The Effects of Ivermectin on Brugia malayi Females In Vitro: A Transcriptomic Approach

PLoS Neglected Tropical Diseases

Volumn 10, Issue 8, 2016, Pages

  Ballesteros, Cristina ^a   Tritten, Lucienne ^a,d   O’Neill, Maeghan ^a   Burkman, Erica ^b,c   Zaky, Weam I ^c   Xia, Jianguo ^a   Moorhead, Andrew ^b,c   Williams, Steven A ^c   Geary, Timothy G ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF GEORGIA   (United States)

^c SMITH COLLEGE   (United States)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

IVERMECTIN; ANTIFILARIAL AGENT; HELMINTH RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROTOZOAL ACTIVITY; ARTICLE; BIOINFORMATICS; BRUGIA MALAYI; BRUGIAN FILARIASIS; CONTROLLED STUDY; DNA LIBRARY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE MAPPING; LYMPHATIC FILARIASIS; MALE; MERIONES UNGUICULATUS; MICROFILARIA (NEMATODE LARVA); NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; RNA SEQUENCE; RNAI THERAPEUTICS; SEQUENCE ALIGNMENT; TRANSCRIPTOMICS; UPREGULATION; WORM; ANIMAL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; METABOLISM;

ANIMALS; BRUGIA MALAYI; FEMALE; FILARICIDES; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IVERMECTIN; METABOLIC NETWORKS AND PATHWAYS; RNA, HELMINTH;

EID: 84988693259     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004929     Document Type: Article

References (71)

1. WHOGlobal programme to eliminate lymphatic filariasis: progress report, 2013. Relevé epidémiologique hebdomadaire / Section d'hygiène du Secretariat de la Société des Nations = Weekly epidemiological record / Health Section of the Secretariat of the League of Nations. 2014;89(38):409–18.
2. WHOAfrican Programme for Onchocerciasis Control: progress report, 2013–2014. Relevé epidémiologique hebdomadaire / Section d'hygiène du Secretariat de la Société des Nations = Weekly epidemiological record / Health Section of the Secretariat of the League of Nations. 2014;89(49):551–60.
3. Ottesen EA, The global programme to eliminate lymphatic filariasis. Tropical Medicine & International Health: TM & IH. 2000;5(9):591–4.
4. APOCFinal communiqué of the 11th session of the Joint Action Forum (JAF) of APOC. Ouagadougou (Burkina Faso): APOC., Paris, France, 6–9December2005.
5. Chabala JC, Mrozik H, Tolman RL, Eskola P, Lusi A, Peterson LH, et al. Ivermectin, a new broad-spectrum antiparasitic agent. Journal of Medicinal Chemistry. 1980;23(10):1134–6. 6893469
6. Prichard R, Menez C, Lespine A, Moxidectin and the avermectins: Consanguinity but not identity. International journal for Parasitology Drugs and Drug Resistance. 2012;2:134–53. doi: 10.1016/j.ijpddr.2012.04.00124533275
7. Ardelli BF, Stitt LE, Tompkins JB, Prichard RK, A comparison of the effects of ivermectin and moxidectin on the nematode Caenorhabditis elegans. Veterinary Parasitology. 2009;165(1–2):96–108. doi: 10.1016/j.vetpar.2009.06.04319631471
8. Takiguchi Y, Mishima H, Okuda M, Terao M, Aoki A, Fukuda R, Milbemycins, a new family of macrolide antibiotics: fermentation, isolation and physico-chemical properties. The Journal of Antibiotics. 1980;33(10):1120–7. 7451362
9. Campbell WC, Ivermectin as an antiparasitic agent for use in humans. Annual Review of Microbiology. 1991;45:445–74. 1741621
10. Wolstenholme AJ, Rogers AT, Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology. 2005;131Suppl:S85–95. 16569295
11. Brownlee DJ, Holden-Dye L, Walker RJ, Actions of the anthelmintic ivermectin on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology. 1997;115 (Pt 5):553–61. 9368907
12. Geary TG, Sims SM, Thomas EM, Vanover L, Davis JP, Winterrowd CA, et al. Haemonchus contortus: ivermectin-induced paralysis of the pharynx. Experimental Parasitology. 1993;77(1):88–96. 8344410
13. Moreno Y, Nabhan JF, Solomon J, Mackenzie CD, Geary TG, Ivermectin disrupts the function of the excretory-secretory apparatus in microfilariae of Brugia malayi. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(46):20120–5. doi: 10.1073/pnas.101198310721041637
14. Li BW, Rush AC, Weil GJ, High level expression of a glutamate-gated chloride channel gene in reproductive tissues of Brugia malayi may explain the sterilizing effect of ivermectin on filarial worms. International Journal for Parasitology Drugs and Drug Resistance. 2014;4(2):71–6. doi: 10.1016/j.ijpddr.2014.01.00225057456
15. Tompkins JB, Stitt LE, Ardelli BF, Brugia malayi: in vitro effects of ivermectin and moxidectin on adults and microfilariae. Experimental Parasitology. 2010;124(4):394–402. doi: 10.1016/j.exppara.2009.12.00320034492
16. Krishna DR, Klotz U, Determination of ivermectin in human plasma by high-performance liquid chromatography. Arzneimittel-Forschung. 1993;43(5):609–11. 8329009
17. Baraka OZ, Mahmoud BM, Marschke CK, Geary TG, Homeida MM, Williams JF, Ivermectin distribution in the plasma and tissues of patients infected with Onchocerca volvulus. European Journal of Clinical Pharmacology. 1996;50(5):407–10. 8839664
18. Gonzalez Canga A, Sahagun Prieto AM, Diez Liebana MJ, Fernandez Martinez N, Sierra Vega M, Garcia Vieitez JJ, The pharmacokinetics and interactions of ivermectin in humans—a mini-review. The AAPS Journal. 2008;10(1):42–6. doi: 10.1208/s12248-007-9000-918446504
19. Jia L, Liu X, The conduct of drug metabolism studies considered good practice (II): in vitro experiments. Current Drug Metabolism. 2007;8(8):822–9. 18220563
20. Ballesteros C, Tritten L, O'Neill M, Burkman E, Zaky WI, Xia J, et al. The effect of in vitro cultivation on the transcriptome of adult Brugia malayi. PLoS Neglected Tropical Diseases2016;10(1):e0004311. doi: 10.1371/journal.pntd.000431126727204
21. Taylor J, Schenck I, Blankenberg D, Nekrutenko A, Baxevanis Andreas D, Using Galaxy to perform large-scale interactive data analyses. Current Protocols in Bioinformatics / editoral board, et al]. 2007;Chapter 10:Unit 10.5.
22. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Ausubel Frederick M, et al. Galaxy: a web-based genome analysis tool for experimentalists. Current Protocols in Molecular Biology / edited by et al]. 2010;Chapter 19:Unit 19.0.1–21.
23. Anders S, Pyl PT, Huber W, HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics (Oxford, England). 2015;31(2):166–9.
24. Robinson MD, McCarthy DJ, Smyth GK, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England). 2010;26(1):139–40.
25. Xia J, Gill EE, Hancock RE, NetworkAnalyst for statistical, visual and network-based meta-analysis of gene expression data. Nature Protocols. 2015;10(6):823–44. doi: 10.1038/nprot.2015.05225950236
26. Xia J, Benner MJ, Hancock RE, NetworkAnalyst—integrative approaches for protein-protein interaction network analysis and visual exploration. Nucleic Acids Research. 2014;42(Web Server issue):W167–74. doi: 10.1093/nar/gku44324861621
27. Robinson MD, Oshlack A, A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology. 2010;11(3):R25. doi: 10.1186/gb-2010-11-3-r2520196867
28. Robinson MD, Smyth GK, Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics (Oxford, England). 2008;9(2):321–32.
29. Benjamini Y, Hochberg Y, Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57(1):289–300.
30. Harris TW, Lee R, Schwarz E, Bradnam K, Lawson D, Chen W, et al. WormBase: a cross-species database for comparative genomics. Nucleic Acids Research. 2003;31(1):133–7. 12519966
31. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics. 2000;25(1):25–9. 10802651
32. Martin J, Abubucker S, Wylie T, Yin Y, Wang Z, Mitreva M, Nematode.net update 2008: improvements enabling more efficient data mining and comparative nematode genomics. Nucleic Acids Research. 2009;37(Database issue):D571–8. doi: 10.1093/nar/gkn74418940860
33. Wylie T, Martin JC, Dante M, Mitreva MD, Clifton SW, Chinwalla A, et al. Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Research. 2004;32(Database issue):D423–6. 14681448
34. Zhang B, Kirov S, Snoddy J, WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Research. 2005;33(Web Server issue):W741–8. 15980575
35. Wall DP, Fraser HB, Hirsh AE, Detecting putative orthologs. Bioinformatics (Oxford, England). 2003;19(13):1710–1.
36. Hirsh AE, Fraser HB, Protein dispensability and rate of evolution. Nature. 2001;411(6841):1046–9. 11429604
37. Melnikow E, Xu S, Liu J, Bell AJ, Ghedin E, Unnasch TR, et al. A potential role for the interaction of Wolbachia surface proteins with the Brugia malayi glycolytic enzymes and cytoskeleton in maintenance of endosymbiosis. PLoS Negl Trop Dis. 2013;7(4):e2151. doi: 10.1371/journal.pntd.000215123593519
38. Vicente JJ, Wordeman L, Mitosis, microtubule dynamics and the evolution of kinesins. Experimental Cell Research. 2015;334(1):61–9. doi: 10.1016/j.yexcr.2015.02.01025708751
39. Ellefson ML, McNally FJ, Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans. Molecular Biology of the Cell. 2009;20(11):2722–30. doi: 10.1091/mbc.E08-12-125319357192
40. Yang HY, Mains PE, McNally FJ, Kinesin-1 mediates translocation of the meiotic spindle to the oocyte cortex through KCA-1, a novel cargo adapter. The Journal of Cell Biology. 2005;169(3):447–57. 15883196
41. Lin MY, Sheng ZH, Regulation of mitochondrial transport in neurons. Experimental Cell Research. 2015;334(1):35–44. doi: 10.1016/j.yexcr.2015.01.00425612908
42. O'Rourke SM, Dorfman MD, Carter JC, Bowerman B, Dynein modifiers in C. elegans: light chains suppress conditional heavy chain mutants. PLoS Genetics. 2007;3(8):e128. 17676955
43. Connolly AA, Osterberg V, Christensen S, Price M, Lu C, Chicas-Cruz K, et al. Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1. Molecular Biology of the Cell. 2014;25(8):1298–311. doi: 10.1091/mbc.E13-11-068724554763
44. Bellanger JM, Carter JC, Phillips JB, Canard C, Bowerman B, Gonczy P, ZYG-9, TAC-1 and ZYG-8 together ensure correct microtubule function throughout the cell cycle of C. elegans embryos. Journal of Cell Science. 2007;120(Pt 16):2963–73. 17666432
45. Bellanger JM, Gonczy P, TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Current Biology: CB. 2003;13(17):1488–98. 12956950
46. Srayko M, Quintin S, Schwager A, Hyman AA, Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Current Biology: CB. 2003;13(17):1506–11. 12956952
47. Morris CP, Bennuru S, Kropp LE, Zweben JA, Meng Z, Taylor RT, et al. A proteomic analysis of the body wall, digestive tract, and reproductive tract of Brugia malayi. PLoS Neglected Tropical Diseases2015;9(9):e0004054. doi: 10.1371/journal.pntd.000405426367142
48. Singaravelu G, Singson A, Calcium signaling surrounding fertilization in the nematode Caenorhabditis elegans. Cell Calcium. 2013;53(1):2–9. doi: 10.1016/j.ceca.2012.11.00923218668
49. Corrigan C, Subramanian R, Miller MA, Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation. Development (Cambridge, England). 2005;132(23):5225–37.
50. Kariya K, Bui YK, Gao X, Sternberg PW, Kataoka T, Phospholipase C-epsilon regulates ovulation in Caenorhabditis elegans. Developmental Biology. 2004;274(1):201–10. 15355798
51. Miller KG, Emerson MD, Rand JB, Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron. 1999;24(2):323–33. 10571227
52. Chen IW, Charalampous CF, Biochemical studies on inositol. IX. D-Inositol 1-phosphate as intermediate in the biosynthesis of inositol from glucose 6-phosphate, and characteristics of two reactions in this biosynthesis. The Journal of Biological Chemistry. 1966;241(10):2194–9. 4287852
53. Eng JK, Blackhall WJ, Osei-Atweneboana MY, Bourguinat C, Galazzo D, Beech RN, et al. Ivermectin selection on beta-tubulin: evidence in Onchocerca volvulus and Haemonchus contortus. Molecular and Biochemical Parasitology. 2006;150(2):229–35. 17007942
54. Duro E, Marston AL, From equator to pole: splitting chromosomes in mitosis and meiosis. Genes & Development. 2015;29(2):109–22.
55. Ashraf S, Beech RN, Hancock MA, Prichard RK, Ivermectin binds to Haemonchus contortus tubulins and promotes stability of microtubules. International Journal for Parasitology. 2015;45(9–10):647–54. doi: 10.1016/j.ijpara.2015.03.01025957159
56. Iwasaki K, McCarter J, Francis R, Schedl T, emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. The Journal of Cell Biology. 1996;134(3):699–714. 8707849
57. Lee KY, Yang I, Park JE, Baek OR, Chung KY, Koo HS, Developmental stage- and DNA damage-specific functions of C. elegans FANCD2. Biochemical and Biophysical Research Communications. 2007;352(2):479–85. 17126808
58. Burns LT, Wente SR, From hypothesis to mechanism: uncovering nuclear pore complex links to gene expression. Molecular and Cellular Biology. 2014;34(12):2114–20. doi: 10.1128/MCB.01730-1324615017
59. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, et al. Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature. 2005;434(7032):462–9. 15791247
60. Minasaki R, Puoti A, Streit A, The DEAD-box protein MEL-46 is required in the germ line of the nematode Caenorhabditis elegans. BMC Developmental Biology. 2009;9:35. doi: 10.1186/1471-213X-9-3519534797
61. Turner AJ, Isaac RE, Coates D, The neprilysin (NEP) family of zinc metalloendopeptidases: genomics and function. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology. 2001;23(3):261–9.
62. Spanier B, Sturzenbaum SR, Holden-Dye LM, Baumeister R, Caenorhabditis elegans neprilysin NEP-1: an effector of locomotion and pharyngeal pumping. Journal of Molecular Biology. 2005;352(2):429–37. 16081104
63. Castanha Zanoli JC, Maioli MA, Medeiros HC, Mingatto FE, Abamectin affects the bioenergetics of liver mitochondria: A potential mechanism of hepatotoxicity. Toxicology in vitro: an international journal published in association with BIBRA. 2012;26(1):51–6.
64. Shin H, Lee H, Fejes AP, Baillie DL, Koo HS, Jones SJ, Gene expression profiling of oxidative stress response of C. elegans aging defective AMPK mutants using massively parallel transcriptome sequencing. BMC Research Notes. 2011;4:34. doi: 10.1186/1756-0500-4-3421303547
65. Behm CA, Metabolism. In: The biology of nematodes. 1st ed.London: Francis and Taylor; 2002.
66. Ramp T, Bachmann R, Kohler P, Respiration and energy conservation in the filarial worm Litomosoides carinii. Molecular and Biochemical Parasitology. 1985;15(1):11–20. 3990708
67. Martin RJ, Robertson AP, Bjorn H, Target sites of anthelmintics. Parasitology. 1997;114Suppl:S111–24. 9309773
68. Yates DM, Wolstenholme AJ, An ivermectin-sensitive glutamate-gated chloride channel subunit from Dirofilaria immitis. International Journal for Parasitology. 2004;34(9):1075–81. 15313134
69. Wolstenholme AJ, Glutamate-gated chloride channels. The Journal of Biological Chemistry. 2012;287(48):40232–8. doi: 10.1074/jbc.R112.40628023038250
70. Laing ST, Ivens A, Butler V, Ravikumar SP, Laing R, Woods DJ, et al. The transcriptional response of Caenorhabditis elegans to ivermectin exposure identifies novel genes involved in the response to reduced food intake. PloS One. 2012;7(2):e31367. doi: 10.1371/journal.pone.003136722348077
71. Tippawangkosol P, Choochote W, Na-Bangchang K, Jitpakdi A, Pitasawat B, Riyong D, The in vitro effect of albendazole, ivermectin, diethylcarbamazine, and their combinations against infective third-stage larvae of nocturnally subperiodic Brugia malayi (Narathiwat strain): scanning electron microscopy. Journal of Vector Ecology: Journal of the Society for Vector Ecology. 2004;29(1):101–8.