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Review Article

The Role of Human-Specific Gene Duplications During Brain Development and Evolution

Pages 86-96 | Received 26 Feb 2013, Accepted 21 Mar 2013, Published online: 20 Jun 2013

REFERENCES

  • Alkan, C., Coe, B. P., & Eichler, E. E. (2011). Genome structural variation discovery and genotyping. Nat Rev Genet, 12, 363–376.
  • Allen, K. M., Gleeson, J. G., Bagrodia, S., Partington, M. W., MacMillan, J. C., Cerione, R. A., Mulley, J. C., & Walsh, C. A. (1998). PAK3 mutation in nonsyndromic X-linked mental retardation. Nat Genet, 20, 25–30.
  • Bacon, C., Endris, V., & Rappold, G. (2009). Dynamic expression of the Slit-Robo GTPase activating protein genes during development of the murine nervous system. J Comp Neurol, 513, 224–236.
  • Bailey, J. A., Gu, Z., Clark, R. A., Reinert, K., Samonte, R. V., Schwartz, S., Adams, M. D., Myers, E. W., Li, P. W., & Eichler, E. E. (2002). Recent segmental duplications in the human genome. Science, 297, 1003–1007.
  • Bailey, J. A., Yavor, A. M., Massa, H. F., Trask, B. J., & Eichler, E. E. (2001). Segmental duplications: Organization and impact within the current human genome project assembly. Genome Res, 11, 1005–1017.
  • Benavides-Piccione, R., Ballesteros-Yáñez, I., DeFelipe, J., & Yuste, R. (2002). Cortical area and species differences in dendritic spine morphology. J Neurocytol, 31, 337–346.
  • Bloodgood, B. L., & Sabatini, B. L. (2005). Neuronal activity regulates diffusion across the neck of dendritic spines. Science, 310, 866–869.
  • Boda, B., Alberi, S., Nikonenko, I., Node-Langlois, R., Jourdain, P., Moosmayer, M., Parisi-Jourdain, L., & Muller, D. (2004). The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J Neurosci, 24, 10816–10825.
  • Boda, B., Nikonenko, I., Alberi, S., & Muller, D. (2006). Central nervous system functions of PAK protein family: From spine morphogenesis to mental retardation. Mol Neurobiol, 34, 67–80.
  • Bourne, J., & Harris, K. M. (2007). Do thin spines learn to be mushroom spines that remember?Curr Opin Neurobiol, 17, 381–386.
  • Bourne, J. N., & Harris, K. M. (2008). Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci, 31, 47–67.
  • Britten, R. J. (2002). Divergence between samples of chimpanzee and human DNA sequences is 5%, counting indels. Proc Natl Acad Sci U S A, 99, 13633–13635.
  • Centonze, D., Grande, C., Saulle, E., Martin, A. B., Gubellini, P., Pavón, N., Pisani, A., Bernardi, G., Moratalla, R., & Calabresi, P. (2003). Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci, 23, 8506–8512.
  • Charrier, C., Joshi, K., Coutinho-Budd, J., Kim, J. E., Lambert, N., de Marchena, J., Jin, W. L., Vanderhaeghen, P., Ghosh, A., Sassa, T., & Polleux, F. (2012). Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell, 149, 923–935.
  • Chen, L. T., Gilman, A. G., & Kozasa, T. (1999). A candidate target for G protein action in brain. J Biol Chem, 274, 26931–26938.
  • Cheng, Z., Ventura, M., She, X., Khaitovich, P., Graves, T., Osoegawa, K., Church, D., DeJong, P., Wilson, R. K., Pääbo, S., Rocchi, M., & Eichler, E. E. (2005). A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature, 437, 88–93.
  • Chimpanzee Sequencing and Analysis Consortium. (2005). Initial sequence of the chimpanzee genome and comparison with the human genome. Nature, 437, 69–87.
  • Coutinho-Budd, J., Ghukasyan, V., Zylka, M. J., & Polleux, F. (2012). The F-BAR domains from srGAP1, srGAP2 and srGAP3 regulate membrane deformation differently. J Cell Sci, 125, 3390–3401.
  • Davoodi, J., Ghahremani, M. H., Es-Haghi, A., Mohammad-Gholi, A., & Mackenzie, A. (2010). Neuronal apoptosis inhibitory protein, NAIP, is an inhibitor of procaspase-9. Int J Biochem Cell Biol, 42, 958–964.
  • Dehay, C., & Kennedy, H. (2007). Cell-cycle control and cortical development. Nat Rev Neurosci, 8, 438–450.
  • Dennis, M. Y., Nuttle, X., Sudmant, P. H., Antonacci, F., Graves, T. A., Nefedov, M., Rosenfeld, J. A., Sajjadian, S., Malig, M., Kotkiewicz, H., Curry, C. J., Shafer, S., Shaffer, L. G., de Jong, P. J., Wilson, R. K., & Eichler, E. E. (2012). Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell, 149, 912–922.
  • Doggett, N. A., Xie, G., Meincke, L. J., Sutherland, R. D., Mundt, M. O., Berbari, N. S., Davy, B. E., Robinson, M. L., Rudd, M. K., Weber, J. L., Stallings, R. L., & Han, C. (2006). A 360-kb interchromosomal duplication of the human HYDIN locus. Genomics, 88, 762–771.
  • Dumas, L., Kim, Y. H., Karimpour-Fard, A., Cox, M., Hopkins, J., Pollack, J. R., & Sikela, J. M. (2007). Gene copy number variation spanning 60 million years of human and primate evolution. Genome Res, 17, 1266–1277.
  • Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., & Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature, 472, 51–56.
  • Elston, G. N., Benavides-Piccione, R., & DeFelipe, J. (2001). The pyramidal cell in cognition: A comparative study in human and monkey. J Neurosci, 21, RC163.
  • Endris, V., Wogatzky, B., Leimer, U., Bartsch, D., Zatyka, M., Latif, F., Maher, E. R., Tariverdian, G., Kirsch, S., Karch, D., & Rappold, G. A. (2002). The novel Rho-GTPase activating gene MEGAP/ srGAP3 has a putative role in severe mental retardation. Proc Natl Acad Sci U S A, 99, 11754–11759.
  • Fortna, A., Kim, Y., MacLaren, E., Marshall, K., Hahn, G., Meltesen, L., Brenton, M., Hink, R., Burgers, S., Hernandez-Boussard, T., Karimpour-Fard, A., Glueck, D., McGavran, L., Berry, R., Pollack, J., & Sikela, J. M. (2004). Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biol, 2, e207.
  • Frost, A., Unger, V. M., & De Camilli, P. (2009). The BAR domain superfamily: Membrane-molding macromolecules. Cell, 137, 191–196.
  • Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., Gaillard, A., & Vanderhaeghen, P. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature, 455, 351–357.
  • Guerrier, S., Coutinho-Budd, J., Sassa, T., Gresset, A., Jordan, N. V., Chen, K., Jin, W. L., Frost, A., & Polleux, F. (2009). The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell, 138, 990–1004.
  • Gunbin, K. V., & Ruvinsky, A. (2013). Evolution of general transcription factors. J Mol Evol, 76, 28–47.
  • Hamilton, G., & Gillingwater, T. H. (2013). Spinal muscular atrophy: Going beyond the motor neuron. Trends Mol Med, 19, 40–50.
  • Han, S. S., Williams, L. A., & Eggan, K. C. (2011). Constructing and deconstructing stem cell models of neurological disease. Neuron, 70, 626–644.
  • Höglund, P. J., Adzic, D., Scicluna, S. J., Lindblom, J., & Fredriksson, R. (2005). The repertoire of solute carriers of family 6: Identification of new human and rodent genes. Biochem Biophys Res Commun, 336, 175–189.
  • Hurles, M. (2004). Gene duplication: The genomic trade in spare parts. PLoS Biol, 2, e206.
  • Jiang, Z., Tang, H., Ventura, M., Cardone, M. F., Marques-Bonet, T., She, X., Pevzner, P. A., & Eichler, E. E. (2007). Ancestral reconstruction of segmental duplications reveals punctuated cores of human genome evolution. Nat Genet, 39, 1361–1368.
  • Johnson, M. E., National Institute of Health Intramural Sequencing Center Comparative Sequencing Program, Cheng, Z., Morrison, V. A., Scherer, S., Ventura, M., Gibbs, R. A., Green, E. D., & Eichler, E. E. (2006). Recurrent duplication-driven transposition of DNA during hominoid evolution. Proc Natl Acad Sci U S A, 103, 17626–17631.
  • Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., & Nakahara, H. (2003). Structure-stability-function relationships of dendritic spines. Trends Neurosci, 26, 360–368.
  • King, M. C., & Wilson, A. C. (1975). Evolution at two levels in humans and chimpanzees. Science, 188, 107–116.
  • Kitzman, J. O., Mackenzie, A. P., Adey, A., Hiatt, J. B., Patwardhan, R. P., Sudmant, P. H., Ng, S. B., Alkan, C., Qiu, R., Eichler, E. E., & Shendure, J. (2011). Haplotype-resolved genome sequencing of a Gujarati Indian individual. Nat Biotechnol, 29, 59–63.
  • Kreis, P., Thévenot, E., Rousseau, V., Boda, B., Muller, D., & Barnier, J. V. (2007). The p21-activated kinase 3 implicated in mental retardation regulates spine morphogenesis through a Cdc42-dependent pathway. J Biol Chem, 282, 21497–21506.
  • Lechtreck, K. F., Delmotte, P., Robinson, M. L., Sanderson, M. J., & Witman, G. B. (2008). Mutations in Hydin impair ciliary motility in mice. J Cell Biol, 180, 633–643.
  • Lemon, N., & Manahan-Vaughan, D. (2006). Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci, 26, 7723–7729.
  • Li, J. P., Fu, Y. N., Chen, Y. R., & Tan, T. H. (2010). JNK pathway-associated phosphatase dephosphorylates focal adhesion kinase and suppresses cell migration. J Biol Chem, 285, 5472–5478.
  • Linardopoulou, E. V., Williams, E. M., Fan, Y., Friedman, C., Young, J. M., & Trask, B. J. (2005). Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature, 437, 94–100.
  • Liu, H., Zhu, F., Yong, J., Zhang, P., Hou, P., Li, H., Jiang, W., Cai, J., Liu, M., Cui, K., Qu, X., Xiang, T., Lu, D., Chi, X., Gao, G., Ji, W., Ding, M., & Deng, H. (2008). Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem Cell, 3, 587–590.
  • Lorson, C. L., Hahnen, E., Androphy, E. J., & Wirth, B. (1999). A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A, 96, 6307–6311.
  • Lorson, C. L., Rindt, H., & Shababi, M. (2010). Spinal muscular atrophy: Mechanisms and therapeutic strategies. Hum Mol Genet, 19, R111–R118.
  • Lupski, J. R. (1998). Genomic disorders: Structural features of the genome can lead to DNA rearrangements and human disease traits. Trends Genet, 14, 417–422.
  • Lynch, M., & Katju, V. (2004). The altered evolutionary trajectories of gene duplicates. Trends Genet, 20, 544–549.
  • Makeyev, A. V., Erdenechimeg, L., Mungunsukh, O., Roth, J. J., Enkhmandakh, B., Ruddle, F. H., & Bayarsaihan, D. (2004). GTF2IRD2 is located in the Williams-Beuren syndrome critical region 7q11.23 and encodes a protein with two TFII-I-like helix-loop-helix repeats. Proc Natl Acad Sci U S A, 101, 11052–11057.
  • Marques-Bonet, T., Girirajan, S., & Eichler, E. E. (2009). The origins and impact of primate segmental duplications. Trends Genet, 25, 443–454.
  • Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., & Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature, 429, 761–766.
  • Mercer, E. A., Korhonen, L., Skoglösa, Y., Olsson, P. A., Kukkonen, J. P., & Lindholm, D. (2000). NAIP interacts with hippocalcin and protects neurons against calcium-induced cell death through caspase-3-dependent and -independent pathways. EMBO J, 19, 3597–3607.
  • O’Bleness, M., Searles, V. B., Varki, A., Gagneux, P., & Sikela, J. M. (2012). Evolution of genetic and genomic features unique to the human lineage. Nat Rev Genet, 13, 853–866.
  • O’Driscoll, M. C., Daly, S. B., Urquhart, J. E., Black, G. C., Pilz, D. T., Brockmann, K., McEntagart, M., Abdel-Salam, G., Zaki, M., Wolf, N. I., Ladda, R. L., Sell, S., D’Arrigo, S., Squier, W., Dobyns, W. B., Livingston, J. H., & Crow, Y. J. (2010). Recessive mutations in the gene encoding the tight junction protein occludin cause band-like calcification with simplified gyration and polymicrogyria. Am J Hum Genet, 87, 354–364.
  • Ohno, S. (1970). Evolution by gene duplication. New York: Springer-Verlag.
  • Palmer, S. J., Taylor, K. M., Santucci, N., Widagdo, J., Chan, Y. K., Yeo, J. L., Adams, M., Gunning, P. W., & Hardeman, E. C. (2012). GTF2IRD2 from the Williams-Beuren critical region encodes a mobile element-derived fusion protein that antagonizes the action of its related family members. J Cell Sci, 125, 5040–5050.
  • Patterson, K. I., Brummer, T., O’Brien, P. M., & Daly, R. J. (2009). Dual-specificity phosphatases: Critical regulators with diverse cellular targets. Biochem J, 418, 475–489.
  • Perrelet, D., Ferri, A., Liston, P., Muzzin, P., Korneluk, R. G., & Kato, A. C. (2002). IAPs are essential for GDNF-mediated neuroprotective effects in injured motor neurons in vivo. Nat Cell Biol, 4, 175–179.
  • Petanjek, Z., Judaš, M., Šimic, G., Rasin, M. R., Uylings, H. B., Rakic, P., & Kostovic, I. (2011). Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A, 108, 13281–13286.
  • Porter, M. A., Dobson-Stone, C., Kwok, J. B., Schofield, P. R., Beckett, W., & Tassabehji, M. (2012). A role for transcription factor GTF2IRD2 in executive function in Williams-Beuren syndrome. PLoS ONE, 7, e47457.
  • Rakic, P. (2009). Evolution of the neocortex: A perspective from developmental biology. Nat Rev Neurosci, 10, 724–735.
  • Ridley, A. J. (2012). Historical overview of Rho GTPases. Methods Mol Biol, 827, 3–12.
  • Riley, B., Williamson, M., Collier, D., Wilkie, H., & Makoff, A. (2002). A 3-Mb map of a large Segmental duplication overlapping the alpha7-nicotinic acetylcholine receptor gene (CHRNA7) at human 15q13-q14. Genomics, 79, 197–209.
  • Rostami, A., Brown, M. J., Lisak, R. P., Sumner, A. J., Zweiman, B., & Pleasure, D. E. (1984). The role of myelin P2 protein in the production of experimental allergic neuritis. Ann Neurol, 16, 680–685.
  • Saitsu, H., Osaka, H., Sugiyama, S., Kurosawa, K., Mizuguchi, T., Nishiyama, K., Nishimura, A., Tsurusaki, Y., Doi, H., Miyake, N., Harada, N., Kato, M., & Matsumoto, N. (2011). Early infantile epileptic encephalopathy associated with the disrupted gene encoding Slit-Robo Rho GTPase activating protein 2 (SRGAP2). Am J Med Genet A, 158A, 199–205.
  • Sharp, A. J., Hansen, S., Selzer, R. R., Cheng, Z., Regan, R., Hurst, J. A., Stewart, H., Price, S. M., Blair, E., Hennekam, R. C., Fitzpatrick, C. A., Segraves, R., Richmond, T. A., Guiver, C., Albertson, D. G., Pinkel, D., Eis, P. S., Schwartz, S., Knight, S. J., & Eichler, E. E. (2006). Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet, 38, 1038–1042.
  • She, X., Cheng, Z., Zöllner, S., Church, D. M., & Eichler, E. E. (2008). Mouse segmental duplication and copy number variation. Nat Genet, 40, 909–914.
  • She, X., Horvath, J. E., Jiang, Z., Liu, G., Furey, T. S., Christ, L., Clark, R., Graves, T., Gulden, C. L., Alkan, C., Bailey, J. A., Sahinalp, C., Rocchi, M., Haussler, D., Wilson, R. K., Miller, W., Schwartz, S., & Eichler, E. E. (2004). The structure and evolution of centromeric transition regions within the human genome. Nature, 430, 857–864.
  • She, X., Jiang, Z., Clark, R. A., Liu, G., Cheng, Z., Tuzun, E., Church, D. M., Sutton, G., Halpern, A. L., & Eichler, E. E. (2004). Shotgun sequence assembly and recent segmental duplications within the human genome. Nature, 431, 927–930.
  • She, X., Liu, G., Ventura, M., Zhao, S., Misceo, D., Roberto, R., Cardone, M. F., Rocchi, M., Green, E. D., Archidiacano, N., Eichler, E. E., & Program, N. C. S. (2006). A preliminary comparative analysis of primate segmental duplications shows elevated substitution rates and a great-ape expansion of intrachromosomal duplications. Genome Res, 16, 576–583.
  • Shinawi, M., Schaaf, C. P., Bhatt, S. S., Xia, Z., Patel, A., Cheung, S. W., Lanpher, B., Nagl, S., Herding, H. S., Nevinny-Stickel, C., Immken, L. L., Patel, G. S., German, J. R., Beaudet, A. L., & Stankiewicz, P. (2009). A small recurrent deletion within 15q13.3 is associated with a range of neurodevelopmental phenotypes. Nat Genet, 41, 1269–1271.
  • Sidman, R. L., & Rakic, P. (1973). Neuronal migration, with special reference to developing human brain: A Review. Brain Res, 62, 1–35.
  • Sinkus, M. L., Lee, M. J., Gault, J., Logel, J., Short, M., Freedman, R., Christian, S. L., Lyon, J., & Leonard, S. (2009). A 2-base pair deletion polymorphism in the partial duplication of the alpha7 nicotinic acetylcholine gene (CHRFAM7A) on chromosome 15q14 is associated with schizophrenia. Brain Res, 1291, 1–11.
  • Smathers, R. L., & Petersen, D. R. (2011). The human fatty acid-binding protein family: Evolutionary divergences and functions. Hum Genomics, 5, 170–191.
  • Soderling, S. H., Binns, K. L., Wayman, G. A., Davee, S. M., Ong, S. H., Pawson, T., & Scott, J. D. (2002). The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat Cell Biol, 4, 970–975.
  • Steed, E., Balda, M. S., & Matter, K. (2010). Dynamics and functions of tight junctions. Trends Cell Biol, 20, 142–149.
  • Sudmant, P. H., Kitzman, J. O., Antonacci, F., Alkan, C., Malig, M., Tsalenko, A., Sampas, N., Bruhn, L., Shendure, J., Eichler, E. E., & Project, G. (2010). Diversity of human copy number variation and multicopy genes. Science, 330, 641–646.
  • Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., & Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.
  • Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., & Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145–1147.
  • van Bokhoven, H. (2011). Genetic and epigenetic networks in intellectual disabilities. Annu Rev Genet, 45, 81–104.
  • Varki, A., Geschwind, D. H., & Eichler, E. E. (2008). Explaining human uniqueness: Genome interactions with environment, behaviour and culture. Nat Rev Genet, 9, 749–763.
  • Wong, K., Ren, X. R., Huang, Y. Z., Xie, Y., Liu, G., Saito, H., Tang, H., Wen, L., Brady-Kalnay, S. M., Mei, L., Wu, J. Y., Xiong, W. C., & Rao, Y. (2001). Signal transduction in neuronal migration: Roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell, 107, 209–221.
  • Yamanaka, S., & Blau, H. M. (2010). Nuclear reprogramming to a pluripotent state by three approaches. Nature, 465, 704–712.
  • Yuste, R. (2011). Dendritic spines and distributed circuits. Neuron, 71, 772–781.
  • Yuste, R., & Bonhoeffer, T. (2001). Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci, 24, 1071–1089.
  • Zheleznyakova, G. Y., Kiselev, A. V., Vakharlovsky, V. G., Rask-Andersen, M., Chavan, R., Egorova, A. A., Schiöth, H. B., & Baranov, V. S. (2011). Genetic and expression studies of SMN2 gene in Russian patients with spinal muscular atrophy type II and III. BMC Med Genet, 12, 96.
  • Zou, J., Maeder, M. L., Mali, P., Pruett-Miller, S. M., Thibodeau-Beganny, S., Chou, B. K., Chen, G., Ye, Z., Park, I. H., Daley, G. Q., Porteus, M. H., Joung, J. K., & Cheng, L. (2009). Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell, 5, 97–110.

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