Subcortical dopaminergic deficits in a DISC1 mutant model: A study in direct reference to human molecular brain imaging

Human Molecular Genetics

Volumn 22, Issue 8, 2013, Pages 1574-1580

  Jaaro Peled, Hanna ^a   Niwa, Minae ^a,b   Foss, Catherine A ^a   Murai, Rina ^b   Reyes, Samantha de los ^a   Kamiya, Atsushi ^a   Mateo, Yolanda ^c   O'Donnell, Patricio ^d   Cascella, Nicola G ^a   Nabeshima, Toshitaka ^b   Guilarte, Tomás R ^e,f   Pomper, Martin G ^a   Sawa, Akira ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEIJO UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^f Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DOPAMINE 2 RECEPTOR; METHAMPHETAMINE; RACLOPRIDE C 11; RADIOLIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTORADIOGRAPHY; BEHAVIOR CHANGE; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; DOPAMINERGIC SYSTEM; DRUG EFFICACY; FORCED SWIMMING TEST; LIGAND BINDING; LOCOMOTION; MALE; MICRODIALYSIS; MOLECULAR BIOLOGY; MOLECULAR IMAGING; MOUSE; NEUROCHEMISTRY; NEUROIMAGING; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOSIS; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BRAIN; BRAIN MAPPING; CORPUS STRIATUM; DOPAMINE; HUMANS; METHAMPHETAMINE; MICE; MICE, TRANSGENIC; MOLECULAR IMAGING; MUTATION; NERVE TISSUE PROTEINS; POSITRON-EMISSION TOMOGRAPHY; PROTEIN BINDING; RECEPTORS, DOPAMINE D2;

ANIMALIA;

EID: 84875764541     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt007     Document Type: Article

References (40)

1. van Rossum, J.M. (1966) The significance of dopamine-receptor blockade for the mechanism of action of neuroleptic drugs. Arch. Int. Pharmacodyn. Ther., 160, 492-494.
2. Laruelle, M. (1998) Imaging dopamine transmission in schizophrenia. A review and meta-analysis. Q. J. Nucl. Med., 42, 211-221.
3. Abi-Dargham, A. (2009). In Charney, D.S. and Nestler, E.J. (eds), Neurobiology of Mental Illness, pp. 321-328.
4. Laruelle, M., Abi-Dargham, A., van Dyck, C.H., Gil, R., D'Souza, C.D., Erdos, J., McCance, E., Rosenblatt, W., Fingado, C., Zoghbi, S.S. et al. (1996) Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc. Natl Acad. Sci. U. S. A., 93, 9235-9240.
5. Abi-Dargham, A., Gil, R., Krystal, J., Baldwin, R.M., Seibyl, J.P., Bowers, M., van Dyck, C.H., Charney, D.S., Innis, R.B. and Laruelle, M. (1998) Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. A. J. Psychiatry, 155, 761-767.
6. Breier, A., Su, T.P., Saunders, R., Carson, R.E., Kolachana, B.S., de Bartolomeis, A., Weinberger, D.R., Weisenfeld, N., Malhotra, A.K., Eckelman, W.C. et al. (1997) Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc. Natl Acad. Sci. U. S. A., 94, 2569-2574.
7. Kellendonk, C. (2009) Modeling excess striatal D2 receptors in mice. Prog. Brain Res., 179, 59-65.
8. Kucinski, A., Syposs, C., Wersinger, S., Bencherif, M., Stachowiak, M.K. and Stachowiak, E.K. (2012) alpha7 neuronal nicotinic receptor agonist (TC-7020) reverses increased striatal dopamine release during acoustic PPI testing in a transgenic mouse model of schizophrenia. Schizophr. Res., 136, 82-87.
9. Winter, C., Reutiman, T.J., Folsom, T.D., Sohr, R., Wolf, R.J., Juckel, G. and Fatemi, S.H. (2008) Dopamine and serotonin levels following prenatal viral infection in mouse-implications for psychiatric disorders such as schizophrenia and autism. Eur. Neuropsychopharmacol., 18, 712-716.
10. Ayhan, Y., Abazyan, B., Nomura, J., Kim, R., Ladenheim, B., Krasnova, I.N., Sawa, A., Margolis, R.L., Cadet, J.L., Mori, S. et al. (2011) Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neurobehavioral phenotypes in transgenic mice: evidence for neurodevelopmental origin of major psychiatric disorders. Mol. Psychiatry, 16, 293-306.
11. Lipina, T.V., Niwa, M., Jaaro-Peled, H., Fletcher, P.J., Seeman, P., Sawa, A. and Roder, J.C. (2010) Enhanced dopamine function in DISC1-L100P mutant mice: implications for schizophrenia. Genes Brain Behav., 9, 777-789.
12. Niwa, M., Kamiya, A., Murai, R., Kubo, K., Gruber, A.J., Tomita, K., Lu, L., Tomisato, S., Jaaro-Peled, H., Seshadri, S. et al. (2010) Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron, 65, 480-489.
13. Porteous, D.J., Millar, J.K., Brandon, N.J. and Sawa, A. (2011) DISC1 at 10: connecting psychiatric genetics and neuroscience. Trends Mol. Med., 17, 699-706.
14. Brandon, N.J. and Sawa, A. (2011) Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci, 12, 707-722.
15. Blackwood, D.H., Fordyce, A., Walker, M.T., St Clair, D.M., Porteous, D.J. and Muir, W.J. (2001) Schizophrenia and affective disorders- cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am. J. Hum. Genet., 69, 428-433.
16. Hikida, T., Jaaro-Peled, H., Seshadri, S., Oishi, K., Hookway, C., Kong, S., Wu, D., Xue, R., Andrade, M., Tankou, S. et al. (2007) Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc. Natl Acad. Sci. U. S. A., 104, 14501-14506.
17. Koike, H., Arguello, P.A., Kvajo, M., Karayiorgou, M. and Gogos, J.A. (2006) Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc. Natl Acad. Sci. U. S. A., 103, 3693-3697.
18. Clapcote, S.J., Lipina, T.V., Millar, J.K., Mackie, S., Christie, S., Ogawa, F., Lerch, J.P., Trimble, K., Uchiyama, M., Sakuraba, Y. et al. (2007) Behavioral phenotypes of Disc1 missense mutations in mice. Neuron, 54, 387-402.
19. Pletnikov, M.V., Ayhan, Y., Nikolskaia, O., Xu, Y., Ovanesov, M.V., Huang, H., Mori, S., Moran, T.H. and Ross, C.A. (2008) Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol. Psychiatry, 13, 173-186, 115.
20. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S.L., Chatzi, C., He, S., Mackie, I., Brandon, N.J. et al. (2008) Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci., 28, 10893-10904.
21. Kuroda, K., Yamada, S., Tanaka, M., Iizuka, M., Yano, H., Mori, D., Tsuboi, D., Nishioka, T., Namba, T., Iizuka, Y. et al. (2011) Behavioral alterations associated with targeted disruption of exons 2 and 3 of the Disc1 gene in the mouse. Hum. Mol. Genet., 20, 4666-4683.
22. Jaaro-Peled, H., Ayhan, Y., Pletnikov, M.V. and Sawa, A. (2010) Review of pathological hallmarks of schizophrenia: comparison of genetic models with patients and nongenetic models. Schizophr. Bull., 36, 301-313.
23. Ibi, D., Nagai, T., Koike, H., Kitahara, Y., Mizoguchi, H., Niwa, M., Jaaro-Peled, H., Nitta, A., Yoneda, Y., Nabeshima, T. et al. (2010) Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav. Brain Res., 206, 32-37.
24. Nagai, T., Kitahara, Y., Ibi, D., Nabeshima, T., Sawa, A. and Yamada, K. (2011) Effects of antipsychotics on the behavioral deficits in human dominant-negative DISC1 transgenic mice with neonatal polyI:C treatment. Behav. Brain Res., 225, 305-310.
25. Wong, D.F., Wagner, H.N. Jr, Tune, L.E., Dannals, R.F., Pearlson, G.D., Links, J.M., Tamminga, C.A., Broussolle, E.P., Ravert, H.T., Wilson, A.A. et al. (1986) Positron emission tomography reveals elevated D2 dopamine receptors in drug-naive schizophrenics. Science, 234, 1558-1563.
26. Seiden, L.S., Sabol, K.E. and Ricaurte, G.A. (1993) Amphetamine: effects on catecholamine systems and behavior. Annu. Rev. Pharmacol. Toxicol., 33, 639-677.
27. Yui, K., Ikemoto, S., Ishiguro, T. and Goto, K. (2000) Studies of amphetamine or methamphetamine psychosis in Japan: relation of methamphetamine psychosis to schizophrenia. Ann. N. Y. Acad. Sci., 914, 1-12.
28. McKetin, R., McLaren, J., Lubman, D.I. and Hides, L. (2006) The prevalence of psychotic symptoms among methamphetamine users. Addiction, 101, 1473-1478.
29. Lieberman, J.A., Kane, J.M. and Alvir, J. (1987) Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology (Berl.), 91, 415-433.
30. Ghisi, V., Ramsey, A.J., Masri, B., Gainetdinov, R.R., Caron, M.G. and Salahpour, A. (2009) Reduced D2-mediated signaling activity and trans-synaptic upregulation of D1 and D2 dopamine receptors in mice overexpressing the dopamine transporter. Cell. Signal., 21, 87-94.
31. Salahpour, A., Ramsey, A.J., Medvedev, I.O., Kile, B., Sotnikova, T.D., Holmstrand, E., Ghisi, V., Nicholls, P.J., Wong, L., Murphy, K. et al. (2008) Increased amphetamine-induced hyperactivity and reward in mice overexpressing the dopamine transporter. Proc. Natl Acad. Sci. U. S. A., 105, 4405-4410.
32. Amsterdam, J.D. and Newberg, A.B. (2007) A preliminary study of dopamine transporter binding in bipolar and unipolar depressed patients and healthy controls. Neuropsychobiology, 55, 167-170.
33. Brunswick, D.J., Amsterdam, J.D., Mozley, P.D. and Newberg, A. (2003) Greater availability of brain dopamine transporters in major depression shown by [99m Tc]TRODAT-1 SPECT imaging. A. J. Psychiatry, 160, 1836-1841.
34. Laasonen-Balk, T., Kuikka, J., Viinamaki, H., Husso-Saastamoinen, M., Lehtonen, J. and Tiihonen, J. (1999) Striatal dopamine transporter density in major depression. Psychopharmacology (Berl.), 144, 282-285.
35. Yang, Y.K., Yeh, T.L., Yao, W.J., Lee, I.H., Chen, P.S., Chiu, N.T. and Lu, R.B. (2008) Greater availability of dopamine transporters in patients with major depression-a dual-isotope SPECT study. Psychiatry Res., 162, 230-235.
36. Amsterdam, J.D., Newberg, A.B., Soeller, I. and Shults, J. (2012) Greater striatal dopamine transporter density may be associated with major depressive episode. J. Affect. Disord.
37. Grace, A.A. (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience, 41, 1-24.
38. Roy, K., Murtie, J.C., El-Khodor, B.F., Edgar, N., Sardi, S.P., Hooks, B.M., Benoit-Marand, M., Chen, C., Moore, H., O'Donnell, P. et al. (2007) Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc. Natl Acad. Sci. U. S. A., 104, 8131-8136.
39. Howes, O.D. and Kapur, S. (2009) The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr. Bull., 35, 549-562.
40. Franklin, K.B.J. and Paxinos, G. (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.