CYP3A5 Mediates Effects of Cocaine on Human Neocorticogenesis: Studies using an in Vitro 3D Self-Organized hPSC Model with a Single Cortex-Like Unit

Neuropsychopharmacology

Volumn 42, Issue 3, 2017, Pages 774-784

  Lee, Chun Ting ^a,b,e   Chen, Jia ^a,e   Kindberg, Abigail A ^a,e   Bendriem, Raphael M ^a   Spivak, Charles E ^a   Williams, Melanie P ^a   Richie, Christopher T ^a   Handreck, Annelie ^c   Mallon, Barbara S ^d   Lupica, Carl R ^a   Lin, Da Ting ^a   Harvey, Brandon K ^a   Mash, Deborah C ^b   Freed, William J ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; 6 [4 (1 PIPERAZINYL)PHENYL] 3 (4 QUINOLINYL)PYRAZOLO[1,5 A]PYRIMIDINE; ACTIVIN; COCAINE; CYTOCHROME P450; CYTOCHROME P450 3A3; CYTOCHROME P450 3A4; CYTOCHROME P450 3A5; CYTOCHROME P450 3A7; FIBROBLAST GROWTH FACTOR; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; OCTAMER TRANSCRIPTION FACTOR 4; POTASSIUM; SMAD PROTEIN; SODIUM; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; CYTOCHROME P450 3A; DOPAMINE UPTAKE INHIBITOR;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE STEADY POTENTIAL; MOUSE; NEOCORTEX; NEOCORTICAL TISSUE; NERVE CELL DIFFERENTIATION; NEUROEPITHELIUM CELL; NONHUMAN; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; POTASSIUM CURRENT; PRIORITY JOURNAL; ROSETTE FORMATION; SODIUM CURRENT; STEM CELL SELF-RENEWAL; CELL LINE; DRUG EFFECTS; METABOLISM; NERVOUS SYSTEM DEVELOPMENT;

CELL LINE; COCAINE; CYTOCHROME P-450 CYP3A; DOPAMINE UPTAKE INHIBITORS; HUMANS; NEOCORTEX; NEUROGENESIS; PLURIPOTENT STEM CELLS;

EID: 84988664616     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.156     Document Type: Article

References (46)

1. Agarwal V, Kommaddi RP, Valli K, Ryder D, Hyde TM, Kleinman JE et al (2008). Drug metabolism in human brain: high levels of cytochrome P4503A43 in brain and metabolism of anti-Anxiety drug alprazolam to its active metabolite. PLoS One 3: e2337.
2. Aigner S, Heckel T, Zhang JD, Andreae LC, Jagasia R (2014). Human pluripotent stem cell models of autism spectrum disorder: emerging frontiers, opportunities, and challenges towards neuronal networks in a dish. Psychopharmacology (Berl) 231: 1089-1104.
3. Anticevic A, Hu X, Xiao Y, Hu J, Li F, Bi F et al (2015). Early-course unmedicated schizophrenia patients exhibit elevated prefrontal connectivity associated with longitudinal change. J Neurosci 35: 267-286.
4. Bandstra ES, Morrow CE, Accornero VH, Mansoor E, Xue L, Anthony JC (2011). Estimated effects of in utero cocaine exposure on language development through early adolescence. Neurotoxicol Teratol 33: 25-35.
5. Bandstra ES, Vogel AL, Morrow CE, Xue L, Anthony JC (2004). Severity of prenatal cocaine exposure and child language functioning through age seven years: A longitudinal latent growth curve analysis. Subst Use Misuse 39: 25-59.
6. Booth Depaz IM, Toselli F, Wilce PA, Gillam EM (2013). Differential expression of human cytochrome P450 enzymes from the CYP3A subfamily in the brains of alcoholic subjects and drug-free controls. Drug Metab Dispos 41: 1187-1194.
7. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S et al (2011). Modelling schizophrenia using human induced pluripotent stem cells. Nature 473: 221-225.
8. Brennand KJ, Simone A, Tran N, Gage FH (2012). Modeling psychiatric disorders at the cellular and network levels. Mol Psychiatry 17: 1239-1253.
9. Cameron RS, Rakic P (1991). Glial cell lineage in the cerebral cortex: A review and synthesis. Glia 4: 124-137.
10. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27: 275-280.
11. Chung K, Wallace J, Kim SY, Kalyanasundaram S, Andalman AS, Davidson TJ et al (2013). Structural and molecular interrogation of intact biological systems. Nature 497: 332-337.
12. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ et al (2011). Neuron number and size in prefrontal cortex of children with autism. JAMA 306: 2001-2010.
13. Dehay C, Kennedy H (2007). Cell-cycle control and cortical development. Nat Rev Neurosci 8: 438-450.
14. Ellenbroek BA, Cools AR (2000). Animal models for the negative symptoms of schizophrenia. Behav Pharmacol 11: 223-233.
15. Greber B, Coulon P, Zhang M, Moritz S, Frank S, Möller-Molina AJ et al (2011). FGF signalling inhibits neural induction in human embryonic stem cells. EMBO J 30: 4874-4884.
16. Grimm FA, Iwata Y, Sirenko O, Bittner M, Rusyn I (2015). Highcontent assay multiplexing for toxicity screening in induced pluripotent stem cell-derived cardiomyocytes and hepatocytes. Assay Drug Dev Technol 13: 529-546.
17. Hasegawa H, Ashigaki S, Takamatsu M, Suzuki-Migishima R, Ohbayashi N, Itoh N et al (2004). Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling. J Neurosci 24: 8711-8719.
18. Hill RS, Walsh CA (2005). Molecular insights into human brain evolution. Nature 437: 64-67.
19. Kindberg AA, Bendriem RM, Spivak CE, Chen J, Handreck A, Lupica CR et al (2014). An in vitro model of human neocortical development using pluripotent stem cells: cocaineinduced cytoarchitectural alterations. Dis Model Mech 7: 1397-1405.
20. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME et al (2013). Cerebral organoids model human brain development and microcephaly. Nature 501: 373-379.
21. Lee CT, Bendriem RM, Freed WJ (2015a). A new technique for modeling neuronal connectivity using human pluripotent stem cells. Restor Neurol Neurosci 33: 347-356.
22. Lee CT, Bendriem RM, Kindberg AA, Worden LT, Williams MP, Drgon T et al (2015b). Functional consequences of 17q21.31/WNT3-WNT9B amplification in hPSCs with respect to neural differentiation. Cell Rep 10: 616-632.
23. Lee CT, Chen J, Hayashi T, Tsai SY, Sanchez JF, Errico SL et al (2008). A mechanism for the inhibition of neural progenitor cell proliferation by cocaine. PLoS Med 5: e117.
24. Lee CT, Chen J, Worden LT, Freed WJ (2011). Cocaine causes deficits in radial migration and alters the distribution of glutamate and GABA neurons in the developing rat cerebral cortex. Synapse 65: 21-34.
25. Lee CT, Freed WJ, Mash DC (2015c). CNVs in neurodevelopmental disorders. Oncotarget 6: 18238-18239.
26. Levison SW, Goldman JE (1993). Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10: 201-212.
27. Lidow MS, Bozian D, Song ZM (2001). Cocaine affects cerebral neocortical cytoarchitecture in primates only if administered during neocortical neuronogenesis. Brain Res Dev Brain Res 128: 45-52.
28. Lidow MS, Song ZM (2001). Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J Comp Neurol 435: 263-275.
29. Mallon BS, Chenoweth JG, Johnson KR, Hamilton RS, Tesar PJ, Yavatkar AS et al (2013). StemCellDB: The human pluripotent stem cell database at the National Institutes of Health. Stem Cell Res 10: 57-66.
30. Martignoni M, Groothuis GM, de Kanter R (2006). Species differences between mouse, rat, dog, monkey and human CYPmediated drug metabolism, inhibition and induction. Expert Opin Drug Metab Toxicol 2: 875-894.
31. McFadyen MC, Melvin WT, Murray GI (1998). Regional distribution of individual forms of cytochrome P450 mRNA in normal adult human brain. Biochem Pharmacol 55: 825-830.
32. Noonan MA, Choi KH, Self DW, Eisch AJ (2008). Withdrawal from cocaine self-Administration normalizes deficits in proliferation and enhances maturity of adult-generated hippocampal neurons. J Neurosci 28: 2516-2526.
33. Pasca AM, Sloan SA, Clarke LE, Tian Y, Makinson CD, Huber N et al (2015). Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat Methods 12: 671-678.
34. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000). Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20: 5012-5023.
35. Rakic P (2009). Evolution of the neocortex: A perspective from developmental biology. Nat Rev Neurosci 10: 724-735.
36. Rando K, Chaplin TM, Potenza MN, Mayes L, Sinha R (2013). Prenatal cocaine exposure and gray matter volume in adolescent boys and girls: relationship to substance use initiation. Biol Psychiatry 74: 482-489.
37. Ruhela RK, Prakash A, Medhi B (2015). An urgent need for experimental animal model of autism in drug development. Ann Neurosci 22: 44-49.
38. Sarnat HB, Nochlin D, Born DE (1998). Neuronal nuclear antigen (NeuN): A marker of neuronal maturation in early human fetal nervous system. Brain Dev 20: 88-94.
39. Sengupta S, Johnson BP, Swanson SA, Stewart R, Bradfield CA, Thomson JA (2014). Aggregate culture of human embryonic stem cell-derived hepatocytes in suspension are an improved in vitro model for drug metabolism and toxicity testing. Toxicol Sci 140: 236-245.
40. Singer LT, Arendt R, Minnes S, Farkas K, Salvator A, Kirchner HL et al (2002). Cognitive and motor outcomes of cocaine-exposed infants. JAMA 287: 1952-1960.
41. Singer LT, Nelson S, Short E, Min MO, Lewis B, Russ S et al (2008). Prenatal cocaine exposure: drug and environmental effects at 9 years. J Pediatr 153: 105-111.
42. Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S et al (2014). Patches of disorganization in the neocortex of children with autism. N Engl J Med 370: 1209-1219.
43. Supèr H, Uylings HB (2001). The early differentiation of the neocortex: A hypothesis on neocortical evolution. Cereb Cortex 11: 1101-1109.
44. Takahashi T, Nowakowski RS, Caviness VS Jr (1993). Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13: 820-833.
45. Valente MJ, Carvalho F, Bastos Md, de Pinho PG, Carvalho M (2012). Contribution of oxidative metabolism to cocaine-induced liver and kidney damage. Curr Med Chem 19: 5601-5606.
46. Zeng X, Chen J, Deng X, Liu Y, Rao MS, Cadet JL et al (2006). An in vitro model of human dopaminergic neurons derived from embryonic stem cells: MPP+ toxicity and GDNF neuroprotection. Neuropsychopharmacology 31: 2708-2715.