Ultrastructural analyses in the hippocampus CA1 field in Shank3-deficient mice

Molecular Autism

Volumn 6, Issue 1, 2015, Pages

  Uppal, Neha ^a,b   Puri, Rishi ^a   Yuk, Frank ^a   Janssen, William G M ^a   Bozdagi Gunal, Ozlem ^a   Harony Nicolas, Hala ^a   Dickstein, Dara L ^a   Buxbaum, Joseph D ^a   Hof, Patrick R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Autism; CA1; Electron microscopy; Hippocampus; Shank3; Stratum radiatum; Synapse

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC VARIABILITY; HETEROZYGOTE; HIPPOCAMPUS; HOMOZYGOTE; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; SHANK3 GENE; STRATUM RADIATUM;

MUS;

EID: 84933531487     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-015-0036-x     Document Type: Article

References (59)

1. Casanova MF, van Kooten IA, Switala AE, van Engeland H, Heinsen H, Steinbusch HW, et al. Minicolumnar abnormalities in autism. Acta Neuropathol. 2006;112:287-303.
2. Jacot-Descombes S, Uppal N, Wicinski B, Santos M, Schmeidler J, Giannakopoulos P, et al. Decreased pyramidal neuron size in Brodmann areas 44 and 45 in patients with autism. Acta Neuropathol. 2012;124:67-79.
3. Raymond GV, Bauman ML, Kemper TL. Hippocampus in autism: a Golgi analysis. Acta Neuropathol. 1996;91:117-9.
4. Uppal N, Wicinski B, Buxbaum JD, Heinsen H, Schmitz C, Hof PR. Neuropathology of the anterior midcingulate cortex in young children with autism. J Neuropathol Exp Neurol. 2014;73:891-902.
5. van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, et al. Neurons in the fusiform gyrus are fewer and smaller in autism. Brain. 2008;131:987-99.
6. Wegiel J, Flory M, Kuchna I, Nowicki K, Ma SY, Imaki H, et al. Neuronal nucleus and cytoplasm volume deficit in children with autism and volume increase in adolescents and adults. Acta Neuropathol Commun. 2015;3:2.
7. Phelan MC, Rogers RC, Saul RA, Stapleton GA, Sweet K, McDermid H, et al. 22q13 deletion syndrome. Am J Med Genet. 2001;101:91-9.
8. Cusmano-Ozog K, Manning MA, Hoyme HE. 22q13.3 deletion syndrome: a recognizable malformation syndrome associated with marked speech and language delay. Am J Med Genet C: Semin Med Genet. 2007;145C:393-8.
9. Dhar SU, del Gaudio D, German JR, Peters SU, Ou Z, Bader PI, et al. 22q13.3 deletion syndrome: clinical and molecular analysis using array CGH. Am J Med Genet A. 2010;152A:573-81.
10. Phelan MC. Deletion 22q13.3 syndrome. Orphanet J Rare Dis. 2008;3:14.
11. Soorya L, Kolevzon A, Zweifach J, Lim T, Dobry Y, Schwartz L, et al. Prospective investigation of autism and genotype-phenotype correlations in 22q13 deletion syndrome and SHANK3 deficiency. Mol Autism. 2013;4:18.
12. Anderlid BM, Schoumans J, Anneren G, Tapia-Paez I, Dumanski J, Blennow E, et al. FISH-mapping of a 100-kb terminal 22q13 deletion. Hum Genet. 2002;110:439-43.
13. Bonaglia MC, Giorda R, Beri S, De Agostini C, Novara F, Fichera M, et al. Molecular mechanisms generating and stabilizing terminal 22q13 deletions in 44 subjects with Phelan/McDermid syndrome. PLoS Genet. 2011;7:e1002173.
14. Bonaglia MC, Giorda R, Borgatti R, Felisari G, Gagliardi C, Selicorni A, et al. Disruption of the ProSAP2 gene in a t(12;22)(q24.1;q13.3) is associated with the 22q13.3 deletion syndrome. Am J Hum Genet. 2001;69:261-8.
15. Bonaglia MC, Giorda R, Mani E, Aceti G, Anderlid BM, Baroncini A, et al. Identification of a recurrent breakpoint within the SHANK3 gene in the 22q13.3 deletion syndrome. J Med Genet. 2006;43:822-8.
16. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, Fauchereau F, et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet. 2007;39:25-7.
17. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, et al. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet. 2008;82:477-88.
18. Moessner R, Marshall CR, Sutcliffe JS, Skaug J, Pinto D, Vincent J, et al. Contribution of SHANK3 mutations to autism spectrum disorder. Am J Hum Genet. 2007;81:1289-97.
19. Kreienkamp HJ. Scaffolding proteins at the postsynaptic density: Shank as the architectural framework. Handb Exp Pharmacol. 2008;186:365-80.
20. Sheng M, Kim E. The Shank family of scaffold proteins. J Cell Sci. 2000;113:1851-6.
21. Boeckers TM, Winter C, Smalla KH, Kreutz MR, Bockmann J, Seidenbecher C, et al. Proline-rich synapse-associated proteins ProSAP1 and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family. Biochem Biophys Res Commun. 1999;264:247-52.
22. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron. 1999;23:569-82.
23. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron. 1999;23:583-92.
24. Uchino S, Wada H, Honda S, Nakamura Y, Ondo Y, Uchiyama T, et al. Direct interaction of post-synaptic density-95/Dlg/ZO-1 domain-containing synaptic molecule Shank3 with GluR1 alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor. J Neurochem. 2006;97:1203-14.
25. Yao I, Hata Y, Hirao K, Deguchi M, Ide N, Takeuchi M, et al. Synamon, a novel neuronal protein interacting with synapse-associated protein 90/postsynaptic density-95-associated protein. J Biol Chem. 1999;274:27463-6.
26. Sugiyama Y, Kawabata I, Sobue K, Okabe S. Determination of absolute protein numbers in single synapses by a GFP-based calibration technique. Nat Methods. 2005;2:677-84.
27. Bozdagi O, Sakurai T, Papapetrou D, Wang X, Dickstein DL, Takahashi N, et al. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol Autism. 2010;1:15.
28. Yang M, Bozdagi O, Scattoni ML, Wohr M, Roullet FI, Katz AM, et al. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. J Neurosci. 2012;32:6525-41.
29. Böckers TM, Segger-Junius M, Iglauer P, Bockmann J, Gundelfinger ED, Kreutz MR, et al. Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3′ untranslated region of Shank1 mRNA. Mol Cell Neurosci. 2004;26:182-90.
30. Boeckers TM, Kreutz MR, Winter C, Zuschratter W, Smalla KH, Sanmarti-Vila L, et al. Proline-rich synapse-associated protein-1/cortactin binding protein 1 (ProSAP1/CortBP1) is a PDZ-domain protein highly enriched in the postsynaptic density. J Neurosci. 1999;19:6506-18.
31. Geinisman Y, de Toledo-Morrell L, Morrell F. Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory. Brain Res. 1986;398:266-75.
32. Geinisman Y, de Toledo-Morrell L, Morrell F. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc Natl Acad Sci U S A. 1986;83:3027-31.
33. Jones DG, Harris RJ. An analysis of contemporary morphological concepts of synaptic remodeling in the CNS: perforated synapses revisited. Rev Neurosci. 1995;6:177-219.
34. Geinisman Y, Disterhoft JF, Gundersen HJ, McEchron M, Persina IS, Power JM, et al. Remodeling of hippocampal synapses after hippocampus-dependent associative learning. J Comp Neurol. 2000;417:49-59.
35. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci. 2004;24:7648-53.
36. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol. 2004;468:86-95.
37. Carlin RK, Siekevitz P. Plasticity in the central nervous system: do synapses divide? Proc Natl Acad Sci U S A. 1983;80:3517-21.
38. Jones DG. Synaptic plasticity and perforated synapses: their relevance for an understanding of abnormal synaptic organization. APMIS Suppl. 1993;40:25-34.
39. Sorra K, Fiala JC, Harris K. Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation. J Comp Neurol. 1998;398:225-40.
40. Bloss EB, Puri R, Yuk F, Punsoni M, Hara Y, Janssen WG, et al. Morphological and molecular changes in aging rat prelimbic prefrontal cortical synapses. Neurobiol Aging. 2013;34:200-10.
41. Adams MM, Shah RA, Janssen WG, Morrison JH. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci U S A. 2001;98:8071-6.
42. Lim S, Naisbitt S, Yoon J, Hwang JI, Suh PG, Sheng M, Kim E. Characterization of the Shank family of synaptic proteins. Multiple genes, alternative splicing, and differential expression in brain and development. J Biol Chem. 1999;274:29510-8.
43. Hayashi MK, Tang C, Verpelli C, Narayanan R, Stearns MH, Xu RM, et al. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell. 2009;137:159-71.
44. Boeckers TM, Liedtke T, Spilker C, Dresbach T, Bockmann J, Kreutz MR, et al. C-terminal synaptic targeting elements for postsynaptic density proteins ProSAP1/Shank2 and ProSAP2/Shank3. J Neurochem. 2005;92:519-24.
45. Tao-Cheng JH, Dosemeci A, Gallant PE, Smith C, Reese T. Activity induced changes in the distribution of Shanks at hippocampal synapses. Neuroscience. 2010;168:11-7.
46. Schmeisser MJ, Ey E, Wegener S, Bockmann J, Stempel AV, Kuebler A, et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature. 2012;486:256-60.
47. Sala C, Piech V, Wilson NR, Passafaro M, Liu G, Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron. 2001;31:115-30.
48. Grabrucker AM. A role for synaptic zinc in ProSAP/Shank PSD scaffold malformation in autism spectrum disorders. Dev Neurobiol. 2013;74:136-46.
49. Isaac JT, Nicoll RA, Malenka RC. Evidence for silent synapses: implications for the expression of LTP. Neuron. 1995;15:427-34.
50. Geinisman Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb Cortex. 2000;10:952-62.
51. Liao D, Hessler NA, Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 1995;375:400-4.
52. Harris KM, Jensen FE, Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci. 1992;12:2685-705.
53. Peters A, Kaiserman-Abramof IR. The small pyramidal neuron of the rat cerebral cortex: the synapses upon dendritic spines. Z Zellforsch Mikrosk Anat. 1969;100:487-506.
54. Shepherd JD, Huganir RL. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol. 2007;23:613-43.
55. Geinisman Y, de Toledo-Morrell L, Morrell F. Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res. 1991;566:77-88.
56. Schultz RT. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Devl Neuroscience. 2005;23:125-41.
57. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, et al. The amygdala is enlarged in children but not adults with autism; the hippocampus is enlarged at all ages. J Neurosci. 2004;24:6392-401.
58. Blatt GJ, Fitzgerald CM, Guptill JT, Booker AB, Kemper TL, Bauman ML. Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J Autism Dev Disord. 2001;31:537-43.
59. Guptill JT, Booker AB, Gibbs TT, Kemper TL, Bauman ML, Blatt GJ. [3H]-flunitrazepam-labeled benzodiazepine binding sites in the hippocampal formation in autism: a multiple concentration autoradiographic study. J Autism Dev Disord. 2007;37:911-20.