Mice with altered serotonin 2C receptor RNA editing display characteristics of Prader-Willi syndrome

Neurobiology of Disease

Volumn 39, Issue 2, 2010, Pages 169-180

  Morabito, Michael V ^a   Abbas, Atheir I ^b   Hood, Jennifer L ^a   Kesterson, Robert A ^c   Jacobs, Michelle M ^a   Kump, David S ^c   Hachey, David L ^a   Roth, Bryan L ^d   Emeson, Ronald B ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

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

Author keywords

Failure to thrive; Feeding behavior; Hyperphagia; Hypotonia; Metabolism; Prader Willi syndrome; RNA Editing; Serotonin receptor

Indexed keywords

ADENOSINE; INOSINE; ISOPROTEIN; SEROTONIN 2C RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BODY GROWTH; CONTROLLED STUDY; FAILURE TO THRIVE; FEMALE; FOOD INTAKE; GENE LOCUS; GENE MUTATION; GENOME IMPRINTING; HYPERPHAGIA; IN VIVO STUDY; MALE; MOUSE; MOUSE MUTANT; MUSCLE HYPOTONIA; NONHUMAN; PHENOTYPE; PRADER WILLI SYNDROME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EDITING;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; HAND STRENGTH; HUMANS; HYPOTHALAMUS; MALE; MICE; MICE, TRANSGENIC; MUTATION; PRADER-WILLI SYNDROME; PSYCHOMOTOR PERFORMANCE; RECEPTOR, SEROTONIN, 5-HT2C; RNA EDITING; RNA, MESSENGER;

EID: 77953708337     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.04.004     Document Type: Article

References (74)

1. Augustine K.A., Rossi R.M. Rodent mutant models of obesity and their correlations to human obesity. Anat. Rec. 1999, 257:64-72.
2. Barrett P.H., et al. SAAM II: Simulation, Analysis, and Modeling Software for tracer and pharmacokinetic studies. Metabolism 1998, 47:484-492.
3. Berg K.A., et al. RNA-editing of the 5-HT(2C) receptor alters agonist-receptor-effector coupling specificity. Br. J. Pharmacol. 2001, 134:386-392.
4. Bischof J.M., et al. Inactivation of the mouse Magel2 gene results in growth abnormalities similar to Prader-Willi syndrome. Hum. Mol. Genet. 2007, 16:2713-2719.
5. Burns C.M., et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997, 387:303-308.
6. Butte N.F., et al. Human-milk intake measured by administration of deuterium oxide to the mother: a comparison with the test-weighing technique. Am. J. Clin. Nutr. 1988, 47:815-821.
7. Canton H., et al. Identification, molecular cloning, and distribution of a short variant of the 5-hydroxytryptamine2C receptor produced by alternative splicing. Mol. Pharmacol. 1996, 50:799-807.
8. Cattanach B.M., et al. A candidate mouse model for Prader-Willi syndrome which shows an absence of Snrpn expression. Nat. Genet. 1992, 2:270-274.
9. Cavaille J., et al. Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14311-14316.
10. Chamberlain S.J., et al. Evidence for genetic modifiers of postnatal lethality in PWS-IC deletion mice. Hum. Mol. Genet. 2004, 13:2971-2977.
11. Crawley J.N. Behavioral phenotyping strategies for mutant mice. Neuron 2008, 57:809-818.
12. Crosson E.R., et al. Stable isotope ratios using cavity ring-down spectroscopy: determination of 13C/12C for carbon dioxide in human breath. Anal. Chem. 2002, 74:2003-2007.
13. de Smith A.J., et al. A deletion of the HBII-85 class of small nucleolar RNAs (snoRNAs) is associated with hyperphagia, obesity and hypogonadism. Hum. Mol. Genet. 2009, 18:3257-3265.
14. Ding F., et al. Lack of Pwcr1/MBII-85 snoRNA is critical for neonatal lethality in Prader-Willi syndrome mouse models. Mamm. Genome 2005, 16:424-431.
15. Ding F., et al. SnoRNA Snord116 (Pwcr1/MBII-85) deletion causes growth deficiency and hyperphagia in mice. PLoS ONE 2008, 3:e1709.
16. Doe C.M., et al. Loss of the imprinted snoRNA mbii-52 leads to increased 5htr2c pre-RNA editing and altered 5HT2CR-mediated behaviour. Hum. Mol. Genet. 2009, 18:2140-2148.
17. Dracheva S., et al. Increased serotonin 2C receptor mRNA editing: a possible risk factor for suicide. Mol. Psychiatry 2008, 13:1001-1010.
18. Dracheva S., et al. Editing of serotonin 2C receptor mRNA in the prefrontal cortex characterizes high-novelty locomotor response behavioral trait. Neuropsychopharmacology 2009, 34:2237-2251.
19. Ellacott K.L., Cone R.D. The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. Recent Prog. Horm. Res. 2004, 59:395-408.
20. Emeson R.B., et al. Alternative production of calcitonin and CGRP mRNA is regulated at the calcitonin-specific splice acceptor. Nature 1989, 341:76-80.
21. Englander M.T., et al. How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing. J. Neurosci. 2005, 25:648-651.
22. Fitzgerald L.W., et al. Messenger RNA editing of the human serotonin 5-HT2C receptor. Neuropsychopharmacology 1999, 21:82S-90S.
23. Flomen R., et al. Evidence that RNA editing modulates splice site selection in the 5-HT2C receptor gene. Nucleic Acids Res. 2004, 32:2113-2122.
24. Gabriel J.M., et al. A transgene insertion creating a heritable chromosome deletion mouse model of Prader-Willi and angelman syndromes. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9258-9263.
25. Gallagher R.C., et al. Evidence for the role of PWCR1/HBII-85 C/D box small nucleolar RNAs in Prader-Willi syndrome. Am. J. Hum. Genet. 2002, 71:669-678.
26. Gerard M., et al. Disruption of the mouse necdin gene results in early post-natal lethality. Nat. Genet. 1999, 23:199-202.
27. Glowinski J., Iversen L.L. Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. J. Neurochem. 1966, 13:655-669.
28. Goldstone A.P. Prader-Willi syndrome: advances in genetics, pathophysiology and treatment. Trends Endocrinol. Metab. 2004, 15:12-20.
29. Gott J.M., Emeson R.B. Functions and mechanisms of RNA editing. Annu. Rev. Genet. 2000, 34:499-531.
30. Gunay-Aygun M., et al. The changing purpose of Prader-Willi syndrome clinical diagnostic criteria and proposed revised criteria. Pediatrics 2001, 108:E92.
31. Gurevich I., et al. Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J. Neurosci. 2002, 22:10529-10532.
32. Heisler L.K., et al. Activation of central melanocortin pathways by fenfluramine. Science 2002, 297:609-611.
33. Hewitt K.N., et al. Serotonin 2C receptor agonists and the behavioural satiety sequence in mice. Pharmacol. Biochem. Behav. 2002, 71:691-700.
34. Ho S.N., et al. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77:51-59.
35. Hoopengardner B., et al. Nervous system targets of RNA editing identified by comparative genomics. Science 2003, 301:832-836.
36. Infante C., et al. Isotope dilution measurement of breast-milk production in Chilean urban mothers. Hum. Nutr. Clin. Nutr. 1985, 39:379-386.
37. Iwamoto K., Kato T. RNA editing of serotonin 2C receptor in human postmortem brains of major mental disorders. Neurosci. Lett. 2003, 346:169-172.
38. Jong M.T., et al. Imprinting of a RING zinc-finger encoding gene in the mouse chromosome region homologous to the Prader-Willi syndrome genetic region. Hum. Mol. Genet. 1999, 8:795-803.
39. Kawahara Y., et al. Dysregulated editing of serotonin 2C receptor mRNAs results in energy dissipation and loss of fat mass. J. Neurosci. 2008, 28:12834-12844.
40. Kishore S., Stamm S. The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 2006, 311:230-232.
41. Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 2002, 109:145-148.
42. Lee J.S., Lifson N. Measurement of total energy and material balance in rats by means of doubly labeled water. Am. J. Physiol. 1960, 199:238-242.
43. Lifson N. Theory of use of the turnover rates of body water for measuring energy and material balance. J. Theor. Biol. 1966, 12:46-74.
44. Marion S., et al. RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J. Biol. Chem. 2004, 279:2945-2954.
45. McClintock R., Lifson N. Applicability of the D2018 method to the measurement of the total carbon dioxide output of obese mice. J. Biol. Chem. 1957, 226:153-156.
46. Mengod G., et al. The distribution and cellular localization of the serotonin 1C receptor mRNA in the rodent brain examined by in situ hybridization histochemistry. Comparison with receptor binding distribution. Neuroscience 1990, 35:577-591.
47. Meyer O.A., et al. A method for the routine assessment of fore- and hindlimb grip strength of rats and mice. Neurobehav. Toxicol. 1979, 1:233-236.
48. Mizuno T.M., et al. Fasting regulates hypothalamic neuropeptide Y, agouti-related peptide, and proopiomelanocortin in diabetic mice independent of changes in leptin or insulin. Endocrinology 1999, 140:4551-4557.
49. Muscatelli F., et al. Disruption of the mouse Necdin gene results in hypothalamic and behavioral alterations reminiscent of the human Prader-Willi syndrome. Hum. Mol. Genet. 2000, 9:3101-3110.
50. Nicholls R.D., Knepper J.L. Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu Rev Genomics Hum Genet. 2001, 2:153-175.
51. Niswender C.M., et al. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J. Biol. Chem. 1999, 274:9472-9478.
52. Niswender C.M., et al. RNA editing of the human serotonin 5-HT2C receptor. Alterations in suicide and implications for serotonergic pharmacotherapy. Neuropsychopharmacology 2001, 24:478-491.
53. Nonogaki K., et al. Leptin-independent hyperphagia and type 2 diabetes in mice with a mutated serotonin 5-HT2C receptor gene. Nat. Med. 1998, 4:1152-1156.
54. Nonogaki K., et al. Hyperactivity and reduced energy cost of physical activity in serotonin 5-HT(2C) receptor mutant mice. Diabetes 2003, 52:315-320.
55. Olaghere da Silva, U.B., et al., 2009. Impact of RNA editing on functions of the serotonin 2C receptor in vivo. Front. Neurosci. 4, e26.
56. Pin J.P., et al. Domains involved in the specificity of G protein activation in phospholipase C-coupled metabotropic glutamate receptors. EMBO J. 1994, 13:342-348.
57. Powell C.S., et al. Effects of energy expenditure and Ucp1 on photoperiod-induced weight gain in collard lemmings. Obes. Res. 2002, 10:541-550.
58. Price R.D., et al. RNA editing of the human serotonin 5-HT2C receptor alters receptor-mediated activation of G13 protein. J. Biol. Chem. 2001, 276:44663-44668.
59. Runte M., et al. Exclusion of the C/D box snoRNA gene cluster HBII-52 from a major role in Prader-Willi syndrome. Hum. Genet. 2005, 116:228-230.
60. Sahoo T., et al. Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat. Genet. 2008, 40:719-721.
61. Schwartz M.W., et al. Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral arcuate nucleus. Diabetes 1997, 46:2119-2123.
62. Singh M., et al. Hyperphagia-mediated obesity in transgenic mice misexpressing the RNA-editing enzyme ADAR2. J. Biol. Chem. 2007, 282:22448-22459.
63. Skryabin B.V., et al. Deletion of the MBII-85 snoRNA gene cluster in mice results in postnatal growth retardation. PLoS Genet. 2007, 3:e235.
64. Sodhi M.S., et al. A rapid new assay to detect RNA editing reveals antipsychotic-induced changes in serotonin-2C transcripts. Mol. Pharmacol. 2005, 68:711-719.
65. Somerville E.M., et al. 5-HT(2C) receptor activation inhibits appetitive and consummatory components of feeding and increases brain c-fos immunoreactivity in mice. Eur. J. NeuroSci. 2007, 25:3115-3124.
66. Stefan M., et al. Hormonal and metabolic defects in a prader-willi syndrome mouse model with neonatal failure to thrive. Endocrinology 2005, 146:4377-4385.
67. Tecott L.H., et al. Eating disorder and epilepsy in mice lacking 5-HT2c serotonin receptors. Nature 1995, 374:542-546.
68. Tsai T.F., et al. Necdin-deficient mice do not show lethality or the obesity and infertility of Prader-Willi syndrome. Nat. Genet. 1999, 22:15-16.
69. Tsai T.F., et al. Paternal deletion from Snrpn to Ube3a in the mouse causes hypotonia, growth retardation and partial lethality and provides evidence for a gene contributing to Prader-Willi syndrome. Hum. Mol. Genet. 1999, 8:1357-1364.
70. Vitali P., et al. ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J. Cell Biol. 2005, 169:745-753.
71. Wang Q., et al. Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors. J. Neurochem. 2000, 74:1290-1300.
72. Xu Y., et al. 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 2008, 60:582-589.
73. Yang T., et al. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat. Genet. 1998, 19:25-31.
74. Zhao S., Fernald R.D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 2005, 12:1047-1064.