The Interleukin 3 Gene (IL3) Contributes to Human Brain Volume Variation by Regulating Proliferation and Survival of Neural Progenitors

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Luo, Xiong jian ^a,b   Li, Ming ^a   Huang, Liang ^b,c   Nho, Kwangsik ^d,e   Deng, Min ^b   Chen, Qiang ^f   Weinberger, Daniel R ^f   Vasquez, Alejandro Arias ^g,h   Rijpkema, Mark ⁱ   Mattay, Venkata S ^f   Saykin, Andrew J ^d,e   Shen, Li ^d,e   Fernández, Guillén ^h,i   Franke, Barbara ^g,h   Chen, Jing chun ^j   Chen, Xiang ning ^j   Wang, Jin kai ^a   Xiao, Xiao ^a   Qi, Xue bin ^a   Xiang, Kun ^a   Peng, Ying Mei ^a   Cao, Xiang yu ^a   Li, Yi ^k   Shi, Xiao dong ^k   Gan, Lin ^b,l   Su, Bing ^a   more..

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c GANNAN MEDICAL UNIVERSITY   (China)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e REGENSTRIEF INSTITUTE   (United States)

^f NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^g RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^h RADBOUD UNIVERSITY   (Netherlands)

ⁱ RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^j VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^k QUJING NORMAL UNIVERSITY   (China)

^l HANGZHOU NORMAL UNIVERSITY   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD123 ANTIGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; INTERLEUKIN 3; TRANSCRIPTION FACTOR SP1;

ACSL 6 GENE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN SIZE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CHINESE; CONTROLLED STUDY; ETHNIC GROUP; EUROPEAN; FEMALE; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN CELL; IL3 GENE; LOC 728637 GENE; MALE; NEOCORTEX; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PDC GEF2 GENE; POPULATION RESEARCH; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; SPEC2 GENE;

ANIMALS; BRAIN; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-3; INTERLEUKIN-3 RECEPTOR ALPHA SUBUNIT; MALE; MICE; NEURAL STEM CELLS; ORGAN SIZE; POLYMORPHISM, GENETIC; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, ESTROGEN; RECEPTORS, IMMUNOLOGIC; SEX CHARACTERISTICS; TUMOR MARKERS, BIOLOGICAL;

EID: 84870600462     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050375     Document Type: Article

References (81)

1. Rushton JP, (1992) Cranial Capacity Related to Sex, Rank, and Race in a stratified Random Sample of 6,325 U.S. Military personnel. Intelligence 16: 401-413.
2. Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen VP, et al. (2001) Genetic influences on brain structure. Nat Neurosci 4: 1253-1258.
3. Posthuma D, De Geus EJ, Baare WF, Hulshoff Pol HE, Kahn RS, et al. (2002) The association between brain volume and intelligence is of genetic origin. Nat Neurosci 5: 83-84.
4. Posthuma D, Baare WF, Hulshoff Pol HE, Kahn RS, Boomsma DI, et al. (2003) Genetic correlations between brain volumes and the WAIS-III dimensions of verbal comprehension, working memory, perceptual organization, and processing speed. Twin Res 6: 131-139.
5. Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA, (2006) Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br J Psychiatry 188: 510-518.
6. Valera EM, Faraone SV, Murray KE, Seidman LJ, (2007) Meta-analysis of structural imaging findings in attention-deficit/hyperactivity disorder. Biol Psychiatry 61: 1361-1369.
7. Kumar A, Markandaya M, Girimaji SC, (2002) Primary microcephaly: microcephalin and ASPM determine the size of the human brain. J Biosci 27: 629-632.
8. Woods CG, Bond J, Enard W, (2005) Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am J Hum Genet 76: 717-728.
9. Wang JK, Li Y, Su B, (2008) A common SNP of MCPH1 is associated with cranial volume variation in Chinese population. Hum Mol Genet 17: 1329-1335.
10. Rimol LM, Agartz I, Djurovic S, Brown AA, Roddey JC, et al. (2009) Sex-dependent association of common variants of microcephaly genes with brain structure. Proc Natl Acad Sci U S A 107: 384-388.
11. Taal HR, St Pourcain B, Thiering E, Das S, Mook-Kanamori DO, et al. (2012) Common variants at 12q15 and 12q24 are associated with infant head circumference. Nat Genet 44: 532-538.
12. Stein JL, Medland SE, Vasquez AA, Hibar DP, Senstad RE, et al. (2012) Identification of common variants associated with human hippocampal and intracranial volumes. Nat Genet 44: 552-561.
13. Ikram MA, Fornage M, Smith AV, Seshadri S, Schmidt R, et al. (2012) Common variants at 6q22 and 17q21 are associated with intracranial volume. Nat Genet 44: 539-544.
14. Honea R, Crow TJ, Passingham D, Mackay CE, (2005) Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry 162: 2233-2245.
15. Cahn W, Hulshoff Pol HE, Lems EB, van Haren NE, Schnack HG, et al. (2002) Brain volume changes in first-episode schizophrenia: a 1-year follow-up study. Arch Gen Psychiatry 59: 1002-1010.
16. Lewis DA, Levitt P, (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25: 409-432.
17. McCarthy SE, Makarov V, Kirov G, Addington AM, McClellan J, et al. (2009) Microduplications of 16p11.2 are associated with schizophrenia. Nat Genet 41: 1223-1227.
18. O'Donovan MC, Craddock N, Norton N, Williams H, Peirce T, et al. (2008) Identification of loci associated with schizophrenia by genome-wide association and follow-up. Nat Genet 40: 1053-1055.
19. Purcell SM, Wray NR, Stone JL, Visscher PM, O'Donovan MC, et al. (2009) Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460: 748-752.
20. Shi J, Levinson DF, Duan J, Sanders AR, Zheng Y, et al. (2009) Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460: 753-757.
21. Stefansson H, Ophoff RA, Steinberg S, Andreassen OA, Cichon S, et al. (2009) Common variants conferring risk of schizophrenia. Nature 460: 744-747.
22. Xu B, Roos JL, Levy S, van Rensburg EJ, Gogos JA, et al. (2008) Strong association of de novo copy number mutations with sporadic schizophrenia. Nat Genet 40: 880-885.
23. Fatemi SH, Folsom TD, (2009) The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 35: 528-548.
24. Mao Y, Ge X, Frank CL, Madison JM, Koehler AN, et al. (2009) Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136: 1017-1031.
25. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, et al. (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130: 1146-1158.
26. Sherrington R, Brynjolfsson J, Petursson H, Potter M, Dudleston K, et al. (1988) Localization of a susceptibility locus for schizophrenia on chromosome 5. Nature 336: 164-167.
27. Bassett AS, McGillivray BC, Jones BD, Pantzar JT, (1988) Partial trisomy chromosome 5 cosegregating with schizophrenia. Lancet 1: 799-801.
28. Paunio T, Ekelund J, Varilo T, Parker A, Hovatta I, et al. (2001) Genome-wide scan in a nationwide study sample of schizophrenia families in Finland reveals susceptibility loci on chromosomes 2q and 5q. Human Molecular Genetics 10: 3037-3048.
29. Straub RE, MacLean CJ, O'Neill FA, Walsh D, Kendler KS, (1997) Support for a possible schizophrenia vulnerability locus in region 5q22-31 in Irish families. Molecular Psychiatry 2: 148-155.
30. Schwab SG, Eckstein GN, Hallmayer J, Lerer B, Albus M, et al. (1997) Evidence suggestive of a locus on chromosome 5q31 contributing to susceptibility for schizophrenia in German and Israeli families by multipoint affected sib-pair linkage analysis. Molecular Psychiatry 2: 156-160.
31. Camp NJ, Neuhausen SL, Tiobech J, Polloi A, Coon H, et al. (2001) Genomewide multipoint linkage analysis of seven extended Palauan pedigrees with schizophrenia, by a Markov-chain Monte Carlo method. American Journal of Human Genetics 69: 1278-1289.
32. Pimm J, McQuillin A, Thirumalai S, Lawrence J, Quested D, et al. (2005) The Epsin 4 gene on chromosome 5q, which encodes the clathrin-associated protein enthoprotin, is involved in the genetic susceptibility to schizophrenia. American Journal of Human Genetics 76: 902-907.
33. Chen X, Wang X, Hossain S, O'Neill FA, Walsh D, et al. (2006) Haplotypes spanning SPEC2, PDZ-GEF2 and ACSL6 genes are associated with schizophrenia. Human Molecular Genetics 15: 3329-3342.
34. Chen X, Wang X, Hossain S, O'Neill FA, Walsh D, et al. (2007) Interleukin 3 and schizophrenia: the impact of sex and family history. Molecular Psychiatry 12: 273-282.
35. Luo XJ, Diao HB, Wang JK, Zhang H, Zhao ZM, et al. (2008) Association of haplotypes spanning PDZ-GEF2, LOC728637 and ACSL6 with schizophrenia in Han Chinese. Journal of Medical Genetics 45: 818-826.
36. Jorgensen JB, Paridon E, Quaade F, (1961) The correlation between external cranial volume and brain volume. Am J Phys Anthropol 19: 317-320.
37. Ricard AS, Desbarats P, Laurentjoye M, Montaudon M, Caix P, et al. (2010) On two equations about brain volume, cranial capacity and age. Surg Radiol Anat 32: 989-995.
38. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81: 559-575.
39. Zhang J, Miller MI, Plachez C, Richards LJ, Yarowsky P, et al. (2005) Mapping postnatal mouse brain development with diffusion tensor microimaging. Neuroimage 26: 1042-1051.
40. Reddy EP, Korapati A, Chaturvedi P, Rane S, (2000) IL-3 signaling and the role of Src kinases, JAKs and STATs: a covert liaison unveiled. Oncogene 19: 2532-2547.
41. Cattaneo E, De Fraja C, Conti L, Reinach B, Bolis L, et al. (1996) Activation of the JAK/STAT pathway leads to proliferation of ST14A central nervous system progenitor cells. J Biol Chem 271: 23374-23379.
42. Kamegai M, Niijima K, Kunishita T, Nishizawa M, Ogawa M, et al. (1990) Interleukin 3 as a trophic factor for central cholinergic neurons in vitro and in vivo. Neuron 4: 429-436.
43. Wen TC, Tanaka J, Peng H, Desaki J, Matsuda S, et al. (1998) Interleukin 3 prevents delayed neuronal death in the hippocampal CA1 field. J Exp Med 188: 635-649.
44. Zambrano A, Otth C, Mujica L, Concha II, Maccioni RB, (2007) Interleukin-3 prevents neuronal death induced by amyloid peptide. BMC Neurosci 8: 82.
45. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, et al. (1995) Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270: 1491-1494.
46. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, et al. (2001) Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 276: 9817-9824.
47. Dean B, (2009) Is schizophrenia the price of human central nervous system complexity? Aust N Z J Psychiatry 43: 13-24.
48. Lewis CM, Levinson DF, Wise LH, DeLisi LE, Straub RE, et al. (2003) Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: Schizophrenia. Am J Hum Genet 73: 34-48.
49. Potvin S, Stip E, Sepehry AA, Gendron A, Bah R, et al. (2008) Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol Psychiatry 63: 801-808.
50. Tabira T, Chui DH, Fan JP, Shirabe T, Konishi Y, (1998) Interleukin-3 and interleukin-3 receptors in the brain. Ann N Y Acad Sci 840: 107-116.
51. Frei K, Bodmer S, Schwerdel C, Fontana A, (1985) Astrocytes of the brain synthesize interleukin 3-like factors. J Immunol 135: 4044-4047.
52. Frei K, Bodmer S, Schwerdel C, Fontana A, (1986) Astrocyte-derived interleukin 3 as a growth factor for microglia cells and peritoneal macrophages. J Immunol 137: 3521-3527.
53. Moroni SC, Rossi A, (1995) Enhanced survival and differentiation in vitro of different neuronal populations by some interleukins. Int J Dev Neurosci 13: 41-49.
54. Appel K, Buttini M, Sauter A, Gebicke-Haerter PJ, (1995) Cloning of rat interleukin-3 receptor beta-subunit from cultured microglia and its mRNA expression in vivo. J Neurosci 15: 5800-5809.
55. Cockayne DA, Bodine DM, Cline A, Nienhuis AW, Dunbar CE, (1994) Transgenic mice expressing antisense interleukin-3 RNA develop a B-cell lymphoproliferative syndrome or neurologic dysfunction. Blood 84: 2699-2710.
56. Chen X, Kendler KS, (2008) Interleukin 3 and schizophrenia. Am J Psychiatry 165: 13-14.
57. Edwards TL, Wang X, Chen Q, Wormly B, Riley B, et al. (2008) Interaction between interleukin 3 and dystrobrevin-binding protein 1 in schizophrenia. Schizophr Res 106: 208-217.
58. Lencz T, Morgan TV, Athanasiou M, Dain B, Reed CR, et al. (2007) Converging evidence for a pseudoautosomal cytokine receptor gene locus in schizophrenia. Mol Psychiatry 12: 572-580.
59. Sun S, Wang F, Wei J, Cao LY, Wu GY, et al. (2008) Association between interleukin-3 receptor alpha polymorphism and schizophrenia in the Chinese population. Neurosci Lett 440: 35-37.
60. Chen Q, Wang X, O'Neill FA, Walsh D, Fanous A, et al. (2008) Association study of CSF2RB with schizophrenia in Irish family and case- control samples. Mol Psychiatry 13: 930-938.
61. Xiu MH, Chen S, Wang F, Cao LY, Qi LY, et al. (2008) Altered interleukin-3 serum levels in drug-naive and neuroleptic-treated schizophrenic patients. Schizophr Res 106: 369-370.
62. Saykin AJ, Shen L, Foroud TM, Potkin SG, Swaminathan S, et al. (2010) Alzheimer's Disease Neuroimaging Initiative biomarkers as quantitative phenotypes: Genetics core aims, progress, and plans. Alzheimers Dement 6: 265-273.
63. Goldman AL, Pezawas L, Mattay VS, Fischl B, Verchinski BA, et al. (2009) Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Arch Gen Psychiatry 66: 467-477.
64. Franke B, Vasquez AA, Veltman JA, Brunner HG, Rijpkema M, et al. (2010) Genetic variation in CACNA1C, a gene associated with bipolar disorder, influences brainstem rather than gray matter volume in healthy individuals. Biol Psychiatry 68: 586-588.
65. Manjunath KY, (2002) Estimation of cranial volume-an overview of methodologies. J Anat Soc India 51: 85-91.
66. Jack CR Jr, Bernstein MA, Fox NC, Thompson P, Alexander G, et al. (2008) The Alzheimer's Disease Neuroimaging Initiative (ADNI): MRI methods. J Magn Reson Imaging 27: 685-691.
67. Risacher SL, Saykin AJ, West JD, Shen L, Firpi HA, et al. (2009) Baseline MRI predictors of conversion from MCI to probable AD in the ADNI cohort. Curr Alzheimer Res 6: 347-361.
68. Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, et al. (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23: 724-738.
69. Goldman AL, Pezawas L, Mattay VS, Fischl B, Verchinski BA, et al. (2008) Heritability of brain morphology related to schizophrenia: a large-scale automated magnetic resonance imaging segmentation study. Biol Psychiatry 63: 475-483.
70. Bralten J, Arias-Vasquez A, Makkinje R, Veltman JA, Brunner HG, et al. (2011) Association of the Alzheimer's gene SORL1 with hippocampal volume in young, healthy adults. Am J Psychiatry 168: 1083-1089.
71. Ashburner J, Friston KJ, (2000) Voxel-based morphometry-the methods. Neuroimage 11: 805-821.
72. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, et al. (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14: 21-36.
73. Cuadra MB, Cammoun L, Butz T, Cuisenaire O, Thiran JP, (2005) Comparison and validation of tissue modelization and statistical classification methods in T1-weighted MR brain images. IEEE Trans Med Imaging 24: 1548-1565.
74. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2010) The UCSC Genome Browser database: update 2011. Nucleic Acids Res 39: D876-882.
75. Bajic VB, Tan SL, Chong A, Tang S, Strom A, et al. (2003) Dragon ERE Finder version 2: A tool for accurate detection and analysis of estrogen response elements in vertebrate genomes. Nucleic Acids Res 31: 3605-3607.
76. Rousset F, Raymond M, (1995) Testing heterozygote excess and deficiency. Genetics 140: 1413-1419.
77. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575.
78. Schaid DJ, Rowland CM, Tines DE, Jacobson RM, Poland GA, (2002) Score tests for association between traits and haplotypes when linkage phase is ambiguous. Am J Hum Genet 70: 425-434.
79. Barrett JC, Fry B, Maller J, Daly MJ, (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265.
80. Stephens M, Smith NJ, Donnelly P, (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68: 978-989.
81. Schneider A, Kruger C, Steigleder T, Weber D, Pitzer C, et al. (2005) The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest 115: 2083-2098.