Variants in SNAP25 are targets of natural selection and influence verbal performances in women

Cellular and Molecular Life Sciences

Volumn 69, Issue 10, 2012, Pages 1705-1715

  Cagliani, Rachele ^a   Riva, Stefania ^a,b   Marino, Cecilia ^a   Fumagalli, Matteo ^a   D'Angelo, Maria Grazia ^a   Riva, Valentina ^a   Comi, Giacomo P ^b   Pozzoli, Uberto ^a   Forni, Diego ^a   Cáceres, Mario ^c,d,e,f   Bresolin, Nereo ^a,b   Clerici, Mario ^a,g   Sironi, Manuela ^a  

^a SCIENTIFIC INSTITUTE   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f UNIVERSITY OF MILAN   (Italy)

^g IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

Balancing selection; Intelligence quotient; SNAP25; Verbal performances

Indexed keywords

ARTICLE; CHILD; COGNITION; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; INTRON; MALE; NORMAL HUMAN; PHYLOGENY; POPULATION GENETICS; POPULATION RESEARCH; PRESCHOOL CHILD; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SNAP25 GENE; VERBAL BEHAVIOR;

CHILD; CHILD, PRESCHOOL; COGNITION; COHORT STUDIES; EVOLUTION, MOLECULAR; FEMALE; GENETICS, POPULATION; GENOTYPE; HUMANS; INTELLIGENCE; ITALY; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; VOCABULARY; WOMEN;

EID: 84863586615     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0896-y     Document Type: Article

References (65)

1. 1000 Genomes Project Consortium, Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Durbin RM, Gibbs RA, Hurles ME, McVean GA (2010) A map of human genome vari-ation from population-scale sequencing. Nature 467:1061-1073
2. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37-48 (Pubitemid 29024937)
3. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. doi: 10.1093/bioinformatics/bth457 (Pubitemid 40202029)
4. Bishop DV (2009) Genes, cognition, and communication: insights from neurodevelopmental disorders. Ann NY Acad Sci 1156:1-18
5. Bruno C, Minetti C (2004) Congenital myopathies. Curr Neurol Neurosci Rep 4:68-73 (Pubitemid 38899055)
6. Bushby K (2009) Diagnosis and management of the limb girdle muscular dystrophies. Pract Neurol 9:314-323
7. Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:e64
8. Condliffe SB, Corradini I, Pozzi D, Verderio C, Matteoli M (2010) Endogenous SNAP-25 regulates native voltage-gated calcium channels in glutamatergic neurons. J Biol Chem 285:24968-24976
9. Corradini I, Verderio C, Sala M, Wilson MC, Matteoli M (2009) SNAP-25 in neuropsychiatric disorders. Ann NY Acad Sci 1152:93-99
10. Downes EC, Robson J, Grailly E, Abdel-All Z, Xuereb J, Brayne C, Holland A, Honer WG, Mukaetova-Ladinska EB (2008) Loss of synaptophysin and synaptosomal-associated protein 25-kDa (SNAP-25) in elderly Down syndrome individuals. Neuropathol Appl Neurobiol 34:12-22
11. Duret L, Galtier N (2009) Biased gene conversion and the evo-lution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10:285-311
12. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human mem-ory and hippocampal function. Cell 112:257-269 (Pubitemid 36144114)
13. Etain B, Dumaine A, Mathieu F, Chevalier F, Henry C, Kahn JP, Deshommes J, Bellivier F, Leboyer M, Jamain S (2010) A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol Psychiatry 15:748-755
14. Evans PD, Gilbert SL, Mekel-Bobrov N, Vallender EJ, Anderson JR, Vaez-Azizi LM, Tishkoff SA, Hudson RR, Lahn BT (2005) Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309:1717-1720 (Pubitemid 41285939)
15. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693-709
16. Fumagalli M, Cagliani R, Pozzoli U, Riva S, Comi GP, Menozzi G, Bresolin N, Sironi M (2009) Widespread balancing selection and pathogen-driven selection at blood group antigen genes. Genome Res 19:199-212
17. Ghezzo A, Guerini FR, Bolognesi E, Matteoli M, Manca S, Sotgiu S, Bejor M, Clerici M, Chiappedi M (2009) Neuropsy-cological gender differences in healthy individuals and in pediatric neurodevelopmental disorders. A role for SNAP-25. Med Hypotheses 73:978-980
18. Glazko GV, Nei M (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20:424-434 (Pubitemid 36427177)
19. Gosso MF, de Geus EJ, Polderman TJ, Boomsma DI, Heutink P, Posthuma D (2008) Common variants underlying cognitive ability: further evidence for association between the SNAP-25 gene and cognition using a family-based study in two indepen-dent Dutch cohorts. Genes Brain Behav 7:355-364 (Pubitemid 351490240)
20. Gosso MF, de Geus EJ, van Belzen MJ, Polderman TJ, Heutink P, Boomsma DI, Posthuma D (2006) The SNAP-25 gene is asso-ciated with cognitive ability: evidence from a family-based study in two independent Dutch cohorts. Mol Psychiatry 11:878-886 (Pubitemid 44299109)
21. Griffiths RC, Tavare S (1995) Unrooted genealogical tree proba-bilities in the infinitely-many-sites model. Math Biosci 127:77-98
22. Griffiths RC, Tavare S (1994) Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci 344:403-410
23. Guerini FR, Bolognesi E, Chiappedi M, Manca S, Ghezzo A, Agliardi C, Sotgiu S, Usai S, Matteoli M and Clerici M (2011) SNAP-25 single nucleotide polymorphisms are associated with hyperactivity in autism spectrum disorders (in press)
24. Haworth CM, Wright MJ, Luciano M, Martin NG, de Geus EJ, van Beijsterveldt CE, Bartels M, Posthuma D, Boomsma DI, Davis OS, Kovas Y, Corley RP, Defries JC, Hewitt JK, Olson RK, Rhea SA, Wadsworth SJ, Iacono WG, McGue M, Thompson LA, Hart SA, Petrill SA, Lubinski D, Plomin R (2010) The heritability of general cognitive ability increases linearly from childhood to young adulthood. Mol Psychiatry 15:1112-1120
25. Haygood R, Fedrigo O, Hanson B, Yokoyama KD, Wray GA (2007) Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolu-tion. Nat Genet 39:1140-1144 (Pubitemid 47340653)
26. Jacobsson G, Razani H, Ogren SO, Meister B (1998) Estrogen down-regulates mRNA encoding the exocytotic protein SNAP-25 in the rat pituitary gland. J Neuroendocrinol 10:157-163 (Pubitemid 28121155)
27. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
28. Lustig RH, Hua P, Wilson MC, Federoff HJ (1993) Ontogeny, sex dimorphism, and neonatal sex hormone determination of synapse-associated messenger RNAs in rat brain. Brain Res Mol Brain Res 20:101-110
29. Marshall C, Hitman GA, Partridge CJ, Clark A, Ma H, Shearer TR, Turner MD (2005) Evidence that an isoform of calpain-10 is a regulator of exocytosis in pancreatic beta-cells. Mol Endocrinol 19:213-224 (Pubitemid 40065971)
30. Mekel-Bobrov N, Gilbert SL, Evans PD, Vallender EJ, Anderson JR, Hudson RR, Tishkoff SA, Lahn BT (2005) Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 309:1720-1722 (Pubitemid 41285940)
31. Mekel-Bobrov N, Posthuma D, Gilbert SL, Lind P, Gosso MF, Luciano M, Harris SE, Bates TC, Polderman TJ, Whalley LJ, Fox H, Starr JM, Evans PD, Montgomery GW, Fernandes C, Heutink P, Martin NG, Boomsma DI, Deary IJ, Wright MJ, de Geus EJ, Lahn BT (2007) The ongoing adaptive evolution of ASPM and Microcephalin is not explained by increased intelligence. Hum Mol Genet 16:600-608 (Pubitemid 46585662)
32. Munsat TL, Davies KE (1992) International SMA consortium meeting. (26-28 June 1992, Bonn, Germany). Neuromuscu1 Disord 2:423-428 (Pubitemid 23104723)
33. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Nat1 Acad Sci USA 76:5269-5273 (Pubitemid 10236121)
34. Padberg GW, Lunt PW, Koch M, Fardeau M (1991) Diagnostic criteria for facioscapulohumeral muscular dystrophy. Neuromuscul Disord 1:231-234
35. Parman Y (2007) Hereditary neuropathies. Curr Opin Neuro1 20:542-547 (Pubitemid 47462283)
36. Petryshen TL, Sabeti PC, Aldinger KA, Fry B, Fan JB, Schaffner SF, Waggoner SG, Tahl AR, Sklar P (2010) Population genetic study of the brain-derived neurotrophic factor (BDNF) gene. Mol Psychiatry 15:810-815
37. Pinker S (2003) Language as an adaptation to the cognitive niche. In: Christiansen M, Kirby S (eds) Language evolution: states of the art. Oxford University Press, New York
38. Pinker S (2010) Colloquium paper: the cognitive niche: coevo-lution of intelligence, sociality, and language. Proc Nat1 Acad Sci USA 107(Suppl 2):8993-8999
39. Pozzi D, Condliffe S, Bozzi Y, Chikhladze M, GrumeHi C, Proux-Gillardeaux V, Takahashi M, Franceschetti S, Verderio C, Matteoli M (2008) Activity-dependent phosphorylation of Serl87 is required for SNAP-25-negative modulation of neuronal vol·t-age-gated calcium channels. Proc Nat1 Acad Sci USA 105:323-328
40. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575 (Pubitemid 47330214)
41. R Development Core Team (2008) R: a language and environ-ment for statistical computing. Vienna, Austria
42. Raber J, Mehta PP, Kreifeldt M, Parsons LH, Weiss F, Bloom FE, Wilson MC (1997) Coloboma hyperactive mutant mice exhibit regional and transmitter-specific deficits in neurotransmission. J Neurochem 68:176-186 (Pubitemid 26427306)
43. Romeo S, SentineHi F, Cavallo MG, Leonetti F, FaUarino M, Mariotti S, Baroni MG (2008) Search for genetic variants of the SYNTAXIN 1A (STXlA) gene: the -352 A > T variant in the STXlA promoter associates with impaired glucose metabolism in an Italian obese population. Int J Obes (Lond) 32:413-420 (Pubitemid 351414813)
44. Schaffner SF, Foo C, Gabriel S, Reich D, Daly MJ, Altshuler D (2005) Calibrating a coalescent simulation of human genome sequence variation. Genome Res 15:1576-1583 (Pubitemid 41545011)
45. Soderqvist S, McNab F, Peyrard-Janvid M, Matsson H, Humphreys K, Kere J, Klingberg T (2010) The SNAP25 gene is linked to working memory capacity and maturation of the pos-terior cingulate cortex during childhood. Biol Psychiatry 68:1120-1125
46. Sorensen JB, Nagy G, Varoqueaux F, Nehring RB, Brose N, Wilson MC, Neher E (2003) Differential control of the releasable vesicle pooIs by SNAP-25 splice variants and SNAP-23. Cell 114:75-86 (Pubitemid 36859842)
47. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputa-tion. Am J Hum Genet 76:449-162
48. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978-989 (Pubitemid 32289743)
49. Tajima F (1989) Statistical method for testing the neutral muta-tion hypothesis by DNA polymorphism. Genetics 123:585-595 (Pubitemid 19274682)
50. Takahashi N, Hatakeyama H, Okado H, Noguchi J, Ohno M, Kasai H (2010) SNARE conformational changes that prepare vesicles for exocytosis. Cell Metab 12:19-29
51. Thornton K (2003) Libsequence: a C++ class library for evo-lutionary genetic analysis. Bioinformatics 19:2325-2327 (Pubitemid 37483994)
52. Tishkoff SA, VerreHi BC (2003) Patterns of human genetic diversity: implications for human evolutionary history and dis-ease. Annu Rev Genomics Hum Genet 4:293-340 (Pubitemid 37392927)
53. Torri F, Akelai A, Lupoli S, Sironi M, Amann-Zalcenstein D, FumagaHi M, Dal Fiume C, Ben-Asher E, Kanyas K, Cagliani R, Cozzi P, Trombetti G, Strik Lievers L, Salvi E, Orro A, Beck-mann JS, Lancet D, Kohn Y, Milanesi L, Ebstein RB, Lerer B, Macciardi F (2010) Fine mapping of AHI1 as a schizophrenia susceptibility gene: from association to evolutionary evidence. FASEB J 24:3066-3082
54. Tsunoda K, Sanke T, Nakagawa T, Furuta H, Nanjo K (2001) Single nucleotide polymorphism (D68D, T to C) in the syntaxin 1A gene correlates to age at onset and insulin requirement in Type ? diabetic patients. Diabetologia 44:2092-2097 (Pubitemid 33124056)
55. Turner MD, Cassell PG, Hitman GA (2005) Calpain-10: from genome search to function. Diabetes Metab Res Rev 21:505-514 (Pubitemid 41646010)
56. Vallender EJ (2008) Exploring the origins of the human brain through molecular evolution. Brain Behav Evol 72:168-177
57. Vander Molen J, Frisse LM, FuUerton SM, Qian Y, Del Bosque-Plata L, Hudson RR, Di Rienzo A (2005) Population genetics of CAPN10 and GPR35: implications for the evolution of type 2 diabetes variants. Am J Hum Genet 76:548-560 (Pubitemid 40432163)
58. Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, Coco S, Proux-Gillardeaux V, GaHi T, Rossetto O, Frassoni C, Matteoli M (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41:599-610 (Pubitemid 38253071)
59. Watterson GA (1975) On the number of segregating sites in genetical modeIs without recombination. Theor Popul Biol 7:256-276
60. Wechsler D (1989) WPPSI-R manual: Wechsler preschool and primary scale of intelligence-revised. The Psychological Corpo-ration, San Antonio, TX
61. Wechsler D (1981) Examiner's manual: Wechsler intelligence scale for children revised. Psychological Corporation, New York
62. Wechsler D (1981) The Psychometric Tradition. Dev Wechsler AduIt Intel Scale 6:82-85
63. Wigginton JE, Cutler DJ, Abecasis GR (2005) A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet 76:887-893 (Pubitemid 40563110)
64. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R (2007) Localizing recent adaptive evolution in the human genome. PLoS Genet 3:e90
65. Wright SI, Charlesworth B (2004) The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168:1071-1076 (Pubitemid 39491480)