Maturation of synaptic contacts in differentiating neural stem cells

Stem Cells

Volumn 25, Issue 7, 2007, Pages 1720-1729

  Liebau, Stefan ^a   Vaida, Bianca ^a   Storch, Alexander ^b   Boeckers, Tobias M ^a  

^a UNIVERSITY OF ULM   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Bassoon; Neural stem cells; ProSAP; Shank; Synaptogenesis; Synaptophysin

Indexed keywords

BASSOON PROTEIN; CYTOSKELETON PROTEIN; PORPHOBILINOGEN DEAMINASE; PROSAP1 PROTEIN; PROSAP2 PROTEIN; PROTEIN; SCAFFOLD PROTEIN; SHANK2 PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; HIPPOCAMPUS; NERVE CELL CULTURE; NEURAL STEM CELL; NONHUMAN; RAT; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; MESENCEPHALON; NERVE TISSUE PROTEINS; NEURONS; RATS; RNA, MESSENGER; STEM CELLS; SYNAPSES; TIME FACTORS;

RATTUS;

EID: 34547184679     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2006-0823     Document Type: Article

References (62)

1. Storch A, Schwarz J. Neural stem cells and neurodegeneration. Curr Opin Investig Drugs 2002;3:774-781.
2. Vicario-Abejón C, Collin C, Tsoulfas P et al. Hippocampal stem cells differentiate into excitatory and inhibitory neurons. Eur J Neurosci 2000;12:677-688.
3. Ge S, Goh EL, Sailor KA et al. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006;439:589-593.
4. Toda H, Takahashi J, Mizoguchi A et al. Neurons generated from adult rat hippocampal stem cells form functional glutamatergic and GABAergic synapses in vitro. Exp Neurol 2000;165:66-76.
5. Kim E, Ko J. Molecular organization and assembly of the postsynaptic density of excitatory brain synapses. Results Probl Cell Differ 2006;43: 1-23.
6. Wenzel J, Bogolepov NN. [Electronmicroscopical and morphometrical study of rat hippocampal synapses]. J Hirnforsch 1976;17:399-448.
7. Dresbach T, Qualmann B, Kessels MM et al. The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 2001;58:94-116.
8. Ziff EB. Enlightening the postsynaptic density. Neuron 1997;19: 1163-1174.
9. Schoch S, Gundelfinger ED. Molecular organization of the presynaptic active zone. Cell Tissue Res 2006;326:379-391.
10. Brose N, Hofmann K, Hata Y et al. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J Biol Chem 1995;270:25273-25280.
11. Wang Y, Okamoto M, Schmitz F et al. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 1997;388:593-598.
12. Wang Y, Sugita S, Sudhof TC. The RIM/NIM family of neuronal C2 domain proteins. Interactions with Rab3 and a new class of Src homology 3 domain proteins. J Biol Chem 2000;275:20033-20044.
13. Ohtsuka T, Takao-Rikitsu E, Inoue E et al. Cast: A novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J Cell Biol 2002;158:577-590.
14. Wang Y, Liu X, Biederer T et al. A family of RIM-binding proteins regulated by alternative splicing: Implications for the genesis of synaptic active zones. Proc Natl Acad Sci U S A 2002;99:14464-14469.
15. Cases-Langhoff C, Voss B, Garner AM et al. Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur J Cell Biol 1996;69:214-223.
16. tom Dieck S, Sanmarti-Vila L, Langnaese K et al. Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 1998;142:499-509.
17. Wang X, Kibschull M, Laue MM et al. Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with Rim and Bassoon and binds profilin. J Cell Biol 1999;147:151-162.
18. Boeckers TM. The postsynaptic density. Cell Tissue Res 2006;326: 409-422.
19. Sampedro MN, Bussineau CM, Cotman CW. Postsynaptic density antigens: Preparation and characterization of an antiserum against postsynaptic densities. J Cell Biol 1981;90:675-686.
20. Boeckers TM, Kreutz MR, Winter C 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;19:6506-6518.
21. Naisbitt S, Kim E, Tu JC et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 1999;23:569-582.
22. Boeckers TM, Bockmann J, Kreutz MR et al. ProSAP/Shank proteins: A family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem 2002;81:903-910.
23. Boeckers TM, Winter C, Smalla KH 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: 247-252.
24. Baron MK, Boeckers TM, Vaida B et al. An architectural framework that may lie at the core of the postsynaptic density. Science 2006; 311:531-535.
25. Zuber B, Nikonenko I, Klauser P et al. The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proc Natl Acad Sci U S A 2005;102:19192-19197.
26. Garner CC, Waites CL, Ziv NE. Synapse development: Still looking for the forest, still lost in the trees. Cell Tissue Res 2006;326:249-262.
27. Bresler T, Shapira M, Boeckers T et al. Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 2004;24:1507-1520.
28. Ziv NE, Garner CC. Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci 2004;5:385-399.
29. Gerrow K, Romorini S, Nabi SM et al. A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 2006;49:547-562.
30. Verderio C, Coco S, Pravettoni E et al. Synaptogenesis in hippocampal cultures. Cell Mol Life Sci 1999;55:1448-1462.
31. Boeckers TM, Liedtke T, Spilker C et al. C-terminal synaptic targeting elements for postsynaptic density proteins ProSAP1/Shank2 and ProSAP2/Shank3. J Neurochem 2005;92:519-524.
32. Carvey PM, Ling ZD, Sortwell CE et al. A clonal line of mesencephalic progenitor cells converted to dopamine neurons by hematopoietic cytokines: A source of cells for transplantation in Parkinson's disease. Exp Neurol 2001;171:98-108.
33. Storch A, Lester HA, Boehm BO et al. Functional characterization of dopaminergic neurons derived from rodent mesencephalic progenitor cells. J Chem Neuroanat 2003;26:133-142.
34. Ling ZD, Potter ED, Lipton JW et al. Differentiation of mesencephalic progenitor cells into dopaminergic neurons by cytokines. Exp Neurol 1998;149:411-423.
35. Milosevic J, Storch A, Schwarz J. Spontaneous apoptosis in murine free-floating neurospheres. Exp Cell Res 2004;294:9-17.
36. Storch A, Paul G, Csete M et al. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp Neurol 2001;170:317-325.
37. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990;60:585-595.
38. Gage FH. Mammalian neural stem cells. Science 2000;287:1433-1438.
39. Bradke F, Dotti CG. Establishment of neuronal polarity: Lessons from cultured hippocampal neurons. Curr Opin Neurobiol 2000;10:574-581.
40. Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988;8:1454-1468.
41. Shapira M, Zhai RG, Dresbach T et al. Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 2003;38: 237-252.
42. Richter K, Langnaese K, Kreutz MR et al. Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J Comp Neurol 1999;408:437-448.
43. Gritti A, Parati EA, Cova L et al. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 1996;16:1091-1100.
44. Johe KK, Hazel TG, Muller T et al. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev 1996;10:3129-3140.
45. Jain M, Armstrong RJ, Tyers P et al. GABAergic immunoreactivity is predominant in neurons derived from expanded human neural precursor cells in vitro. Exp Neurol 2003;182:113-123.
46. Milosevic J, Brandt A, Roemuss U et al. Uracil nucleotides stimulate human neural precursor cell proliferation and dopaminergic differentiation: Involvement of MEK/ERK signalling. J Neurochem 2006;99: 913-923.
47. Knaus P, Betz H, Rehm H. Expression of synaptophysin during postnatal development of the mouse brain. J Neurochem 1986;47:1302-1304.
48. Rehm H, Wiedenmann B, Betz H. Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J 1986;5:535-541.
49. Wiedenmann B, Franke WW. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 1985;41:1017-1028.
50. Masliah E, Honer WG, Mallory M et al. Topographical distribution of synaptic-associated proteins in the neuritic plaques of Alzheimer's disease hippocampus. Acta Neuropathol (Berl) 1994;87:135-142.
51. Rubenstein JL, Greengard P, Czernik AJ. Calcium-dependent serine phosphorylation of synaptophysin. Synapse 1993;13:161-172.
52. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C et al. Assembling the presynaptic active zone: A characterization of an active one precursor vesicle. Neuron 2001;29:131-143.
53. Fenster SD, Chung WJ, Zhai R et al. Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 2000;25:203-214.
54. Fenster SD, Garner CC. Gene structure and genetic localization of the PCLO gene encoding the presynaptic active zone protein Piccolo. Int J Dev Neurosci 2002;20:161-171.
55. Sheng M, Kim E. The Shank family of scaffold proteins. J Cell Sci 2000;113:1851-1856.
56. Tu JC, Xiao B, Naisbitt S et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 1999;23:583-592.
57. Du Y, Weed SA, Xiong WC et al. Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 1998;18:5838-5851.
58. Dresbach T, Torres V, Wittenmayer N et al. Assembly of active zone precursor vesicles: Obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J Biol Chem 2006;281:6038-6047.
59. Guan K, Chang H, Rolletschek A et al. Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res 2001;305:171-176.
60. Rohwedel J, Kleppisch T, Pich U et al. Formation of postsynaptic-like membranes during differentiation of embryonic stem cells in vitro. Exp Cell Res 1998;239:214-225.
61. Song HJ, Stevens CF, Gage FH. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 2002;5:438-445.
62. Bresler T, Ramati Y, Zamorano PL et al. The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol Cell Neurosci 2001; 18:149-167.