ChIP and Chips: Introducing the WormPharm for correlative studies employing pharmacology and genome-wide analyses in C. elegans
Main Article Content
Keywords
WormPharm, Wormchip, ChIp-seq, CeHR, NGM, OP50
Abstract
We present the WormPharm, an automated microfluidic platform that utilizes an axenic medium to culture C. elegans. The WormPharm is capable of sustaining C elegans for extended periods, while recording worm development and growth with high temporal resolution ranging from seconds to minutes over several days to months. We demonstrate the utility of the device to monitor C. elegans growth in the presence of varying doses of nicotine and alcohol. Furthermore, we show that C. elegans cultured in the WormPharm are amendable for high-throughput genomic assays, i.e. chromatin-immunoprecipitation followed by next generation sequencing, and confirm that nematodes grown in monoxenic and axenic cultures exhibit genetic modifications that correlate with observed phenotypes. The WormPharm is a powerful tool for analyzing the effects of chemical, nutritional and environmental variations on organism level responses in conjunction with genome-wide changes in C. elegans.
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References
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2. Lewis JA, Fleming JT. Basic culture methods. Methods in cell biology 1995;48:3-29.
3. Adenle A, Johnsen B, Szewczyk N. Review of the results from the International C. elegans first experiment (ICE-FIRST). Advances in Space Research 2009;44(2):210-16.
4. Dougherty EC. Introduction to axenic culture of invertebrate metazoa: a goal*. Ann N Y Acad Sci 1959;77(2):27-54.
5. Nicholas WL. Axenic cultivation of Caenorhabditis briggsae (Nematoda: Rhabditidae) with unsupplemented and supplemented chemically defined media. Ann N Y Acad Sci 1959;77:176-217.
6. Sayre FW, Hansen EL, Yarwood EA. Biochemical aspects of the nutrition of Caenorhabditis briggsae. Exp Parasitol 1963;13(2):98-107.
7. Rothstein M, Cook E. Nematode biochemistry—VI. Conditions for axenic culture of Turbatrix aceti, Panagrellus redivivus, Rhabditis anomala and Caenorhabditis briggsae. Comparative biochemistry and physiology 1966;17(2):683-92.
8. Lu N, Goetsch K. Carbohydrate requirement of Caenorhabditis elegans and the final development of a chemically defined medium. Nematologica 1993;39(1):303-11.
9. Szewczyk N, Kozak E, Conley C. Chemically Defined Medium and Caenorhabditis elegans: A Powerful Approach. 2003.
10. Xian B, Shen J, Chen W, Sun N, Qiao N, Jiang D, et al. WormFarm: a quantitative control and measurement device toward automated Caenorhabditis elegans aging analysis. Aging cell 2013;12(3):398-409.
11. Szewczyk NJ, Udranszky IA, Kozak E, Sunga J, Kim SK, Jacobson LA, et al. Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J Exp Biol 2006;209(20):4129-39.
12. Selch F, Higashibata A, Imamizo-Sato M, Higashitani A, Ishioka N, Szewczyk NJ, et al. Genomic response of the nematode Caenorhabditis elegans to spaceflight. Advances in Space Research 2008;41(5):807-15.
13. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, et al. Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in Caenorhabditis elegans. Experimental gerontology 2002;37(12):1371-78.
14. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, et al. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Experimental gerontology 2002;37(12):1359-69.
15. Hansen E, Buecher E, Yarwood E. Development and maturation of Caenorhabditis briggsae in response to growth factor. Nematologica 1964;10(4):623-30.
16. Croll NA, Smith JM, Zuckerman BM. The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Experimental aging research 1977;3(3):175-89.
17. Gems D, Riddle DL. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 2000;154(4):1597-610.
18. Hulme SE, Shevkoplyas SS, McGuigan AP, Apfeld J, Fontana W, Whitesides GM. Lifespan-on-a-chip: microfluidic chambers for performing lifelong observation of C. elegans. Lab on a Chip 2010;10(5):589-97.
19. Chokshi TV, Ben-Yakar A, Chronis N. CO 2 and compressive immobilization of C. elegans on-chip. Lab on a Chip 2009;9(1):151-57.
20. Chronis N, Zimmer M, Bargmann CI. Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 2007;4(9):727-31.
21. Chung K, Crane MM, Lu H. Automated on-chip rapid microscopy, phenotyping and sorting of C. elegans. Nat Methods 2008;5(7):637-43.
22. Cui X, Lee LM, Heng X, Zhong W, Sternberg PW, Psaltis D, et al. Lensless high-resolution on-chip optofluidic microscopes for Caenorhabditis elegans and cell imaging. Proceedings of the National Academy of Sciences 2008;105(31):10670-75.
23. Hulme SE, Shevkoplyas SS, Apfeld J, Fontana W, Whitesides GM. A microfabricated array of clamps for immobilizing and imaging C. elegans. Lab on a Chip 2007;7(11):1515-23.
24. Lange D, Storment CW, Conley CA, Kovacs GT. A microfluidic shadow imaging system for the study of the nematode Caenorhabditis elegans in space. Sensors Actuators B: Chem 2005;107(2):904-14.
25. Park S, Hwang H, Nam S-W, Martinez F, Austin RH, Ryu WS. Enhanced Caenorhabditis elegans locomotion in a structured microfluidic environment. PLoS One 2008;3(6):e2550.
26. Shi W, Qin J, Ye N, Lin B. Droplet-based microfluidic system for individual Caenorhabditis elegans assay. Lab on a Chip 2008;8(9):1432-35.
27. Wen H, Yu Y, Zhu G, Jiang L, Qin J. A droplet microchip with substance exchange capability for the developmental study of C. elegans. Lab on a Chip 2015;15(8):1905-11.
28. Gilleland CL, Rohde CB, Zeng F, Yanik MF. Microfluidic immobilization of physiologically active Caenorhabditis elegans. Nature protocols 2010;5(12):1888-902.
29. Yang J, Chen Z, Ching P, Shi Q, Li X. An integrated microfluidic platform for evaluating in vivo antimicrobial activity of natural compounds using a whole-animal infection model. Lab on a Chip 2013;13(17):3373-82.
30. Salam S, Ansari A, Amon S, Rezai P, Selvaganapathy PR, Mishra RK, et al. A microfluidic phenotype analysis system reveals function of sensory and dopaminergic neuron signaling in C. elegans electrotactic swimming behavior. 2013. Taylor & Francis. p e24558.
31. Solomon MJ, Larsen PL, Varshavsky A. Mapping proteinDNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene. Cell 1988;53(6):937-47.
32. Daxinger L, Whitelaw E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res 2010;20(12):1623-28.
33. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33:245-54.
34. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics international 2004;11(7):36-42.
35. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 2009;41(3):376-81.
36. Andrews S. FastQC: A quality control tool for high throughput sequence data. Reference Source 2010.
37. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25(14):1754-60.
38. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010;26(5):589-95.
39. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome biology 2008;9(9):R137.
40. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol 2011;29(1):24-26.
41. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010;38(4):576-89.
42. Stark R, Brown G. DiffBind: differential binding analysis of ChIP-Seq peak data. R package version 2011;100.
43. Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, Chen WJ, et al. WormBase 2012: more genomes, more data, new website. Nucleic Acids Res 2011:gkr954.
44. Rao AU, Carta LK, Lesuisse E, Hamza I. Lack of heme synthesis in a free-living eukaryote. Proceedings of the National Academy of Sciences of the United States of America 2005;102(12):4270-75.
45. Hunt PR, Olejnik N, Sprando RL. Toxicity ranking of heavy metals with screening method using adult Caenorhabditis elegans and propidium iodide replicates toxicity ranking in rat. Food Chem Toxicol 2012;50(9):3280-90.
46. Greer EL, Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging cell 2009;8(2):113-27.
47. Riddle DL, Blumenthal T, Meyer B, Priess J. C. elegans II. 1997. Cold Spring Harbor Laboratory Press, New York, USA.[PubMed].
48. Barker DM. Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav 1994;48(1):147-56.
49. Abdul Kader N, Côté M. Isolement, identification et caractérisation de souches québécoises du nématode Caenorhabditis elegans. Fundam Appl Nematol 1996;19(4):381-89.
50. Davis JR, Li Y, Rankin CH. Effects of developmental exposure to ethanol on Caenorhabditis elegans. Alcoholism: Clinical and Experimental Research 2008;32(5):853-67.
51. Sobkowiak R, Kowalski M, Lesicki A. Concentration-and time-dependent behavioral changes in Caenorhabditis elegans after exposure to nicotine. Pharmacol Biochem Behav 2011;99(3):365-70.
52. Davies AG, Pierce-Shimomura JT, Kim H, VanHoven MK, Thiele TR, Bonci A, et al. A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 2003;115(6):655-66.
53. Polli JR, Dobbins DL, Kobet RA, Farwell MA, Zhang B, Lee M-H, et al. Drug-dependent behaviors and nicotinic acetylcholine receptor expressions in Caenorhabditis elegans following chronic nicotine exposure. Neurotoxicology 2015;47:27-36.
54. Kanteti R, Dhanasingh I, El-Hashani E, Riehm JJ, Stricker T, Nagy S, et al. C. elegans and mutants with chronic nicotine exposure as a novel model of cancer phenotype. Cancer biology & therapy 2015(just-accepted):00-00.
55. Taki FA, Pan X, Zhang B. Chronic Nicotine Exposure Systemically Alters MicroRNA Expression Profiles During Post‐Embryonic Stages in Caenorhabditis elegans. Journal of cellular physiology 2014;229(1):79-89.
56. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011;471(7339):480-85.
57. Li JJ, Huang H, Bickel PJ, Brenner SE. Comparison of D. melanogaster and C. elegans developmental stages, tissues, and cells by modENCODE RNA-seq data. Genome Res 2014;24(7):1086-101.
58. Waterston R. Genome sequence of the nematode C. elegans: a platform for investigating biology. The C. elegans Sequencing Consortium. Science 1998;282(5396):2012-18.
59. Pierce-Shimomura JT, Chen BL, Mun JJ, Ho R, Sarkis R, McIntire SL. Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proceedings of the National Academy of Sciences 2008;105(52):20982-87.
60. Tain LS, Lozano E, Sáez AG, Leroi AM. Dietary regulation of hypodermal polyploidization in C. elegans. BMC Dev Biol 2008;8(1):1.
61. Heestand BN, Shen Y, Liu W, Magner DB, Storm N, Meharg C, et al. Dietary restriction induced longevity is mediated by nuclear receptor NHR-62 in Caenorhabditis elegans. PLoS Genet 2013;9(7):e1003651.
62. Cypser JR, Kitzenberg D, Park S-K. Dietary restriction in C. elegans: recent advances. Experimental gerontology 2013;48(10):1014-17.
63. Castelein N, Cai H, Rasulova M, Braeckman B. Lifespan regulation under axenic dietary restriction: a close look at the usual suspects. Experimental gerontology 2014;58:96-103.
64. Sterken MG, Snoek LB, Kammenga JE, Andersen EC. The laboratory domestication of Caenorhabditis elegans. Trends Genet 2015;31(5):224-31.
65. McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 2011;477(7364):321-25.
66. Wolff S, Dillin A. The trifecta of aging in Caenorhabditis elegans. Experimental gerontology 2006;41(10):894-903.
67. Sonnhammer EL, Durbin R. Analysis of Protein Domain Families inCaenorhabditis elegans. Genomics 1997;46(2):200-16.
68. Kuwabara P, O'Neil N. The use of functional genomics in C. elegans for studying human development and disease. J Inherited Metab Dis 2001;24(2):127-38.
69. Jamal R, Nurul-Faizah J, Then S, Szewczyk N, Stodieck L, Harun R. Gene expression changes in space flown Caenorhabditis elegans exposed to a long period of microgravity. Gravitational and Space Research 2011;23(2).
70. Oczypok EA, Etheridge T, Freeman J, Stodieck L, Johnsen R, Baillie D, et al. Remote automated multi-generational growth and observation of an animal in low Earth orbit. Journal of The Royal Society Interface 2012;9(68):596-99.
2. Lewis JA, Fleming JT. Basic culture methods. Methods in cell biology 1995;48:3-29.
3. Adenle A, Johnsen B, Szewczyk N. Review of the results from the International C. elegans first experiment (ICE-FIRST). Advances in Space Research 2009;44(2):210-16.
4. Dougherty EC. Introduction to axenic culture of invertebrate metazoa: a goal*. Ann N Y Acad Sci 1959;77(2):27-54.
5. Nicholas WL. Axenic cultivation of Caenorhabditis briggsae (Nematoda: Rhabditidae) with unsupplemented and supplemented chemically defined media. Ann N Y Acad Sci 1959;77:176-217.
6. Sayre FW, Hansen EL, Yarwood EA. Biochemical aspects of the nutrition of Caenorhabditis briggsae. Exp Parasitol 1963;13(2):98-107.
7. Rothstein M, Cook E. Nematode biochemistry—VI. Conditions for axenic culture of Turbatrix aceti, Panagrellus redivivus, Rhabditis anomala and Caenorhabditis briggsae. Comparative biochemistry and physiology 1966;17(2):683-92.
8. Lu N, Goetsch K. Carbohydrate requirement of Caenorhabditis elegans and the final development of a chemically defined medium. Nematologica 1993;39(1):303-11.
9. Szewczyk N, Kozak E, Conley C. Chemically Defined Medium and Caenorhabditis elegans: A Powerful Approach. 2003.
10. Xian B, Shen J, Chen W, Sun N, Qiao N, Jiang D, et al. WormFarm: a quantitative control and measurement device toward automated Caenorhabditis elegans aging analysis. Aging cell 2013;12(3):398-409.
11. Szewczyk NJ, Udranszky IA, Kozak E, Sunga J, Kim SK, Jacobson LA, et al. Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J Exp Biol 2006;209(20):4129-39.
12. Selch F, Higashibata A, Imamizo-Sato M, Higashitani A, Ishioka N, Szewczyk NJ, et al. Genomic response of the nematode Caenorhabditis elegans to spaceflight. Advances in Space Research 2008;41(5):807-15.
13. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, et al. Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in Caenorhabditis elegans. Experimental gerontology 2002;37(12):1371-78.
14. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, et al. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Experimental gerontology 2002;37(12):1359-69.
15. Hansen E, Buecher E, Yarwood E. Development and maturation of Caenorhabditis briggsae in response to growth factor. Nematologica 1964;10(4):623-30.
16. Croll NA, Smith JM, Zuckerman BM. The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Experimental aging research 1977;3(3):175-89.
17. Gems D, Riddle DL. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 2000;154(4):1597-610.
18. Hulme SE, Shevkoplyas SS, McGuigan AP, Apfeld J, Fontana W, Whitesides GM. Lifespan-on-a-chip: microfluidic chambers for performing lifelong observation of C. elegans. Lab on a Chip 2010;10(5):589-97.
19. Chokshi TV, Ben-Yakar A, Chronis N. CO 2 and compressive immobilization of C. elegans on-chip. Lab on a Chip 2009;9(1):151-57.
20. Chronis N, Zimmer M, Bargmann CI. Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 2007;4(9):727-31.
21. Chung K, Crane MM, Lu H. Automated on-chip rapid microscopy, phenotyping and sorting of C. elegans. Nat Methods 2008;5(7):637-43.
22. Cui X, Lee LM, Heng X, Zhong W, Sternberg PW, Psaltis D, et al. Lensless high-resolution on-chip optofluidic microscopes for Caenorhabditis elegans and cell imaging. Proceedings of the National Academy of Sciences 2008;105(31):10670-75.
23. Hulme SE, Shevkoplyas SS, Apfeld J, Fontana W, Whitesides GM. A microfabricated array of clamps for immobilizing and imaging C. elegans. Lab on a Chip 2007;7(11):1515-23.
24. Lange D, Storment CW, Conley CA, Kovacs GT. A microfluidic shadow imaging system for the study of the nematode Caenorhabditis elegans in space. Sensors Actuators B: Chem 2005;107(2):904-14.
25. Park S, Hwang H, Nam S-W, Martinez F, Austin RH, Ryu WS. Enhanced Caenorhabditis elegans locomotion in a structured microfluidic environment. PLoS One 2008;3(6):e2550.
26. Shi W, Qin J, Ye N, Lin B. Droplet-based microfluidic system for individual Caenorhabditis elegans assay. Lab on a Chip 2008;8(9):1432-35.
27. Wen H, Yu Y, Zhu G, Jiang L, Qin J. A droplet microchip with substance exchange capability for the developmental study of C. elegans. Lab on a Chip 2015;15(8):1905-11.
28. Gilleland CL, Rohde CB, Zeng F, Yanik MF. Microfluidic immobilization of physiologically active Caenorhabditis elegans. Nature protocols 2010;5(12):1888-902.
29. Yang J, Chen Z, Ching P, Shi Q, Li X. An integrated microfluidic platform for evaluating in vivo antimicrobial activity of natural compounds using a whole-animal infection model. Lab on a Chip 2013;13(17):3373-82.
30. Salam S, Ansari A, Amon S, Rezai P, Selvaganapathy PR, Mishra RK, et al. A microfluidic phenotype analysis system reveals function of sensory and dopaminergic neuron signaling in C. elegans electrotactic swimming behavior. 2013. Taylor & Francis. p e24558.
31. Solomon MJ, Larsen PL, Varshavsky A. Mapping proteinDNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene. Cell 1988;53(6):937-47.
32. Daxinger L, Whitelaw E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res 2010;20(12):1623-28.
33. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33:245-54.
34. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics international 2004;11(7):36-42.
35. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 2009;41(3):376-81.
36. Andrews S. FastQC: A quality control tool for high throughput sequence data. Reference Source 2010.
37. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25(14):1754-60.
38. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010;26(5):589-95.
39. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome biology 2008;9(9):R137.
40. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol 2011;29(1):24-26.
41. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010;38(4):576-89.
42. Stark R, Brown G. DiffBind: differential binding analysis of ChIP-Seq peak data. R package version 2011;100.
43. Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, Chen WJ, et al. WormBase 2012: more genomes, more data, new website. Nucleic Acids Res 2011:gkr954.
44. Rao AU, Carta LK, Lesuisse E, Hamza I. Lack of heme synthesis in a free-living eukaryote. Proceedings of the National Academy of Sciences of the United States of America 2005;102(12):4270-75.
45. Hunt PR, Olejnik N, Sprando RL. Toxicity ranking of heavy metals with screening method using adult Caenorhabditis elegans and propidium iodide replicates toxicity ranking in rat. Food Chem Toxicol 2012;50(9):3280-90.
46. Greer EL, Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging cell 2009;8(2):113-27.
47. Riddle DL, Blumenthal T, Meyer B, Priess J. C. elegans II. 1997. Cold Spring Harbor Laboratory Press, New York, USA.[PubMed].
48. Barker DM. Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav 1994;48(1):147-56.
49. Abdul Kader N, Côté M. Isolement, identification et caractérisation de souches québécoises du nématode Caenorhabditis elegans. Fundam Appl Nematol 1996;19(4):381-89.
50. Davis JR, Li Y, Rankin CH. Effects of developmental exposure to ethanol on Caenorhabditis elegans. Alcoholism: Clinical and Experimental Research 2008;32(5):853-67.
51. Sobkowiak R, Kowalski M, Lesicki A. Concentration-and time-dependent behavioral changes in Caenorhabditis elegans after exposure to nicotine. Pharmacol Biochem Behav 2011;99(3):365-70.
52. Davies AG, Pierce-Shimomura JT, Kim H, VanHoven MK, Thiele TR, Bonci A, et al. A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 2003;115(6):655-66.
53. Polli JR, Dobbins DL, Kobet RA, Farwell MA, Zhang B, Lee M-H, et al. Drug-dependent behaviors and nicotinic acetylcholine receptor expressions in Caenorhabditis elegans following chronic nicotine exposure. Neurotoxicology 2015;47:27-36.
54. Kanteti R, Dhanasingh I, El-Hashani E, Riehm JJ, Stricker T, Nagy S, et al. C. elegans and mutants with chronic nicotine exposure as a novel model of cancer phenotype. Cancer biology & therapy 2015(just-accepted):00-00.
55. Taki FA, Pan X, Zhang B. Chronic Nicotine Exposure Systemically Alters MicroRNA Expression Profiles During Post‐Embryonic Stages in Caenorhabditis elegans. Journal of cellular physiology 2014;229(1):79-89.
56. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011;471(7339):480-85.
57. Li JJ, Huang H, Bickel PJ, Brenner SE. Comparison of D. melanogaster and C. elegans developmental stages, tissues, and cells by modENCODE RNA-seq data. Genome Res 2014;24(7):1086-101.
58. Waterston R. Genome sequence of the nematode C. elegans: a platform for investigating biology. The C. elegans Sequencing Consortium. Science 1998;282(5396):2012-18.
59. Pierce-Shimomura JT, Chen BL, Mun JJ, Ho R, Sarkis R, McIntire SL. Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proceedings of the National Academy of Sciences 2008;105(52):20982-87.
60. Tain LS, Lozano E, Sáez AG, Leroi AM. Dietary regulation of hypodermal polyploidization in C. elegans. BMC Dev Biol 2008;8(1):1.
61. Heestand BN, Shen Y, Liu W, Magner DB, Storm N, Meharg C, et al. Dietary restriction induced longevity is mediated by nuclear receptor NHR-62 in Caenorhabditis elegans. PLoS Genet 2013;9(7):e1003651.
62. Cypser JR, Kitzenberg D, Park S-K. Dietary restriction in C. elegans: recent advances. Experimental gerontology 2013;48(10):1014-17.
63. Castelein N, Cai H, Rasulova M, Braeckman B. Lifespan regulation under axenic dietary restriction: a close look at the usual suspects. Experimental gerontology 2014;58:96-103.
64. Sterken MG, Snoek LB, Kammenga JE, Andersen EC. The laboratory domestication of Caenorhabditis elegans. Trends Genet 2015;31(5):224-31.
65. McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 2011;477(7364):321-25.
66. Wolff S, Dillin A. The trifecta of aging in Caenorhabditis elegans. Experimental gerontology 2006;41(10):894-903.
67. Sonnhammer EL, Durbin R. Analysis of Protein Domain Families inCaenorhabditis elegans. Genomics 1997;46(2):200-16.
68. Kuwabara P, O'Neil N. The use of functional genomics in C. elegans for studying human development and disease. J Inherited Metab Dis 2001;24(2):127-38.
69. Jamal R, Nurul-Faizah J, Then S, Szewczyk N, Stodieck L, Harun R. Gene expression changes in space flown Caenorhabditis elegans exposed to a long period of microgravity. Gravitational and Space Research 2011;23(2).
70. Oczypok EA, Etheridge T, Freeman J, Stodieck L, Johnsen R, Baillie D, et al. Remote automated multi-generational growth and observation of an animal in low Earth orbit. Journal of The Royal Society Interface 2012;9(68):596-99.
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Doh JH, Moore AB, Celen I, Moore MT, Sabanayagam CR. ChIP and Chips: Introducing the WormPharm for correlative studies employing pharmacology and genome-wide analyses in C. elegans. J Biol Methods [Internet]. 2016 Jun. 10 [cited 2024 Apr. 20];3(2):e44. Available from: https://jbmethods.org/index.php/jbm/article/view/109
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