Survival, differentiation, and reversal of heroin neurobehavioral teratogenicity in mice by transplanted neural stem cells derived from embryonic stem cells

Journal of Neuroscience Research

Volumn 88, Issue 2, 2010, Pages 315-323

  Kazma, Meital ^a   Izrael, Michal ^b   Revel, Michel ^b   Chebath, Judith ^b   Yanai, Joseph ^a,c  

^a HEBREW UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

ES culture; Heroin; Mice; Morris maze; Neural stem cell therapy; Neural stem cells; Prenatal exposure; Transplantation

Indexed keywords

CARBOCYANINE; CELL MARKER; DIAMORPHINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GROWTH FACTOR; INTERMEDIATE FILAMENT PROTEIN; NESTIN; NEUROFILAMENT PROTEIN; PROTEIN PRECURSOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL ELONGATION; CELL FATE; CELL FUNCTION; CELL LABELING; CELL POLARITY; CELL RENEWAL; CELL SURVIVAL; CELL THERAPY; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GESTATIONAL AGE; HEROIN DEPENDENCE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; LATENT PERIOD; LEARNING; MALE; MAZE TEST; MENTAL PERFORMANCE; MOUSE; NERVE CELL; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PRENATAL DRUG EXPOSURE; PRENATAL EXPOSURE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TERATOGENICITY; TREATMENT OUTCOME;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; FEMALE; HEROIN; MALE; MAZE LEARNING; MICE; NARCOTICS; NEUROGENESIS; NEURONS; OPIOID-RELATED DISORDERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 74049146340     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22193     Document Type: Article

References (61)

1. Abu-Roumi M, Newman ME, Yanai J. 1996. Inositol phosphate formation in mice prenatally exposed to drugs: relation to muscarinic receptors and postreceptor effects. Brain Res Bull 40:183-186.
2. Aubert J, Stavridis MP, Tweedie S, O'Reilly M, Vierlinger K, Li M, Ghazal P, Pratt T, Mason JO, Roy D, Smith A. 2003. Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc Natl Acad Sci USA 100 (Suppl 1):11836-11841.
3. Barker RA, Widner H. 2004. Immune problems in central nervous system cell therapy. NeuroRx 1:472-481.
4. Beer A, Slotkin TA, Seidler FJ, Yanai J. 2005. Nicotine therapy in adulthood reverses the synaptic and behavioral deficits elicited by prenatal exposure to phenobarbital. Neuropsychopharmacology 30:156-165.
5. Ben-Shaanan TL, Ben-Hur T, Yanai J. 2008. Transplantation of neural progenitors enhances production of endogenous cells in the impaired brain. Mol Psychiatry 13:222-231.
6. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O. 2002. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci USA 99:2344-2349.
7. Brustle O, Jones KN, Learish RD, Karram K, Choudhary K, Wiestler OD, Duncan ID, McKay RD. 1999. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 285:754-756.
8. Capela A, Temple S. 2002. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865-875.
9. Dang L, Tropepe V. 2006. Neural induction and neural stem cell development. Regen Med 1:635-652.
10. Jeltsch H, Yee J, Aloy E, Marques Pereira P, Schimchowitsch S, Grandbarbe L, Caillard S, Mohier E, Cassel JC. 2003. Transplantation of neurospheres after granule cell lesions in rats: cognitive improvements despite no long-term immunodetection of grafted cells. Behav Brain Res 143:177-191.
11. Katz S, Ben-Hur T, Ben-Shaanan TL, Yanai J. 2008. Reversal of heroin neurobehavioral teratogenicity by grafting of neural progenitors. J Neurochem 104:38-49.
12. Kim JH, Auerbach JM, Rodriguez-Gomez JA, Velasco I, Gavin D, Lumelsky N, Lee SH, Nguyen J, Sanchez-Pernaute R, Bankiewicz K, McKay R. 2002. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418:50-56.
13. Kruyt MC, De Bruijn J, Veenhof M, Oner FC, Van Blitterswijk CA, Verbout AJ, Dhert WJ. 2003. Application and limitations of chloromethyl- benzamidodialkylcarbocyanine for tracing cells used in bone tissue engineering. Tissue Eng 9:105-115.
14. Kuan WL, Barker RA. 2005. New therapeutic approaches to Parkinson's disease including neural transplants. Neurorehabil Neural Repair 19:155-181.
15. Lasky DI, Zagon IS, McLaughlin PJ. 1977. Effect of maternally administered heroin on the motor activity of rat offspring. Pharmacol Biochem Behav 7:281-284.
16. Lindvall O, Hagell P. 2002. Role of cell therapy in Parkinson disease. Neurosurg Focus 13:e2.
17. McClearn GE, Wilson JR, Meredith W. 1970. The use of isogenic and heterogenic mouse stock in behavioral research. In: Lindzey G, Thiessen DD, editors. Contributions to behavior-genetic analysis; the mouse as a prototype. New York: Appleton-Century-Crofts. p 3-22.
18. McDonald JW, Liu XZ, Qu Y, Liu S, Mickey SK, Turetsky D, Gottlieb DI, Choi DW. 1999. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5:1410-1412.
19. Modo M, Rezaie P, Heuschling P, Patel S, Male DK, Hodges H. 2002. Transplantation of neural stem cells in a rat model of stroke: assessment of short-term graft survival and acute host immunological response. Brain Res 958:70-82.
20. Morris R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
21. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
22. National Institute on Drug Abuse DoEaSARTI. 1994. National household survey on drug abuse: main findings 1992. Rockville, MD: National Institute on Drug Abuse Division of Epidemiology and Prevention Research U.S. Dept. of Health and Human Services Public Health Service Alcohol Drug Abuse and Mental Health Administration.
23. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD. 1996. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59:89-102.
24. Okada Y, Matsumoto A, Shimazaki T, Enoki R, Koizumi A, Ishii S, Itoyama Y, Sobue G, Okano H. 2008. Spatio-temporal recapitulation of central nervous system development by murine ES cell-derived neural stem/progenitor cells. Stem Cells (in press).
25. Ornoy A, Michailevskaya V, Lukashov I, Bar-Hamburger R, Harel S. 1996. The developmental outcome of children born to heroin-dependent mothers, raised at home or adopted. Child Abuse Neglect 20:385-396.
26. Ornoy A, Segal J, Bar-Hamburger R, Greenbaum C. 2001. Developmental outcome of school-age children born to mothers with heroin dependency: importance of environmental factors. Dev Med Child Neurol 43:668-675.
27. Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY. 2002. Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol 20:1103-1110.
28. Qu T, Brannen CL, Kim HM, Sugaya K. 2001. Human neural stem cells improve cognitive function of aged brain. Neuroreport 12:1127-1132.
29. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. 2001. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412:736-739.
30. Riley EP, Barron S. 1989. The behavioral and neuroanatomical effects of prenatal alcohol exposure in animals. Ann NY Acad Sci 562:173-177.
31. Rodier PM. 1976. Critical periods for behavioral anomalies in mice. Environ Health Perspect 18:79-83.
32. Rogel-Fuchs Y, Newman ME, Trombka D, Zahalka EA, Yanai J. 1992. Hippocampal cholinergic alterations and related behavioral deficits after early exposure to phenobarbital. Brain Res Bull 29:1-6.
33. Rogel-Fuchs Y, Zahalka EA, Yanai J. 1994. Reversal of early phenobarbital-induced cholinergic and related behavioral deficits by neuronal grafting. Brain Res Bull 33:273-279.
34. Schormann W, Hammersen FJ, Brulport M, Hermes M, Bauer A, Rudolph C, Schug M, Lehmann T, Nussler A, Ungefroren H, Hutchinson J, Fandrich F, Petersen J, Wursthorn K, Burda MR, Brustle O, Krishnamurthi K, von Mach M, Hengstler JG. 2008. Tracking of human cells in mice. Histochem Cell Biol 130:329-338.
35. Sobrian SK. 1977. Prenatal morphine administration alters behavioral development in the rat. Pharmacol Biochem Behav 7:285-288.
36. Steingart RA, Barg J, Maslaton J, Nesher M, Yanai J. 1998. Pre- and postsynaptic alterations in the septohippocampal cholinergic innervations after prenatal exposure to drugs. Brain Res Bull 46:203-209.
37. Steingart RA, Abu-Roumi M, Newman ME, Silverman WF, Slotkin TA, Yanai J. 2000a. Neurobehavioral damage to cholinergic systems caused by prenatal exposure to heroin or phenobarbital: cellular mechanisms and the reversal of deficits by neural grafts. Brain Res Dev Brain Res 122:125-133.
38. Steingart RA, Silverman WF, Barron S, Slotkin TA, Awad Y, Yanai J. 2000b. Neural grafting reverses prenatal drug-induced alterations in hippocampal PKC and related behavioral deficits. Brain Res Dev Brain Res 125:9-19.
39. Strubing C, Ahnert-Hilger G, Shan J, Wiedenmann B, Hescheler J, Wobus AM. 1995. Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech Dev 53:275-287.
40. Tang J, Xu HW, Fan XT, Li ZF, Li DB, Yang L, Zhou GJ. 2007. Targeted migration and differentiation of engrafted neural precursor cells in amyloid beta-treated hippocampus in rats. Neurosci Bull 23:263-270.
41. Toda H, Takahashi J, Iwakami N, Kimura T, Hoki S, Mozumi-Kitamura K, Ono S, Hashimoto N. 2001. Grafting neural stem cells improved the impaired spatial recognition in ischemic rats. Neurosci Lett 316:9-12.
42. van Baar A. 1990. Development of infants of drug dependent mothers. J Child Psychol Psychiatry 31:911-920.
43. van Baar A, de Graaff BM. 1994. Cognitive development at preschoolage of infants of drug-dependent mothers. Dev Med Child Neurol 36:1063-1075.
44. Vathy I, Katay L. 1992. Effects of prenatal morphine on adult sexual behavior and brain catecholamines in rats. Brain Res Dev Brain Res 68:125-131.
45. Vathy I, Rimanoczy A, Eaton RC, Katay L. 1994. Modulation of catecholamine turnover rate in brain regions of rats exposed prenatally to morphine. Brain Res 662:209-215.
46. Vega WA, Kolody B, Hwang J, Noble A. 1993. Prevalence and magnitude of perinatal substance exposures in California. N Engl J Med 329: 850-854.
47. Wang X, Lu Y, Zhang H, Wang K, He Q, Wang Y, Liu X, Li L. 2004. Distinct efficacy of predifferentiated versus intact fetal mesencephalonderived human neural progenitor cells in alleviating rat model of Parkinson's disease. Int J Dev Neurosci 22:175-183.
48. Wilson GS, Desmond MM, Verniaud WM. 1973. Early development of infants of heroin-addicted mothers. Am J Dis Child 126:457-462.
49. Wilson GS, McCreary R, Kean J, Baxter JC. 1979. The development of preschool children of heroin-addicted mothers: a controlled study. Pediatrics 63:135-141.
50. Winer BJ. 1971. Statistical principles in experimental design. New York: McGraw-Hill. xv, 907 p.
51. Wu DC, Boyd AS, Wood KJ. 2008. Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells 26:1939-1950.
52. Yanai J, Pick CG. 1988. Neuron transplantation reverses phenobarbitalinduced behavioral birth defects in mice. Int J Dev Neurosci 6:409-416.
53. Yanai J, Greenfeld Z, Laxer U, Pick CG, Trombka D, Weinstein D. 1987. CNS changes after early barbiturate exposure: mechanisms and reversal. In: Fujii T, Adams P, editors. Functional teratogenesis. Tokyo: Tokyo University Press. p 121-130.
54. Yanai J, Laxer U, Pick CG, Trombka D. 1989. Dopaminergic denervation reverses behavioral deficits induced by prenatal exposure to phenobarbital. Brain Res Dev Brain Res 48:255-261.
55. Yanai J, Avraham Y, Levy S, Maslaton J, Pick CG, Rogel-Fuchs Y, Zahalka EA. 1992a. Alterations in septohippocampal cholinergic innervations and related behaviors after early exposure to heroin and phencyclidine. Brain Res Dev Brain Res 69:207-214.
56. Yanai J, Pick CG, Rogel-Fuchs Y, Zahalka EA. 1992b. Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine. Brain Res Bull 29:363-368.
57. Yanai J, Rogel-Fuchs Y, Pick CG, Slotkin T, Seidler FJ, Zahalka EA, Newman ME. 1993. Septohippocampal cholinergic changes after destruction of the A10-septal dopaminergic pathways. Neuropharmacology 32:113-117.
58. Yanai J, Ben-Shaanan TL, Haimovitch H, Katz S, Kazma M. 2006. Mechanism-based approaches for the reversal of drug neurobehavioral teratogenicity. Ann NY Acad Sci 1074:659-671.
59. Yaniv SP, Naor Z, Yanai J. 2004. Prenatal heroin exposure alters cholinergic receptor stimulated translocation and basal levels of the PKCbetaII and PKCgamma isoforms. Brain Res Bull 63:339-349.
60. Zhang PL, Izrael M, Ainbinder E, Ben-Simchon L, Chebath J, Revel M. 2006. Increased myelinating capacity of embryonic stem cell derived oligodendrocyte precursors after treatment by interleukin-6/soluble interleukin-6 receptor fusion protein. Mol Cell Neurosci 31:387-398.
61. Zhu JH, Stadlin A. 2000. Prenatal heroin exposure. Effects on development, acoustic startle response, and locomotion in weanling rats. Neurotoxicol Teratol 22:193-203.