Abnormal serotonergic development in a mouse model for the Smith-Lemli-Opitz syndrome: Implications for autism

International Journal of Developmental Neuroscience

Volumn 21, Issue 8, 2003, Pages 451-459

  Waage Baudet, H ^a,b   Lauder, J M ^a   Dehart, D B ^a,b   Kluckman, K ^b   Hiller, S ^b   Tint, G S ^c   Sulik, K K ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN COMMISSURE; BRAIN NERVE CELL; BRAIN TISSUE; CELL COUNT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; HIPPOCAMPUS; HORMONE ACTION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; SEROTONINERGIC SYSTEM; SMITH LEMLI OPITZ SYNDROME; WILD TYPE;

ANIMALIA;

EID: 0345376666     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2003.09.002     Document Type: Article

References (70)

1. Aman M.G., Kern R.A. Review of fenfluramine in the treatment of the developmental disabilities. J. Am. Acad. Child Adolesc. Psychiatry. 28:1989;549-565.
2. August G.J., Raz N., Papanicolaou A.C., Baird T.D., Hirsh S.L., Hsu L.L. Fenfluramine treatment in infantile autism, electrophysiological, and behavioral effects. Neurochem. J. Nerv. Ment. Dis. 172:1984;604-612.
3. Betancur C., Corbex M., Spielewoy C., Philippe A., Laplanche J.L., Launay J.M., Gillberg C., Mouren-Simeoni M.C., Hamon M., Giros B., Nosten-Bertrand M., Leboyer M. Serotonin transporter gene polymorphisms and hyperserotonemia in autistic disorder. Mol. Psychiatry. 7:2002;67-71.
4. Bou-Flores C., Lajard A.M., Monteau R., De Maeyer E., Seif I., Lanoir J., Hilaire G. Abnormal phrenic motoneuron activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice: possible role of a serotonin excess. J. Neurosci. 20:2000;4646-4656.
5. Bruning G., Liangos O., Baumgarten H.G. Prenatal development of the serotonin transporter in mouse brain. Cell Tissue Res. 289:1997;211-221.
6. Caramona M.M., Cotrim M.D., Figueiredo I.V., Tavares P., Ribeiro C.A., Beja M.L., Wulfroth P., Teixeira F. Influence of experimental hypercholesterolemia on the monoamine oxidase activity in rabbit arteries. Pharmacol. Res. 33:1996;245-249.
7. Carlsson M.L. Hypothesis: is infantile autism a hypoglutamatergic disorder? Relevance of glutamate-serotonin interactions for pharmacotherapy. J. Neural Transm. 105:1998;525-535.
8. Cases O., Lebrand C., Giros B., Vitalis T., De Maeyer E., Caron M.G., Price D.J., Gaspar P., Seif I. Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs. J. Neurosci. 18:1998;6914-6927.
9. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell. 113:2003;11-23.
10. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 383:1996;407-413.
11. Chugani D.C., Muzik O., Rothermel R., Behen M., Chakraborty P., Mangner T., da Silva E.A., Chugani H.T. Altered serotonin synthesis in the dentatothalamocortical pathway in autistic boys. Ann. Neurol. 42:1997;666-669.
12. Chugani D.C., Muzik O., Behen M., Rothermel R., Janisse J.J., Lee J., Chugani H.T. Developmental changes in brain serotonin synthesis capacity in autistic and nonautistic children. Ann. Neurol. 45:1999;287-295.
13. Cvijic G., Djordjevic J., Davidovic V. Effect of fasting and refeeding on the activities of monoamine oxidase and antioxidant enzymes in rat hypothalamus and brown adipose tissue. Gen. Physiol Biophys. 19:2000;305-316.
14. Di Pasquale E., Monteau R., Hilaire G. Endogenous serotonin modulates the fetal respiratory rhythm: an in vitro study in the rat. Brain Res. Dev. Brain Res. 80:1994;222-232.
15. Filinger E.J., Garcia-Cotto M.A., Vila S., Gerbaldo H., Jerez D. Possible relationship between pervasive developmental disorders and platelet monoamine oxidase activity. Braz. J. Med. Biol. Res. 20:1987;161-164.
16. Fitzky B.U., Witsch-Baumgartner M., Erdel M., Lee J.N., Paik Y.K., Glossmann H., Utermann G., Moebius F.F. Mutations in the Delta7-sterol reductase gene in patients with the Smith-Lemli-Opitz syndrome. Proc. Natl. Acad. Sci. U.S.A. 95:1998;8181-8186.
17. Fitzky B.U., Moebius F.F., Asaoka H., Waage-Baudet H., Xu L., Xu G., Maeda N., Kluckman K., Hiller S., Yu H., Batta A.K., Shefer S., Chen T., Salen G., Sulik K., Simoni R.D., Ness G.C., Glossmann H., Patel S.B., Tint G.S. 7-Dehydrocholesterol-dependent proteolysis of HMG-CoA reductase suppresses sterol biosynthesis in a mouse model of Smith-Lemli-Opitz/RSH syndrome. J. Clin. Invest. 108:2001;905-915.
18. Golden G.S. Prenatal development of the biogenic amine systems of the mouse brain. Dev. Biol. 33:1973;300-311.
19. Gorlin, R.J., Cohen, M.M., Levin, L.S., Syndromes of the Head and Neck. Oxford University Press, New York; Oxford, 1990.
20. Gorwood P. Biological markers for suicidal behavior in alcohol dependence. Eur. Psychiatry. 16:2001;410-417.
21. Gruneberg H. The development of some external features in mouse embryos. J. Heredity. 34:1943;89-92.
22. Hanley H.G., Stahl S.M., Freedman D.X. Hyperserotonemia and amine metabolites in autistic and retarded children. Arch. Gen. Psychiatry. 34:1977;521-531.
23. Hynes M., Porter J.A., Chiang C., Chang D., Tessier-Lavigne M., Beachy P.A., Rosenthal A. Induction of midbrain dopaminergic neurons by Sonic hedgehog. Neuron. 15:1995;35-44.
24. Hynes M., Ye W., Wang K., Stone D., Murone M., Sauvage F., Rosenthal A. The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nat. Neurosci. 3:2000;41-46.
25. Irons M., Elias E.R., Salen G., Tint G.S., Batta A.K. Defective cholesterol biosynthesis in Smith-Lemli-Opitz syndrome. Lancet. 341:1993;1414.
26. Jurevics H.A., Kidwai F.Z., Morell P. Sources of cholesterol during development of the rat fetus and fetal organs. J. Lipid Res. 38:1997;723-733.
27. Kaufman, M.H., 1992. The Atlas of Mouse Development. Academic Press, London; San Diego.
28. Kelley R.I., Hennekam R.C. The Smith-Lemli-Opitz syndrome. J. Med. Genet. 37:2000;321-335.
29. Kelley R.L., Roessler E., Hennekam R.C., Feldman G.L., Kosaki K., Jones M.C., Palumbos J.C., Muenke M. Holoprosencephaly in RSH/Smith-Lemli-Opitz syndrome: does abnormal cholesterol metabolism affect the function of sonic hedgehog? Am. J. Med. Genet. 66:1996;478-484.
30. Klein U., Gimpl G., Fahrenholz F. Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry. 34:1995;13784-13793.
31. Lanoue L., Dehart D.B., Hinsdale M.E., Maeda N., Tint G.S., Sulik K.K. Limb, genital, CNS, and facial malformations result from gene/environment- induced cholesterol deficiency: further evidence for a link to sonic hedgehog. Am. J. Med. Genet. 73:1997;24-31.
32. Launay J.M., Ferrari P., Haimart M., Bursztejn C., Tabuteau F., Braconnier A., Pasques-Bondoux D., Luong C., Dreux C. Serotonin metabolism and other biochemical parameters in infantile autism. A controlled study of 22 autistic children. Neuropsychobiology. 20:1988;1-11.
33. Lidov H.G., Molliver M.E. Immunohistochemical study of the development of serotonergic neurons in the rat CNS. Brain Res. Bull. 9:1982;559-604.
34. Luo X.P.A.L.J. Serotonergic regulation of somatosensory cortical development: lessons from genetic mouse models. Dev. Neurosci. 25:2003;173-183.
35. Matise M.P., Lustig M., Sakurai T., Grumet M., Joyner A.L. Ventral midline cells are required for the local control of commissural axon guidance in the mouse spinal cord. Development. 126:1999;3649-3659.
36. McDougle C.J., Holmes J.P., Carlson D.C., Pelton G.H., Cohen D.J., Price L.H. A double-blind, placebocontrolled study of risperidone in adults with autistic disorder and other pervasive developmental disorders. Arch. Gen. Psychiatry. 55:1998;633-641.
37. McDougle C.J., Scahill L., McCracken J.T., Aman M.G., Tierney E., Arnold L.E., Freeman B.J., Martin A., McGough J.J., Cronin P., Posey D.J., Riddle M.A., Ritz L., Swiezy N.B., Vitiello B., Volkmar F.R., Votolato N.A., Walson P. Research units on pediatric psychopharmacology (RUPP) autism network. Background and rationale for an initial controlled study of risperidone. Child Adolesc. Psychiatr. Clin. N. Am. 9:2000;201-224.
38. Ming J.E., Muenke M. Holoprosencephaly: from homer to hedgehog. Clin. Genet. 53:1998;155-163.
39. Nowaczyk M.J., Nakamura L.M., Eng B., Porter F.D., Waye J.S. Frequency and ethnic distribution of the common DHCR7 mutation in Smith-Lemli-Opitz syndrome. Am. J. Med. Genet. 102:2001;383-386.
40. Nunez M.T., Glass J. Reconstitution of the transferrin receptor in lipid vesicles. Effect of cholesterol on the binding of transferrin. Biochemistry. 21:1982;4139-4143.
41. Olson L., Seiger A. Early prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z. Anat. Entwicklungsgesch. 137:1972;301-316.
42. Opitz J.M., de la Cruz F. Cholesterol metabolism in the RSH/Smith-Lemli-Opitz syndrome: summary of an NICHD conference. Am. J. Med. Genet. 50:1994;326-338.
43. Opitz J.M., Gilbert-Barness E., Ackerman J., Lowichik A. Cholesterol and development: the RSH ("Smith-Lemli-Opitz") syndrome and related conditions. Pediatr. Pathol. Mol. Med. 21:2002;153-181.
44. Pang L., Graziano M., Wang S. Membrane cholesterol modulates galanin-GalR2 interaction. Biochemistry. 38:1999;12003-12011.
45. Pepinsky R.B., Zeng C., Wen D., Rayhorn P., Baker D.P., Williams K.P., Bixler S.A., Ambrose C.M., Garber E.A., Miatkowski K., Taylor F.R., Wang E.A., Galdes A. Identification of a palmitic acid-modified form of human sonic hedgehog. J. Biol. Chem. 273:1998;14037-14045.
46. Porter J.A., Young K.E., Beachy P.A. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274:1996;255-259.
47. Roux C., Dupuis R., Horvath C., Talbot J.N. Teratogenic effect of an inhibitor of cholesterol synthesis (AY 9944) in rats: correlation with maternal cholesterolemia. J. Nutr. 110:1980;2310-2312.
48. Rubenstein J.L. Development of serotonergic neurons and their projections. Biol. Psychiatry. 44:1998;145-150.
49. Sanz-Ezquerro J.J., Tickle C. Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development. Development. 127:2000;4811-4823.
50. Scanlon S.M., Williams D.C., Schloss P. Membrane cholesterol modulates serotonin transporter activity. Biochemistry. 40:2001;10507-10513.
51. Schambra, U.B., Lauder, J.M., Silver, J., 1992. Atlas of the Prenatal Mouse Brain. Academic Press, San Diego.
52. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell. 87:1996;1001-1014.
53. Shih J.C., Chen K. MAO-A and -B gene knock-out mice exhibit distinctly different behavior. Neurobiology (Bp). 7:1999;235-246.
54. Smith D.W., Lemli L., Opitz J.M. A newly recognized syndrome of multiple congenital abnormalities. J. Pediatrics. 64:1964;210-217.
55. Sooksawate T., Simmonds M.A. Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology. 40:2001;178-184.
56. Tanabe Y., Jessell T.M. Diversity and pattern in the developing spinal cord. Science. 274:1996;1115-1123.
57. Tierney E., Nwokoro N.A., Kelley R.I. Behavioral phenotype of RSH/Smith-Lemli-Opitz syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 6:2000;131-134.
58. Tierney E., Nwokoro N.A., Porter F.D., Freund L.S., Ghuman J.K., Kelley R.I. Behavior phenotype in the RSH/Smith-Lemli-Opitz syndrome. Am. J. Med. Genet. 98:2001;191-200.
59. Tint G. A mouse model for the Smith-Lemli-Opitz syndrome (SLOS). Am. J. Hum. Genet. 65(Suppl. 4):1999;96.
60. Tint G.S., Irons M., Elias E.R., Batta A.K., Frieden R., Chen T.S., Salen G. Defective cholesterol biosynthesis associated with the Smith-Lemli-Opitz syndrome. N. Engl. J. Med. 330:1994;107-113.
61. Upton A.L., Salichon N., Lebrand C., Ravary A., Blakely R., Seif I., Gaspar P. Excess of serotonin (5-HT) alters the segregation of ispilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J. Neurosci. 19:1999;7007-7024.
62. Wallace J.A., Lauder J.M. Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res. Bull. 10:1983;459-479.
63. Wallace J.A., Petrusz P., Lauder J.M. Serotonin immunocytochemistry in the adult and developing rat brain: methodological and pharmacological considerations. Brain Res. Bull. 9:1982;117-129.
64. Wassif C.A., Zhu P., Kratz L., Krakowiak P.A., Battaile K.P., Weight F.F., Grinberg A., Steiner R.D., Nwokoro N.A., Kelley R.I., Stewart R.R., Porter F.D. Biochemical, phenotypic and neurophysiological characterization of a genetic mouse model of RSH/Smith-Lemli-Opitz syndrome. Hum. Mol. Genet. 10:2001;555-564.
65. Waye J.S., Nakamura L.M., Eng B., Hunnisett L., Chitayat D., Costa T., Nowaczyk M.J. Smith-Lemli-Opitz syndrome: carrier frequency and spectrum of DHCR7 mutations in Canada. J. Med. Genet. 39:2002;E31.
66. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell. 93:1998;755-766.
67. Yuwiler A., Shih J.C., Chen C.H., Ritvo E.R., Hanna G., Ellison G.W., King B.H. Hyperserotoninemia and antiserotonin antibodies in autism and other disorders. J. Autism Dev. Disord. 22:1992;33-45.
68. Zhang X.M., Yang X.J. Regulation of retinal ganglion cell production by Sonic hedgehog. Development. 128:2001;943-957.
69. Zhou F.C., Sari Y., Zhang J.K. Expression of serotonin transporter protein in developing rat brain. Brain Res. Dev. Brain Res. 119:2000;33-45.
70. Zhou F.C., Sari Y., Zhang J.K., Goodlett C.R., Li T. Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Brain Res. Dev. Brain Res. 126:2001;147-155.