Prenatal neurogenesis in autism spectrum disorders

Frontiers in Chemistry

Volumn 4, Issue MAR, 2016, Pages

  Kaushik, Gaurav ^a,b   Zarbalis, Konstantinos S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

Author keywords

Autism spectrum disorders; Cerebral cortex; Megalencephaly; Neural progenitors; Neuronal migration

Indexed keywords

EID: 84969540886     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2016.00012     Document Type: Short Survey

References (82)

1. Amaral, D. G., Schumann, C. M., and Nordahl, C. W. (2008). Neuroanatomy of autism. Trends Neurosci. 31, 137-145. doi: 10.1016/j.tins.2007.12.005
2. Bailey, A., Luthert, P., Dean, A., Harding, B., Janota, I., Montgomery, M., et al. (1998). A clinicopathological study of autism. Brain J. Neurol. 121 (Pt 5), 889-905. doi: 10.1093/brain/121.5.889
3. Baron-Cohen, S., and Belmonte, M. K. (2005). Autism: a window onto the development of the social and the analytic brain. Ann.Rev. Neurosci. 28, 109-126. doi: 10.1146/annurev.neuro.27.070203.144137
4. Bernier, R., Golzio, C., Xiong, B., Stessman, H. A., Coe, B. P., Penn, O., et al. (2014). Disruptive CHD8 mutations define a subtype of autism early in development. Cell 158, 263-276. doi: 10.1016/j.cell.2014.06.017
5. Bloss, C. S., and Courchesne, E. (2007). MRI neuroanatomy in young girls with autism: a preliminary study. J. Am. Acad. Child Adolesc. Psychiatry 46, 515-523. doi: 10.1097/chi.0b013e318030e28b
6. Blumberg, S. J., Bramlett, M. D., Kogan, M. D., Schieve, L. A., Jones, J. R., and Lu, M. C. (2013). Changes in Prevalence of Parent-Reported Autism Spectrum Disorder in School-Aged U.S. Children: 2007 to 2011-2012, Vol. 65. National Health Statistics Reports, 1-12.
7. Braunschweig, D., Krakowiak, P., Duncanson, P., Boyce, R., Hansen, R. L., Ashwood, P., et al. (2013). Autism-specific maternal autoantibodies recognize critical proteins in developing brain. Transl. Psychiatry 3, e277. doi: 10.1038/tp.2013.50
8. Butler, M. G., Dasouki, M. J., Zhou, X. P., Talebizadeh, Z., Brown, M., Takahashi, T. N., et al. (2005). Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J. Med. Genet. 42, 318-321. doi: 10.1136/jmg.2004.024646
9. Buxbaum, J. D., Cai, G., Chaste, P., Nygren, G., Goldsmith, J., Reichert, J., et al. (2007). Mutation screening of the PTEN gene in patients with autism spectrum disorders and macrocephaly. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B, 484-491. doi: 10.1002/ajmg.b.30493
10. Campbell, D. J., Chang, J., and Chawarska, K. (2014). Early generalized overgrowth in autism spectrum disorder: prevalence rates, gender effects, and clinical outcomes. J. Am. Acad. Child Adolesc. Psychiatry 53, 1063.e5-1073.e5. doi: 10.1016/j.jaac.2014.07.008
11. Carper, R. A., Moses, P., Tigue, Z. D., and Courchesne, E. (2002). Cerebral lobes in autism: early hyperplasia and abnormal age effects. Neuroimage 16, 1038-1051. doi: 10.1006/nimg.2002.1099
12. Casanova, M. F., El-Baz, A. S., Kamat, S. S., Dombroski, B. A., Khalifa, F., Elnakib, A., et al. (2013). Focal cortical dysplasias in autism spectrum disorders. Acta Neuropatholog. Commun. 1, 67. doi: 10.1186/2051-5960-1-67
13. Caviness, V. S. Jr., Nowakowski, R. S., and Bhide, P. G. (2009). Neocortical neurogenesis: morphogenetic gradients and beyond. Trends Neurosci. 32, 443-450. doi: 10.1016/j.tins.2009.05.003
14. Courchesne, E., Campbell, K., and Solso, S. (2011a). Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res. 1380, 138-145. doi: 10.1016/j.brainres.2010.09.101
15. Courchesne, E., Carper, R., and Akshoomoff, N. (2003). Evidence of brain overgrowth in the first year of life in autism. JAMA 290, 337-344. doi: 10.1001/jama.290.3.337
16. Courchesne, E., Karns, C. M., Davis, H. R., Ziccardi, R., Carper, R. A., Tigue, Z. D., et al. (2001). Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology 57, 245-254. doi: 10.1212/WNL.57.2.245
17. Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., et al. (2011b). Neuron number and size in prefrontal cortex of children with autism. JAMA 306, 2001-2010. doi: 10.1001/jama.2011.1638
18. Courchesne, 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
19. Danielsson, S., Gillberg, I. C., Billstedt, E., Gillberg, C., and Olsson, I. (2005). Epilepsy in young adults with autism: a prospective population-based follow-up study of 120 individuals diagnosed in childhood. Epilepsia 46, 918-923. doi: 10.1111/j.1528-1167.2005.57504.x
20. Ettinger, A. W., Wilsch-Bräuninger, M., Marzesco, A. M., Bickle, M., Lohmann, A., Maliga, Z., et al. (2011). Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat. Commun. 2, 503. doi: 10.1038/ncomms1511
21. Fidler, D. J., Bailey, J. N., and Smalley, S. L. (2000). Macrocephaly in autism and other pervasive developmental disorders. Dev. Med. Child Neurol. 42, 737-740. doi: 10.1017/S0012162200001365
22. Filimonenko, M., Isakson, P., Finley, K. D., Anderson, M., Jeong, H., Melia, T. J., et al. (2010). The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 38, 265-279. doi: 10.1016/j.molcel.2010.04.007
23. Fischbach, G. D., and Lord, C. (2010). The Simons Simplex Collection: a resource for identification of autism genetic risk factors. Neuron 68, 192-195. doi: 10.1016/j.neuron.2010.10.006
24. Fish, J. L., Dehay, C., Kennedy, H., and Huttner, W. B. (2008). Making bigger brains-the evolution of neural-progenitor-cell division. J. Cell Sci. 121, 2783-2793. doi: 10.1242/jcs.023465
25. Fombonne, E., Rogé, B., Claverie, J., Courty, S., and Fremolle, J. (1999). Microcephaly and macrocephaly in autism. J. Autism Dev. Disord. 29, 113-119. doi: 10.1023/A:1023036509476
26. Friedman, S. D., Shaw, D. W., Artru, A. A., Dawson, G., Petropoulos, H., and Dager, S. R. (2006). Gray and white matter brain chemistry in young children with autism. Arch. Gen. Psychiatry 63, 786-794. doi: 10.1001/archpsyc.63.7.786
27. Froehlich, W., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., et al. (2013). Head circumferences in twins with and without autism spectrum disorders. J. Autism Dev. Disord. 43, 2026-2037. doi: 10.1007/s10803-012-1751-1
28. Gasquoine, P. G. (2014). Contributions of the insula to cognition and emotion. Neuropsychol. Rev. 24, 77-87. doi: 10.1007/s11065-014-9246-9
29. Geschwind, D. H. (2011). Genetics of autism spectrum disorders. Trends Cogn. Sci. (Regul. Ed). 15, 409-416. doi: 10.1016/j.tics.2011.07.003
30. Goffin, A., Hoefsloot, L. H., Bosgoed, E., Swillen, A., and Fryns, J. P. (2001). PTEN mutation in a family with Cowden syndrome and autism. Am. J. Med. Genet. 105, 521-524. doi: 10.1002/ajmg.1477
31. Golzio, C., Willer, J., Talkowski, M. E., Oh, E. C., Taniguchi, Y., Jacquemont, S., et al. (2012). KCTD13 is a major driver of mirrored neuroanatomical phenotypes of the 16p11.2 copy number variant. Nature 485, 363-367. doi: 10.1038/nature11091
32. Gotts, S. J., Simmons, W. K., Milbury, L. A., Wallace, G. L., Cox, R. W., and Martin, A. (2012). Fractionation of social brain circuits in autism spectrum disorders. Brain J.Neurol. 135, 2711-2725. doi: 10.1093/brain/aws160
33. Groszer, M., Erickson, R., Scripture-Adams, D. D., Lesche, R., Trumpp, A., Zack, J. A., et al. (2001). Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186-2189. doi: 10.1126/science.1065518
34. Gupta, A., Tsai, L. H., and Wynshaw-Boris, A. (2002). Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3, 342-355. doi: 10.1038/nrg799
35. Happé, F., Ronald, A., and Plomin, R. (2006). Time to give up on a single explanation for autism. Nat. Neurosci. 9, 1218-1220. doi: 10.1038/nn1770
36. Hazlett, H. C., Poe, M., Gerig, G., Smith, R. G., Provenzale, J., Ross, A., et al. (2005). Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. Arch. Gen. Psychiatry 62, 1366-1376. doi: 10.1001/archpsyc.62.12.1366
37. He, H., Tan, C. K., Downey, K. M., and So, A. G. (2001). A tumor necrosis factor alpha-and interleukin 6-inducible protein that interacts with the small subunit of DNA polymerase delta and proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. U.S.A. 98, 11979-11984. doi: 10.1073/pnas.221452098
38. Hutsler, J. J., Love, T., and Zhang, H. (2007). Histological and magnetic resonance imaging assessment of cortical layering and thickness in autism spectrum disorders. Biol. Psychiatry 61, 449-457. doi: 10.1016/j.biopsych.2006.01.015
39. Iossifov, I., O'Roak, B. J., Sanders, S. J., Ronemus, M., Krumm, N., Levy, D., et al. (2014). The contribution of de novo coding mutations to autism spectrum disorder. Nature 515, 216-221. doi: 10.1038/nature13908
40. Iossifov, I., Ronemus, M., Levy, D., Wang, Z., Hakker, I., Rosenbaum, J., et al. (2012). De novo gene disruptions in children on the autistic spectrum. Neuron 74, 285-299. doi: 10.1016/j.neuron.2012.04.009
41. Isakson, P., Lystad, A. H., Breen, K., Koster, G., Stenmark, H., and Simonsen, A. (2013). TRAF6 mediates ubiquitination of KIF23/MKLP1 and is required for midbody ring degradation by selective autophagy. Autophagy 9, 1955-1964. doi: 10.4161/auto.26085
42. Kates, W. R., Burnette, C. P., Eliez, S., Strunge, L. A., Kaplan, D., Landa, R., et al. (2004). Neuroanatomic variation in monozygotic twin pairs discordant for the narrow phenotype for autism. Am. J. Psychiatry 161, 539-546. doi: 10.1176/appi.ajp.161.3.539
43. Kong, A., Frigge, M. L., Masson, G., Besenbacher, S., Sulem, P., Magnusson, G., et al. (2012). Rate of de novo mutations and the importance of father's age to disease risk. Nature 488, 471-475. doi: 10.1038/nature11396
44. Kong, S. W., Collins, C. D., Shimizu-Motohashi, Y., Holm, I. A., Campbell, M. G., Lee, I. H., et al. (2012). Characteristics and predictive value of blood transcriptome signature in males with autism spectrum disorders. PLoS ONE 7:e49475. doi: 10.1371/journal.pone.0049475
45. Kriegstein, A. R., and Noctor, S. C. (2004). Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392-399. doi: 10.1016/j.tins.2004.05.001
46. Kuo, T. C., Chen, C. T., Baron, D., Onder, T. T., Loewer, S., Almeida, S., et al. (2011). Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat. Cell Biol. 13, 1214-1223. doi: 10.1038/ncb2332
47. Lin, G. N., Corominas, R., Lemmens, I., Yang, X., Tavernier, J., Hill, D. E., et al. (2015). Spatiotemporal 16p11.2 protein network implicates cortical late mid-fetal brain development and KCTD13-Cul3-RhoA pathway in psychiatric diseases. Neuron 85, 742-754. doi: 10.1016/j.neuron.2015.01.010
48. Lundström, S., Reichenberg, A., Anckarsater, H., Lichtenstein, P., and Gillberg, C. (2015). Autism phenotype versus registered diagnosis in Swedish children: prevalence trends over 10 years in general population samples. BMJ 350, h1961. doi: 10.1136/bmj.h1961
49. Martínez-Cerdeno, V., Camacho, J., Fox, E., Miller, E., Ariza, J., Kienzle, D., et al. (2014). Prenatal exposure to autism-specific maternal autoantibodies alters proliferation of cortical neural precursor cells, enlarges brain, and increases neuronal size in adult animals. Cereb. Cortex. 26, 374-383. doi: 10.1093/cercor/bhu291
50. McCarthy, S. E., Makarov, V., Kirov, G., Addington, A. M., McClellan, J., Yoon, S., et al. (2009). Microduplications of 16p11.2 are associated with schizophrenia. Nat. Genet. 41, 1223-1227. doi: 10.1038/ng.474
51. McPartland, J. C., Coffman, M., and Pelphrey, K. A. (2011). Recent advances in understanding the neural bases of autism spectrum disorder. Curr. Opin. Pediatr. 23, 628-632. doi: 10.1097/MOP.0b013e32834cb9c9
52. Morgan, J. T., Barger, N., Amaral, D. G., and Schumann, C. M. (2014). Stereological study of amygdala glial populations in adolescents and adults with autism spectrum disorder. PLoS ONE 9:e110356. doi: 10.1371/journal.pone.0110356
53. Mouridsen, S. E., Rich, B., and Isager, T. (2011). A longitudinal study of epilepsy and other central nervous system diseases in individuals with and without a history of infantile autism. Brain Dev. 33, 361-366. doi: 10.1016/j.braindev.2010.07.002
54. Nadarajah, B., and Parnavelas, J. G. (2002). Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 3, 423-432. doi: 10.1038/nrn845
55. Neale, B. M., Kou, Y., Liu, L., Ma'ayan, A., Samocha, K. E., and Sabo, A. (2012). Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 485, 242-245. doi: 10.1038/nature11011
56. Nordahl, C. W., Braunschweig, D., Iosif, A. M., Lee, A., Rogers, S., Ashwood, P., et al. (2013). Maternal autoantibodies are associated with abnormal brain enlargement in a subgroup of children with autism spectrum disorder. Brain Behav. Immun. 30, 61-65. doi: 10.1016/j.bbi.2013.01.084
57. Nordahl, C. W., Lange, N., Li, D. D., Barnett, L. A., Lee, A., Buonocore, M. H., et al. (2011). Brain enlargement is associated with regression in preschool-age boys with autism spectrum disorders. Proc. Natl. Acad. Sci. U.S.A. 108, 20195-20200. doi: 10.1073/pnas.1107560108
58. O'Roak, B. J., Deriziotis, P., Lee, C., Vives, L., Schwartz, J. J., Girirajan, S., et al. (2011). Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat. Genet. 43, 585-589. doi: 10.1038/ng.835
59. O'Roak, B. J., Vives, L., Girirajan, S., Karakoc, E., Krumm, N., Coe, B. P., et al. (2012). Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485, 246-250. doi: 10.1038/nature10989
60. Orosco, L. A., Ross, A. P., Cates, S. L., Scott, S. E., Wu, D., Sohn, J., et al. (2014). Loss of Wdfy3 in mice alters cerebral cortical neurogenesis reflecting aspects of the autism pathology. Nat. Commun. 5, 4692. doi: 10.1038/ncomms5692
61. Palmer, R. F., Walker, T., Mandell, D., Bayles, B., and Miller, C. S. (2010). Explaining low rates of autism among hispanic schoolchildren in Texas. Am. J. Public Health 100, 270-272. doi: 10.2105/AJPH.2008.150565
62. Parikshak, N. N., Luo, R., Zhang, A., Won, H., Lowe, J. K., Chandran, V., et al. (2013). Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell 155, 1008-1021. doi: 10.1016/j.cell.2013.10.031
63. Parner, E. T., Thorsen, P., Dixon, G., de Klerk, N., Leonard, H., Nassar, N., et al. (2011). A comparison of autism prevalence trends in Denmark and Western Australia. J. Autism Dev. Disord. 41, 1601-1608. doi: 10.1007/s10803-011-1186-0
64. Paula, C. S., Ribeiro, S. H., Fombonne, E., and Mercadante, M. T. (2011). Brief report: prevalence of pervasive developmental disorder in brazil: a pilot study. J. Autism Dev. Disord. 41, 1738-1742. doi: 10.1007/s10803-011-1200-6
65. Pelphrey, K. A., and Carter, E. J. (2008). Brain mechanisms for social perception: lessons from autism and typical development. Ann. N.Y. Acad. Sci. 1145, 283-299. doi: 10.1196/annals.1416.007
66. Rakic, S., and Zecevic, N. (2000). Programmed cell death in the developing human telencephalon. Eur. J. Neurosci. 12, 2721-2734. doi: 10.1046/j.1460-9568.2000.00153.x
67. Redcay, E. (2008). The superior temporal sulcus performs a common function for social and speech perception: implications for the emergence of autism. Neurosci. Biobehav. Rev. 32, 123-142. doi: 10.1016/j.neubiorev.2007.06.004
68. Redcay, E., and Courchesne, E. (2005). When is the brain enlarged in autism? A meta-analysis of all brain size reports. Biol. Psychiatry 58, 1-9. doi: 10.1016/j.biopsych.2005.03.026
69. Sacco, R., Militerni, R., Frolli, A., Bravaccio, C., Gritti, A., Elia, M., et al. (2007). Clinical, morphological, and biochemical correlates of head circumference in autism. Biol. Psychiatry 62, 1038-1047. doi: 10.1016/j.biopsych.2007.04.039
70. Sanders, S. J., Murtha, M. T., Gupta, A. R., Murdoch, J. D., Raubeson, M. J., Willsey, A. J., et al. (2012). De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 485, 237-241. doi: 10.1038/nature10945
71. Schumann, C. M., Bloss, C. S., Barnes, C. C., Wideman, G. M., Carper, R. A., Akshoomoff, N., et al. (2010). Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J. Neurosci. 30, 4419-4427. doi: 10.1523/JNEUROSCI.5714-09.2010
72. Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., Buonocore, M. H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci. 24, 6392-6401. doi: 10.1523/JNEUROSCI.1297-04.2004
73. Singer, J. D., Gurian-West, M., Clurman, B., and Roberts, J. M. (1999). Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev. 13, 2375-2387. doi: 10.1101/gad.13.18.2375
74. Sparks, B. F., Friedman, S. D., Shaw, D. W., Aylward, E. H., Echelard, D., Artru, A. A., et al. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology 59, 184-192. doi: 10.1212/WNL.59.2.184
75. Stoner, R., Chow, M. L., Boyle, M. P., Sunkin, S. M., Mouton, P. R., Roy, S., et al. (2014). Patches of disorganization in the neocortex of children with autism. N. Engl. J. Med. 370, 1209-1219. doi: 10.1056/NEJMoa1307491
76. Sugathan, A., Biagioli, M., Golzio, C., Erdin, S., Blumenthal, I., Manavalan, P., et al. (2014). CHD8 regulates neurodevelopmental pathways associated with autism spectrum disorder in neural progenitors. Proc. Natl. Acad. Sci. U.S.A. 111, E4468-E4477. doi: 10.1073/pnas.1405266111
77. Toro, R., Konyukh, M., Delorme, R., Leblond, C., Chaste, P., Fauchereau, F., et al. (2010). Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet. 26, 363-372. doi: 10.1016/j.tig.2010.05.007
78. Varga, E. A., Pastore, M., Prior, T., Herman, G. E., and McBride, K. L. (2009). The prevalence of PTEN mutations in a clinical pediatric cohort with autism spectrum disorders, developmental delay, and macrocephaly. Genet. Med. 11, 111-117. doi: 10.1097/GIM.0b013e31818fd762
79. Wegiel, J., Kuchna, I., Nowicki, K., Imaki, H., Wegiel, J., Marchi, E., et al. (2010). The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 119, 755-770. doi: 10.1007/s00401-010-0655-4
80. Weiss, L. A., Shen, Y., Korn, J. M., Arking, D. E., Miller, D. T., Fossdal, R., et al. (2008). Association between microdeletion and microduplication at 16p11.2 and autism. N. Engl. J. Med. 358, 667-675. doi: 10.1056/NEJMoa075974
81. Willsey, A. J., Sanders, S. J., Li, M., Dong, S., Tebbenkamp, A. T., Muhle, R. A., et al. (2013). Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell 155, 997-1007. doi: 10.1016/j.cell.2013.10.020
82. Zhao, H., Dupont, J., Yakar, S., Karas, M., and LeRoith, D. (2004). PTEN inhibits cell proliferation and induces apoptosis by downregulating cell surface IGF-IR expression in prostate cancer cells. Oncogene 23, 786-794. doi: 10.1038/sj.onc.1207162