A role for synaptopodin and the spine apparatus in hippocampal synaptic plasticity

Annals of Anatomy

Volumn 189, Issue 1, 2007, Pages 5-16

  Deller, Thomas ^a   Bas Orth, Carlos ^a   Del Turco, Domenico ^a   Vlachos, Andreas ^a   Burbach, Guido J ^a   Drakew, Alexander ^b   Chabanis, Sophie ^c   Korte, Martin ^d   Schwegler, Herbert ^e   Haas, Carola A ^b   Frotscher, Michael ^b  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^e OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Actin; Calcium stores; Cytoskeleton; Dendritic plasticity; Excitatory synapse

Indexed keywords

ACTIN; CALCIUM ION; MESSENGER RNA; PROTEIN; SYNAPTOPODIN;

ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; BRAIN REGION; CALCIUM CELL LEVEL; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION; GENE TARGETING; HIPPOCAMPUS; IMMUNOGOLD LABELING; LEARNING DISORDER; LONG TERM POTENTIATION; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SPINE APPARATUS;

MUS; RODENTIA;

EID: 33845991837     PISSN: 09409602     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aanat.2006.06.013     Document Type: Article

References (79)

1. Adam G., and Matus A. Role of actin in the organisation of brain postsynaptic densities. Brain Res. Mol. Brain Res. 43 (1996) 246-250
2. Asanuma K., Kim K., Oh J., Giardino L., Chabanis S., Faul C., Reiser J., and Mundel P. Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner. J. Clin. Invest. 115 (2005) 1188-1198
3. Asanuma K., Yanagida-Asanuma E., Faul C., Tomino Y., Kim K., and Mundel P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol. 8 (2006) 485-491
4. Bas Orth C., Vlachos A., Del Turco D., Burbach G.J., Haas C.A., Mundel P., Feng G., Frotscher M., and Deller T. Lamina-specific distribution of synaptopodin, an actin-associated molecule essential for the spine apparatus, in identified principal cell dendrites of the mouse hippocampus. J. Comp. Neurol. 487 (2005) 227-239
5. Bayer S.A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J. Comp. Neurol. 190 (1980) 87-114
6. Bayer S.A. Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J. Comp. Neurol. 190 (1980) 115-134
7. Brunig I., Kaech S., Brinkhaus H., Oertner T.G., and Matus A. Influx of extracellular calcium regulates actin-dependent morphological plasticity in dendritic spines. Neuropharmacology 47 (2004) 669-676
8. Buchs P.A., and Muller D. LTP induction is associated with major ultrastructural changes of activated synapses. Proc. Natl. Acad. Sci. USA 96 (2002) 8040-8045
9. Burgoyne R.D., Barron J., and Geisow M.J. Cytochemical localisation of calcium binding sites in adrenal chromaffin cells and their relation to secretion. Cell Tissue Res. 229 (1983) 207-217
10. Carlin R.K., Bartelt D.C., and Siekevitz P. Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations. J. Cell Biol. 96 (1983) 443-448
11. Carlisle H.J., and Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci. 28 (2005) 182-187
12. Cohen R.S., Chung S.K., and Pfaff D.W. Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe. Cell. Mol. Neurobiol. 5 (1985) 271-284
13. Czarnecki K., Haas C.A., Bas Orth C., Deller T., and Frotscher M. Postnatal development of synaptopodin expression in the rodent hippocampus. J. Comp. Neurol. 490 (2005) 133-144
14. Dailey M.E., and Smith S.J. The dynamics of dendritic structures in developing hippocampal slices. J. Neurosci. 16 (1996) 2983-2994
15. Deller T., Merten T., Roth S.U., Mundel P., and Frotscher M. Actin-associated protein synaptopodin in the rat hippocampal formation: localization in the spine neck and close association with the spine apparatus of principal neurons. J. Comp. Neurol. 418 (2000) 164-181
16. Deller T., Haas C.A., Deissenrieder K., Del Turco D., Coulin C., Gebhardt C., Drakew A., Schwarz K., Mundel P., and Frotscher M. Laminar distribution of synaptopodin in normal and reeler mouse brain depends on the position of spine-bearing neurons. J. Comp. Neurol. 453 (2002) 33-44
17. Deller, T., Bas Orth, C., Vlachos, A., Merten, T., Del Turco, D., Dehn, D., Mundel, P., Frotscher, M., 2006. Plasticity of synaptopodin and the spine apparatus organelle in the rat fascia dentata following entorhinal cortex lesion. J. Comp. Neurol., in press.
18. Deller T., Korte M., Chabanis S., Drakew A., Schwegler H., Stefani G.G., Zuniga A., Schwarz K., Bonhoeffer T., Zeller R., Frotscher M., and Mundel P. Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc. Natl. Acad. Sci. USA 100 (2003) 10494-10499
19. Denk W., Yuste R., Svoboda K., and Tank D.W. Imaging calcium dynamics in dendritic spines. Curr. Opin. Neurobiol. 6 (1996) 372-378
20. Dillon C., and Goda Y. The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28 (2005) 25-55
21. Drenckhahn D., and Kaiser H.W. Evidence for the concentration of F-actin and myosin in synapses and in the plasmalemmal zone of axons. Eur. J. Cell Biol. 31 (1983) 235-240
22. Dunaevsky A., Tashiro A., Majewska A., Mason C., and Yuste R. Developmental regulation of spine motility in the mammalian central nervous system. Proc. Natl. Acad. Sci. USA 96 (1999) 13438-13443
23. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtmann J.W., and Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28 (2000) 41-51
24. Fifkova E. A possible mechanism of morphometric changes in dendritic spines induced by stimulation. Cell. Mol. Neurobiol. 5 (1985) 47-63
25. Fifkova E., and Delay R.J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J. Cell Biol. 95 (1982) 345-350
26. Fifkova E., and van Harreveld A. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6 (1977) 211-230
27. Fifkova E., Markham J.A., and Delay R.J. Calcium in the spine apparatus of dendritic spines in the dentate molecular layer. Brain Res. 266 (1983) 163-168
28. Fischer M., Kaech S., Knutti D., and Matus A. Rapid actin-based plasticity in dendritic spines. Neuron 20 (1998) 847-854
29. Fischer M., Kaech S., Wagner U., Brinkhaus H., and Matus A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat. Neurosci. 3 (2000) 887-894
30. Frotscher M., Hamori J., and Wenzel H.J. Transneuronal effects of entorhinal lesions in the early postnatal period on synaptogenesis in the hippocampus of the rat. Exp. Brain Res. 30 (1977) 549-560
31. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., and Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38 (2003) 447-460
32. Furukawa K., Fu W., Li Y., Witke W., Kwiatkowski D.J., and Mattson M.P. The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons. J. Neurosci. 17 (1997) 8178-8186
33. Gray E.G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. J. Anat. 83 (1959) 420-433
34. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 9 (1999) 343-348
35. Harris K.M., and Stevens J.K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9 (1989) 2982-2997
36. Harris K.M., Jensen F.E., and Tsao B.H. Ultrastructure, development, and plasticity of dendritic synapses in area CA1 of the rat hippocampus: extending our vision with serial electron microscopy and three-dimensional analyses. In: Chan-Palay V., and Köhler C. (Eds). The Hippocampus: New Vistas (1989), Alan Liss, New York 33-52
37. Harris K.M., Jensen F.E., and Tsao B.H. 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. 12 (1992) 2685-2705
38. Hayashi Y., and Majewska A.K. Dendritic spine geometry: functional implication and regulation. Neuron 46 (2005) 529-532
39. Hayashi K., Ishikawa R., Ye L.H., He X.L., Takata K., Kohama K., and Shirao T. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J. Neurosci. 16 (1996) 7161-7170
40. Holcman D., Korkotian E., and Segal M. Calcium dynamics in dendritic spines, modeling and experiments. Cell Calc. 37 (2005) 467-475
41. Kennedy M.B., Beale H.C., Carlisle H.J., and Washburn L.R. Integration of biochemical signalling in spines. Nat. Rev. Neurosci. 6 (2005) 423-434
42. Kobayashi N. Mechanism of the process formation; podocytes vs. neurons. Microsc. Res. Technol. 57 (2002) 217-223
43. Korkotian E., and Segal M. Bidirectional regulation of dendritic spine dimensions by glutamate receptors. Neuroreport 10 (1999) 2875-2877
44. Korkotian E., and Segal M. Release of calcium from stores alters the morphology of dendritic spines in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 96 (1999) 12068-12072
45. Korkotian E., Holcman D., and Segal M. Dynamic regulation of spine-dendrite coupling in cultured hippocampal neurons. Eur. J. Neurosci. 20 (2004) 2649-2663
46. Kremerskothen J., Plaas C., Kindler S., Frotscher M., and Barnekow A. Synaptopodin, a molecule involved in the formation of the dendritic spine apparatus, is a dual actin/alpha-actinin binding protein. J. Neurochem. 92 (2005) 597-606
47. Kretz O., Fester L., Wehrenberg U., Zhou L., Brauckmann S., Zhao S., Prange-Kiel J., Naumann T., Jarry H., Frotscher M., and Rune G.M. Hippocampal synapses depend on hippocampal estrogen synthesis. J. Neurosci. 24 (2004) 5913-5921
48. Leinweber B.D., Fredricksen R.S., Hoffman D.R., and Chalovich J.M. Fesselin: a novel synaptopodin-like actin binding protein from muscle tissue. J. Muscle Res. Cell Motil. 20 (1999) 539-545
49. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., and Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4 (2001) 1086-1092
50. Matsuzaki M., Honkura N., Ellis-Davies G.C., and Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 429 (2004) 761-766
51. Matus A., Ackermann M., Pehling G., Byers H.R., and Fujiwara K. High actin concentrations in brain dendritic spines and postsynaptic densities. Proc. Natl. Acad. Sci. USA 79 (1982) 7590-7594
52. Matus A., Brinkhaus H., and Wagner U. Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 10 (2000) 555-560
53. McKinney R.A., Capogna M., Dürr R., Gähwiler B.H., and Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nature Neurosci. 2 (1999) 44-49
54. Morales M., and Fifkova E. In situ localization of myosin and actin in dendritic spines with the immunogold technique. J. Comp. Neurol. 279 (1989) 666-674
55. Muller D., Toni N., and Buchs P.A. Spine changes associated with long-term potentiation. Hippocampus 10 (2000) 596-604
56. Mundel P., Heid H.W., Mundel T.M., Kruger M., Reiser J., and Kriz W. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J. Cell Biol. 139 (1997) 193-204
57. Murphy D.D., and Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J. Neurosci. 16 13 (1996) 4059-4068
58. Noguchi J., Matsuzaki M., Ellis-Davies G.C., and Kasai H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46 (2005) 609-622
59. Oertner T.G., and Matus A. Calcium regulation of actin dynamics in dendritic spines. Cell Calc. 37 (2005) 477-482
60. Pierce J.P., van Leyen K., and McCarthy J.B. Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat. Neurosci. 3 (2000) 311-313
61. Pierce J.P., Mayer T., and McCarthy J.B. Evidence for a satellite secretory pathway in neuronal dendritic spines. Curr. Biol. 11 (2001) 351-355
62. Racca C., Stephenson F.A., Streit P., Roberts J.D., and Somogyi P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J. Neurosci. 20 (2000) 2512-2522
63. Roth S.U., Sommer C., Mundel P., and Kiessling M. Expression of synaptopodin, an actin-associated protein, in the rat hippocampus after limbic epilepsy. Brain Pathol. 11 (2001) 169-181
64. Segal M. Dentritic spines for neuroprotection: a hypothesis. Trends Neurosci. 18 (1995) 468-471
65. Segal M. Dendritic spines and long-term plasticity. Nat. Rev. Neurosci. 6 (2005) 277-284
66. Spacek J. Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components. Anat. Embryol. 171 (1985) 235-243
67. Spacek J., and Harris K.M. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17 (1997) 190-203
68. Steward O., and Schuman E.M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24 (2001) 299-325
69. Svoboda K., and Mainen Z.F. Synaptic [Ca2+]: intracellular stores spill their guts. Neuron 22 (1999) 427-430
70. Svoboda K., Tank D.W., and Denk W. Direct measurement of coupling between dendritic spines and shafts. Science 272 (1996) 716-719
71. Valverde F. Apical dendritic spines of the visual cortex and light deprivation in the mouse. Exp. Brain Res. 3 (1967) 337-352
72. Volfovsky N., Parnas H., Segal M., and Korkotian E. Geometry of dendritic spines affects calcium dynamics in hippocampal neurons: theory and experiments. J. Neurophysiol. 82 (1999) 450-462
73. Weins A., Schwarz K., Faul C., Barisoni L., Linke W.A., and Mundel P. Differentiation- and stress-dependent nuclear cytoplasmic redistribution of myopodin, a novel actin-bundling protein. J. Cell Biol. 155 (2001) 393-404
74. Woolley C.S., and McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993) 293-306
75. Wyszynski M., Lin J., Rao A., Nigh E., Beggs A.H., Craig A.M., and Sheng M. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385 (1997) 439-442
76. Wyszynski M., Kharazia V., Shanghvi R., Rao A., Beggs A.H., Craig A.M., Weinberg R., and Sheng M. Differential regional expression and ultrastructural localization of alpha-actinin-2, a putative NMDA receptoranchoring protein, in rat brain. J. Neurosci. 18 (1998) 1383-1392
77. Yamazaki M., Matsuo R., Fukazawa Y., Ozawa F., and Inokuchi K. Regulated expression of an actin-associated protein, synaptopodin, during long-term potentiation. J. Neurochem. 79 (2001) 192-199
78. Yuste R., Majewska A., and Holthoff K. From form to function: calcium compartmentalization in dendritic spines. Nat. Neurosci. 3 (2000) 653-659
79. Ziv N.E., and Smith S.J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17 (1996) 91-102