Genetic background modulates phenotypes of serotonin transporter Ala56 knock-in mice

Molecular Autism

Volumn 4, Issue 1, 2013, Pages

  Kerr, Travis M ^a   Muller, Christopher L ^b   Miah, Mahfuzur ^b   Jetter, Christopher S ^a   Pfeiffer, Rita ^b   Shah, Charisma ^a   Baganz, Nicole ^b   Anderson, George M ^c   Crawley, Jacqueline N ^d   Sutcliffe, James S ^a,e   Blakely, Randy D ^a,b,f   Veenstra Vanderweele, Jeremy ^a,b,f,g  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Silvio O Conte Center for Neuroscience Research ^*  (United States)

^f Silvio O Conte Center for Neuroscience Research   (United States)

^g VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autism; Compulsive; Monoamine; Receptor; Serotonin; Transporter

Indexed keywords

SEROTONIN; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; BACKCROSSING; C57BL 6 MOUSE; COMPULSION; CONGENIC STRAIN; CONTROLLED STUDY; DOMINANCE BEHAVIOR; FEMALE; GENE INTERACTION; GENE TARGETING; GENETIC VARIABILITY; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; SEROTONIN BLOOD LEVEL; SEROTONINERGIC SYSTEM; SOCIAL BEHAVIOR; SOCIAL ISOLATION; ULTRASOUND; VOCALIZATION; WILD TYPE;

MUS;

EID: 84884804976     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-4-35     Document Type: Article

References (67)

1. Networking in autism: leveraging genetic, biomarker and model system findings in the search for new treatments. Veenstra-VanderWeele J, Blakely RD, Neuropsychopharmacology 2012 37 196 212 10.1038/npp.2011.185 21937981
2. Platelet serotonin levels in pervasive developmental disorders and mental retardation: diagnostic group differences, within-group distribution, and behavioral correlates. Mulder EJ, Anderson GM, Kema IP, de Bildt A, van Lang ND, den Boer JA, Minderaa RB, J Am Acad Child Adolesc Psychiatry 2004 43 491 499 10.1097/00004583-200404000-00016 15187810 (Pubitemid 38812390)
3. The serotonin system in autism. Cook E, Leventhal B, Curr Opin Pediatr 1996 8 348 354 10.1097/00008480-199608000-00008 9053096 (Pubitemid 26393877)
4. Broad and narrow heritabilities of quantitative traits in a founder population. Abney M, McPeek MS, Ober C, Am J Hum Genet 2001 68 1302 1307 10.1086/320112 11309690 (Pubitemid 32424431)
5. Genetic heritability and shared environmental factors among twin pairs with autism. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, Miller J, Fedele A, Collins J, Smith K, Lotspeich L, Croen LA, Ozonoff S, Lajonchere C, Grether JK, Risch N, Arch Gen Psychiatry 2011 68 1095 1102 10.1001/archgenpsychiatry.2011.76 21727249
6. Infantile autism: a genetic study of 21 twin pairs. Folstein S, Rutter M, J Child Psychol Psychiatry 1977 18 297 321 10.1111/j.1469-7610.1977.tb00443.x 562353
7. Autism as a strongly genetic disorder: evidence from a British twin study. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, Rutter M, Psychol Med 1995 25 63 78 10.1017/S0033291700028099 7792363
8. Sex-specific genetic architecture of whole blood serotonin levels. Weiss LA, Abney M, Cook EH Jr, Ober C, Am J Hum Genet 2005 76 33 41 10.1086/426697 15526234 (Pubitemid 40023763)
9. Genome-wide association study identifies ITGB3 as a QTL for whole blood serotonin. Weiss LA, Veenstra-Vanderweele J, Newman DL, Kim SJ, Dytch H, McPeek MS, Cheng S, Ober C, Cook EH Jr, Abney M, Eur J Hum Genet 2004 12 949 954 10.1038/sj.ejhg.5201239 15292919 (Pubitemid 39462129)
10. Interactions between integrin alphaIIbbeta3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. Carneiro AM, Cook EH, Murphy DL, Blakely RD, J Clin Invest 2008 118 1544 1552 10.1172/JCI33374 18317590 (Pubitemid 351500447)
11. A genome wide screen for autism: Strong evidence for linkage to chromosomes 2q, 7q and 16p. International Molecular Genetic Study of Autism Consortium, Am J Hum Genet 2001 69 570 581 11481586
12. A genomewide screen of 345 families for autism-susceptibility loci. Yonan AL, Alarcon M, Cheng R, Magnusson PK, Spence SJ, Palmer AA, Grunn A, Juo SH, Terwilliger JD, Liu J, Cantor RM, Geschwind DH, Gilliam TC, Am J Hum Genet 2003 73 886 897 10.1086/378778 13680528 (Pubitemid 37271891)
13. Evidence for sex-specific risk alleles in autism spectrum disorder. Stone JL, Merriman B, Cantor RM, Yonan AL, Gilliam TC, Geschwind DH, Nelson SF, Am J Hum Genet 2004 75 1117 1123 10.1086/426034 15467983 (Pubitemid 39532079)
14. Allelic heterogeneity at the serotonin transporter locus (SLC6A4) confers susceptibility to autism and rigid-compulsive behaviors. Sutcliffe JS, Delahanty RJ, Prasad HC, McCauley JL, Han Q, Jiang L, Li C, Folstein SE, Blakely RD, Am J Hum Genet 2005 77 265 279 10.1086/432648 15995945 (Pubitemid 41022709)
15. Replication of autism linkage: fine-mapping peak at 17q21. Cantor RM, Kono N, Duvall JA, Alvarez-Retuerto A, Stone JL, Alarcon M, Nelson SF, Geschwind DH, Am J Hum Genet 2005 76 1050 1056 10.1086/430278 15877280 (Pubitemid 40705438)
16. Autism and the serotonin transporter: the long and short of it. Devlin B, Cook EH Jr, Coon H, Dawson G, Grigorenko EL, McMahon W, Minshew N, Pauls D, Smith M, Spence MA, Rodier PM, Stodgell C, Schellenberg GD, CPEA Genetics Network, Mol Psychiatry 2005 10 1110 1116 10.1038/sj.mp.4001724 16103890 (Pubitemid 43251101)
17. Transmission disequilibrium mapping at the serotonin transporter gene (SLC6A4) region in autistic disorder. Kim SJ, Cox N, Courchesne R, Lord C, Corsello C, Akshoomoff N, Guter S, Leventhal BL, Courchesne E, Cook EH Jr, Mol Psychiatry 2002 7 278 288 10.1038/sj.mp.4001033 11920155 (Pubitemid 34280636)
18. Evidence of linkage between the serotonin transporter and autistic disorder. Cook EH Jr, Courchesne R, Lord C, Cox NJ, Yan S, Lincoln A, Haas R, Courchesne E, Leventhal BL, Mol Psychiatry 1997 2 247 250 10.1038/sj.mp.4000266 9152989 (Pubitemid 27217689)
19. How the serotonin story is being rewritten by new gene-based discoveries principally related to SLC6A4, the serotonin transporter gene, which functions to influence all cellular serotonin systems. Murphy DL, Fox MA, Timpano KR, Moya PR, Ren-Patterson R, Andrews AM, Holmes A, Lesch KP, Wendland JR, Neuropharmacology 2008 55 932 960 10.1016/j.neuropharm.2008.08.034 18824000
20. Enhanced activity of human serotonin transporter variants associated with autism. Prasad HC, Steiner JA, Sutcliffe JS, Blakely RD, Philos Trans R Soc Lond B Biol Sci 2009 364 163 173 10.1098/rstb.2008.0143 18957375
21. Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-activated protein kinase. Prasad HC, Zhu CB, McCauley JL, Samuvel DJ, Ramamoorthy S, Shelton RC, Hewlett WA, Sutcliffe JS, Blakely RD, Proc Natl Acad Sci U S A 2005 102 11545 11550 10.1073/pnas. 0501432102 16055563 (Pubitemid 41153856)
22. A large-scale screen for coding variants in SERT/SLC6A4 in autism spectrum disorders. Sakurai T, Reichert J, Hoffman EJ, Cai G, Jones HB, Faham M, Buxbaum JD, Autism Res 2008 1 251 257 10.1002/aur.30 19360675
23. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Veenstra-VanderWeele J, Muller CL, Iwamoto H, Sauer JE, Owens WA, Shah CR, Cohen J, Mannangatti P, Jessen T, Thompson BJ, Ye R, Kerr TM, Carneiro AM, Crawley JN, Sanders-Bush E, McMahon DG, Ramamoorthy S, Daws LC, Sutcliffe JS, Blakely RD, Proc Natl Acad Sci U S A 2012 109 5469 5474 10.1073/pnas.1112345109 22431635
24. Functional coding variation in recombinant inbred mouse lines reveals multiple serotonin transporter-associated phenotypes. Carneiro AM, Airey DC, Thompson B, Zhu CB, Lu L, Chesler EJ, Erikson KM, Blakely RD, Proc Natl Acad Sci U S A 2009 106 2047 2052 10.1073/pnas.0809449106 19179283
25. Modeling rare gene variation to gain insight into the oldest biomarker in autism: construction of the serotonin transporter Gly56Ala knock-in mouse. Veenstra-Vanderweele J, Jessen TN, Thompson BJ, Carter M, Prasad HC, Steiner JA, Sutcliffe JS, Blakely RD, J Neurodev Disord 2009 1 158 171 10.1007/s11689-009- 9020-0 19960097
26. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. Yang M, Bozdagi O, Scattoni ML, Wohr M, Roullet FI, Katz AM, Abrams DN, Kalikhman D, Simon H, Woldeyohannes L, Zhang JY, Harris MJ, Saxena R, Silverman JL, Buxbaum JD, Crawley JN, J Neurosci 2012 32 6525 6541 10.1523/JNEUROSCI.6107-11.2012 22573675
27. Autism-relevant social abnormalities and cognitive deficits in engrailed-2 knockout mice. Brielmaier J, Matteson PG, Silverman JL, Senerth JM, Kelly S, Genestine M, Millonig JH, DiCicco-Bloom E, Crawley JN, PLoS One 2012 7 40914 10.1371/journal.pone.0040914 22829897
28. Neurobehavioral phenotyping of G(alphaq) knockout mice reveals impairments in motor functions and spatial working memory without changes in anxiety or behavioral despair. Frederick AL, Saborido TP, Stanwood GD, Front Behav Neurosci 2012 6 29 22723772
29. Deficits in acetylcholine homeostasis, receptors and behaviors in choline transporter heterozygous mice. Bazalakova MH, Wright J, Schneble EJ, McDonald MP, Heilman CJ, Levey AI, Blakely RD, Genes Brain Behav 2007 6 411 424 10.1111/j.1601-183X.2006.00269.x 17010154 (Pubitemid 47024956)
30. Automated three-chambered social approach task for mice. Yang M, Silverman JL, Crawley JN, Curr Protoc Neurosci 2011 Chapter 8: Unit 8.26
31. Haploinsufficiency of the E3 ubiquitin ligase C-terminus of heat shock cognate 70 interacting protein (CHIP) produces specific behavioral impairments. McLaughlin B, Buendia MA, Saborido TP, Palubinsky AM, Stankowski JN, Stanwood GD, PLoS One 2012 7 36340 10.1371/journal.pone.0036340 22606257
32. Quantitative assessment of tactile allodynia in the rat paw. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL, J Neurosci Methods 1994 53 55 63 10.1016/0165-0270(94)90144-9 7990513 (Pubitemid 24238751)
33. Determination of serotonin in whole blood, platelet-rich plasma, platelet-poor plasma and plasma ultrafiltrate. Anderson GM, Feibel FC, Cohen DJ, Life Sci 1987 40 1063 1070 10.1016/0024-3205(87)90568-6 3821372 (Pubitemid 17025624)
34. Transgenic elimination of high-affinity antidepressant and cocaine sensitivity in the presynaptic serotonin transporter. Thompson BJ, Jessen T, Henry LK, Field JR, Gamble KL, Gresch PJ, Carneiro AM, Horton RE, Chisnell PJ, Belova Y, McMahon DG, Daws LC, Blakely RD, Proc Natl Acad Sci U S A 2011 108 3785 3790 10.1073/pnas.1011920108 21282638
35. Ontogeny of brain and blood serotonin levels in 5-HT receptor knockout mice: potential relevance to the neurobiology of autism. Janusonis S, Anderson GM, Shifrovich I, Rakic P, J Neurochem 2006 99 1019 1031 10.1111/j.1471-4159. 2006.04150.x 16981893 (Pubitemid 44583458)
36. A new set of BXD recombinant inbred lines from advanced intercross populations in mice. Peirce JL, Lu L, Gu J, Silver LM, Williams RW, BMC Genet 2004 5 7 15117419
37. Going with the flow: trafficking-dependent and -independent regulation of serotonin transport. Steiner JA, Carneiro AM, Blakely RD, Traffic 2008 9 1393 1402 10.1111/j.1600-0854.2008.00757.x 18445122
38. Regulation of monoamine transporters: Role of transporter phosphorylation. Ramamoorthy S, Shippenberg TS, Jayanthi LD, Pharmacol Ther 2011 129 220 238 10.1016/j.pharmthera.2010.09.009 20951731
39. Modifying behavioral phenotypes in Fmr1KO mice: genetic background differences reveal autistic-like responses. Spencer CM, Alekseyenko O, Hamilton SM, Thomas AM, Serysheva E, Yuva-Paylor LA, Paylor R, Autism Res 2011 4 40 56 10.1002/aur.168 21268289
40. Minimal aberrant behavioral phenotypes o f neuroligin-3 R451C knockin mice. Chadman KK, Gong S, Scattoni ML, Boltuck SE, Gandhy SU, Heintz N, Crawley JN, Autism Res 2008 1 147 158 10.1002/aur.22 19360662
41. Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Etherton M, Foldy C, Sharma M, Tabuchi K, Liu X, Shamloo M, Malenka RC, Sudhof TC, Proc Natl Acad Sci U S A 2011 108 13764 13769 10.1073/pnas.1111093108 21808020
42. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM, Sudhof TC, Science 2007 318 71 76 10.1126/science.1146221 17823315 (Pubitemid 47538032)
43. Abnormal anxiety-related behavior in serotonin transporter null mutant mice: the influence of genetic background. Holmes A, Lit Q, Murphy DL, Gold E, Crawley JN, Genes Brain Behav 2003 2 365 380 10.1046/j.1601-1848.2003.00050.x 14653308 (Pubitemid 37463201)
44. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Spencer CM, Alekseyenko O, Serysheva E, Yuva-Paylor LA, Paylor R, Genes Brain Behav 2005 4 420 430 10.1111/j.1601-183X.2005.00123.x 16176388 (Pubitemid 41428518)
45. Mice with Truncated MeCP2 Recapitulate Many Rett Syndrome Features and Display Hyperacetylation of Histone H3. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, Armstrong D, Paylor R, Zoghbi H, Neuron 2002 35 243 10.1016/S0896-6273(02)00768-7 12160743 (Pubitemid 34876728)
46. A triplet repeat expansion genetic mouse model of infantile spasms syndrome, Arx(GCG)10+7, with interneuronopathy, spasms in infancy, persistent seizures, and adult cognitive and behavioral impairment. Price MG, Yoo JW, Burgess DL, Deng F, Hrachovy RA, Frost JD Jr, Noebels JL, J Neurosci 2009 29 8752 8763 10.1523/JNEUROSCI.0915-09.2009 19587282
47. Abnormal social behaviors and altered gene expression rates in a mouse model for Potocki-Lupski syndrome. Molina J, Carmona-Mora P, Chrast J, Krall PM, Canales CP, Lupski JR, Reymond A, Walz K, Hum Mol Genet 2008 17 2486 2495 10.1093/hmg/ddn148 18469339
48. Behavioral and serotonergic response changes in the Dhcr7-HET mouse model of Smith-Lemli-Opitz syndrome. Korade Z, Folkes OM, Harrison FE, Pharmacol Biochem Behav 2013 106 101 108 23541496
49. Crawley JN, What's Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice Hoboken, NJ: John Wiley & Sons, Inc. 2 2007
50. Zic2 hypomorphic mutant mice as a schizophrenia model and ZIC2 mutations identified in schizophrenia patients. Hatayama M, Ishiguro A, Iwayama Y, Takashima N, Sakoori K, Toyota T, Nozaki Y, Odaka YS, Yamada K, Yoshikawa T, Aruga J, Sci Rep 2011 1 16 22355535
51. Autism-like socio-communicative deficits and stereotypies in mice lacking heparan sulfate. Irie F, Badie-Mahdavi H, Yamaguchi Y, Proc Natl Acad Sci U S A 2012 109 5052 5056 10.1073/pnas.1117881109 22411800
52. Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. Semple BD, Canchola SA, Noble-Haeusslein LJ, J Neurotrauma 2012 29 2672 2683 10.1089/neu.2012.2595 22888909
53. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Moretti P, Bouwknecht JA, Teague R, Paylor R, Zoghbi HY, Hum Mol Genet 2005 14 205 220 15548546
54. Genetic progressive hearing loss in the C57-b16 mouse. Relation of behavioral responses to chochlear anatomy. Mikaelian DO, Warfield D, Norris O, Acta Otolaryngol 1974 77 327 334 10.3109/00016487409124632 4835632
55. Autism before diagnosis: crying, feeding and sleeping problems in the first two years of life. Barnevik Olsson M, Hoglund Carlsson L, Westerlund J, Gillberg C, Fernell E, Acta Paediatr 2013 102 635 9 10.1111/apa.12229 23480473
56. Temperament and its relationship to autistic symptoms in a high-risk infant sib cohort. Garon N, Bryson SE, Zwaigenbaum L, Smith IM, Brian J, Roberts W, Szatmari P, J Abnorm Child Psychol 2009 37 59 78 10.1007/s10802-008-9258-0 18704676
57. Increased expression of the 5-HT transporter confers a low-anxiety phenotype linked to decreased 5-HT transmission. Jennings KA, Loder MK, Sheward WJ, Pei Q, Deacon RM, Benson MA, Olverman HJ, Hastie ND, Harmar AJ, Shen S, Sharp T, J Neurosci 2006 26 8955 8964 10.1523/JNEUROSCI.5356-05.2006 16943551 (Pubitemid 44319384)
58. Opposing alterations in anxiety and species-typical behaviours in serotonin transporter overexpressor and knockout mice. Line SJ, Barkus C, Coyle C, Jennings KA, Deacon RM, Lesch KP, Sharp T, Bannerman DM, Eur Neuropsychopharmacol 2011 21 108 116 10.1016/j.euroneuro.2010.08.005 20863670
59. Targeting the murine serotonin transporter: insights into human neurobiology. Murphy DL, Lesch KP, Nat Rev Neurosci 2008 9 85 96 18209729 (Pubitemid 351164876)
60. Modifications of the serotonergic system in mice lacking serotonin transporters: an in vivo electrophysiological study. Gobbi G, Murphy DL, Lesch K, Blier P, J Pharmacol Exp Ther 2001 296 987 995 11181933 (Pubitemid 32187374)
61. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Lira A, Zhou M, Castanon N, Ansorge MS, Gordon JA, Francis JH, Bradley-Moore M, Lira J, Underwood MD, Arango V, Kung HF, Hofer MA, Hen R, Gingrich JA, Biol Psychiatry 2003 54 960 971 10.1016/S0006-3223(03)00696-6 14625138 (Pubitemid 37415032)
62. Non-linear relationship between 5-HT transporter gene expression and frequency sensitivity of 5-HT signals. Jennings KA, Lesch KP, Sharp T, Cragg SJ, J Neurochem 2010 115 965 973 10.1111/j.1471-4159.2010.07001.x 20854367
63. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY, Nat Genet 1999 23 185 188 10.1038/13810 10508514 (Pubitemid 29455390)
64. The MECP2 duplication syndrome. Ramocki MB, Tavyev YJ, Peters SU, Am J Med Genet A 2010 152A 1079 1088 10.1002/ajmg.a.33184 20425814
65. Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Van Esch H, Bauters M, Ignatius J, Jansen M, Raynaud M, Hollanders K, Lugtenberg D, Bienvenu T, Jensen LR, Gecz J, Moraine C, Marynen P, Fryns JP, Froyen G, Am J Hum Genet 2005 77 442 453 10.1086/444549 16080119 (Pubitemid 41192650)
66. Association between microdeletion and microduplication at 16p11.2 and autism. Weiss LA, Shen Y, Korn JM, Arking DE, Miller DT, Fossdal R, Saemundsen E, Stefansson H, Ferreira MA, Green T, Platt OS, Ruderfer DM, Walsh CA, Altshuler D, Chakravarti A, Tanzi RE, Stefansson K, Santangelo SL, Gusella JF, Sklar P, Wu BL, Daly MJ, Autism Consortium, N Engl J Med 2008 358 667 675 10.1056/NEJMoa075974 18184952 (Pubitemid 351240746)
67. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, Fauchereau F, Nygren G, Rastam M, Gillberg IC, Anckarsater H, Sponheim E, Goubran-Botros H, Delorme R, Chabane N, Mouren-Simeoni MC, de Mas P, Bieth E, Rogé B, Héron D, Burglen L, Gillberg C, Leboyer M, Bourgeron T, Nat Genet 2007 39 25 27 10.1038/ng1933 17173049 (Pubitemid 46026497)