The case for DUF1220 domain dosage as a primary contributor to anthropoid brain expansion

Frontiers in Human Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Keeney, Jonathon G ^a   Dumas, Laura ^a   Sikela, James M ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Anthropoid brain evolution; Copy number; DUF1220; Gene dosage; Gene duplication and evolution; Human brain expansion; Protein domain

Indexed keywords

PHOSPHODIESTERASE; PHOSPHODIESTERASE FAMILY MEMBER 4D INTERACTING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTISM; BRAIN EXPANSION; BRAIN SIZE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTROSOME; CHROMOSOME 1Q; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; COGNITION; COPY NUMBER VARIATION; DUF1220 PROTEIN DOMAIN; EVOLUTION; GENE; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION; GENETIC SELECTION; GRAY MATTER; HEAD CIRCUMFERENCE; HOMO NEANDERTHALENSIS; HUMAN; HUMAN ACCELERATED REGION 1F GENE; HUMAN GENOME; MACROCEPHALY; MICROCEPHALY; NBPF GENE; NEOTENY; NONHUMAN; POSITIVE SELECTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; RGAP2 GENE; SCHIZOPHRENIA; SIMIAN;

EID: 84921938071     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00427     Document Type: Article

References (50)

1. Anderson, C. T., Castillo, A. B., Brugmann, S. A., Helms, J. A., Jacobs, C. R., and Stearns, T. (2008). Primary cilia: cellular sensors for the skeleton. Anat. Rec. 291, 1074-1078. doi: 10.1002/ar.20754
2. Brunetti-Pierri, N., Berg, J. S., Scaglia, F., Belmont, J., Bacino, C. A., Sahoo, T., et al. (2008). Recurrent reciprocal 1q21.1 deletions and duplications associated with microcephaly or macrocephaly and developmental and behavioral abnormalities. Nat. Genet. 40, 1466-1471. doi: 10.1038/ng.279
3. Capra, J. A., Erwin, G. D., McKinsey, G., Rubenstein, J. L., and Pollard, K. S. (2013). Many human accelerated regions are developmental enhancers. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20130025. doi: 10.1098/rstb.2013.0025
4. Corchesne, E., Pierce, K., Schumann, C. M., Redcay, E., Buckwalter, J. A., Kennedy, D. P., et al. (2007). Mapping early brain development in autism. Neuron 56, 399-413. doi: 10.1016/j.neuron.2007.10.016
5. Cox, J., Jackson, A. P., Bond, J., and Woods, C. G. (2006). What primary microcephaly can teach us about brain growth. Trends Mol. Med. 12, 358-366. doi: 10.1016/j.molmed.2006.06.006
6. Crespi, B. (2013). Diametric gene-dosage effects as windows into neurogenetic architecture. Curr. Opin. Neurobiol. 23, 143-151. doi: 10.1016/j.conb.2012.08.005
7. Crow, T. J. (1995). A continuum of psychosis, one human gene, and not much else-the case for homogeneity. Schizophr. Res. 17, 135-145. doi: 10.1016/0920-9964(95)00059-U
8. Davis, J. M., Searles, V. B., Anderson, N., Keeney, J., Dumas, L., and Sikela, J. M. (2014). DUF1220 Dosage is linearly associated with increasing severity of the three primary symptoms of autism. PLoS Genet. 10:e1004241. doi: 10.1371/journal.pgen.1004241
9. Dennis, M. Y., Nuttle, X., Sudmant, P. H., Antonacci, F., Graves, T. A., Nefedov, M., et al. (2012). Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149, 912-922. doi: 10.1016/j.cell.2012.03.033
10. Dumas, L., and Sikela, J. M. (2009). DUF1220 domains, cognitive disease, and human brain evolution. Cold Spring Harb. Symp. Quant. Biol. 74, 375-382. doi: 10.1101/sqb.2009.74.025
11. Dumas, L. J., O'Bleness, M. S., Davis, J. M., Dickens, C. M., Anderson, N., Keeney, J. G., et al. (2012). DUF1220-domain copy number implicated in human brain-size pathology and evolution. Am. J. Hum. Genet. 91, 444-454. doi: 10.1016/j.ajhg.2012.07.016
12. Fortna, A., Kim, Y., MacLaren, E., Marshall, K., Hahn, G., Meltesen, L., et al. (2004). Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biol. 2:E207. doi: 10.1371/journal.pbio.0020207
13. Golovanova, L. V., Doronichev, V. B., Cleghorn, N. E., Koulkova, M. A., Sapelko, T. V., and Shackley, M. S. (2010). Significance of ecological factors in the middle to upper Paleolithic transition. Curr. Anthropol. 51, 655-691. doi: 10.1086/656185
14. Goodman, M. (1999). The genomic record of humankind's evolutionary roots. Am. J. Hum. Genet. 64, 31-39. doi: 10.1086/302218
15. Haijma, S. V., Van Haren, N., Cahn, W., Koolschijn, P. C., Hulshoff Pol, H. E., and Kahn, R. S. (2013). Brain volumes in schizophrenia: a meta-analysis of over 18,000 subjects. Schizophr. Bull. 39, 1129-1138. doi: 10.1093/schbul/sbs118
16. Han, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., et al. (2013). Forebrain Engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12, 342-353. doi: 10.1016/j.stem.2012.12.015
17. Herculano-Houzel, S. (2009). The human brain in numbers: a linearly scaled-up primate brain. Front. Hum. Neurosci. 3:31. doi: 10.3389/neuro.09.031.2009
18. Herculano-Houzel, S., Collins, C. E., Wong, P., and Kaas, J. H. (2007). Cellular scaling rules for primate brains. Proc. Natl. Acad. Sci. U.S.A. 104, 3562-3567. doi: 10.1073/pnas.0611396104
19. Herculano-Houzel, S., Mota, B., and Lent, R. (2006). Cellular scaling rules for rodent brains. Proc. Natl. Acad. Sci. U.S.A. 103, 12138-12143. doi: 10.1073/pnas.0604911103
20. Holloway, R. L. (1985). "The poor brain of Homo sapiens neanderthalensis: see what you please, " in Ancestors: the Hard Evidence, ed E. Delson (New York, NY: A.R. Liss, Inc.), 319-324.
21. Itsara, A., Wu, H., Smith, J. D., Nickerson, D. A., Romieu, I., London, S. J., et al. (2010). De novo rates and selection of large copy number variation. Genome Res. 20, 1469-1481. doi: 10.1101/gr.107680.110
22. Johnson, M. B., Kawasawa, Y. I., Mason, C. E., Krsnik, Z., Coppola, G., Bogdanović, D., et al. (2009). Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62, 494-509. doi: 10.1016/j.neuron.2009.03.027
23. Kamm, G. B., López-Leal, R., Lorenzo, J. R., and Franchini, L. F. (2013b). A fast-evolving human NPAS3 enhancer gained reporter expression in the developing forebrain of transgenic mice. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20130019. doi: 10.1098/rstb.2013.0019
24. Kamm, G. B., Pisciottano, F., Kliger, R., and Franchini, L. F. (2013a). The developmental brain gene NPAS3 contains the largest number of accelerated regulatory sequences in the human genome. Mol. Biol. Evol. 30, 1088-1102. doi: 10.1093/molbev/mst023
25. Karakoula, K., Suarez-Merino, B., Ward, S., Phipps, K. P., Harkness, W., Hayward, R., et al. (2008). Real-time quantitative PCR analysis of pediatric ependymomas identifies novel candidate genes including TPR at 1q25 and CHIBBY at 22q12-q13. Genes Chromosomes Cancer 47, 1005-1022. doi: 10.1002/gcc.20607
26. Keeney, J. G., Davis, J. M., Siegenthaler, J., Post, M., Nielsen, B. S., Hopkins, W. D., et al. (in press). DUF1220 protein domains drive proliferation in human neural stem cells and are associated with increased cortical volume in anthropoid primates. Brain Struct. Funct. doi: 10.1007/s00429-014-0814-9
27. Kornack, D. R., and Rakic, P. (1998). Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc. Natl. Acad. Sci. U.S.A. 95, 1242-1246. doi: 10.1073/pnas.95.3.1242
28. Li, F. Q., Mofunanya, A., Harris, K., and Takemaru, K. (2008). Chibby cooperates with 14-3-3 to regulate beta-catenin subcellular distribution and signaling activity. J. Cell Biol. 181, 1141-1154. doi: 10.1083/jcb.200709091
29. Marques-Bonet, T., and Eichler, E. E. (2009). The evolution of human segmental duplications and the core duplicon hypothesis. Cold Spring Harb. Symp. Quant. Biol. 74, 355-362. doi: 10.1101/sqb.2009.74.011
30. Mefford, H. C., Sharp, A. J., Baker, C., Itsara, A., Jiang, Z., Buysse, K., et al. (2008). Recurrent rearrangements of chromosome 1q21.1 and variable pediatric phenotypes. N. Engl. J. Med. 359, 1685-1699. doi: 10.1056/NEJMoa0805384
31. Megraw, T. L., Sharkey, J. T., and Nowakowski, R. S. (2011). Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 21, 470-480. doi: 10.1016/j.tcb.2011.04.007
32. Mendrzyk, F., Korshunov, A., Benner, A., Toedt, G., Pfister, S., Radlwimmer, B., et al. (2006). Identification of gains on 1q and epidermal growth factor receptor overexpression as independent prognostic markers in intracranial ependymoma. Clin. Cancer Res. 12(7 pt 1), 2070-2079. doi: 10.1158/1078-0432.CCR-05-2363
33. O'Bleness, M. S., Dickens, C. M., Dumas, L. J., Kehrer-Sawatzki, H., Wyckoff, G. J., and Sikela, J. M. (2012a). Evolutionary history and genome organization of DUF1220 domains. G3 (Bethesda). 2, 977-986. doi: 10.1534/g3.112.003061
34. O'Bleness, M., Searles, V. B., Varki, A., Gagneux, P., and Sikela, J. M. (2012b). Evolution of genetic and genomic features unique to the human lineage. Nat. Rev. Genet. 13, 853-866. doi: 10.1038/nrg3336
35. Ogawa, L. M., and Vallender, E. J. (2014). Evolutionary conservation in genes underlying human psychiatric disorders. Front. Hum. Neurosci. 8:283. doi: 10.3389/fnhum.2014.00283
36. Plotnikova, O. V., Pugacheva, E. N., and Golemis, E. A. (2009). Primary cilia and the cell cycle. Methods Cell Biol. 94, 137-160. doi: 10.1016/S0091-679X(08)94007-3
37. Pollard, K. S., Salama, S. R., Lambert, N., Lambot, M. A., Coppens, S., Pedersen, J. S., et al. (2006). An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167-172. doi: 10.1038/nature05113
38. Popesco, M. C., Maclaren, E. J., Hopkins, J., Dumas, L., Cox, M., Meltesen, L., et al. (2006). Human lineage-specific amplification, selection, and neuronal expression of DUF1220 domains. Science 313, 1304-1307. doi: 10.1126/science.1127980
39. Rendu, W., Beauval, C., Crevecoeur, I., Bayle, P., Balzeau, A., Bismuth, T., et al. (2013). Evidence supporting an intentional Neandertal burial at La Chapelle-aux-Saints. Proc. Natl. Acad. Sci. U.S.A. 111, 81-86. doi: 10.1073/pnas.1316780110
40. Rouquier, S., Blancher, A., and Giorgi, D. (2000). The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc. Natl. Acad. Sci. U.S.A. 97, 2870-2874. doi: 10.1073/pnas.040580197
41. Sikela, J. M. (2006). The jewels of our genome: the search for the genomic changes underlying the evolutionarily unique capacities of the human brain. PLoS Genet. 2:e80. doi: 10.1371/journal.pgen.0020080
42. Soressi, M., McPherron, S. P., Lenoir, M., Dogandžić, T., Goldberg, P., Jacobs, Z., et al. (2013). Neanderthals made the first specialized bone tools in Europe. Proc. Natl. Acad. Sci. U.S.A. 110, 14186-14190. doi: 10.1073/pnas.1302730110
43. Steere, N., Chae, V., Burke, M., Li, F. Q., Takemaru, K., and Kuriyama, R. (2012). A Wnt/beta-catenin pathway antagonist chibby binds cenexin at the distal end of mother centrioles and functions in primary cilia formation. PLoS ONE 7:e41077. doi: 10.1371/journal.pone.0041077
44. Takemaru, K., Yamaguchi, S., Lee, Y. S., Zhang, Y., Carthew, R. W., and Moon, R. T. (2003). Chibby, a nuclear beta-catenin-associated antagonist of the Wnt/Wingless pathway. Nature 422, 905-909. doi: 10.1038/nature01570
45. Thornton, G. K., and Woods, C. G. (2009). Primary microcephaly: do all roads lead to Rome? Trends Genet. 25, 501-510. doi: 10.1016/j.tig.2009.09.011
46. Vandepoele, K., Andries, V., and van Roy, F. (2009). The NBPF1 promoter has been recruited from the unrelated EVI5 gene before anthropoid radiation. Mol. Biol. Evol. 26, 1321-1332. doi: 10.1093/molbev/msp047
47. Vandepoele, K., Staes, K., Andries, V., and van Roy, F. (2010). Chibby interacts with NBPF1 and clusterin, two candidate tumor suppressors linked to neuroblastoma. Exp. Cell Res. 316, 1225-1233. doi: 10.1016/j.yexcr.2010.01.019
48. Vandepoele, K., Van Roy, N., Staes, K., Speleman, F., and van Roy, F. (2005). A novel gene family NBPF: intricate structure generated by gene duplications during primate evolution. Mol. Biol. Evol. 22, 2265-2274. doi: 10.1093/molbev/msi222
49. Verde, I., Pahlke, G., Salanova, M., Zhang, G., Wang, S., Coletti, D., et al. (2001). Myomegalin is a novel protein of the golgi/centrosome that interacts with a cyclic nucleotide phosphodiesterase. J. Biol. Chem. 276, 11189-11198. doi: 10.1074/jbc.M006546200
50. Zhou, F., Xing, Y., Xu, X., Yang, Y., Zhang, J., Ma, Z., et al. (2013). NBPF is a potential DNA-binding transcription factor that is directly regulated by NF-κB. Int. J. Biochem. Cell Biol. 45, 2479-2490. doi: 10.1016/j.biocel.2013.07.022