Cell and Tissue Research

, Volume 326, Issue 2, pp 301–310

Giant reticulospinal synapse in lamprey: molecular links between active and periactive zones

Review

Abstract

Deciphering the function of synaptic release sites is central to understanding neuronal communication. Here, we review studies of the lamprey giant reticulospinal synapse, a model that can be used to dissect synaptic vesicle trafficking at single release sites. The presynaptic axon is large and contains active zones that are spatially separated from each other. During activity, synaptic vesicle membrane is shuttled between the active zone and the periactive zone at which endocytosis occurs. Recent studies have shown that the periactive zone contains an actin-rich cytomatrix that expands during synaptic activity. This cytomatrix has been implicated in multiple functions that include (1) activity-dependent trafficking of proteins between the synaptic vesicle cluster and the periactive zone, (2) synaptic vesicle endocytosis, and (3) the movement of newly formed synaptic vesicles to the vesicle cluster. The actin cytomatrix thus provides a link between the active zone and the periactive zone; this link appears to be critical for sustained cycling of synaptic vesicles.

Keywords

Actin Active zone Endocytosis Exocytosis Synaptic vesicle Lamprey 

References

  1. Blackmer T, Larsen EC, Takahashi M, Martin TF, Alford S, Hamm HE (2001) G protein betagamma subunit-mediated presynaptic inhibition: regulation of exocytotic fusion downstream of Ca2+ entry. Science 292:293–297PubMedCrossRefGoogle Scholar
  2. Blackmer T, Larsen EC, Bartleson C, Kowalchyk JA, Yoon EJ, Preininger AM, Alford S, Hamm HE, Martin TF (2005) G protein betagamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat Neurosci 8:421–425PubMedGoogle Scholar
  3. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Löw P, Brodin L, Pieribone VA, Greengard P, Shupliakov O (2003) Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161:737–747PubMedCrossRefGoogle Scholar
  4. Brodin L, Shupliakov O (1994) Functional diversity of central glutamate synapses—pre- and post-synaptic mechanisms. Acta Physiol Scand 150:1–10PubMedCrossRefGoogle Scholar
  5. Brodin L, Bakeeva L, Shupliakov O (1999) Presynaptic mitochondria and the temporal pattern of neurotransmitter release. Philos Trans R Soc Lond Biol 354:365–372PubMedCrossRefGoogle Scholar
  6. Brodin L, Löw P, Shupliakov O (2000) Sequential steps in clathrin-mediated synaptic vesicle endocytosis. Curr Opin Neurobiol 10:312–320PubMedCrossRefGoogle Scholar
  7. Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobiol 63:441–466PubMedCrossRefGoogle Scholar
  8. Darcy KJ, Staras K, Collinson LM, Goda Y (2006) Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9:315–321PubMedCrossRefGoogle Scholar
  9. Deliagina TG, Fagerstedt P (2000) Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs. J Neurophysiol 83:864–878PubMedGoogle Scholar
  10. Dillon C, Goda Y (2005) The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 28:25–55PubMedCrossRefGoogle Scholar
  11. Doussau F, Augustine GJ (2000) The actin cytoskeleton and neurotransmitter release: an overview. Biochimie 82:353–363PubMedCrossRefGoogle Scholar
  12. Dunaevsky A, Connor EA (2000) F-actin is concentrated in nonrelease domains at frog neuromuscular junctions. J Neurosci 20:6007–6012PubMedGoogle Scholar
  13. Engqvist-Goldstein AE, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287–332PubMedCrossRefGoogle Scholar
  14. Estes PS, Roos J, Bliek A van der, Kelly RB, Krishnan KS, Ramaswami M (1996) Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J Neurosci 16:5443–5456PubMedGoogle Scholar
  15. Evergren E, Tomilin N, Vasylieva E, Sergeeva V, Bloom O, Gad H, Capani F, Shupliakov O (2004a) A pre-embedding immunogold approach for detection of synaptic endocytic proteins in situ. J Neurosci Methods 135:169–174PubMedCrossRefGoogle Scholar
  16. Evergren E, Marcucci M, Tomilin N, Löw P, Slepnev V, Andersson F, Gad H, Brodin L, De Camilli P, Shupliakov O (2004b) Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 5:514–528PubMedCrossRefGoogle Scholar
  17. Evergren E, Zotova E, Brodin L, Shupliakov O (2006) Efficiency of synaptic vesicle recycling in tonic and phasic central synapses. In: 5th Forum of European Neuroscience. Vienna, AustriaGoogle Scholar
  18. Fenster SD, Kessels MM, Qualmann B, Chung WJ, Nash J, Gundelfinger ED, Garner CC (2003) Interactions between Piccolo and the actin/dynamin-binding protein Abp1 link vesicle endocytosis to presynaptic active zones. J Biol Chem 278:20268–20277PubMedCrossRefGoogle Scholar
  19. Gad H, Löw P, Zotova E, Brodin L, Shupliakov O (1998) Dissociation between Ca2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21:607–616PubMedCrossRefGoogle Scholar
  20. Gad H, Ringstad N, Löw P, Kjaerulff O, Gustafsson J, Wenk M, Di Paolo G, Nemoto Y, Crun J, Ellisman MH, De Camilli P, Shupliakov O, Brodin L (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27:301–312PubMedCrossRefGoogle Scholar
  21. Genko S, Tomilin N, Evergren E, Brodin L, Karlsson R, Shupliakov O (2005) Profilin:actin operates in signaling synapses in the lamprey spinal chord. American Society for Cell Biology, 45th Annual Meeting, San Francisco, Calif., USAGoogle Scholar
  22. Grillner S, Wallen P (2002) Cellular bases of a vertebrate locomotor system—steering, intersegmental and segmental co-ordination and sensory control. Brain Res Brain Res Rev 40:92–106PubMedCrossRefGoogle Scholar
  23. Guichet A, Wucherpfennig T, Dudu V, Etter S, Wilsch-Brauniger M, Hellwig A, Gonzalez-Gaitan M, Huttner WB, Schmidt AA (2002) Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J 21:1661–1672PubMedCrossRefGoogle Scholar
  24. Gundelfinger ED, Kessels MM, Qualmann B (2003) Temporal and spatial coordination of exocytosis and endocytosis. Nat Rev Mol Cell Biol 4:127–139PubMedCrossRefGoogle Scholar
  25. Gustafsson JS, Birinyi A, Crum J, Ellisman M, Brodin L, Shupliakov O (2002) Ultrastructural organization of lamprey reticulospinal synapses in three dimensions. J Comp Neurol 450:167–182PubMedCrossRefGoogle Scholar
  26. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J Cell Biol 108:111–126PubMedCrossRefGoogle Scholar
  27. Kavalali ET (2006) Synaptic vesicle reuse and its implications. Neuroscientist 12:57–66PubMedCrossRefGoogle Scholar
  28. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43:193–205PubMedCrossRefGoogle Scholar
  29. Kuromi H, Kidokoro Y (1998) Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20:917–925PubMedCrossRefGoogle Scholar
  30. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P, et al (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9235–9239PubMedCrossRefGoogle Scholar
  31. Marie B, Sweeney ST, Poskanzer KE, Roos J, Kelly RB, Davis GW (2004) Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43:207–219PubMedCrossRefGoogle Scholar
  32. Morales M, Colicos MA, Goda Y (2000) Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27:539–550PubMedCrossRefGoogle Scholar
  33. Morgan JR, Di Paolo G, Werner H, Shchedrina VA, Pypaert M, Pieribone VA, De Camilli P (2004) A role for talin in presynaptic function. J Cell Biol 167:43–50PubMedCrossRefGoogle Scholar
  34. Murthy VN, De Camilli P (2003) Cell biology of the nerve terminal. Annu Rev Neurosci 26:701–728PubMedCrossRefGoogle Scholar
  35. Photowala H, Freed R, Alford S (2005) Location and function of vesicle clusters, active zones and Ca2+ channels in the lamprey presynaptic terminal. J Physiol (Lond) 569:119–135CrossRefGoogle Scholar
  36. Photowala H, Blackmer T, Schwartz E, Hamm HE, Alford S (2006) G protein beta gamma-subunits activated by serotonin mediate presynaptic inhibition by regulating vesicle fusion properties. Proc Natl Acad Sci USA 103:4281–4286CrossRefGoogle Scholar
  37. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493–497PubMedCrossRefGoogle Scholar
  38. Qualmann B, Kessels MM, Kelly RB (2000) Molecular links between endocytosis and the actin cytoskeleton. J Cell Biol 150:111–116CrossRefGoogle Scholar
  39. Richards DA, Rizzoli SO, Betz WJ (2004) Effects of wortmannin and latrunculin A on slow endocytosis at the frog neuromuscular junction. J Physiol (Lond) 557:77–91CrossRefGoogle Scholar
  40. Ringstad N, Gad H, Low P, Di Paolo G, Brodin L, Shupliakov O, De Camilli P (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24:143–154PubMedCrossRefGoogle Scholar
  41. Roos J, Kelly RB (1999) The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr Biol 9:1411–1414PubMedCrossRefGoogle Scholar
  42. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488–493PubMedCrossRefGoogle Scholar
  43. Rovainen CM (1979) Neurobiology of lampreys. Physiol Rev 59:1007–1077PubMedGoogle Scholar
  44. Royle SJ, Lagnado L (2003) Endocytosis at the synaptic terminal. J Physiol (Lond) 553:345–355CrossRefGoogle Scholar
  45. Sakaba T, Neher E (2003) Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J Neurosci 23:837–846PubMedGoogle Scholar
  46. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127–135PubMedCrossRefGoogle Scholar
  47. Schoch S, Gundelfinger ED (2006) Molecular organization of the presynaptic active zone. Cell and Tissue Res (this issue)Google Scholar
  48. Shupliakov O, Brodin L (2000) A model glutamate synapse - the lamprey giant reticulospinal axon. In: Ottersen OP, Storm-Mathisen J (eds) Handbook of chemical neuroanatomy. Elsevier, Amsterdam, pp 273–288Google Scholar
  49. Shupliakov O, Brodin L, Cullheim S, Ottersen OP, Storm-Mathisen J (1992) Immunogold quantification of glutamate in two types of excitatory synapse with different firing patterns. J Neurosci 12:3789–3803PubMedGoogle Scholar
  50. Shupliakov O, Ottersen OP, Storm-Mathisen J, Brodin L (1997a) Glial and neuronal glutamine pools at glutamatergic synapses with distinct properties. Neuroscience 77:1201–1212PubMedCrossRefGoogle Scholar
  51. Shupliakov O, Löw P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L (1997b) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259–263PubMedCrossRefGoogle Scholar
  52. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Löw P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476–14481PubMedCrossRefGoogle Scholar
  53. Wickelgren WO, Leonard JP, Grimes MJ, Clark RD (1985) Ultrastructural correlates of transmitter release in presynaptic areas of lamprey reticulospinal axons. J Neurosci 5:1188–1201PubMedGoogle Scholar
  54. Zelenin PV (2005) Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey. Eur J Neurosci 22:2271–2282PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Neuroscience, CEDBKarolinska InstitutetStockholmSweden

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