Novel tools, classic techniques: Evolutionary studies using primate pluripotent stem cells

Biological Psychiatry

Volumn 75, Issue 12, 2014, Pages 929-935

  Hrvoj Mihic, Branka ^a,b   Marchetto, Maria C N ^c   Gage, Fred H ^c,d   Semendeferi, Katerina ^a,d,e   Muotri, Alysson R ^b,d,e  

^a Department of Anthropology ^*  (United States)

^b RADY CHILDREN'S HOSPITAL   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d San Diego   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain development; evolutionary model; induced pluripotent stem cells

Indexed keywords

ADAPTATION; EVOLUTION; HOMINID; HUMAN; MEDICAL RESEARCH; MORPHOLOGY; NEUROLOGIC DISEASE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; STEM CELL RESEARCH; ANIMAL; CYTOLOGY; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PATHOPHYSIOLOGY; PRIMATE;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NERVOUS SYSTEM DISEASES; NEUROGENESIS; PHENOTYPE; PRIMATES; PYRAMIDAL CELLS;

EID: 84901313977     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.08.007     Document Type: Review

References (89)

1. J. Bond, E. Roberts, G.H. Mochida, D.J. Hampshire, S. Scott, and J.M. Askham et al. ASPM is a major determinant of cerebral cortical size Nat Genet 32 2002 316 320
2. P.D. Evans, E.J. Vallender, and B.T. Lahn Molecular evolution of the brain size regulators CDK5RAP and CENPJ Gene 375 2006 75 79
3. P.D. Evans, S.L. Gilbert, N. Mekel-Bobov, E.J. Vallender, J.R. Anderson, and L.M. Vaez-Azizi et al. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans Science 309 2005 1717 1720
4. J. Zhang Evolution of the human ASPM gene, a major determinant of brain size Genetics 165 2003 2063 2070
5. N. Mekel-Bobov, S.L. Gilbert, P.D. Evans, E.J. Vallender, J.R. Anderson, and R.R. Hudson et al. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens Science 309 2005 1720 1722
6. W. Enard, M. Przeworski, S.E. Fisher, C.S. Lai, V. Wiebe, and T. Kitano et al. Molecular evolution of FOXP2, a gene involved in speech and language Nature 418 2002 869 872
7. C.S. Lai, S.E. Fisher, J.A. Hurst, F. Vargha-Khadem, and A.P. Monaco A forkhead-domain gene is mutated in severe speech and language disorder Nature 413 2001 519 523
8. C.S. Lai, D. Garrelli, A.P. Monaco, S.E. Gisher, and A.J. Copp FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder Brain 126 2003 2455 2462
9. S.C. Vernes, D.F. Newbury, B.S. Abrahams, L. Winchester, J. Nicod, and M. Groszer et al. A functional genetic link between distinct developmental language disorders N Engl J Med 359 2008 2337 2345
10. B.S. Abrahams, D. Tentler, J.V. Perederiy, M.C. Oldham, G. Coppola, and D.H. Geschwind Genome-wide analyses of human perisylvian cerebral cortical patterning Proc Natl Acad Sci U S A 104 2007 17849 17854
11. F. Vargha-Khadem, K. Watkins, K. Alcock, P. Fletchers, and R. Passingham Praxic and nonverbal cognitive deficits in a large family with a genetically transmitted speech and language disorder Proc Natl Acad Sci U S A 92 1995 930 933
12. M. Cáceres, J. Lachuer, M.A. Zapala, J.C. Redmond, L. Kudo, and D.H. Geschwind et al. Elevated gene expression levels distinguish human from non-human primate brains Proc Natl Acad Sci U S A 100 2003 13030 13035
13. M. Cáceres, C. Suwyn, M. Maddox, J.W. Thomas, and T.M. Preuss Increased cortical expression of two synaptogenic thrombospondins in human brain evolution Cereb Cortex 17 2007 2312 2321
14. W. Enard, P. Khaitovich, J. Klose, S. Zöllner, F. Heissig, and P. Giavalisco et al. Intra- and interspecific variation in primate gene expression patterns Science 296 2002 340 343
15. P. Khaitovich, B. Muetzel, X. She, M. Lachmann, I. Hellmann, and J. Dietzsch et al. Regional patterns of gene expression in human and chimpanzee brains Genome Res 14 2004 1462 1473
16. B. Jacobs, M. Schall, M. Prather, E. Kapler, L. Driscoll, and S. Baca et al. Regional dendritic and spine variation in human cerebral cortex: A quantitative Golgi study Cereb Cortex 11 2001 558 571
17. T.G. Belgard, A.C. Marques, P.L. Oliver, H.O. Abaan, T.M. Sirey, and A. Hoerder-Suabedissen et al. A transcriptomic atlas of mouse neocortical layers Neuron 71 2011 605 616
18. A. Bernard, L.S. Lubbers, K.Q. Tanis, R. Luo, A.A. Podtelezhnikov, and E.M. Finney et al. Transcriptional architecture of the primate neocortex Neuron 73 2012 1083 1099
19. Z. Petanjek, M. Judas, I. Kostovic, and H.B.M. Uylings Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: A layer-specific pattern Cereb Cortex 18 2008 915 929
20. J.J. Hutsler, and H. Zhang Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders Brain Res 1309 2010 83 94
21. L.A. Glantz, and D.A. Lewis Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia Arch Gen Psychiatry 57 2000 65 73
22. R. Nielsen, C. Bustamate, A.G. Clark, S. Glanowski, T.B. Sackton, and M.J. Hubisz et al. A scan for positively selected genes in the genomes of humans and chimpanzees PLoS Biol 3 2005 e170
23. K.S. Pollard, S.R. Slama, N. Lambert, M.A. Lambot, S. Coppens, and J.S. Pedersen et al. An RNA gene expressed during cortical development evolved rapidly in humans Nature 443 2006 167 172
24. S. Prabhakar, J.P. Noonan, S. Paabo, and E.M. Rubin Accelerated evolution of conserved noncoding sequences in humans Science 314 2006 786
25. K.S. Pollard, S.R. Salama, B. King, A.D. Kern, T. Dreszer, and S. Katzman et al. Forces shaping the fastest evolving regions in the human genome PLoS Genet 2 2006 e168
26. M.B. Johnson, Y.I. Kawasawa, C.E. Mason, Z. Krsnik, G. Coppola, and D. Bogdanovic et al. Functional and evolutionary insights into human brain development through global transcriptome analysis Neuron 62 2009 494 509
27. S. Dorus, E.J. Vallender, P.D. Evans, J.R. Anderson, S.L. Gilbert, and M. Mahowald et al. Accelerated evolution of nervous system genes in the origin of Homo sapiens Cell 119 2004 1027 1040
28. P. Mazin, J. Xiong, X. Liu, Z. Yan, X. Zhang, and M. Li et al. Widespread splicing changes in human brain development and aging Mol Syst Biol 9 2013 633
29. J. Zeng, G. Konopka, B.G. Hunt, T.M. Preuss, D. Geschwind, and S.V. Yi Divergent whole-genome methylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution Am J Hum Genet 91 2012 455 465
30. J.A. Calarco, Y. Xing, M. Cáceres, J.P. Calarco, X. Xiao, and Q. Pan et al. Global analysis of alternative splicing differences between humans and chimpanzees Genes Dev 21 2007 2963 2975
31. E. Berezikov, F. Thuemmler, L.W. van Laake, I. Kondova, R. Bontrop, E. Cuppen, and R.H. Plasterk Diversity of microRNAs in human and chimpanzee brain Nat Genet 38 2006 1375 1377
32. H.Y. Hu, S. Guo, J. Xi, Z. Yan, N. Fu, and X. Zhang et al. MicroRNA expression and regulation in human, chimpanzee, and macaque brains PLoS Genet 7 2011 e1002327
33. N. Lambert, M.A. Lambot, A. Bilheu, V. Albert, Y. Englert, and F. Libert et al. Genes expressed in specific areas in the human fetal cerebral cortex display distinct patterns of evolution PLoS One 6 2011 e17753
34. M. Somel, H. Franz, Z. Yan, A. Lorenc, S. Guo, and T. Giger et al. Transcriptional neoteny in the human brain Proc Natl Acad Sci U S A 106 2009 5743 5748
35. X. Liu, M. Somel, L. Tang, Z. Yan, X. Jiang, and S. Guo et al. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques Genome Res 22 2012 611 622
36. J.H. Kaas Why is brain size so important: Design problems and solutions as neocortex gets bigger or smaller Brain and Mind 1 2000 7 23
37. J. DeFelipe, L. Alonso-Nanclares, and J.I. Arellano Microstructure of the neocortex: Comparative aspects J Neurocytol 31 2002 299 316
38. J. DeFelipe, and I. Farinas The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs Prog Neurobiol 39 1992 563 607
39. R. Nieuwenhuys The neocortex: An overview of its evolutionary development, structural organization and synaptology Anat Embryol (Berl) 190 1994 307 337
40. N. Spruston Pyramidal neurons: Dendritic structure and synaptic integration Nat Rev Neurosci 9 2008 206 221
41. G.N. Elston Cortex, cognition and the cell: New insights into the pyramidal neuron and prefrontal function Cereb Cortex 13 2003 1124 1138
42. R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yanez, J. DeFelipe, and R. Yuste Dendritic size of pyramidal neurons differs among mouse cortical regions Cereb Cortex 16 2006 990 1001
43. S. Bianchi, C.D. Stimpson, A.L. Bauernfeind, S.J. Schapiro, W.B. Baze, and M.J. McArthur et al. Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: Regional specializations and comparison to humans [published online ahead of print August 8] Cereb Cortex. 2012
44. G.N. Elston, A. Elston, V. Casagrande, and J.H. Kaas Pyramidal neurons of granular prefrontal cortex of the galago: Complexity in evolution of the psychic cell in primates Anat Rec A Discov Mol Cell Evol Biol 285 2005 610 618
45. K. Semendeferi, E. Armstrong, A. Schleicher, K. Zilles, and G.W. van Hoesen Prefrontal cortex in humans and apes: A comparative study of area 10 Am J Phys Anthropol 114 2001 224 241
46. K. Semendeferi, K. Teffer, D.P. Buxhoeveden, M.S. Park, S. Bludau, and K. Amunts et al. Spatial organization of neurons in the frontal pole sets humans apart from great apes Cereb Cortex 21 2011 1485 1497
47. A.B. Scheibel, L.A. Paul, I. Fried, A.B. Forsythe, U. Tomiyasu, and A. Wechsler et al. Dendritic organization of the anterior speech area Exp Neurol 87 1985 109 117
48. B. Jacobs, and A.B. Scheibel A quantitative dendritic analysis of Wernicke's area in humans. I. Lifespan changes J Comp Neurol 327 1993 83 96
49. E.S. Vrba Multiphasic growth models and the evolution of prolonged growth exemplified by human brain evolution J Theor Biol 190 1998 227 239
50. K.J. McNamara What is heterochrony? N. Minugh-Purvis, K.J. McNamara, Human Evolution Through Developmental Change 2002 The Johns Hopkins University Press Baltimore 7 27
51. M.L. McKinney Brain evolution by stretching the global mitotic clock of development N. Minugh-Purvis, K.J. McNamara, Human Evolution Through Developmental Change 2002 The Johns Hopkins University Press Baltimore 173 188
52. S.H. Rice The role of heterochrony in primate brain evolution N. Minugh-Purvis, K.J. McNamara, Human Evolution Through Developmental Change 2002 The Johns Hopkins University Press Baltimore 154 170
53. S.R. Leigh Brain growth, life history, and cognition in primate and human evolution Am J Primatol 62 2004 139 164
54. E.K. Scott, and L. Luo How do dendrites take their shape? Nat Neurosci 4 2001 359 365
55. M. Urbanska, M. Blazejczyk, and J. Jaworski Molecular basis of dendritic arborization Acta Neurobiol Exp (Wars) 68 2008 264 288
56. K.L. Whitford, P. Dijkhuizen, F. Polleux, and A. Ghosh Molecular control of cortical dendrite development Annu Rev Neurosci 25 2002 127 149
57. P. Rakic Organizing principles for development of primate cerebral cortex S.C. Sharma, Organizing Principles of Neural Development 1982 Plenum Press New York 21 48
58. P. Rakic Specification of cerebral cortical areas Science 241 1988 170 176
59. P. Rakic A small step for the cell, a giant leap for mankind: A hypothesis of neocortical expansion during evolution Trends Neurosci 18 1995 383 388
60. A. Lukaszewicz, P. Savatier, V. Cortay, P. Giroud, C. Huissoud, and M. Berland et al. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex Neuron 47 2005 353 364
61. L. Mrzljak, H.B.M. Uylings, I. Kostovic, and C.G. van Eden Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study J Comp Neurol 271 1988 355 386
62. L.E. Becker, D.L. Armstrong, G. Chan, and M.M. Wood Dendritic development in human occipital cortical neurons Brain Res 13 1984 117 124
63. M. Marin-Padilla Prenatal and early postnatal ontogenesis of the human motor cortex: A Golgi study. II. The basket-pyramidal system Brain Res 23 1970 185 191
64. S. Takashima, F. Chan, L.E. Becker, and D.L. Armstrong Morphology of the developing visual cortex of the human infant: A quantitative and qualitative Golgi study J Neuropathol Exp Neurol 39 1978 487 501
65. Z. Petanjek, M. Judas, G. Simic, M.R. Rasina, H.B.M. Uylings, P. Rakic, and I. Kostovic Extraordinary neoteny of synaptic spines in the human prefrontal cortex Proc Natl Acad Sci U S A 108 2011 13281 13286
66. E. Anisfeld The onset of social smiling in preterm and full-term infants from two ethnic backgrounds Infant Behav Dev 5 1982 387 395
67. V. Southgate, A. Senju, and G. Csibra Action anticipation through attribution of false belief by two-year-olds Psychol Sci 18 2007 587 592
68. M. Vuksic, Z. Petanjek, M.R. Rasin, and I. Kostovic Perinatal growth of prefrontal layer III pyramids in Down syndrome Pediatr Neurol 27 2002 36 38
69. S. Bianchi, C.D. Stimpson, T. Duka, M.D. Larsen, W.G. Janssen, and Z. Collins et al. Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans Proc Natl Acad Sci U S A 110 suppl 2 2013 10395 10401
70. C.J. Cupp, and E. Uemura Age-related changes in prefrontal cortex of Macaca mulatta: Quantitative analysis of dendritic branching patterns Exp Neurol 69 1980 143 163
71. S.S. Han, L.A. Williams, and K.C. Eggan Constructing and deconstructing stem cell models of neurological disease Neuron 70 2011 626 644
72. G. Konopka, E. Wexler, E. Rosen, Z. Mukamel, G.E. Osborn, and L. Chen Modeling the functional genomics of autism using human neurons Mol Psychiatry 17 2011 202 214
73. M.C. Marchetto, B. Winner, and F.H. Gage Pluripotent stem cells in neurodegenerative and neurodevelopmental diseases Hum Mol Genet 19 2010 R71 R76
74. M. Chahrour, S.Y. Jung, C. Shaw, X. Zhou, S.T. Wong, J. Qin, and H.Y. Zoghbi MeCP2, a key contributor to neurological disease, activates and represses transcription Science 320 2008 1224 1229
75. D.D. Armstrong Neuropathology of Rett syndrome J Child Neurol 20 2005 747 753
76. B. Schule, D.D. Armstrong, H. Vogel, A. Oviedo, and U. Francke Severe congenital encephalopathy caused by mecp2 null mutations in males: Central hypoxia and reduced neuronal dendritic structure Clin Genet 74 2008 116 126
77. M. Amenduni, R. De Filippis, A.Y. Cheung, V. Disciglio, M.C. Epistolato, and F. Ariani et al. iPS cells to model CDKL5-related disorders Eur J Human Genet 19 2011 1246 1255
78. S. Ricciardi, F. Ungaro, M. Hambrock, N. Rademacher, G. Stefanelli, and D. Brambilla et al. CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons Nat Cell Biol 14 2012 911 923
79. K.C. Koenen, T.E. Moffitt, A.L. Roberts, L.T. Martin, L. Kubzansky, and H. Harrington Childhood IQ and adult mental disorders: A test of the cognitive reserve hypothesis Am J Psychiatry 166 2009 50 57
80. K.J. Brennand, and F.H. Gage Modeling psychiatric disorders through reprogramming Dis Model Mech 5 2012 26 32
81. D. Falk Brain lateralization in primates and its evolution in hominids Yearb Phys Anthropol 30 1987 107 125
82. D. Falk, J.C. Redmond Jr, J. Guyer, G.C. Conroy, W. Recheis, G.W. Weber, and H. Seidler Early hominid brain evolution: A new look at old endocasts J Hum Evol 38 2000 695 717
83. C.C. Sherwood, C.D. Stimpson, M.A. Raghanti, D.E. Wildman, M. Uddin, and L.I. Grossman et al. Evolution of increased glia-neuron ratios in the human frontal cortex Proc Natl Acad Sci U S A 103 2006 13606 13611
84. R.A. Raff, and G.A. Wray Heterochrony: Developmental mechanisms and evolutionary results J Evol Biol 2 1989 409 434
85. C.P.E. Zollikofer, and M.S. Ponce De León Kinematics of cranial ontogeny: Heterotopy, heterochrony, and geometric morphometric analysis of growth models J Exp Zool B Mol Dev Evol 302 2004 322 340
86. N. Kouprina, A. Pavlicek, G.H. Mochida, G. Solomon, W. Gersch, and Y.H. Yoon et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion PLoS Biol 2 2004 e126
87. J. Zhang, D.M. Webb, and O. Podlaha Accelerated protein evolution and origins of humans-specific features: Foxp2 as an example Genetics 162 2002 1825 1835
88. Y.Q. Wang, and B. Su Molecular evolution of microcephalin, a gene determining human brain size Hum Mol Genet 13 2004 1131 1137
89. A.P. Jackson, H. Eastwood, S.M. Bell, J. Adu, C. Toomes, and I.M. Carr et al. Identification of Microcephalin, a protein implicated in determining the size of the human brain Am J Hum Genet 71 2002 136 142