Microfluidic tools for developmental studies of small model organisms -nematodes, fruit flies, and zebrafish

Biotechnology Journal

Volumn 8, Issue 2, 2013, Pages 192-205

  Hwang, Hyundoo ^a   Lu, Hang ^a  

^a Georgia Institute of Technology   (United States)

Author keywords

Developmental biology; Fruit fly; Microfluidics; Nematode; Zebrafish

Indexed keywords

BIOLOGICAL STUDIES; CAENORHABDITIS ELEGANS; DANIO RERIO; DEVELOPMENTAL BIOLOGY; DROSOPHILA MELANOGASTER; DRUG DISCOVERY; FRUIT FLIES; HIGH-THROUGHPUT; MICROFLUIDIC TECHNOLOGIES; MODEL ORGANISMS; NEMATODE; RECENT PROGRESS; SMALL OBJECTS; SOIL-DWELLING; ZEBRAFISH;

BIOLOGY; GEOLOGIC MODELS;

MICROFLUIDICS;

ARTICLE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EPIFLUORESCENCE MICROSCOPE; EYE MOVEMENT; FLOW RATE; FLUORESCENCE IMAGING; GENE ACTIVATION; GENE EXPRESSION; KNOCKOUT GENE; LARVA; LIFE CYCLE; MICROFLUIDICS; MOTONEURON; NANOSURGERY; NEMATODE; NERVE CELL PLASTICITY; NERVE REGENERATION; NONHUMAN; OVARY CYCLE; PHENOTYPE; PRIORITY JOURNAL; SURVIVAL RATE; TIME LAPSE IMAGING; WILD TYPE; ZEBRA FISH;

ANIMALS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; DRUG DISCOVERY; EMBRYONIC DEVELOPMENT; MICROFLUIDICS; MODELS, ANIMAL; ZEBRAFISH;

EID: 84873427107     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201200129     Document Type: Article

References (107)

1. Tissenbaum, H. A., Guarente, L., Model organisms as a guide to mammalian aging. Dev. Cell 2002, 2, 9-19.
2. Jenner, R. A., Wills, M. A., The choice of model organisms in evo-devo. Nat. Rev. Genet. 2007, 8, 311-314.
3. Narashimhan, M. G., Model organisms in biology: Scientific and other uses. J. Biosci. 1999, 24, 141-142.
4. Brenner, S., The genetics of Caenorhabditis elegans. Genetics 1974, 77, 71-94.
5. Berghmans, S., Butler, P., Goldsmith, P., Waldron, G. et al., Zebrafish based assays for the assessment of cardiac, visual and gut function Ñ potential safety screens for early drug discovery. J. Pharmacol. Toxicol. Methods 2008, 58, 59-68.
6. Brittijn, S. A., Duivesteijn, S. J., Belmamoune, M., Bertens, L. F. et al., Zebrafish development and regeneration: New tools for biomedical research. Int. J. Dev. Biol. 2009, 53, 835-850.
7. Meeker, N. D., Trede, N. S., Immunology and zebrafish: Spawning new models of human disease. Dev. Comp. Immunol. 2008, 32, 745-757.
8. Kaletta, T., Hengartner, M. O., Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 2006, 5, 387-399.
9. Leung, M. C. K., Williams, P. L., Benedetto, A., Au, C. et al., Caenorhabditis elegans: An emerging model in biomedical and environmental toxicology. Toxicol. Sci. 2008, 106, 5-28.
10. Pandey, U. B., Nichols, C. D., Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Phamacol. Rev. 2011, 63, 411-436.
11. O'Kane, C. J., Drosophila as a model organism for the study of neuropsychiatric disorders, in: J. J. Hagan (Ed.), Molecular and Functional Models in Neuropsychiatry, Springer-Verlag, Berlin, Heidelberg 2011, pp. 37-60.
12. Sulston, J. E., Horvitz, H. R., Post-embryonic cell lineages of the nematodes. Dev. Biol. 1977, 56, 110-156.
13. White, J. G., Southgate, E., Thomson, J. N., Brenner, S., The structure of the nervous system of the nematode. Philos. Trans. R. Soc. Lond. Ser. B 1986, 314, 1-340.
14. C. elegans Sequencing Consortium, Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 1998, 282, 2012-2018.
15. Hilliard, M. A., Apicella, A. J., Kerr, R., Suzuki, H. et al., In vivo imaging of C. elegans ASH neurons: Cellular response and adaptation to chemical repellents. EMBO J. 2005, 24, 63-72.
16. Kerr, R., Lev-Ram, V., Baird, G., Vincent, P. et al., Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 2000, 26, 583-594.
17. Avery, L., Shtonda, B. B., Food transport in the C. elegans pharynx. J. Exp. Biol. 2003, 206, 2441-2457.
18. Yanik, M. F., Cinar, H., Cinar, H. N., Chisholm, A. D. et al., Neurosurgery: Functional regeneration after laser axotomy. Nature 2004, 432, 822.
19. Chung, S. H., Clark, D. A., Gabel, C. V., Mazur, E. et al., The role of the AFD neuron in C. elegans thermotaxis analyzed using femtosecond laser ablation. BMC Neurosci. 2006, 7, 30.
20. Hulme, S. E., Shevkoplyas, S. S., Apfeld, J., Fontana, W. et al., A microfabricated array of clamps for immobilizing and imaging C. elegans. Lab Chip 2007, 7, 1515-1523.
21. Allen, P. B., Sgro, A. E., Chao, D. L., Doepker, B. E. et al., Single-synapse ablation and long-term imaging in live C. elegans. J. Neurosci. Methods 2008, 173, 20-26.
22. Hulme, S. E., Shevkoplyas, S. S., McGuigan, A. P., Apfeld, J. et al., Lifespan-on-a-chip: Microfluidic chambers for performing lifelong observation of C. elegans. Lab Chip 2010, 10, 589-597.
23. Weibel, D. B., Kruithof, M., Potenta, S., Sia, S. K. et al., Torque-actuated valves for microfluidics. Anal. Chem. 2005, 77, 4726-4733.
24. Golden, T. R., Melov, S., Gene expression changes associated with aging in C. elegans (January 2, 2007), in: W. The C. elegans Research Community, doi/10.1895/wormbook.1.127.1, http://www.wormbook.org. (Ed.), WormBook, 2006.
25. Antebi, A., Genetics of aging in Caenorhabditis elegans. PLoS Genet. 2007, 3, e129.
26. Clausell-Tormos, J., Lieber, D., Baret, J.-C., El-Harrak, A. et al., Droplet-based microfluidic platforms for the encapsulation and screening of mammalian cells and multicellular organism. Chem. Biol. 2008, 15, 427-437.
27. Shi, W., Qin, J., Ye, N., Lin, B., Droplet-based microfluidic system for individual Caenorhabditis elegans assay. Lab Chip 2008, 8, 1432-1435.
28. Shi, W., Wen, H., Lu, Y., Shi, Y. et al., Droplet microfluidics for characterizing the neurotoxin-induced responses in individual Caenorhabditis elegans. Lab Chip 2010, 10, 2855-2863.
29. Rohde, C. B., Zeng, F., Gonzalez-Rubio, R., Angel, M. et al., Microfluidic system for on-chip high-throughput whole-animal sorting and screening at subcellular resolution. Proc. Natl. Acad. Sci. USA 2007, 104, 13891-13895.
30. Guo, S. X., Bourgeois, F., Chokshi, T., Durr, N. J. et al., Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies. Nat. Methods 2008, 5, 531-533.
31. Zeng, F., Rohde, C. B., Yanik, M. F., Sub-cellular precision on-chip small-animal immobilization, multi-photon imaging and femtosecond-laser manipulation. Lab Chip 2008, 8, 653-656.
32. Gilleland, C. L., Rohde, C. B., Zeng, F., Yanik, M. F., Microfluidic immobilization of physiologically active Caenorhabditis elegans. Nat. Protoc. 2010, 5, 1888-1902.
33. Samara, C., Rohde, C. B., Gilleland, C. L., Norton, S. et al., Large-scale in vivo femtosecond laser neurosurgery screen reveals small-molecule enhancer of regeneration. Proc. Natl. Acad. Sci. USA 2010, 107, 18342-18347.
34. Ma, H., Jiang, L., Shi, W., Qin, J. et al., A programmable microvalve-based microfluidic array for characterization of neurotoxin-induced responses of individual C. elegans. Biomicrofluidics 2009, 3, 044114.
35. 2 and compressive immobilization of C. elegans on-chip. Lab Chip 2009, 9, 151-157.
36. Chung, K., Crane, M. M., Lu, H., Automated on-chip rapid microscopy, phenotyping and sorting of C. elegans. Nat. Methods 2008, 5, 637-643.
37. Rohde, C. B., Yanik, M. F., Subcellular in vivo time-lapse imaging and optical manipulation of Caenorhabditis elegans in standard multiwell plates. Nat. Communications 2011, 2, 271.
38. Krajniak, J., Lu, H., Long-term high-resolution imaging and culture of C. elegans in chip-gel hybrid microfluidic device for developmental studies. Lab Chip 2010, 10, 1862-1868.
39. Chokshi, T. V., Bazopoulou, D., Chronis, N., An automated microfluidic platform for calcium imaging of chemosensory neurons in Caenorhabditis elegans. Lab Chip 2010, 10, 2758-2763.
40. Cáceres, I. d. C., Valmas, N., Hilliard, M. A., Lu, H., Laterally orienting C. elegans using geometry at microscale for high-throughput visual screens in neurodegeneration and neuronal development studies. PLoS ONE 2012, 7, e35037.
41. Crane, M. M., Chung, K., Lu, H., Computer-enhanced high-throughput genetic screens of C. elegans in a microfluidic system. Lab Chip 2009, 9, 38-40.
42. Crane, M. M., Stirman, J. N., Ou, C.-Y., Kurshan, P. T. et al., Autonomous screening of C. elegans identifies genes implicated in synaptogenesis. Nat. Methods 2012, 9, 977-980.
43. Deisseroth, K., Optogenetics. Nat. Methods 2011, 8, 26-29.
44. Nagel, G., Szellas, T., Huhn, W., Kateriya, S. et al., Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 2003, 100, 13940-13945.
45. Kolbe, M., Besir, H., Essen, L. O., Oesterhelt, D., Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution. Science 2000, 288, 1390-1396.
46. Zhang, F., Wang, L.-P., Brauner, M., Liewald, J. F. et al., Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446, 633-639.
47. Guo, Z. V., Hart, A. C., Ramanathan, S., Optical interrogation of neural circuits in Caenorhabditis elegans. Nat. Methods 2009, 6, 891-896.
48. Stirman, J. N., Crane, M. M., Husson, S. J., Wabnig, S. et al., Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat. Methods 2011, 8, 153-158.
49. Wyart, C., Bene, F. D., Warp, E., Scott, E. K. et al., Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 2009, 461, 407-410.
50. Schoonheim, P. J., Arrenberg, A. B., Bene, F. D., Baier, H., Optogenetic localization and genetic perturbation of saccade-generating neurons in zebrafish. J. Neurosci. 2010, 30, 7111-7120.
51. Leifer, A. M., Fang-Yen, C., Gershow, M., Alkema, M. J. et al., Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat. Methods 2011, 8, 147-152.
52. Stirman, J. N., Brauner, M., Gottschalk, A., Lu, H., High-throughput study of synaptic transmission at the neuromuscular junction enabled by optogenetics and microfluidics. J. Neurosci. Methods 2010, 191, 90-93.
53. Lockery, S. R., Lawton, K. J., Doll, J. C., Faumont, S. et al., Artificial dirt: microfluidic substrates for nematode neurobiology and behavior. J. Neurophysiol. 2008, 99, 3136-3143.
54. Park, S., Hwang, H., Nam, S.-W., Martinez, F. et al., Enhanced Caenorhabditis elegans locomotion in a structured microfluidic environment. PLoS ONE 2008, 3, e2550.
55. Lee, H., Choi, M.-K., Lee, D., Kim, H.-S. et al., Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat. Neurosci. 2012, 15, 107-112.
56. Kim, N., Dempsey, C. M., Zoval, J. V., Sze, J.-Y. et al., Automated microfluidic compact disc (CD) cultivation system of Caenorhabditis elegans. Sens. Actuators B 2007, 122, 511-518.
57. Kim, N., Dempsey, C. M., Kuan, C.-J., Zovel, J. V. et al., Gravity force transduced by the MEC-4/MEC-10 DEG/ENaC channel modulates DAF-16/FoxO activity in Caenorhabditis elegans. Genetics 2007, 177, 835-845.
58. Rezai, P., Siddiqui, A., Selvaganapathy, P. R., Gupta, B. P., Electrotaxis of Caenorhabditis elegans in a microfluidic environment. Lab Chip 2010, 10, 220-226.
59. Manière, X., Lebois, F., Matic, I., Ladoux, B. et al., Running Worms: C. elegans self-sorting by electrotaxis. PLoS ONE 2011, 6, e16637.
60. Rubin, G. M., Lewis, E. B., A brief history of Drosophila's contributions to genome research. Science 2000, 24, 2216-2218.
61. Nüsslein-Volhard, C., Wieschaus, E., Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287, 795-801.
62. Driever, W., Nüsslein-Volhard, C., The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 1988, 54, 95-104.
63. Frohnhöfer, H. G., Nüsslein-Volhard, C., Maternal genes required for the anterior localization of bicoid activity in the embryo of Drosophila. Genes Dev. 1987, 1, 880-890.
64. Lucchetta, E. M., Lee, J. H., Fu, L. A., Patel, N. H. et al., Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics. Nature 2005, 434, 1134-1138.
65. Kenis, P. J. A., Ismagilov, R. F., Whitesides, G. M., Microfabrication inside capillaries using multiphase laminar flow patterning. Science 1999, 285, 83-85.
66. Takayama, S., Ostuni, E., LeDuc, P., Naruse, K. et al., Subcellular positioning of small molecules. Nature 2001, 411, 1016.
67. Lucchetta, E. M., Munson, M. S., Ismagilov, R. F., Characterization of the local temperature in space and time around developing Drosophila embryo in a microfluidic device. Lab Chip 2006, 6, 185-190.
68. Dagani, G. T., Monzo, K., Fakhoury, J. R., Chen, C.-C. et al., Microfluidic self-assembly of live Drosophila embryos for versatile high-throughput analysis of embryonic morphogenesis. Biomed. Microdevices 2007, 9, 681-694.
69. Bernstein, R. W., Zhang, X., Zapp, S., Fish, M. et al., Characterization of fluidic microassembly for immobilization and positioning of Drosophila embryos in 2-D arrays. Sens. Actuators A 2004, 114, 191-196.
70. Chun, K., Hashiguchi, G., Toshiyoshi, H., Fujita, H., Fabrication of array of hollow microcapillaries used for injection of genetic materials into animal/plant cells. Jpn. J. Appl. Phys. 1999, 38, L279-L281.
71. Zhang, X., Scott, M. P., Quate, C. F., Solgaard, O., Microoptical characterization of piezoelectric vibratory microinjections in Drosophila embryos for genome-wide RNAi screen. J. Microelectromech. Syst. 2006, 15, 1-11.
72. Chung, K., Kim, Y., Kanodia, J. S., Gong, E. et al., A microfluidic array for large-scale ordering and orientation of embryos. Nat. Methods 2011, 8, 171-176.
73. Dahm, R., Geisler, R., Learning from small fry: The zebrafish as a genetic model organism for aquaculture fish species. Mar. Biotechnol. 2006, 8, 329-345.
74. Kinkel, M. D., Prince, V. E., On the diabetic menu: Zebrafish as a model for pancreas development and function. Bioessays 2009, 31, 139-152.
75. Bretaud, S., Allen, C., Ingham, P. W., Bandmann, O., p53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson's disease. J. Neurochem. 2007, 100, 1626-1636.
76. Ramesh, T., Lyon, A. N., Pineda, R. H., Wang, C. et al., A genetic model of amyotrophic lateral sclerosis in zebrafish displays phenotypic hallmarks of motoneuron disease. Dis. Model. Mech. 2010, 3, 652-662.
77. Lieschke, G. J., Currie, P. D., Animal models of human disease: Zebrafish swim into view. Nat. Rev. Genet. 2007, 8, 353-367.
78. Penberthy, W. T., Shafizadeh, E., Lin, S., The zebrafish as a model for human disease. Front. Biosci. 2002, 7, 1439-1453.
79. Tamplin, O. J., White, R. M., Jing, L., Kaufman, C. K. et al., Small molecule screening in zebrafish: Swimming in potential drug therapies. WIREs Dev. Biol. 2012, 1, 459-468.
80. Funfak, A., Brösing, A., Brand, M., Köhler, J. M., Micro fluid segment technique for screening and development studies on Danio rerio embryos. Lab Chip 2007, 7, 1132-1138.
81. Yang, F., Chen, Z., Pan, J., Li, X. et al., An integrated microfluidic array system for evaluating toxicity and teratogenicity of drugs on embryonic zebrafish developmental dynamics. Biomicrofluidics 2011, 5, 024115.
82. Liu, D., Wang, L., Zhong, R., Li, B. et al., Parallel microfluidic networks for studying cellular response to chemical modulation. J. Biotechnol. 2007, 131, 286-292.
83. Jeon, N. L., Dertinger, S. K. W., Chiu, D. T., Choi, I. S. et al., Generation of solution and surface gradients using microfluidic systems. Langmuir 2000, 16, 8311-8316.
84. Choudhury, D., Noort, D. v., Iliescu, C., Poon, B. Z. K.-L. et al., Fish and Chips: a microfluidic perfusion platform for monitoring zebrafish development. Lab Chip 2012, 12, 892-900.
85. Shen, Y.-c., Li, D., Al-Shoaibi, A., Bersano-Begey, T. et al., Zebrafish in education: A student team in a University of Michigan biomedical engineering design course constructs a microfluidic bioreactor for studies of zebrafish development. Zebrafish 2009, 6, 201-213.
86. Wielhouwer, E. M., Ali, S., Al-Afandi, A., Blom, M. T. et al., Zebrafish embryo development in a microfluidic flow-through system. Lab Chip 2011, 11, 1815-1824.
87. Lammer, E., Kamp, H. G., Hisgen, V., Koch, M. et al., Development of a flow-through system for the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Toxicol. in vitro 2009, 23, 1436-1442.
88. Akagi, J., Khoshmanesh, K., Evans, B., Hall, C. J. et al., Miniaturized embryo array for automated trapping, immobilization and microperfusion of zebrafish embryos. PLoS ONE 2012, 7, e36630.
89. Huang, K.-S., Lin, Y.-C., Su, K.-C., Chen, H.-Y., An electroporation microchip system for the transfection of zebrafish embryos using quantum dots and GFP genes for evaluation. Biomed. Microdevices 2007, 9, 761-768.
90. Son, S. U., Garrell, R. L., Transport of live yeast and zebrafish embryo on a droplet ("digital") microfluidic platform. Lab Chip 2009, 9, 2398-2401.
91. Noori, A., Selvaganapathy, P. R., Wilson, J., Microinjection in a microfluidic format using flexible and compliant channels and electroosmotic dosage control. Lab Chip 2009, 9, 3202-3211.
92. Ghazali, I. E., Saqrane, S., Carvalho, A. P., Ouahid, Y. et al., Compensatory growth induced in zebrafish larvae after pre-exposure to a Microcystis aeruginosa natural bloom extract containing microcystins. Int. J. Mol. Sci. 2009, 10, 133-146.
93. Pardo-Martin, C., Chang, T.-Y., Koo, B. K., Gilleland, C. L. et al., High-throughput in vivo vertebrate screening. Nat. Methods 2010, 7, 634-636.
94. Chang, T.-Y., Pardo-Martin, C., Allalou, A., Wählby, C. et al., Fully automated cellular-resolution vertebrate screening platform with parallel animal processing. Lab Chip 2012, 12, 711-716.
95. Huisken, J., Swoger, J., Bene, F. D., Wittbrodt, J. et al., Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 2004, 305, 1007-1009.
96. Keller, P. J., Schmidt, A. D., Wittbrodt, J., Stelzer, E. H. K., Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 2008, 322, 1065-1069.
97. Keller, P. J., Schmidt, A. D., Santella, A., Khairy, K. et al., Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nat. Methods 2010, 7, 637-642.
98. O'Brien, G. S., Rieger, S., Martin, S. M., Cavanaugh, A. M. et al., Two-photon axotomy and time-lapse confocal imaging in live zebrafish embryos. J. Vis. Exp. 2009, 24, e1129.
99. Li, J., Mack, J. A., Souren, M., Yaksi, E. et al., Early development of functional spatial maps in the zebrafish olfactory bulb. J. Neurocsci. 2005, 25, 5784-5795.
100. Mohler, W. A., Visual reality: Using computer reconstruction and animation to magnify the microscopist's perception. Mol. Biol. Cell. 1999, 10, 3061-3065.
101. Zhao, T., Xie, J., Amat, F., Clack, N. et al., Automated reconstruction of neuronal morphology based on local geometrical and global structural models. Neuroinform. 2011, 9, 247-261.
102. Long, F., Peng, H., Liu, X., Kim, S. K. et al., A 3D digital atlas of C. elegans and its application to single-cell analyses. Nat. Methods 2009, 6, 667-672.
103. Bao, Z., Murray, J. I., Boyle, T., Ooi, S. L. et al., Automated cell lineage tracing in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2006, 103, 2707-2712.
104. Murray, J. I., Bao, Z., Boyle, T. J., Boeck, M. E. et al., Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nat. Methods 2008, 5, 703-709.
105. Nahabedian, J. F., Qadota, H., Stirman, J. N., Lu, H. et al., Bending amplitude - A new quantitative assay of C. elegans locomotion: Identification of phenotypes for mutants in genes encoding muscle focal adhesion components. Methods 2012, 56, 95-102.
106. Swierczek, N. A., Giles, A. C., Rankin, C. H., Kerr, R. A., High-throughput behavioral analysis in C. elegans. Nat. Methods 2011, 8, 592-598.
107. Mo, W., Chen, F., Nechiporuk, A., Nicolson, T., Quantification of vestibular-induced eye movements in zebrafish larvae. BMC Neurosci. 2010, 11, 110.