Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling

Journal of Neuroscience

Volumn 25, Issue 1, 2005, Pages 96-107

  Collin, Thibault ^a   Chat, Mireille ^a   Lucas, Marie Gabrielle ^a   Moreno, Herman ^b   Racay, Peter ^c,d   Schwaller, Beat ^b   Marty, Alain ^a   Llano, Isabel ^a  

^a CNRS   (France)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

^d University Teaching Hospital in Martin   (Slovakia)

Author keywords

Calcium; Cerebellum; Development; Imaging; Patch clamp; Synapses

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM BINDING PROTEIN; NEUROTRANSMITTER; PARVALBUMIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CEREBELLUM CORTEX; CHEMICAL ANALYSIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; IMMUNOCYTOCHEMISTRY; INTERNEURON; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SIMULATION; WHOLE CELL; WILD TYPE;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CEREBELLAR CORTEX; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; KINETICS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; NEURAL INHIBITION; PARVALBUMINS; PRESYNAPTIC TERMINALS;

EID: 12144282737     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3748-04.2005     Document Type: Article

References (63)

1. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94:1488-1493.
2. Atluri PP, Regehr WG (1998) Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci 18:8214-8227.
3. Auger C, Marty A (1997) Heterogeneity of functional synaptic parameters among single release sites. Neuron 19:139-150.
4. Barski JJ, Hartmann J, Rose CR, Hoebeek F, Mörl K, Noli-Hussong M, De Zeeuw CI, Konnerth A, Meyer M (2003) Calbindin in cerebellar Purkinje cell is a critical determinant of the precision of motor coordination. J Neurosci 23:3469-3477.
5. 2+ binding and diffusion, during activation of frog skeletal muscle. J Gen Physiol 112:297-316.
6. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13-26.
7. 2+ buffer saturation underlies paired pulse facilitation in caibindin-D28k- containing terminals. Neuron 38:79-88.
8. Burrone J, Neves G, Gomis A, Cooke A, Lagnado L (2002) Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar ceils. Neuron 33:101-112.
9. Caillard O, Moreno H, Schwaller B, Llano I, Celio M, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci USA 97:13372-13377.
10. Celio MR (1986) Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cortex. Science 231:995-999.
11. Coutu P, Metzger M (2002) Optimal range for parvalbumin as relaxing agent in adult cardiac myocytes: gene transfer and mathematical modeling. Biophys J 82:2565-2579.
12. 2+-binding proteins. J Physiol (Lond) 556:447-461.
13. Eberhard M, Erne P (1991) Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochem Biophys Res Commun 180:209-215.
14. Eccles JC, Llinás R, Sasaki K (1966) The inhibitory interneurones within the cerebellar cortex. Exp Brain Res 1:1-16.
15. Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786-790.
16. Ekerot C-F, Jörntell H (2001) Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 13:1303-1310.
17. Felmy F, Neher E, Schneggenburger R (2003) Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37:801-811.
18. Fierro L, Llano I (1996) High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J Physiol (Lond) 496:617-625.
19. Fierro L, DiPolo R, Llano I (1998) Intracellular calcium clearance in Purkinje cell somata from rat cerebellar slices. J Physiol (Lond) 510:499-512.
20. 2+ signals in axons of developing rat cerebellar interneurons. J Physiol (Lond) 527:31-47.
21. Goda Y, Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci USA 91:12942-12946.
22. Haiech J, Derancourt J, Pechere JF, Demaille JG (1979) Magnesium and calcium binding to parvalbumins: evidence for differences between parvalbumins and an explanation of their relaxing function. Biochemistry 18:2752-2758.
23. Helmchen F, Borst JGJ, Sakmann B (1997) Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471.
24. Jackson MB, Redman SJ (2003) Calcium dynamics, buffering, and buffer saturation in the boutons of dentate granule-cell axons in the hilus. J Neurosci 23:1612-1624.
25. 2+-binding protein parvalbumin. J Physiol (Lond) 535:3-16.
26. 2+ concentration and asynchronous transmitter release at single GABAergic boutons in rat collicular cultures. J Physiol (Lond) 548:753-764.
27. Koester HJ, Sakmann B (2000) Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J Physiol (Lond) 529:625-646.
28. Kosaka T, Kosaka K, Nakayama T, Hunziker W, Heizmann CW (1993) Axons and axon terminals of cerebellar Purkinje cells and basket cells have higher levels of parvalbumin immunoreactivity than somata and dendrites: quantitative analysis by immunogold labeling. Exp Brain Res 93:483-491.
29. 2+] transients of neuronal dendrites. J Physiol (Lond) 525:419-432.
30. 2+ concentration and inhibition of NMDA responses in cultured rat neurons. J Physiol (Lond) 533:729-743.
31. Llano I, Marty A, Armstrong CM, Konnerth A (1991) Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol (Lond) 434:183-213.
32. 2+ signals in axons of basket cells from rat cerebellar slices. J Physiol (Lond) 502:509-519.
33. 2+ transients at Purkinje cell synapses. Nat Neurosci 3:1256-1265.
34. Llinás R, Sugimori M, Silver RB (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256:677-679.
35. Lu T, Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 28:683-694.
36. 2+ buffering in Purkinje neurons. Neuron 24:989-1002.
37. Majewska A, Brown E, Ross J, Yuste R (2000) Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci 20:1722-1734.
38. Markram H, Roth A, Helmchen F (1998) Competitive calcium binding: implications for dendritic calcium signaling. J Comp Neurosci 5:331-348.
39. 2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol (Lond) 547:665-689.
40. Meyer AH, Katona I, Blatow M, Rozov, Monyer H (2002) In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22:7055-7064.
41. 2+ signals. Cell Calcium 24:345-357.
42. Neher E, Augustine GJ (1992) Calcium gradients and buffers in bovine chromaffin. J Physiol (Lond) 450:273-301.
43. Palay L, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Berlin: Springer.
44. Pozzan T, Rizzuto R, Volpe P, Meldolesi J (1994) Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74:595-636.
45. Ricci AJ, Wu Y-C, Fettiplace R (1998) The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cell. J Neurosci 18:8261-8277.
46. Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74-76.
47. Roberts WM (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14:3246-3262.
48. Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M, Moreno H, Nadal MS, Hernandez-Pineda R, Hernandez-Cruz A, Erisir A, Leonard C, VegaZaenz de Meira E (1999) Contribution of Kv3 channels to neuronal excitability. In: Molecular and functional diversity of ion channels and receptors. Ann NY Acad Sci 868:304-343.
49. 28k. J Physiol (Lond) 551:13-32.
50. Schmidt H, Brown EB, Schwaller B, Eilers J (2003b) Diffusional mobility of parvalbumin in spiny dendrites of cerebellar Purkinje neurons quantified by fluorescence recovery after photobleaching. Biophys J 84:2599-2608.
51. Schwaller B, Dick J, Dhoot G, Carroll S, Vrbova G, Nicoretta P, Pette D, Wyss A, Bluethmann H, Hunziker W, Celio M (1999) Prolonged contraction- relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol 276:C395-C403.
52. Schwaller B, Meyer M, Schiffmann S (2002) "New" functions for "old" proteins: the role of the calcium-binding proteins calbindin D-28K, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241-258.
53. Simon SM, Llinás RR (1985) Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 48:485-498.
54. Sinha SR, Wu L-G, Saggau P (1997) Presynaptic calcium dynamics and transmitter release evoked by single action potentials at mammalian central synapses. Biophys J 72:637-651.
55. 2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20:1243-1253.
56. Sultan F, Bower JM (1998) Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis. J Comp Neurol 393:353-373.
57. 2+ rises in rat cerebellar basket cell axons. J Physiol (Lond) 520:65-78.
58. Tan YP, Llano I, Hopt A, Würriehausen F, Neher E (1999) Fast scanning and efficient photodetection in a simple two-photon microscope. J Neurosci Methods 92:123-135.
59. Van der Kloot W, Molgo J (1993) Quantal acetlycholine release at the vertebrate neuromuscular junction. Physiol Rev 74:899-991.
60. Vincent P, Marty A (1996) Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. J Physiol (Lond) 494:183-199.
61. Westerblad H, Lannergren J (1991) Slowing of relaxation during fatigue in single mouse muscle fibres. J Physiol (Lond) 434:323-336.
62. Zhang L, Goldman JE (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16:47-54.
63. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.