Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques

Genome Research

Volumn 22, Issue 4, 2012, Pages 611-622

  Liu, Xiling ^a   Somel, Mehmet ^a,b   Tang, Lin ^a,c   Yan, Zheng ^a   Jiang, Xi ^a   Guo, Song ^a   Yuan, Yuan ^a,d   He, Liu ^a,c   Oleksiak, Anna ^a   Zhang, Yan ^e   Li, Na ^f   Hu, Yuhui ^f   Chen, Wei ^f,g   Qiu, Zilong ^e   Pääbo, Svante ^b   Khaitovich, Philipp ^a,b  

^a MAX PLANCK INSTITUTE   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d LA TROBE UNIVERSITY   (Australia)

^e INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^g MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 2; EARLY GROWTH RESPONSE FACTOR 3; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2A; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM CORTEX; CHIMPANZEE; ELECTRON MICROSCOPY; EMBRYO; GENE EXPRESSION; GENETIC CODE; HOMO NEANDERTHALENSIS; HUMAN; HUMAN TISSUE; MICROARRAY ANALYSIS; MOUSE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; POSTNATAL DEVELOPMENT; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY; RNA SEQUENCE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CEREBELLUM; CHILD; CHILD, PRESCHOOL; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INFANT; INFANT, NEWBORN; MACACA MULATTA; MIDDLE AGED; NEUROMUSCULAR JUNCTION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAN TROGLODYTES; PREFRONTAL CORTEX; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; SYNAPSES; YOUNG ADULT;

MACACA; MACACA MULATTA; PAN; PRIMATES;

EID: 84859541449     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.127324.111     Document Type: Article

References (70)

1. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. 2000. Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29. (Pubitemid 30257031)
2. Barbey AK, Krueger F, Grafman J. 2009. An evolutionarily adaptive neural architecture for social reasoning. Trends Neurosci 32: 603-610.
3. Barbosa AC, Kim MS, Ertunc M, Adachi M, Nelson ED, McAnally J, Richardson JA, Kavalali ET, Monteggia LM, Bassel-Duby R, et al. 2008. MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc Natl Acad Sci 105: 9391-9396.
4. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39. (Pubitemid 23020772)
5. Bogin B. 1997. Evolutionary hypotheses for human childhood. Yearb Phys Anthropol 40: 63-89. (Pubitemid 127458471)
6. Bogin B. 2009. Childhood, adolescence, and longevity: a multilevel model of the evolution of reserve capacity in human life history. Am J Hum Biol 21: 567-577.
7. Caceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, Geschwind DH, Lockhart DJ, Preuss TM, Barlow C. 2003. Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci 100: 13030-13035. (Pubitemid 37340020)
8. Caceres M, Suwyn C, Maddox M, Thomas JW, Preuss TM. 2007. Increased cortical expression of two synaptogenic thrombospondins in human brain evolution. Cereb Cortex 17: 2312-2321. (Pubitemid 47517467)
9. Carroll SB. 2003. Genetics and the making of Homo sapiens. Nature 422: 849-857. (Pubitemid 36520033)
10. Chen FC, Li WH. 2001. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68: 444-456.
11. Clark DA, Mitra PP, Wang SSH. 2001. Scalable architecture in mammalian brains. Nature 411: 189-193. (Pubitemid 32455176)
12. Cooke SF, Bliss TV. 2006. Plasticity in the human central nervous system. Brain 129: 1659-1673. (Pubitemid 43999401)
13. Davis S, Bozon B, Laroche S. 2003. How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 142: 17-30. (Pubitemid 36677587)
14. de Magalhães JP. 2006. AnAge: the Animal Ageing Database, Build 9. http://genomics.senescence.info/species.
15. de Magalhães J, Costa J. 2009. A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol 22: 1770-1774.
16. + and NMDA correlate with c-fos proto-oncogene expression. Neurosci Lett 107: 55-62.
17. Ebersberger I, Metzler D, Schwarz C, Pääbo S. 2002. Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet 70: 1490-1497. (Pubitemid 34533896)
18. Faraway J. 2002. Practical regression and ANOVA using R. http://cran.rproject.org/doc/contrib/Faraway-PRA.pdf.
19. Finlay BL, Darlington RB. 1995. Linked regularities in the development and evolution of mammalian brains. Science 268: 1578-1584.
20. Flavell SW, Cowan CW, Kim T, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME. 2006. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311: 1008-1012. (Pubitemid 43271729)
21. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME. 2008. Genomewide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60: 1022-1038.
22. Fu X, Giavalisco P, Liu X, Catchpole G, Fu N, Ning ZB, Guo S, Yan Z, Somel M, Pääbo S, et al. 2011. Rapid metabolic evolution in human prefrontal cortex. Proc Natl Acad Sci 108: 6181-6186.
23. Gavan JA. 1969. A handbook of living primates: morphology, ecology and behaviour of nonhuman primates. J. R. Napier and P. H. Napier. Am Anthropol 71: 357-358.
24. Gilad Y, Oshlack A, Rifkin SA. 2006. Natural selection on gene expression. Trends Genet 22: 456-461. (Pubitemid 44093766)
25. Glantz LA, Gilmore JH, Hamer RM, Lieberman JA, Jarskog LF. 2007. Synaptophysin and postsynaptic density protein 95 in the human prefrontal cortex from mid-gestation into early adulthood. Neuroscience 149: 582-591. (Pubitemid 47633016)
26. Gould SJ. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge, MA.
27. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, et al. 2010. A draft sequence of the Neanderthal genome. Science 328: 710-722.
28. Hardingham GE, Fukunaga Y, Bading H. 2002. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5: 405-414. (Pubitemid 34454245)
29. Hawkes K, O'Connell JF, Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci 95: 1336-1339. (Pubitemid 28124959)
30. Hinds DA, Stuve LL, Nilsen GB, Halperin E, Eskin E, Ballinger DG, Frazer KA, Cox DR. 2005. Whole-genome patterns of common DNA variation in three human populations. Science 307: 1072-1079. (Pubitemid 40262106)
31. Hunt CA, Schenker LJ, Kennedy MB. 1996. PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J Neurosci 16: 1380-1388. (Pubitemid 26145918)
32. Huttenlocher PR, Dabholkar AS. 1997. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387: 167-178. (Pubitemid 27430343)
33. Johnson MH. 2001. Functional brain development in humans. Nat Rev Neurosci 2: 475-483. (Pubitemid 33676582)
34. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, et al. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480-D484. (Pubitemid 351149770)
35. Kaplan H, Hill K, Lancaster J, Hurtado AM. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9: 156-185.
36. Khaitovich P, Enard W, Lachmann M, Pääbo S. 2006. Evolution of primate gene expression. Nat Rev Genet 7: 693-702. (Pubitemid 44260005)
37. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science 188: 107-116.
38. Kumar S, Hedges SB. 1998. A molecular timescale for vertebrate evolution. Nature 392: 917-920. (Pubitemid 28232061)
39. Langer J. 2006. The heterochronic evolution of primate cognitive development. Biol Theory 1: 41-43.
40. Leigh S. 2004. Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62: 139-164. (Pubitemid 38463896)
41. Li L, Yun SH, Keblesh J, Trommer BL, Xiong H, Radulovic J, Tourtellotte WG. 2007. Egr3, a synaptic activity regulated transcription factor that is essential for learning and memory. Mol Cell Neurosci 35: 76-88. (Pubitemid 46636302)
42. Liu L, Cavanaugh JE, Wang Y, Sakagami H, Mao Z, Xia Z. 2003. ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc Natl Acad Sci 100: 8532-8537. (Pubitemid 36842579)
43. Lynch MA. 2004. Long-term potentiation and memory. Physiol Rev 84: 87-136. (Pubitemid 38049877)
44. Lyons GE, Micales BK, Schwarz J, Martin JF, Olson EN. 1995. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 15: 5727-5738.
45. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21. (Pubitemid 39348827)
46. Mao Z, Bonni A, Xia F, Nadal-Vicens M, Greenberg ME. 1999. Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286: 785-790.
47. Masliah E, Terry RD, Alford M, DeTeresa R. 1990. Quantitative immunohistochemistry of synaptophysin in human neocortex: an alternative method to estimate density of presynaptic terminals in paraffin sections. J Histochem Cytochem 38: 837-844. (Pubitemid 20177851)
48. McKinsey TA, Zhang CL, Olson EN. 2002. MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27: 40-47. (Pubitemid 34131624)
49. McNamara KJ. 1997. Shapes of time. Johns Hopkins University Press, Baltimore.
50. Mochida GH, Walsh CA. 2001. Molecular genetics of human microcephaly. Curr Opin Neurol 14: 151-156. (Pubitemid 32281266)
51. Pääbo S. 1999. Human evolution. Trends Cell Biol 9: M13-M16.
52. Penin X, Berge C, Baylac M. 2002. Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional procrustes analysis. Am J Phys Anthropol 118: 50-62. (Pubitemid 34327046)
53. Povinelli DJ, Preuss TM. 1995. Theory of mind: evolutionary history of a cognitive specialization. Trends Neurosci 18: 418-424.
54. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, et al. 2008. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59: 621-633.
55. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS. 1986. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232: 232-235. (Pubitemid 16046605)
56. Ramnani N. 2006. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7: 511-522. (Pubitemid 43989772)
57. Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL, et al. 2010. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053-1060.
58. Reichert H. 2009. Evolutionary conservation of mechanisms for neural regionalization, proliferation and interconnection in brain development. Biol Lett 5: 112-116.
59. Rilling JK. 2006. Human and nonhuman primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15: 65-77. (Pubitemid 43734422)
60. Semendeferi K, Teffer K, Buxhoeveden DP, Park MS, Bludau S, Amunts K, Travis K, Buckwalter J. 2010. Spatial organization of neurons inthe frontal pole sets humans apart from great apes. Cereb Cortex 21: 1485-1497.
61. Shalizi A, Lehtinen M, Gaudilliere B, Donovan N, Han J, Konishi Y, Bonni A. 2003. Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23: 7326-7336. (Pubitemid 36999522)
62. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A. 2006. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311: 1012-1017. (Pubitemid 43271730)
63. Smith BH, Crummett TL, Brandt KL. 1994. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories. Am J Phys Anthropol 37: 177-231.
64. Smith TM, Tafforeau P, Reid DJ, Pouech J, Lazzari V, Zermeno JP, Guatelli-Steinberg D, Olejniczak AJ, Hoffman A, Radovcic J, et al. 2010. Dental evidence for ontogenetic differences between modern humans and Neanderthals. Proc Natl Acad Sci 107: 20923-20928.
65. Somel M, Franz H, Yan Z, Lorenc A, Guo S, Giger T, Kelso J, Nickel B, Dannemann M, Bahn S, et al. 2009. Transcriptional neoteny in the human brain. Proc Natl Acad Sci 106: 5743-5748.
66. Somel M, Liu X, Tang L, Yan Z, Hu H, Guo S, Jiang X, Zhang X, Xu G, Xie G et al. 2011. MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol 9: e1001214. doi:1001210.1001371/journal.pbio.1001214.
67. Stringer C, Gamble C. 1993. In search of the Neanderthals: solving the puzzle of human origins. Thames and Hudson, New York.
68. Tomasello M. 2008. Origins of human communication. MIT Press, Cambridge, MA.
69. Wood JN, Grafman J. 2003. Human prefrontal cortex: processing and representational perspectives. Nat Rev Neurosci 4: 139-147. (Pubitemid 37279130)
70. Yuan Y, Chen YP, Ni S, Xu AG, Tang L, Vingron M, Somel M, Khaitovich P. 2011. Development and application of a modified dynamic time warping algorithm (DTW-S) to analyses of primate brain expression time series. BMC Bioinformatics 12: 347. doi: 10.1186/1471-2105-12-347.