Effects of nitric oxide on neuromuscular properties of developing zebrafish embryos

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Jay, Michael ^a   Bradley, Sophie ^a   McDearmid, Jonathan Robert ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; NITRIC OXIDE; 18ALPHA-GLYCYRRHETINIC ACID; BIOLOGICAL MARKER; GLYCYRRHETINIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DENSITY; EMBRYO; EXPOSURE; HISTOCHEMISTRY; IN VIVO STUDY; KINETICS; LOCOMOTION; MINIATURE ENDPLATE POTENTIAL; MUSCLE CELL; NEUROMUSCULAR SYNAPSE; NONHUMAN; PATCH CLAMP TECHNIQUE; SIGNAL TRANSDUCTION; SWIMMING; SYNAPTOGENESIS; ZEBRA FISH; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL EMBRYO; DRUG EFFECTS; EMBRYO DEVELOPMENT; EMBRYOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; BIOLOGICAL MARKERS; CYCLIC GMP; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCYRRHETINIC ACID; KINETICS; LOCOMOTION; MINIATURE POSTSYNAPTIC POTENTIALS; MUSCLE FIBERS, SKELETAL; NEUROMUSCULAR JUNCTION; NITRIC OXIDE; PATCH-CLAMP TECHNIQUES; SIGNAL TRANSDUCTION; SWIMMING; ZEBRAFISH;

EID: 84900315231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086930     Document Type: Article

References (80)

1. Roskams AJ, Bredt DS, Dawson TM, Ronnett GV (1994) Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons. Neuron 13: 289-299. (Pubitemid 24275088)
2. Schwarte RC, Godfrey EW (2004) Nitric oxide synthase activity is required for postsynaptic differentiation of the embryonic neuromuscular junction. Dev Biol 273: 276-284. (Pubitemid 39140903)
3. Jones MA, Werle MJ (2000) Nitric oxide is a downstream mediator of agrin-induced acetylcholine receptor aggregation. Mol Cell Neurosci 16: 649-660. (Pubitemid 32001312)
4. Godfrey EW, Schwarte RC (2003) The role of nitric oxide signaling in the formation of the neuromuscular junction. J Neurocytol 32: 591-602. (Pubitemid 39011248)
5. Godfrey EW, Longacher M, Neiswender H, Schwarte RC, Browning DD (2007) Guanylate cyclase and cyclic GMP-dependent protein kinase regulate agrin signaling at the developing neuromuscular junction. Dev Biol 307: 195-201. (Pubitemid 47001352)
6. Cogen J, Cohen-Cory S (2000) Nitric oxide modulates retinal ganglion cell axon arbor remodeling in vivo. J Neurobiol 45: 120-133.
7. Wu J, Fang L, Lin Q, Willis WD (2001) Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain 94: 47-58. (Pubitemid 32907557)
8. Ernst AF, Wu HH, El-Fakahany EE, McLoon SC (1999) NMDA receptor-mediated refinement of a transient retinotectal projection during development requires nitric oxide. J Neurosci 19: 229-235. (Pubitemid 29028964)
9. Forstermann U, Mulsch A, Bohme E, Busse R (1986) Stimulation of soluble guanylate cyclase by an acetylcholine-induced endothelium-derived factor from rabbit and canine arteries. Circ Res 58: 531-538. (Pubitemid 16102209)
10. Ignarro LJ, Harbison RG, Wood KS, Kadowitz PJ (1986) Activation of purified soluble guanylate cyclase by endothelium-derived relaxing factor from intrapulmonary artery and vein: stimulation by acetylcholine, bradykinin and arachidonic acid. J Pharmacol Exp Ther 237: 893-900. (Pubitemid 16088110)
11. Ignarro LJ, Adams JB, Horwitz PM, Wood KS (1986) Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. Comparison of heme-containing and heme-deficient enzyme forms. J Biol Chem 261: 4997-5002. (Pubitemid 17204293)
12. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, et al. (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7: 615-624.
13. Judas M, Sestan N, Kostovic I (1999) Nitrinergic neurons in the developing and adult human telencephalon: transient and permanent patterns of expression in comparison to other mammals. Microsc Res Tech 45: 401-419. (Pubitemid 29321054)
14. Zhang YT, Zhang DL, Cao YL, Zhao BL (2002) Developmental expression and activity variation of nitric oxide synthase in the brain of golden hamster. Brain Res Bull 58: 385-389.
15. Gotti S, Sica M, Viglietti-Panzica C, Panzica G (2005) Distribution of nitric oxide synthase immunoreactivity in the mouse brain. Microsc Res Tech 68: 13-35. (Pubitemid 41464006)
16. Oermann E, Bidmon HJ, Mayer B, Zilles K (1999) Differential maturational patterns of nitric oxide synthase-I and NADPH diaphorase in functionally distinct cortical areas of the mouse cerebral cortex. Anat Embryol (Berl) 200: 27-41. (Pubitemid 29261623)
17. Chung YH, Joo KM, Lee YJ, Shin DH, Cha CI (2004) Postnatal development and age-related changes in the distribution of nitric oxide synthase-immunore- active neurons in the visual system of rats. Neurosci Lett 360: 1-4. (Pubitemid 38471973)
18. Terada H, Nagai T, Kimura H, Kitahama K, Okada S (1996) Distribution of nitric oxide synthase-immunoreactive neurons in fetal rat brains at embryonic day 15 and day 19. J Chem Neuroanat 10: 273-278. (Pubitemid 26196655)
19. Terada H, Nagai T, Okada S, Kimura H, Kitahama K (2001) Ontogenesis of neurons immunoreactive for nitric oxide synthase in rat forebrain and midbrain. Brain Res Dev Brain Res 128: 121-137. (Pubitemid 32539177)
20. Iwase K, Iyama K, Akagi K, Yano S, Fukunaga K, et al. (1998) Precise distribution of neuronal nitric oxide synthase mRNA in the rat brain revealed by non-radioisotopic in situ hybridization. Brain Res Dev Brain Res 53: 1-12. (Pubitemid 28085437)
21. Poon KL, Richardson M, Lam CS, Khoo HE, Korzh V (2003) Expression pattern of neuronal nitric oxide synthase in embryonic zebrafish. Gene Expr Patterns 3: 463-466. (Pubitemid 36950422)
22. Holmqvist B, Ellingsen B, Forsell J, Zhdanova I, Alm P (2004) The early ontogeny of neuronal nitric oxide synthase systems in the zebrafish. J Exp Biol 207: 923-935. (Pubitemid 38370747)
23. Bruning G, Mayer B (1996) Prenatal development of nitric oxide synthase in the mouse spinal cord. Neurosci Lett 202: 189-192. (Pubitemid 26029833)
24. Hess DT, Patterson SI, Smith DS, Skene JH (1993) Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366: 562-565. (Pubitemid 24035995)
25. Hindley S, Juurlink BH, Gysbers JW, Middlemiss PJ, Herman MA, et al. (1997) Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism. J Neurosci Res 47: 427-439. (Pubitemid 27097757)
26. Gibbs SM, Becker A, Hardy RW, Truman JW (2001) Soluble guanylate cyclase is required during development for visual system function in Drosophila. J Neurosci 21: 7705-7714. (Pubitemid 32904969)
27. Gibbs SM, Truman JW (1998) Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20: 83-93. (Pubitemid 28078351)
28. Tojima T, Itofusa R, Kamiguchi H (2009) The nitric oxide-cGMP pathway controls the directional polarity of growth cone guidance via modulating cytosolic Ca2+ signals. J Neurosci 29: 7886-7897.
29. Yamazaki M, Chiba K, Mohri T (2006) Differences in neuritogenic response to nitric oxide in PC12 and PC12h cells. Neurosci Lett 393: 222-225. (Pubitemid 41821112)
30. Yamada RX, Matsuki N, Ikegaya Y (2006) Nitric oxide/cyclic guanosine monophosphate-mediated growth cone collapse of dentate granule cells. Neuroreport 17: 661-665.
31. Ernst AF, Gallo G, Letourneau PC, McLoon SC (2000) Stabilization of growing retinal axons by the combined signaling of nitric oxide and brain-derived neurotrophic factor. J Neurosci 20: 1458-1469. (Pubitemid 30220425)
32. Tornieri K, Rehder V (2007) Nitric oxide release from a single cell affects filopodial motility on growth cones of neighboring neurons. Dev Neurobiol 67: 1932-1943. (Pubitemid 350223928)
33. Welshhans K, Rehder V (2005) Local activation of the nitric oxide/cyclic guanosine monophosphate pathway in growth cones regulates filopodial length via protein kinase G, cyclic ADP ribose and intracellular Ca2+ release. Eur J Neurosci 22: 3006-3016. (Pubitemid 43001984)
34. Welshhans K, Rehder V (2007) Nitric oxide regulates growth cone filopodial dynamics via ryanodine receptor-mediated calcium release. Eur J Neurosci 26: 1537-1547. (Pubitemid 47416519)
35. Trimm KR, Rehder V (2004) Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19: 809-818. (Pubitemid 38297018)
36. Van Wagenen S, Rehder V (1999) Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39: 168-185. (Pubitemid 29190624)
37. Van Wagenen S, Rehder V (2001) Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46: 206-219. (Pubitemid 32105832)
38. Wu HH, Cork RJ, Huang PL, Shuman DL, Mize RR (2000) Refinement of the ipsilateral retinocollicular projection is disrupted in double endothelial and neuronal nitric oxide synthase gene knockout mice. Brain Res Dev Brain Res 120: 105-111. (Pubitemid 30155874)
39. Campello-Costa P, Fosse AM, Jr., Ribeiro JC, Paes-De-Carvalho R, Serfaty CA (2000) Acute blockade of nitric oxide synthesis induces disorganization and amplifies lesion-induced plasticity in the rat retinotectal projection. J Neurobiol 44: 371-381.
40. Wang T, Xie Z, Lu B (1995) Nitric oxide mediates activity-dependent synaptic suppression at developing neuromuscular synapses. Nature 374: 262-266.
41. Bradley S, Tossell K, Lockley R, McDearmid J (2010) Nitric oxide synthase regulates morphogenesis of zebrafish spinal cord motoneurons. J Neurosci 30: 16818-16831.
42. Westerfield M (1994) The Zebrafish Book: a Guide to the Laboratory Use of the Zebrafish (Brachydanio rerio): Eugene, OR: University of Oregon Press.
43. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
44. Luna VM, Brehm P (2006) An electrically coupled network of skeletal muscle in zebrafish distributes synaptic current. J Gen Physiol 128: 89-102. (Pubitemid 43967553)
45. del Castillo J, Escalona de Motta G (1978) A new method for excitation-contraction uncoupling in frog skeletal muscle. J Cell Biol 78: 782-784.
46. Buss RR, Drapeau P (2002) Activation of embryonic red and white muscle fibers during fictive swimming in the developing zebrafish. J Neurophysiol 87: 1244-1251. (Pubitemid 34670791)
47. Herberich E, Sikorski J, Hothorn T (2010) A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PloS One 5: e9788.
48. Panzer JA, Gibbs SM, Dosch R, Wagner D, Mullins MC, et al. (2005) Neuromuscular synaptogenesis in wild-type and mutant zebrafish. Dev Biol 285: 340-357. (Pubitemid 41394024)
49. van Raamsdonk W, Pool CW, te Kronnie G (1978) Differentiation of muscle fiber types in the teleost Brachydanio rerio. Anat Embryol (Berl) 153: 137-155. (Pubitemid 8342768)
50. Buss RR, Drapeau P (2000) Physiological properties of zebrafish embryonic red and white muscle fibers during early development. J Neurophysiol 84: 1545-1557.
51. Buckingham SD, Ali DW (2004) Sodium and potassium currents of larval zebrafish muscle fibres. J Exp Biol 207: 841-852. (Pubitemid 38261398)
52. Flanagan-Steet H, Fox MA, Meyer D, Sanes JR (2005) Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132: 4471-4481. (Pubitemid 41632226)
53. Jing L, Lefebvre JL, Gordon LR, Granato M (2009) Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61: 721-733.
54. Liu DW, Westerfield M (1992) Clustering of muscle acetylcholine receptors requires motoneurons in live embryos, but not in cell culture. J Neurosci 12: 1859-1866.
55. Sylvain NJ, Brewster DL, Ali DW (2011) Embryonic ethanol exposure alters synaptic properties at zebrafish neuromuscular junctions. Neurotoxicol Teratol 33: 313-321.
56. Drapeau P, Buss RR, Ali DW, Legendre P, Rotundo RL (2001) Limits to the development of fast neuromuscular transmission in zebrafish. J Neurophysiol 86: 2951-2956. (Pubitemid 33139062)
57. Nguyen PV, Aniksztejn L, Catarsi S, Drapeau P (1999) Maturation of neuromuscular transmission during early development in zebrafish. J Neurophysiol 81: 2852-2861. (Pubitemid 29283940)
58. Kullberg RW, Mikelberg FS, Cohen MW (1980) Contribution of Cholinesterase to Developmental Decreases in the Time Course of Synaptic Potentials at an Amphibian Neuromuscular-Junction. Dev Biol 75: 255-267. (Pubitemid 10115552)
59. Mongeon R, Walogorsky M, Urban J, Mandel G, Ono F, et al. (2011) An acetylcholine receptor lacking both gamma and epsilon subunits mediates transmission in zebrafish slow muscle synapses. J Gen Physiol 138: 353-366.
60. Mishina M, Takai T, Imoto K, Noda M, Takahashi T, et al. (1986) Molecular Distinction between Fetal and Adult Forms of Muscle Acetylcholine-Receptor. Nature 321: 406-411. (Pubitemid 16055490)
61. Naranjo D, Brehm P (1993) Modal shifts in acetylcholine receptor channel gating confer subunit-dependent desensitization. Science 260: 1811-1814. (Pubitemid 23244208)
62. Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP (1996) Maturation of the acetylcholine receptor in skeletal muscle: Regulation of the AChR gamma-toepsilon switch. Dev Biol 179: 223-238. (Pubitemid 26363259)
63. Gu Y, Hall ZW (1988) Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1: 117-125.
64. Kyriakatos A, Molinari M, Mahmood R, Grillner S, Sillar KT, et al. (2009) Nitric oxide potentiation of locomotor activity in the spinal cord of the lamprey. J Neurosci 29: 13283-13291.
65. McLean DL, Sillar KT (2004) Metamodulation of a spinal locomotor network by nitric oxide. J Neurosci 24: 9561-9571. (Pubitemid 39441510)
66. Luna VM, Wang M, Ono F, Gleason MR, Dallman JE, et al. (2004) Persistent electrical coupling and locomotory dysfunction in the zebrafish mutant shocked. J Neurophysiol 92: 2003-2009. (Pubitemid 39298658)
67. Katz B, Miledi R (1965) The Measurement of Synaptic Delay, and the Time Course of Acetylcholine Release at the Neuromuscular Junction. Proc R Soc Lond B Biol Sci 161: 483-495.
68. Wen H, Brehm P (2005) Paired motor neuron-muscle recordings in zebrafish test the receptor blockade model for shaping synaptic current. J Neurosci 25: 8104-8111. (Pubitemid 41254414)
69. Samigullin D, Bukharaeva EA, Nikolsky E, Adamek S, Vyskocil F (2003) Long release latencies are increased by acetylcholine at frog endplate. Physiol Res 52: 475-480. (Pubitemid 37039913)
70. Bukcharaeva EA, Kim KC, Moravec J, Nikolsky EE, Vyskocil F (1999) Noradrenaline synchronizes evoked quantal release at frog neuromuscular junctions. J Physiol 517: 879-888. (Pubitemid 29306472)
71. Datyner NB, Gage PW (1980) Phasic Secretion of Acetylcholine at a Mammalian Neuromuscular-Junction. J Physiol 303: 299-314. (Pubitemid 10078587)
72. Ribera J, Marsal J, Casanovas A, Hukkanen M, Tarabal O, et al. (1998) Nitric oxide synthase in rat neuromuscular junctions and in nerve terminals of Torpedo electric organ: Its role as regulator of acetylcholine release. J Neurosci Res 51: 90-102. (Pubitemid 28063152)
73. Tricoire L, Vitalis T (2012) Neuronal nitric oxide synthase expressing neurons: a journey from birth to neuronal circuits. Front Neural Circuits 6: 82.
74. Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37: 622-632. (Pubitemid 28549222)
75. McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR (2008) Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neuro 11: 1419-1429.
76. McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR (2007) A topographic map of recruitment in spinal cord. Nature 446: 71-75. (Pubitemid 46348046)
77. Bhatt DH, McLean DL, Hale ME, Fetcho JR (2007) Grading movement strength by changes in firing intensity versus recruitment of spinal interneurons. Neuron 53: 91-102. (Pubitemid 44969484)
78. Menelaou E, McLean DL (2012) A gradient in endogenous rhythmicity and oscillatory drive matches recruitment order in an axial motor pool. J Neurosci 32: 10925-10939.
79. Ausborn J, Mahmood R, El Manira A (2012) Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network. Proc Natl Acad Sci U S A 109: E3631-3639.
80. Gabriel JP, Ausborn J, Ampatzis K, Mahmood R, Eklof-Ljunggren E, et al. (2011) Principles governing recruitment of motoneurons during swimming in zebrafish. Nat Neurosci 14: 93-99.