek B.W., Eller P.M., Strahan R.C. The effect of chronic cocaine abuse on human olfaction. Arch. Otolaryngol. Head Neck Surg. 1990, 116:1415-1418.
29. Gressens P., Kosofsky B.E., Evrard P. Cocaine-induced disturbances of corticogenesis in the developing murine brain. Neurosci. Lett. 1992, 140:113-116.
30. Heyser C.J., Goodwin G.A., Moody C.A., Spear L.P. Prenatal cocaine exposure attenuates cocaine-induced odor preference in infant rats. Pharmacol. Biochem. Behav. 1992, 42:169-173.
31. Höglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004, 7:726-735.
32. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
33. Johnston L.D., O'Malley P.M., Bachman J.G., Schulenberg J.E. Monitoring the Future National Survey Results on Drug Use, 1975-2009. Secondary School Students (NIH Publication No. 10-7584) 2010, vol. I. National Institute on Drug Abuse, Bethesda, MD, 734 pp.
34. Kosofsky B.E., Wilkins A.S., Gressens P., Evrard P. Transplacental cocaine exposure: a mouse model demonstrating neuroanatomic and behavioral abnormalities. J. Child Neurol. 1994, 9:234-241.
35. LaBella F.S., Queen G. General anesthetics inhibit cytochrome P450 monoxygenases and arachidonic acid metabolism. Can. J. Physiol. Pharmacol. 1993, 71:48-53.
36. Lauder J.M. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 1993, 16:233-240.
37. Lee C.T., Chen J., Hayashi T., Tsai S.Y., Sanchez J.F., Errico S.L., Amable R., Su T.P., Lowe R.H., Huestis M.A., Shen J., Becker K.G., Geller H.M., Freed W.J. A mechanism for the inhibition of neural progenitor cell proliferation by cocaine. PLoS Med. 2008, 5(6):e117.
38. Lendahl U., Zimmerman L.B., McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 1990, 60:585-595.
39. Leslie F.M. Neurotransmitters as neurotrophic factors. Neurotrophic Factors 1993, 565-598. Academic Press, San Diego. J.H. Fallon, S.E. Loughlin (Eds.).
40. Libby D.M., Klein L., Altorki N.K. Aspiration of the nasal septum: a new complication of cocaine abuse. Ann. Intern. Med. 1992, 116:567-568.
41. Lidow M.S., Bozian D., Song Z.M. Cocaine affects cerebral neocortical cytoarchitecture in primates only if administered during neocortical neuronogenesis. Brain Res. Dev. Brain Res. 2001, 128:45-52.
42. Lidow M.S. Prenatal cocaine exposure adversely affects development of the primate cerebral cortex. Synapse 1995, 21:332-341.
43. Lidow M.S., Song Z.M. Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J. Comp. Neurol. 2001, 435:263-275.
44. Lipton S.A., Kater S.B. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci. 1989, 12:265-270.
45. Lledo P.M., Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 2005, 28:248-254.
46. Lledo P.M., Gheusi G., Vincent J.D. Information processing in the mammalian olfactory system. Physiol. Rev. 2005, 85:281-317.
47. Lloyd S.A., Balest Z.R., Corotto F.S., Smeyne R.J. Cocaine selectively increases proliferation in the adult murine hippocampus. Neurosci. Lett. 2010, 485:112-116.
48. Loch J.M., Potter J., Bachmann K.A. The influence of anesthetic agents on rat hepatic cytochromes P450 in vivo. Pharmacology 1995, 50:146-153.
49. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
50. Lumeng J.C., Cabral H.J., Gannon K., Heeren T., Frank D.A. Pre-natal exposures to cocaine and alcohol and physical growth patterns to age 8 years. Neurotoxicol. Teratol. 2007, 29:446-457.
51. Mactutus C.F., Herman A.S., Booze R.M. Chronic intravenous model for studies of drug abuse in the pregnant and/or group-housed rat: an initial study with cocaine. Neurotoxicol. Teratol. 1994, 16:183-191.
52. Mactutus C.F. Prenatal intravenous cocaine adversely affects attentional processing in preweanling rats. Neurotoxicol. Teratol. 1999, 21:539-550.
53. Mactutus C.F., Booze R.M., Dowell R.T. The influence of route of administration on the acute cardiovascular effects of cocaine in conscious unrestrained pregnant rats. Neurotoxicol. Teratol. 2000, 22:357-368.
54. McKay R. Stem cells in the central nervous system. Science 1997, 276:66-71.
55. Nissant A., Pallotto M. Integration and maturation of newborn neurons in the adult olfactory bulb - from synapses to function. Eur. J. Neurosci. 2011, 33:1069-1077.
56. Noonan M.A., Choi K.H., Self D.W., Eisch A.J. Withdrawal from cocaine self-administration normalizes deficits in proliferation and enhances maturity of adult-generated hippocampal neurons. J. Neurosci. 2008, 28:2516-2526.
57. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2006, NY, Academic Press. 6th ed.
58. Petreanu L., Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 2002, 22:6106-6113.
59. Podskarbi-Fayette R., Rydzewski B., Lipińska M. Smell and taste in drug addicts. Otolaryngol. Pol. 2005, 59:585-590. (article in Polish).
60. Reinoso B.S., Undie A.S., Levitt P. Dopamine receptors mediate differential morphological effects on cerebral cortical neurons in vitro. J. Neurosci. Res. 1996, 43:439-453.
61. Rivkin M.J., Davis P.E., Lemaster J.L., Cabral H.J., Warfield S.K., Mulkern R.V., Robson C.D., Rose-Jacobs R., Frank D.A. Volumetric MRI study of brain in children with intrauterine exposure to cocaine, alcohol, tobacco, and marijuana. Pediatrics 2008, 121:741-750.
62. Robinson S.E., Enters E.K., Jackson G.F., Chinchilli V.M., Maher J.R., McDowell K.P., Allen H.M., Guo H. Maternal and fetal brain and plasma levels of cocaine and benzoylecgonine after acute or chronic maternal intravenous administration of cocaine. J. Pharmacol. Exp. Ther. 1994, 271:1234-1239.
63. Robinson T.E., Gorny G., Mitton E., Kolb B. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 2001, 39:257-266.
64. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 2002, 22:2679-2689.
65. Roussotte F., Soderberg L., Sowell E. Structural, metabolic, and functional brain abnormalities as a result of prenatal exposure to drugs of abuse: evidence from neuroimaging. Neuropsychol. Rev. 2010, 20:376-397.
66. Sanai N., Tramontin A.D., Quiñones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-García V.J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
67. Schwartz R.H., Estroff T., Fairbanks D.N., Hoffmann N.G. Nasal symptoms associated with cocaine abuse during adolescence. Arch. Otolaryngol. Head Neck Surg. 1989, 115:63-64.
68. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
69. Silvers J.M., Wallace D.R., Harrod S.B., Mactutus C.F., Booze R.M. Prenatal cocaine alters dopamine and sigma receptor binding in nucleus accumbens and striatum in dams and adolescent offspring. Neurotoxicol. Teratol. 2006, 28:173-180.
70. Singer L.T., Lewin J., Minnes S., Weishampel P., Drake K., Satayathum S., Boll D.T., Zijdenbos A., Paus T., Evans A. Neuroimaging of 7-8 year-old children exposed prenatally to cocaine. Neurotoxicol. Teratol. 2006, 28:393-396.
71. Singer L.T., Nelson S., Short E., Min M.O., Lewis B., Russ S., Minnes S. Prenatal cocaine exposure: drug and environmental effects at 9 years. J. Pediatr. 2008, 153:105-111.
72. Snow D.M., Carman H.M., Smith J.D., Booze R.M., Welch M.A., Mactutus C.F. Cocaine-induced inhibition of process outgrowth in locus coeruleus neurons: role of gestational exposure period and offspring sex. Int. J. Dev. Neurosci. 2004, 22:297-308.
73. Snow D.M., Smith J.D., Booze R.M., Welch M.A., Mactutus C.F. Cocaine decreases cell survival and inhibits neurite extension of rat locus coeruleus neurons. Neurotoxicol. Teratol. 2001, 23:225-234.
74. Stanwood G.D., Washington R.A., Levitt P. Identification of a sensitive period of prenatal cocaine exposure that alters the development of the anterior cingulate cortex. Cereb. Cortex 2001, 11:430-440.
75. Statistical Solutions, Ltd. BMDP 2009 2009, Statistical Solutions, Cork, Ireland.
76. Stripling J.S., Ellinwood E.H. Sensitization to cocaine following chronic administration in the rat. Cocaine and Other Stimulants 1977, 327-351. Plenum Press, New York. E.H. Ellinwood, M.M. Kilbey (Eds.).
77. Substance Abuse and Mental Health Services Administration Results from the 2009 National Survey on Drug Use and Health. Summary of National Findings 2010, vol. I. Office of Applied Studies, NSDUH Series H-38A, HHS Publication No. SMA 10-4586Findings, Rockville, MD.
78. Temple S., Alvarez-Buylla A. Stem cells in the adult mammalian central nervous system. Curr. Opin. Neurobiol. 1999, 9:135-141.
79. von Bohlen, Halbach O. Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res. 2011, 345:1-19.
80. Weiss S., Reynolds B.A., Vescovi A.L., Morshead C., Craig C.G., van der Kooy D. Is there a neural stem cell in the mammalian forebrain?. Trends Neurosci. 1996, 19:387-393.
81. Winer B.J. Statistical Principles in Experimental Design 1971, McGraw-Hill, New York. 2nd ed.
82. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.