Evidence of cell-nonautonomous changes in dendrite and dendritic spine morphology in the met-signaling-deficient mouse forebrain

Journal of Comparative Neurology

Volumn 518, Issue 21, 2010, Pages 4463-4478

  Judson, Matthew C ^a   Eagleson, Kathie L ^b   Wang, Lily ^c   Levitt, Pat ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Anterior cingulate cortex; Autism spectrum disorders; Emx1Cre Metfx fx; Met receptor tyrosine kinase signaling

Indexed keywords

LUCIFER YELLOW; SCATTER FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL COUNT; CELL STRUCTURE; CINGULATE GYRUS; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DENDRITIC SPINE; FOREBRAIN; IN VIVO STUDY; MALE; MORPHOMETRICS; MOUSE; NEOCORTEX; NERVE CELL DIFFERENTIATION; NONHUMAN; POSTNATAL DEVELOPMENT; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY NERVE; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; CEREBRAL CORTEX; DENDRITES; DENDRITIC SPINES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PROTO-ONCOGENE PROTEINS C-MET; PYRAMIDAL CELLS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 77957924746     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22467     Document Type: Article

References (67)

1. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R.2007. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1:131-143.
2. Bill BR, Geschwind DH. 2009. Genetic advances in autism: heterogeneity and convergence on shared pathways. Curr Opin Genet Dev 19:271-278.
3. Bolshakov VY, Siegelbaum SA. 1995. Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269:1730-1734.
4. Box GEP, Cox DR. 1964. An analysis of transformations. J Roy Stat Soc B 26:211-252.
5. Campbell DB, Sutcliffe JS, Ebert PJ, Militerni R, Bravaccio C, Trillo S, Elia M, Schneider C, Melmed R, Sacco R, Persico AM, Levitt P. 2006. A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci USA 103:16834-16839.
6. Campbell DB, D'Oronzio R, Garbett K, Ebert PJ, Mirnics K, Levitt P, Persico AM. 2007. Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann Neurol 62: 243-250.
7. Campbell DB, Li C, Sutcliffe JS, Persico AM, Levitt P. 2008. Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder. Autism Res 1:159-168.
8. Campbell DB, Warren D, Sutcliffe JS, Lee EB, Levitt P. 2009. Association of MET with social and communication phenotypes in individuals with autism spectrum disorder. Am J Med Genet B Neuropsychiatr Genet (in press).
9. Casanova MF. 2006. Neuropathological and genetic findings in autism: the significance of a putative minicolumnopathy. Neuroscientist 12:435-441.
10. Casanova MF, Buxhoeveden DP, Switala AE, Roy E. 2002. Minicolumnar pathology in autism. Neurology 58:428-432.
11. Caton A, Hacker A, Naeem A, Livet J, Maina F, Bladt F, Klein R, Birchmeier C, Guthrie S. 2000. The branchial arches and HGF are growth-promoting and chemoattractant for cranial motor axons. Development 127:1751-1766.
12. Chavis P, Westbrook G. 2001. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411:317-321.
13. David MD, Yeramian A, Dunach M, Llovera M, Canti C, de Herreros AG, Comella JX, Herreros J. 2008. Signalling by neurotrophins and hepatocyte growth factor regulates axon morphogenesis by differential beta-catenin phospho-rylation. J Cell Sci 121:2718-2730.
14. Dierssen M, Benavides-Piccione R, Martinez-Cue C, Estivill X, Florez J, Elston GN, DeFelipe J. 2003. Alterations of neocortical pyramidal cell phenotype in the Ts65Dn mouse model of Down syndrome: effects of environmental enrichment. Cereb Cortex 13:758-764.
15. Ebens A, Brose K, Leonardo ED, Hanson MG Jr, Bladt F, Birchmeier C, Barres BA, Tessier-Lavigne M. 1996. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157-1172.
16. Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA. 2008. Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc Natl Acad Sci USA 105:20953-20958.
17. Engert F, Bonhoeffer T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
18. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H. 1997. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17: 2469-2476.
19. Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S. 2008. Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci 28:5901-5909.
20. Gelfo F, De Bartolo P, Giovine A, Petrosini L, Leggio MG. 2009. Layer and regional effects of environmental enrichment on the pyramidal neuron morphology of the rat. Neurobiol Learn Mem 91:353-365.
21. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133-139.
22. Giacobini P, Messina A, Wray S, Giampietro C, Crepaldi T, Carmeliet P, Fasolo A. 2007. Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J Neurosci 27:431-445.
23. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. 2002. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22:6309-6314.
24. Gutierrez H, Dolcet X, Tolcos M, Davies A. 2004. HGF regulates the development of cortical pyramidal dendrites. Development 131:3717-3726.
25. Hamanoue M, Takemoto N, Matsumoto K, Nakamura T, Nakajima K, Kohsaka S. 1996. Neurotrophic effect of hepatocyte growth factor on central nervous system neurons in vitro. J Neurosci Res 43:554-564.
26. Harris KM, Teyler TJ. 1984. Developmental onset of long-term potentiation in area CA1 of the rat hippocampus. J Physiol 346:27-48.
27. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. 2004. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci USA 101:4477-4482.
28. Hung AY, Futai K, Sala C, Valtschanoff JG, Ryu J, Woodworth MA, Kidd FL, Sung CC, Miyakawa T, Bear MF, Weinberg RJ, Sheng M. 2008. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J Neurosci 28:1697-1708.
29. Ieraci A, Forni PE, Ponzetto C. 2002. Viable hypomorphic signaling mutant of the Met receptor reveals a role for hepatocyte growth factor in postnatal cerebellar development. Proc Natl Acad Sci USA 99:15200-15205.
30. Jackson PB, Boccuto L, Skinner C, Collins JS, Neri G, Gurrieri F, Schwartz CE. 2009. Further evidence that the rs1858830 C variant in the promoter region of the MET gene is associated with autistic disorder. Autism Res 2:232-236.
31. Jones EG. 2002. Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci 357:1659-1673.
32. Judson MC, Bergman MY, Campbell DB, Eagleson KL, Levitt P. 2009. Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J Comp Neurol 513:511-531.
33. Just MA, Cherkassky VL, Keller TA, Minshew NJ. 2004. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127:1811-1821.
34. Kenward MG, Roger JH. 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983-997.
35. Koshino H, Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. 2008. fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cereb Cortex 18:289-300.
36. Kuhn B, Denk W, Bruno RM. 2008. In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc Natl Acad Sci USA 105:7588-7593.
37. Lim CS, Walikonis RS. 2008. Hepatocyte growth factor and c-Met promote dendritic maturation during hippocampal neuron differentiation via the Akt pathway. Cell Signal 20:825-835.
38. Lund JS, Holbach SM, Chung WW. 1991. Postnatal development of thalamic recipient neurons in the monkey striate cortex: II. Influence of afferent driving on spine acquisition and dendritic growth of layer 4C spiny stellate neurons. J Comp Neurol 309:129-140.
39. Madhavan R, Peng HB. 2006. HGF induction of postsynaptic specializations at the neuromuscular junction. J Neurobiol 66:134-147.
40. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
41. McAllister AK. 2000. Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10:963-973.
42. McAllister AK, Katz LC, Lo DC. 1996. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17: 1057-1064.
43. Muller D, Oliver M, Lynch G. 1989. Developmental changes in synaptic properties in hippocampus of neonatal rats. Brain Res Dev Brain Res 49:105-114.
44. Murthy VN, Schikorski T, Stevens CF, Zhu Y. 2001. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682.
45. Nakano M, Takagi N, Takagi K, Funakoshi H, Matsumoto K, Nakamura T, Takeo S. 2007. Hepatocyte growth factor promotes the number of PSD-95 clusters in young hippo-campal neurons. Exp Neurol 207:195-202.
46. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD. 2006. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817-830.
47. Perez Velazquez JL, Barcelo F, Hung Y, Leshchenko Y, Nenadovic V, Belkas J, Raghavan V, Brian J, Garcia Dominguez L. 2009. Decreased brain coordinated activity in autism spectrum disorders during executive tasks: reduced long-range synchronization in the fronto-parietal networks. Int J Psychophysiol 73:341-349.
48. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R. 1999. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2:31-36.
49. Petreanu L, Mao T, Sternson SM, Svoboda K. 2009. The sub-cellular organization of neocortical excitatory connections. Nature 457:1142-1145.
50. Powell EM, Muhlfriedel S, Bolz J, Levitt P. 2003. Differential regulation of thalamic and cortical axonal growth by hepatocyte growth factor/scatter factor. Dev Neurosci 25:197-206.
51. Rinaldi T, Perrodin C, Markram H. 2008a. Hyperconnectivity and hyper-plasticity in the medial prefrontal cortex in the valproic Acid animal model of autism. Front Neural Circuits 2:4.
52. Rinaldi T, Silberberg G, Markram H. 2008b. Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18:763-770.
53. Roberts AC, Diez-Garcia J, Rodriguiz RM, Lopez IP, Lujan R, Martinez-Turrillas R, Pico E, Henson MA, Bernardo DR, Jarrett TM, Clendeninn DJ, Lopez-Mascaraque L, Feng G, Lo DC, Wesseling JF, Wetsel WC, Philpot BD, Perez-Otano I. 2009. Down-regulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 63:342-356.
54. Rosario M, Birchmeier W. 2003. How to make tubes: signaling by the Met receptor tyrosine kinase. Trends Cell Biol 13:328-335.
55. Rubio-Garrido P, Perez-de-Manzo F, Porrero C, Galazo MJ, Clasca F. 2009. Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent. Cereb Cortex 19:2380-2395.
56. Russell FA, Moore DR. 1999. Effects of unilateral cochlear removal on dendrites in the gerbil medial superior olivary nucleus. Eur J Neurosci 11:1379-1390.
57. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
58. Shen H, Sesack SR, Toda S, Kalivas PW. 2008. Automated quantification of dendritic spine density and spine head diameter in medium spiny neurons of the nucleus accumbens. Brain Struct Funct 213:149-157.
59. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. 1994. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
60. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
61. Sorensen SA, Rubel EW. 2006. The level and integrity of synaptic input regulates dendrite structure. J Neurosci 26:1539-1550.
62. Sousa I, Clark TG, Toma C, Kobayashi K, Choma M, Holt R, Sykes NH, Lamb JA, Bailey AJ, Battaglia A, Maestrini E, Monaco AP. 2009. MET and autism susceptibility: family and case-control studies. Eur J Hum Genet 17:749-758.
63. Tripodi M, Evers JF, Mauss A, Bate M, Landgraf M. 2008. Structural homeostasis: compensatory adjustments of dendritic arbor geometry in response to variations of synaptic input. PLoS Biol 6:e260.
64. Tyndall SJ, Walikonis RS. 2006. The receptor tyrosine kinase Met and its ligand hepatocyte growth factor are clustered at excitatory synapses and can enhance clustering of synaptic proteins. Cell Cycle 5:1560-1568.
65. Tyndall SJ, Patel SJ, Walikonis RS. 2007. Hepatocyte growth factor-induced enhancement of dendritic branching is blocked by inhibitors of N-methyl-D-aspartate receptors and calcium/calmodulin-dependent kinases. J Neurosci Res 85:2343-2351.
66. Welch JM, Lu J, Rodriguiz RM, Trotta NC, Peca J, Ding JD, Feliciano C, Chen M, Adams JP, Luo J, Dudek SM, Weinberg RJ, Calakos N, Wetsel WC, Feng G. 2007. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 448:894-900.
67. Zhang YW, Vande Woude GF. 2003. HGF/SF-met signaling in the control of branching morphogenesis and invasion. J Cell Biochem 88:408-417.