Active zone protein Bassoon co-localizes with presynaptic calcium channel, modifies channel function, and recovers from aging related loss by exercise

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Nishimune, Hiroshi ^a   Numata, Tomohiro ^b   Chen, Jie ^a   Aoki, Yudai ^b   Wang, Yonghong ^a   Starr, Miranda P ^a   Mori, Yasuo ^b   Stanford, John A ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM ION; CELL PROTEIN; PROTEIN BASSOON; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; BSN PROTEIN, RAT; CACNA1A PROTEIN, MOUSE; CALCIUM; NERVE PROTEIN;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL SIZE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOREACTIVITY; ISOMETRIC EXERCISE; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE EXERCISE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RESISTANCE TRAINING; SYNAPTIC TRANSMISSION; SYNAPTOSOME; ANIMAL; C57BL MOUSE; CELL LINE; CONFOCAL MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE MUTANT; PATCH CLAMP; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

MAMMALIA; RATTUS; RODENTIA;

AGING; ANIMALS; CALCIUM; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, Q-TYPE; CELL LINE; CRICETINAE; GENE EXPRESSION REGULATION; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; PHYSICAL CONDITIONING, ANIMAL; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 84862005644     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038029     Document Type: Article

References (55)

1. Rosato Siri MD, Uchitel OD, (1999) Calcium channels coupled to neurotransmitter release at neonatal rat neuromuscular junctions. J Physiol 514 (Pt 2): 533-540.
2. 2+ channels. Proc Natl Acad Sci U S A 100: 3491-3496.
3. Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, et al. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81: 275-300.
4. Pumplin DW, Reese TS, Llinas R, (1981) Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A 78: 7210-7213.
5. Robitaille R, Adler EM, Charlton MP, (1990) Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5: 773-779.
6. Llinas R, Sugimori M, Silver RB, (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256: 677-679.
7. Haydon PG, Henderson E, Stanley EF, (1994) Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13: 1275-1280.
8. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20: 389-399.
9. 2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals. J Neurosci 18: 6319-6330.
10. Day NC, Wood SJ, Ince PG, Volsen SG, Smith W, et al. (1997) Differential localization of voltage-dependent calcium channel alpha1 subunits at the human and rat neuromuscular junction. J Neurosci 17: 6226-6235.
11. De Laet A, Adriaensen D, Van Bogaert PP, Scheuermann DW, Timmermans JP, (2002) Immunohistochemical localization of voltage-activated calcium channels in the rat oesophagus. Neurogastroenterology and motility 14: 173-181.
12. Santafé MM, Sabaté MM, Garcia N, Ortiz N, Lanuza MA, et al. (2005) Changes in the neuromuscular synapse induced by an antibody against gangliosides. Annals of Neurology 57: 396-407.
13. Rowley KL, Mantilla CB, Ermilov LG, Sieck GC, (2007) Synaptic vesicle distribution and release at rat diaphragm neuromuscular junctions. J Neurophysiol 98: 478-487.
14. Chen J, Billings SE, Nishimune H, (2011) Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. J Neurosci 31: 512-525.
15. Chen J, Mizushige T, Nishimune H, (2012) Active zone density is conserved during synaptic growth but impaired in aged mice. J Comp Neurol 520: 434-452.
16. Nishimune H, Sanes JR, Carlson SS, (2004) A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432: 580-587.
17. 2+ channels. Nature neuroscience 10: 691-701.
18. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144: 282-295.
19. 2+ channels. J Biol Chem 285: 21750-21767.
20. Carlson SS, Valdez G, Sanes JR, (2010) Presynaptic calcium channels and α3-Integrins are complexed with synaptic cleft laminins, cytoskeletal elements and active zone components. Journal of Neurochemistry 115: 654-666.
21. Fouquet W, Owald D, Wichmann C, Mertel S, Depner H, et al. (2009) Maturation of active zone assembly by Drosophila Bruchpilot. J Cell Biol 186: 129-145.
22. Muller C, Haupt A, Bildl W, Schindler J, Knaus H, et al. (2010) Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proceedings of the National Academy of Sciences 107: 14950-14957.
23. 2+ Signals in Insulin Granule Exocytosis. Diabetes 53: S59-62.
24. 2+ channel in insulin granule exocytosis. Journal of Biological Chemistry 279: 7956-7961.
25. Banker BQ, Kelly SS, Robbins N, (1983) Neuromuscular transmission and correlative morphology in young and old mice. J Physiol 339: 355-377.
26. Gutmann E, Hanzlikova V, Vysokocil F, (1971) Age changes in cross striated muscle of the rat. J Physiol 216: 331-343.
27. Fahim MA, (1997) Endurance exercise modulates neuromuscular junction of C57BL/6NNia aging mice. Journal of applied physiology 83: 59-66.
28. Fahim MA, Robbins N, (1982) Ultrastructural studies of young and old mouse neuromuscular junctions. J Neurocytol 11: 641-656.
29. Balice-Gordon RJ, (1997) Age-related changes in neuromuscular innervation. Muscle Nerve (Suppl 5): S83-87.
30. Valdez G, Tapia JC, Kang H, Clemenson GD Jr, Gage FH, et al. (2010) Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise. Proc Natl Acad Sci U S A 107: 14863-14868.
31. Cote MP, Azzam GA, Lemay MA, Zhukareva V, Houle JD, (2011) Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury. J Neurotrauma 28: 299-309.
32. Dupont-Versteegden EE, Houle JD, Dennis RA, Zhang J, Knox M, et al. (2004) Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve 29: 73-81.
33. McCullough MJ, Peplinski NG, Kinnell KR, Spitsbergen JM, (2011) Glial cell line-derived neurotrophic factor protein content in rat skeletal muscle is altered by increased physical activity in vivo and in vitro. Neuroscience 174: 234-244.
34. Udina E, Puigdemasa A, Navarro X, (2011) Passive and active exercise improve regeneration and muscle reinnervation after peripheral nerve injury in the rat. Muscle Nerve 43: 500-509.
35. Schaser AJ, Stang K, Connor NP, Behan M, (2012) The effect of age and tongue exercise on BDNF and TrkB in the hypoglossal nucleus of rats. Behav Brain Res 226: 235-241.
36. 2+ channels in smooth muscle cells from human umbilical artery. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology 20: 55-64.
37. Hallermann S, Fejtova A, Schmidt H, Weyhersmüller A, Silver RA, et al. (2010) Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68: 710-723.
38. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, et al. (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci U S A 107: 6504-6509.
39. 2+ channels and vesicles to add release sites and promote refilling. Neuron 68: 724-738.
40. Smith DO, (1984) Acetylcholine storage, release and leakage at the neuromuscular junction of mature adult and aged rats. J Physiol 347: 161-176.
41. Smittkamp SE, Spalding HN, Brown JW, Gupte AA, Chen J, et al. (2010) Measures of bulbar and spinal motor function, muscle innervation, and mitochondrial function in ALS rats. Behav Brain Res 211: 48-57.
42. Guggenmos DJ, Barbay S, Bethel-Brown C, Nudo RJ, Stanford JA, (2009) Effects of tongue force training on orolingual motor cortical representation. Behavioural Brain Research 201: 229-232.
43. Hubert MF, Laroque P, Gillet JP, Keenan KP, (2000) The effects of diet, ad Libitum feeding, and moderate and severe dietary restriction on body weight, survival, clinical pathology parameters, and cause of death in control Sprague-Dawley rats. Toxicol Sci 58: 195-207.
44. Fregosi RF, Fuller DD, (1997) Respiratory-related control of extrinsic tongue muscle activity. Respiration physiology 110: 295-306.
45. Hodges SH, Anderson AL, Connor NP, (2004) Remodeling of neuromuscular junctions in aged rat genioglossus muscle. Ann Otol Rhinol Laryngol 113: 175-179.
46. Uchitel OD, Protti DA, Sanchez V, Cherksey BD, Sugimori M, et al. (1992) P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses. Proc Natl Acad Sci U S A 89: 3330-3333.
47. 2+ channel subunit beta4 interact and colocalize at cerebellar synapses. Neuroreport 23: 49-54.
48. Liu KS, Siebert M, Mertel S, Knoche E, Wegener S, et al. (2011) RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334: 1565-1569.
49. Knight D, Tolley LK, Kim DK, Lavidis NA, Noakes PG, (2003) Functional analysis of neurotransmission at beta2-laminin deficient terminals. J Physiol 546: 789-800.
50. Maselli RA, Ng JJ, Anderson JA, Cagney O, Arredondo J, et al. (2009) Mutations in LAMB2 causing a severe form of synaptic congenital myasthenic syndrome. J Med Genet 46: 203-208.
51. 2+ channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci U S A 96: 15245-15250.
52. Bolte S, Cordelieres FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. Journal of Microscopy 224: 213-232.
53. Chakkalakal JV, Nishimune H, Ruas JL, Spiegelman BM, Sanes JR, (2010) Retrograde influence of muscle fibers on their innervation revealed by a novel marker for slow motoneurons. Development 137: 3489-3499.
54. Prakash YS, Miller SM, Huang M, Sieck GC, (1996) Morphology of diaphragm neuromuscular junctions on different fibre types. J Neurocytol 25: 88-100.
55. Narusawa M, Fitzsimons RB, Izumo S, Nadal-Ginard B, Rubinstein NA, et al. (1987) Slow myosin in developing rat skeletal muscle. J Cell Biol 104: 447-459.