Subcellular distribution of the Rho-GEF Lfc in primate prefrontal cortex: Effect of neuronal activation

Journal of Comparative Neurology

Volumn 508, Issue 6, 2008, Pages 927-939

  Muly, E Chris ^a,b   Nairn, Angus C ^c,d   Greengard, Paul ^c   Rainnie, Donald G ^a  

^a EMORY UNIVERSITY   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Dendritic spines; Electrophysiology; Immunoelectron microscopy; In vitro; Neuronal plasticity; Ultrastructure

Indexed keywords

PROTEIN SUBUNIT; RHO FACTOR; RHO GUANINE EXCHANGE FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; DENDRITE; DENDRITIC SPINE; ELECTRON MICROSCOPY; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MONKEY; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE ENDING; NEUROPIL; NONHUMAN; PREFRONTAL CORTEX; PRIMATE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TISSUE SLICE;

ANIMALS; ANIMALS, NEWBORN; DENDRITIC SPINES; EXCITATORY AMINO ACID AGONISTS; GABA ANTAGONISTS; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MACACA MULATTA; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICROSCOPY, IMMUNOELECTRON; N-METHYLASPARTATE; NEURONS; NEUROPIL; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS; SUBCELLULAR FRACTIONS;

EID: 43749083047     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21703     Document Type: Article

References (70)

1. Aijaz S, D'Atri F, Citi S, Balda MS, Matter K. 2005. Binding of GEF-H1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition. Dev Cell 8:777-786.
2. Altemus KL, Lavenex P, Ishizuka N, Amaral DG. 2005. Morphological characteristics and electrophysiological properties of CA1 pyramidal neurons in macaque monkeys. Neuroscience 136:741-756.
3. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, Ito K, Hama C. 2000. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26:119-131.
4. Bakal CJ, Finan D, LaRose J, Wells CD, Gish G, Kulkarni S, DeSepulveda P, Wilde A, Rottapel R. 2005. The Rho GTP exchange factor Lfc promotes spindle assembly in early mitosis. Proc Natl Acad Sci USA 102:9529-9534.
5. Bernstein BW, Bamburg JR. 2003. Actin-ATP hydrolysis is a major energy drain for neurons. J Neurosci 23:1-6.
6. Braitenburg V, Schuz A. 1998. Cortex: statistics and geometry of neuronal connectivity. Berlin: Springer.
7. Calabrese B, Wilson MS, Halpain S. 2006. Development and regulation of dendritic spine synapses. Physiology 21:38-47.
8. Callow MG, Zozulya S, Gishizky ML, Jallal B, Smeal T. 2005. PAK4 mediates morphological changes through the regulation of GEF-H1. J Cell Sci 118:1861-1872.
9. Carlisle HJ, Kennedy MB. 2005. Spine architecture and synaptic plasticity. Trends Neurosci 28:182-187.
10. Chang ZF, Lee HH. 2006. RhoA signaling in phorbol ester-induced apoptosis. J Biomed Sci 13:173-180.
11. Deuten AY, Lee MC, Gillham MH, Cameron DA, Goldstein M, Iadarola MJ. 1991. Stress selectively increases fos protein in dopamine neurons innervating the prefrontal cortex. Cereb Cortex 1:273-292.
12. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K. 2003. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447-460.
13. Glaven JA, Whitehead IP, Nomanbhoy T, Kay R, Cerione RA. 1996. Lfc and Lsc oncoproteins represent two new guanine nucleotide exchange factors for the Rho GTP-binding protein. J Biol Chem 271:27374-27381.
14. Glaven JA, Whitehead I, Bagrodia S, Kay R, Cerione RA. 1999. The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J Biol Chem 274:2279-2285.
15. Gogolla N, Galimberti I, Caroni P. 2007. Structural plasticity of axon terminals in the adult. Curr Opin Neurobiol 17:1-9.
16. Hao J, Rapp PR, Leffler AE, Leffler SR, Janssen WG, Lou W, McKay H, Roberts JA, Wearne SL, Hof PR, Morrison JH. 2006. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 26:2571-2578.
17. Hao J, Rapp PR, Janssen WG, Lou W, Lasley BL, Hof PR, Morrison JH. 2007. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci USA 104:11465-11470.
18. Harms KJ, Dunaevsky A. 2006. Dendritic spine plasticity: looking beyond development. Brain Res (in press).
19. Henze DA, Gonzalez-Burgos GR, Urban NN, Lewis DA, Barrionuevo G. 2000. Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84:2799-2809.
20. Hering H, Sheng M. 2003. Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J Neurosci 23:11759-11769.
21. Keady BT, Kuo P, Martinez SE, Yuan L, Hake LE. 2007. MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J Cell Sci 120:1093-1103.
22. Kennedy MB, Beale HC, Carlisle HJ, Washburn LR. 2005. Integration of biochemical signalling in spines. Nat Rev Neurosci 6:423-434.
23. Kins S, Betz H, Kirsch J. 2000. Collybistin, a newly identified brain-specific GEF, induces submembrane clustering of gephyrin. Nat Neurosci 3:22-29.
24. Kirov SA, Harris KM. 1999. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2:878-883.
25. Kirov SA, Sorra KE, Harris KM. 1999. Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876-2886.
26. Koh CG. 2006. Rho GTPases and their regulators in neuronal functions and development. Neurosignals 15:228-237.
27. Krendel M, Zenke FT, Bokoch GM. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4:294-301.
28. Lambert PD, Ely TD, Gross RE, Kilts CD. 1996. Neurotensin induces Fos and Zif268 expression in limbic nuclei of the rat brain. Neurosci 75:1141-1151.
29. LeBeux YJ, Willemot J. 1975. An ultrastructural study of the microfilaments in rat brain by means of heavy meromyosin labeling. I. The perikaryon, the dendrites and the axon. Cell Tissue Res 160:1-36.
30. Luebke JI, Chang YM, Moore TL, Rosene DL. 2004. Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex. Neuroscience 125:277-288.
31. Meng Y, Zhang Y, Tregoubov V, Falls DL, Jia Z. 2003. Regulation of spine morphology and synaptic function by LIMK and the actin cytoskeleton. Rev Neurosci 14:233-240.
32. Morishita W, Connor JH, Xia H, Quinlan EM, Shenolikar S, Malenka RC. 2001. Regulation of synaptic strength by protein phosphatase 1. Neuron 32:1133-1148.
33. Mulkey RM, Endo S, Shenolikar S, Malenka RC. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
34. Muly EC, Maddox M, Smith Y. 2003. Distribution of mGluR1α and mGluR5 immunolabeling in primate prefrontal cortex. J Comp Neurol 467:521-535.
35. Muly EC, Allen P, Mazloom M, Aranbayeva Z, Greenfield AT, Greengard P. 2004a. Subcellular distribution of neurabin immunolabeling in primate prefrontal cortex: comparison with spinophilin. CC 14:1398-1407.
36. Muly EC, Smith Y, Allen P, Greengard P. 2004b. Subcellular distribution of spinophilin immunolabeling in primate prefrontal cortex: localization to and within dendritic spines. J Comp Neurol 469:185-197.
37. Murase S, Mosser E, Schuman EM. 2002. Depolarization drives beta-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35:91-105.
38. Nakayama AY, Harms MB, Luo L. 2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and brances in hippocampal pyramdial neurons. J Neurosci 20:5329-5338.
39. Okamoto K, Nagai T, Miyawaki A, Hayashi Y. 2004. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
40. Okuda T, Yu LM, Cingolani LA, Kemler R, Goda Y. 2007. Beta-catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proc Natl Acad Sci U S A 104:13479-13484.
41. Otmakhov N, Tao-Cheng JH, Carpenter S, Asrican B, Dosemeci A, Reese TS, Lisman J. 2004. Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J Neurosci 24:9324-9331.
42. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
43. Peters A, Palay SL, Webster Hd. 1991. The fine structure of the nervous system: neurons and their supporting cells. New York: Oxford University Press.
44. Popov VI, Davies HA, Rogachevsky W, Patrushev IV, Errington ML, Gabbott PL, Bliss TV, Stewart MG. 2004. Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation (LTP): a serial section electron micrograph study in the dentate gyrus in the anaesthetised rat. Neuroscience 128:251-262.
45. Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, McEwen BS, Morrison JH. 2006. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 16:313-320.
46. Rainnie DG. 1999. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69-85.
47. Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, Shekar A. 2004. Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J. Neurosci 24:3471-3479.
48. Rainnie DG, Asprodini EK, Shinnick-Gallagher P. 1993. Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69:1350-1362.
49. Rainnie DG, Mania I, Mascagni F, McDonald AJ. 2006. Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498:142-161.
50. Ren Y, Li R, Zheng Y, Busch H. 1998. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem 273:34954-34960.
51. Rico B, Beggs HE, Schahin-Reed D, Kimes N, Schmidt A, Reichardt LF. 2004. Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 7:1059-1069.
52. Robinson TE, Kolb B. 1999. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 11:1598-1604.
53. Robinson TE, Gorny G, Mitton E, Kolb B. 2001. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39:257-266.
54. Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu GY, Nairn AC, Greengard P. 2005. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47:85-100.
55. Sankaranarayanan S, Atluri PP, Ryan TA. 2003. Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-135.
56. Schmidt U, Beyer C, Oestreicher AB, Reisert I, Schilling K, Pilgrim C. 1996. Activation of dopaminergic D1 receptors promotes morphogenesis of developing striatal neurons. Neuroscience 74:453-460.
57. Schuz A, Palm G. 1989. Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286:442-455.
58. Sorra KE, Harris KM. 1998. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci 18:658-671.
59. Star EN, Kwiatkowski DJ, Murthy VN. 2002. Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246.
60. Stendel C, Roos A, Deconinck T, Pereira J, Castagner F, Niemann A, Kirschner J, Korinthenberg R, Ketelsen UP, Battaloglu E, Parman Y, Nicholson G, Ouvrier R, Seeger J, De Jonghe P, Weis J, Kruttgen A, Rudnik-Schoneborn S, Bergmann C, Suter U, Zerres K, Timmerman V, Relvas JB, Senderek J. 2007. Peripheral nerve demyelination caused by a mutant Rho GTPase guanine nucleotide exchange factor, frabin/FGD4. Am J Hum Genet 81:158-164.
61. Steward O, Wallace CS, Lyford GL, Worley PF. 1998. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741-751.
62. Tada T, Sheng M. 2006. Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101.
63. Takeichi M, Abe K. 2005. Synaptic contact dynamics controlled by cadherin and catenins. Trends Cell Biol 15:216-221.
64. Tashiro A, Minden A, Yuste R. 2000. Regulation of dendritic spine morphology by the Rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb Cortex 10:927-938.
65. Thiels E, Kanterewicz BI, Knapp LT, Barrionuevo G, Klann E. 2000. Protein phosphatase-mediated regulation of protein kinase C during long-term depression in the adult hippocampus in vivo. J Neurosci 20:7199-7207.
66. Van de Ven TJ, VanDongen HM, VanDongen AM. 2005. The nonkinase phorbol ester receptor alpha 1-chimerin binds the NMDA receptor NR2A subunit and regulates dendritic spine density. J Neurosci 25:9488-9496.
67. Verhoeven K, De Jonghe P, Van de PT, Nelis E, Zwijsen A, Verpoorten N, De Vriendt E, Jacobs A, Van G, Francis A, Ceuterick C, Huylebroeck D, Timmerman V. 2003. Slowed conduction and thin myelination of peripheral nerves associated with mutant rho guanine-nucleotide exchange factor 10. Am J Hum Genet 73:926-932.
68. Westwick JK, Lee RJ, Lambert QT, Symons M, Pestell RG, Der CJ, Whitehead IP. 1998. Transforming potential of Dbl family proteins correlates with transcription from the cyclin D1 promoter but not with activation of Jun NH2-terminal kinase, p38/Mpk2, serum response factor, or c-Jun. J Biol Chem 273:16739-16747.
69. Whitehead I, Kirk H, Tognon C, Trigo-Gonzalez G, Kay R. 1995. Expression cloning of lfc, a novel oncogene with structural similarities to guanine nucleotide exchange factors and to the regulatory region of protein kinase C. J Biol Chem 270:18388-18395.
70. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.