An autism-associated variant of epac2 reveals a role for ras/epac2 signaling in controlling basal dendrite maintenance in mice

PLoS Biology

Volumn 10, Issue 6, 2012, Pages

  Srivastava, Deepak P ^a,b   Woolfrey, Kevin M ^a   Jones, Kelly A ^a   Anderson, Charles T ^a   Smith, Katharine R ^a   Russell, Theron A ^a   Lee, Hyerin ^c   Yasvoina, Marina V ^a   Wokosin, David L ^a   Ozdinler, P Hande ^a   Shepherd, Gordon M G ^a   Penzes, Peter ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CYCLIC AMP2; GUANOSINE TRIPHOSPHATASE; INITIATION FACTOR; RAP PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAPGEF4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTISM; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; EMBRYO; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CYCLIC AMP2 GENE; FEMALE; GENE; GENETIC VARIABILITY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PYRAMIDAL NERVE CELL; RNA INTERFERENCE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL COMMUNICATION; CELL STRAIN HEK293; GENETICS; HUMAN; METABOLISM; NERVE CELL; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

MUS;

ANIMALS; AUTISTIC DISORDER; CELL COMMUNICATION; DENDRITES; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEURONS; RAS PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84863668613     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001350     Document Type: Article

References (53)

1. Jan Y. N, Jan L. Y, (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11: 316-328.
2. Parrish J. Z, Emoto K, Kim M. D, Jan Y. N, (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30: 399-423.
3. Broadbelt K, Byne W, Jones L. B, (2002) Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res 58: 75-81.
4. Mukaetova-Ladinska E. B, Arnold H, Jaros E, Perry R, Perry E, (2004) Depletion of MAP2 expression and laminar cytoarchitectonic changes in dorsolateral prefrontal cortex in adult autistic individuals. Neuropathol Appl Neurobiol 30: 615-623.
5. Raymond G. V, Bauman M. L, Kemper T. L, (1996) Hippocampus in autism: a Golgi analysis. Acta Neuropathol 91: 117-119.
6. Armstrong D, Dunn J. K, Antalffy B, Trivedi R, (1995) Selective dendritic alterations in the cortex of Rett syndrome. J Neuropathol Exp Neurol 54: 195-201.
7. Becker L, Mito T, Takashima S, Onodera K, (1991) Growth and development of the brain in Down syndrome. Prog Clin Biol Res 373: 133-152.
8. Becker L. E, Armstrong D. L, Chan F, (1986) Dendritic atrophy in children with Down's syndrome. Ann Neurol 20: 520-526.
9. Kaufmann W. E, Moser H. W, (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10: 981-991.
10. London M, Hausser M, (2005) Dendritic computation. Annu Rev Neurosci 28: 503-532.
11. Spruston N, (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9: 206-221.
12. Milojkovic B. A, Radojicic M. S, Goldman-Rakic P. S, Antic S. D, (2004) Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree. J Physiol 558: 193-211.
13. Petreanu L, Mao T, Sternson S. M, Svoboda K, (2009) The subcellular organization of neocortical excitatory connections. Nature 457: 1142-1145.
14. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
15. Bose M, Munoz-Llancao P, Roychowdhury S, Nichols J. A, Jakkamsetti V, et al. (2009) Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse 64: 97-110.
16. Gelfo F, De Bartolo P, Giovine A, Petrosini L, Leggio M. G, (2009) Layer and regional effects of environmental enrichment on the pyramidal neuron morphology of the rat. Neurobiol Learn Mem 91: 353-365.
17. Maravall M, Koh I. Y, Lindquist W. B, Svoboda K, (2004) Experience-dependent changes in basal dendritic branching of layer 2/3 pyramidal neurons during a critical period for developmental plasticity in rat barrel cortex. Cereb Cortex 14: 655-664.
18. Chow D. K, Groszer M, Pribadi M, Machniki M, Carmichael S. T, et al. (2009) Laminar and compartmental regulation of dendritic growth in mature cortex. Nat Neurosci 12: 116-118.
19. Wang H. D, Stanwood G. D, Grandy D. K, Deutch A. Y, (2009) Dystrophic dendrites in prefrontal cortical pyramidal cells of dopamine D1 and D2 but not D4 receptor knockout mice. Brain Res 1300: 58-64.
20. Ye X, Carew T. J, (2010) Small G protein signaling in neuronal plasticity and memory formation: the specific role of ras family proteins. Neuron 68: 340-361.
21. Kawasaki H, Springett G. M, Mochizuki N, Toki S, Nakaya M, et al. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282: 2275-2279.
22. Woolfrey K. M, Srivastava D. P, Photowala H, Yamashita M, Barbolina M. V, et al. (2009) Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat Neurosci 12: 1275-1284.
23. Gelinas J. N, Banko J. L, Peters M. M, Klann E, Weeber E. J, et al. (2008) Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn Mem 15: 403-411.
24. Kelly M. P, Stein J. M, Vecsey C. G, Favilla C, Yang X, et al. (2009) Developmental etiology for neuroanatomical and cognitive deficits in mice overexpressing Galphas, a G-protein subunit genetically linked to schizophrenia. Mol Psychiatry 14: 347, 398-415.
25. Yang Y, Shu X, Liu D, Shang Y, Wu Y, et al. (2012) EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73: 774-788.
26. Mironov S. L, Skorova E. Y, Kugler S, (2011) Epac-mediated cAMP-signalling in the mouse model of Rett Syndrome. Neuropharmacology 60: 869-877.
27. Kiermayer S, Biondi R. M, Imig J, Plotz G, Haupenthal J, et al. (2005) Epac activation converts cAMP from a proliferative into a differentiation signal in PC12 cells. Mol Biol Cell 16: 5639-5648.
28. McClellan J, King M. C, (2010) Genomic analysis of mental illness: a changing landscape. JAMA 303: 2523-2524.
29. Bacchelli E, Blasi F, Biondolillo M, Lamb J. A, Bonora E, et al. (2003) Screening of nine candidate genes for autism on chromosome 2q reveals rare nonsynonymous variants in the cAMP-GEFII gene. Mol Psychiatry 8: 916-924.
30. Taniguchi Y, Young-Pearse T, Sawa A, Kamiya A, (2011) In utero electroporation as a tool for genetic manipulation in vivo to study psychiatric disorders: from genes to circuits and behaviors. Neuroscientist.
31. Qiu S, Anderson C. T, Levitt P, Shepherd G. M, (2011) Circuit-specific intracortical hyperconnectivity in mice with deletion of the autism-associated met receptor tyrosine kinase. J Neurosci 31: 5855-5864.
32. Xie Z, Srivastava D. P, Photowala H, Kai L, Cahill M. E, et al. (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56: 640-656.
33. Cohen S, Gabel H. W, Hemberg M, Hutchinson A. N, Sadacca L. A, et al. (2011) Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function. Neuron 72: 72-85.
34. Horton A. C, Racz B, Monson E. E, Lin A. L, Weinberg R. J, et al. (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48: 757-771.
35. Horton A. C, Yi J. J, Ehlers M. D, (2006) Cell type-specific dendritic polarity in the absence of spatially organized external cues. Brain Cell Biol 35: 29-38.
36. Threadgill R, Bobb K, Ghosh A, (1997) Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19: 625-634.
37. Sholl D. A, (1956) The measurable parameters of the cerebral cortex and their significance in its organization. Prog Neurobiol pp. 324-333.
38. Chen Y, Wang P. Y, Ghosh A, (2005) Regulation of cortical dendrite development by Rap1 signaling. Mol Cell Neurosci 28: 215-228.
39. Kumar V, Zhang M. X, Swank M. W, Kunz J, Wu G. Y, (2005) Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25: 11288-11299.
40. Huang J, Furuya A, Furuichi T, (2007) Very-KIND, a KIND domain containing RasGEF, controls dendrite growth by linking Ras small GTPases and MAP2. J Cell Biol 179: 539-552.
41. Gartner U, Alpar A, Reimann F, Seeger G, Heumann R, et al. (2004) Constitutive Ras activity induces hippocampal hypertrophy and remodeling of pyramidal neurons in synRas mice. J Neurosci Res 77: 630-641.
42. Alpar A, Naumann N, Hartig W, Arendt T, Gartner U, (2008) Enhanced Ras activity preserves dendritic size and extension as well as synaptic contacts of neurons after functional deprivation in synRas mice. Eur J Neurosci 27: 3083-3094.
43. Li Y, Asuri S, Rebhun J. F, Castro A. F, Paranavitana N. C, et al. (2006) The RAP1 guanine nucleotide exchange factor Epac2 couples cyclic AMP and Ras signals at the plasma membrane. J Biol Chem 281: 2506-2514.
44. Gartner U, Alpar A, Behrbohm J, Heumann R, Arendt T, (2005) Enhanced Ras activity promotes spine formation in synRas mice neocortex. Neuroreport 16: 149-152.
45. Vazquez L. E, Chen H. J, Sokolova I, Knuesel I, Kennedy M. B, (2004) SynGAP regulates spine formation. J Neurosci 24: 8862-8872.
46. Jones K. A, Srivastava D. P, Allen J. A, Strachan R. T, Roth B. L, et al. (2009) Rapid modulation of spine morphology by the 5-HT2A serotonin receptor through kalirin-7 signaling. Proc Natl Acad Sci U S A 106: 19575-19580.
47. Takashima S, Becker L. E, Armstrong D. L, Chan F, (1981) Abnormal neuronal development in the visual cortex of the human fetus and infant with Down's Syndrome. A quantitative and qualitative Golgi study. Brain Res 225: 1-21.
48. Romand S, Wang Y, Toledo-Rodriguez M, Markram H, (2011) Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat 5: 5.
49. Liu C, Takahashi M, Li Y, Song S, Dillon T. J, et al. (2008) Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Mol Cell Biol 28: 7109-7125.
50. McClellan J, King M. C, (2010) Genetic heterogeneity in human disease. Cell 141: 210-217.
51. Kryukov G. V, Pennacchio L. A, Sunyaev S. R, (2007) Most rare missense alleles are deleterious in humans: implications for complex disease and association studies. Am J Hum Genet 80: 727-739.
52. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
53. Meijering E, Jacob M, Sarria J. C, Steiner P, Hirling H, et al. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58: 167-176.