A New Fiji-Based Algorithm That Systematically Quantifies Nine Synaptic Parameters Provides Insights into Drosophila NMJ Morphometry

PLoS Computational Biology

Volumn 12, Issue 3, 2016, Pages

  Nijhof, Bonnie ^a   Castells Nobau, Anna ^a   Wolf, Louis ^b   Scheffer de Gooyert, Jolanda M ^a   Monedero, Ignacio ^c,d   Torroja, Laura ^c   Coromina, Lluis ^e   van der Laak, Jeroen A W M ^b   Schenck, Annette ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d LINKÖPING UNIVERSITY   (Sweden)

^e UNIVERSITY OF GIRONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; DROSOPHILLA; GENE MANIPULATION; MORPHOLOGICAL FEATURES; MORPHOMETRICS; MORPHOMETRY; NEUROMUSCULAR JUNCTIONS; QUALITATIVE APPROACH; STRUCTURAL ASPECTS; SYNAPTIC PARAMETERS;

PRINCIPAL COMPONENT ANALYSIS;

DROSOPHILA; FIJI; GENDER; GENETIC BACKGROUND; GEOMETRY; HUMAN; IDENTITY; IMAGE ANALYSIS; MODEL; MORPHOMETRICS; MUSCLE MASS; NEUROMUSCULAR SYNAPSE; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE ANALYSIS; SYNAPSE; ALGORITHM; ANATOMIC MODEL; ANIMAL; BIOLOGICAL MODEL; COMPUTER ASSISTED DIAGNOSIS; CYTOLOGY; DATA MINING; FACTUAL DATABASE; NEUROMUSCULAR JUNCTION; PROCEDURES;

ALGORITHMS; ANIMALS; DATA MINING; DATABASES, FACTUAL; DROSOPHILA; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MODELS, ANATOMIC; MODELS, NEUROLOGICAL; NEUROMUSCULAR JUNCTION;

EID: 84962090070     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004823     Document Type: Article

References (69)

1. Lin YC, Koleske AJ, (2010) Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci33: 349–378. doi: 10.1146/annurev-neuro-060909-15320420367247
2. van Bokhoven H, (2011) Genetic and epigenetic networks in intellectual disabilities. Annu Rev Genet45: 81–104. doi: 10.1146/annurev-genet-110410-13251221910631
3. Penzes P, Buonanno A, Passafaro M, Sala C, Sweet RA, (2013) Developmental vulnerability of synapses and circuits associated with neuropsychiatric disorders. J Neurochem126: 165–182. doi: 10.1111/jnc.1226123574039
4. Wondolowski J, Dickman D, (2013) Emerging links between homeostatic synaptic plasticity and neurological disease. Front Cell Neurosci7: 223. doi: 10.3389/fncel.2013.0022324312013
5. Banerjee S, Riordan M, Bhat MA, (2014) Genetic aspects of autism spectrum disorders: insights from animal models. Front Cell Neurosci8: 58. doi: 10.3389/fncel.2014.0005824605088
6. Mainen ZF, Sejnowski TJ, (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature382: 363–366. 8684467
7. Yuste R, Majewska A, Holthoff K, (2000) From form to function: calcium compartmentalization in dendritic spines. Nat Neurosci3: 653–659. 10862697
8. Vetter P, Roth A, Hausser M, (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol85: 926–937. 11160523
9. Dahlhaus M, Levelt CN, (2010) Structure and function relationships during ocular dominance plasticity in the visual cortex. Rev Neurosci21: 223–237. 20879693
10. Bosch M, Hayashi Y, (2012) Structural plasticity of dendritic spines. Curr Opin Neurobiol22: 383–388. doi: 10.1016/j.conb.2011.09.00221963169
11. Fortin DA, Srivastava T, Soderling TR, (2012) Structural modulation of dendritic spines during synaptic plasticity. Neuroscientist18: 326–341. doi: 10.1177/107385841140720621670426
12. Mehnert KI, Cantera R, (2011) Circadian rhythms in the morphology of neurons in Drosophila. Cell Tissue Res344: 381–389. doi: 10.1007/s00441-011-1174-x21562943
13. Gorska-Andrzejak J, Makuch R, Stefan J, Gorlich A, Semik D, et al. (2013) Circadian expression of the presynaptic active zone protein Bruchpilot in the lamina of Drosophila melanogaster. Dev Neurobiol73: 14–26. doi: 10.1002/dneu.2203222589214
14. Muraro NI, Pirez N, Ceriani MF, (2013) The circadian system: plasticity at many levels. Neuroscience247: 280–293. doi: 10.1016/j.neuroscience.2013.05.03623727010
15. Ruiz S, Ferreiro MJ, Menhert KI, Casanova G, Olivera A, et al. (2013) Rhythmic changes in synapse numbers in Drosophila melanogaster motor terminals. PLoS One8: e67161. doi: 10.1371/journal.pone.006716123840613
16. Sigrist SJ, Reiff DF, Thiel PR, Steinert JR, Schuster CM, (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci23: 6546–6556. 12878696
17. Ataman B, Ashley J, Gorczyca M, Ramachandran P, Fouquet W, et al. (2008) Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron57: 705–718. doi: 10.1016/j.neuron.2008.01.02618341991
18. Ruiz-Canada C, Budnik V, (2006) Introduction on the use of the Drosophila embryonic/larval neuromuscular junction as a model system to study synapse development and function, and a brief summary of pathfinding and target recognition. Int Rev Neurobiol75: 1–31. 17137921
19. Menon KP, Carrillo RA, Zinn K, (2013) Development and plasticity of the Drosophila larval neuromuscular junction. Wiley Interdiscip Rev Dev Biol2: 647–670. doi: 10.1002/wdev.10824014452
20. Collins CA, DiAntonio A, (2007) Synaptic development: insights from Drosophila. Curr Opin Neurobiol17: 35–42. 17229568
21. Atwood HL, Govind CK, Wu CF, (1993) Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol24: 1008–1024. 8409966
22. Kraut R, Menon K, Zinn K, (2001) A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. Curr Biol11: 417–430. 11301252
23. Parnas D, Haghighi AP, Fetter RD, Kim SW, Goodman CS, (2001) Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron32: 415–424. 11709153
24. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, et al. (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron33: 545–558. 11856529
25. Eaton BA, Fetter RD, Davis GW, (2002) Dynactin is necessary for synapse stabilization. Neuron34: 729–741. 12062020
26. Rohrbough J, Rushton E, Palanker L, Woodruff E, Matthies HJ, et al. (2004) Ceramidase regulates synaptic vesicle exocytosis and trafficking. J Neurosci24: 7789–7803. 15356190
27. Laviolette MJ, Nunes P, Peyre JB, Aigaki T, Stewart BA, (2005) A genetic screen for suppressors of Drosophila NSF2 neuromuscular junction overgrowth. Genetics170: 779–792. 15834148
28. Collins CA, Wairkar YP, Johnson SL, DiAntonio A, (2006) Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron51: 57–69. 16815332
29. Liebl FL, Werner KM, Sheng Q, Karr JE, McCabe BD, et al. (2006) Genome-wide P-element screen for Drosophila synaptogenesis mutants. J Neurobiol66: 332–347. 16408305
30. Valakh V, Naylor SA, Berns DS, DiAntonio A, (2012) A large-scale RNAi screen identifies functional classes of genes shaping synaptic development and maintenance. Dev Biol366: 163–171. doi: 10.1016/j.ydbio.2012.04.00822542760
31. Blunk AD, Akbergenova Y, Cho RW, Lee J, Walldorf U, et al. (2014) Postsynaptic actin regulates active zone spacing and glutamate receptor apposition at the Drosophila neuromuscular junction. Mol Cell Neurosci61: 241–254. doi: 10.1016/j.mcn.2014.07.00525066865
32. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods9: 676–682. doi: 10.1038/nmeth.201922743772
33. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature448: 151–156. 17625558
34. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron49: 833–844. 16543132
35. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, et al. (2006) Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science312: 1051–1054. 16614170
36. Nijhof B, Castells-Nobau A, Wolf L, Scheffer-de Gooyert JM, Monedero I, et al. (2016) Drosophila NMJ Morphometrics.
37. Lin LI, (1989) A concordance correlation coefficient to evaluate reproducibility. Biometrics45: 255–268. 2720055
38. Koch I, Schwarz H, Beuchle D, Goellner B, Langegger M, et al. (2008) Drosophila ankyrin 2 is required for synaptic stability. Neuron58: 210–222. doi: 10.1016/j.neuron.2008.03.01918439406
39. Pielage J, Cheng L, Fetter RD, Carlton PM, Sedat JW, et al. (2008) A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron58: 195–209. doi: 10.1016/j.neuron.2008.02.01718439405
40. Iqbal Z, Vandeweyer G, van der Voet M, Waryah AM, Zahoor MY, et al. (2013) Homozygous and heterozygous disruptions of ANK3: at the crossroads of neurodevelopmental and psychiatric disorders. Hum Mol Genet22: 1960–1970. doi: 10.1093/hmg/ddt04323390136
41. Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, et al. (2000) Highwire regulates synaptic growth in Drosophila. Neuron26: 313–329. 10839352
42. Graf ER, Daniels RW, Burgess RW, Schwarz TL, DiAntonio A, (2009) Rab3 dynamically controls protein composition at active zones. Neuron64: 663–677. doi: 10.1016/j.neuron.2009.11.00220005823
43. Prokop A, (2006) Organization of the efferent system and structure of neuromuscular junctions in Drosophila. Int Rev Neurobiol75: 71–90. 17137924
44. Sutcliffe B, Forero MG, Zhu B, Robinson IM, Hidalgo A, (2013) Neuron-type specific functions of DNT1, DNT2 and Spz at the Drosophila neuromuscular junction. PLoS One8: e75902. doi: 10.1371/journal.pone.007590224124519
45. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol7: R100. 17076895
46. Mittag A, Pinto FE, Endringer DC, Tarnok A, Lenz D, (2011) Cellular analysis by open-source software for affordable cytometry. Scanning33: 33–40. doi: 10.1002/sca.2022021319173
47. Osaka I, Hills JM, Kieweg SL, Shinogle HE, Moore DS, et al. (2012) An automated image-based method for rapid analysis of Chlamydia infection as a tool for screening antichlamydial agents. Antimicrob Agents Chemother56: 4184–4188. doi: 10.1128/AAC.00427-1222615279
48. Gonzalez JE, Lee M, Barquinero JF, Valente M, Roch-Lefevre S, et al. (2012) Quantitative image analysis of gamma-H2AX foci induced by ionizing radiation applying open source programs. Anal Quant Cytol Histol34: 66–71. 22611761
49. Wahlby C, Kamentsky L, Liu ZH, Riklin-Raviv T, Conery AL, et al. (2012) An image analysis toolbox for high-throughput C. elegans assays. Nat Methods9: 714–716. doi: 10.1038/nmeth.198422522656
50. Vincent L, Soille P, (1991) Watersheds in digital spaces: an efficient algorithm based on immersion simulations. Pattern Analysis and Machine Intelligence, IEEE Transactions13: 583–598.
51. Mirth CK, Shingleton AW, (2012) Integrating body and organ size in Drosophila: recent advances and outstanding problems. Front Endocrinol (Lausanne)3: 49.
52. Demerec M, Kaufmann BP, (1996) Drosophila Guide: Introduction to the Genetics and Cytology of Drosophila melanogaster. Tenth Edition. Washington, D.C.: Carnegie Institution of Washington.
53. Bellen HJ, Budnik V, (2000) Drosophila protocols, chapter 11: The Neuromuscular Junction. New York: Cold Spring Harbor Laboratory Press.
54. Budnik V, Gorczyca M, Prokop A, (2006) Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int Rev Neurobiol75: 323–365. 17137935
55. Brent JR, Werner KM, McCabe BD, (2009) Drosophila larval NMJ dissection. J Vis Exp.
56. Brent J, Werner K, McCabe BD, (2009) Drosophila larval NMJ immunohistochemistry. J Vis Exp.
57. Ramachandran P, Budnik V, (2010) Drosophila Neurobiology. A laboratory manual, chapter 7: Enmbryonic and Larval Neuromuscular Junction: An overview with Selected Methods and Protocols. New York: Cold Spring Harbor Laboratory Press.
58. Smith R, Taylor JP, (2011) Dissection and imaging of active zones in the Drosophila neuromuscular junction. J Vis Exp.
59. Lnenicka GA, Theriault K, Monroe R, (2006) Sexual differentiation of identified motor terminals in Drosophila larvae. J Neurobiol66: 488–498. 16470738
60. Campbell M, Ganetzky B, (2012) Extensive morphological divergence and rapid evolution of the larval neuromuscular junction in Drosophila. Proc Natl Acad Sci U S A109: E648–655. doi: 10.1073/pnas.120117610922355119
61. St Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase C, (2014) FlyBase 102—advanced approaches to interrogating FlyBase. Nucleic Acids Res42: D780–788. doi: 10.1093/nar/gkt109224234449
62. Schuster CM, Davis GW, Fetter RD, Goodman CS, (1996) Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron17: 641–654. 8893022
63. Sternberg SR, (1983) Biomedical Image Processing. Computer16: 22–34.
64. Sahoo P, Wilkins C, Yeager J, (1997) Threshold selection using Renyi's entropy. Pattern Recognition30: 71–84.
65. Şengür A, Türkoğlu İ, ve İnce MC, (2006) A Comparative Study On Entropic Thresholding Methods. Istanbul University—Journal of Electrical & Electronics Engineering6: 183–188.
66. Stevenson M, Nunes T, Heuer C, Marshall J, Sanchez J, et al. (2014) epiR: An R package for the analysis of epidemiological data. R package version 0.9–59. The Comprehensive R Archive Network.
67. R-Development-Core-Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
68. Hurley C (2012) gclus: Clustering Graphics. R package version 1.3.1.
69. Husson FJ, J.; Le, S.; Mazet, J. (2014) FactoMineR: Multivariate Exploratory Data Analysis and Data Mining with R. R package version 1.26.