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Int J Parasitol Drugs Drug Resist. 2014 Aug 13;4(3):164-84. doi: 10.1016/j.ijpddr.2014.07.007. eCollection 2014 Dec.

Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions.

International journal for parasitology. Drugs and drug resistance

Andrew C Kotze, Peter W Hunt, Philip Skuce, Georg von Samson-Himmelstjerna, Richard J Martin, Heinz Sager, Jürgen Krücken, Jane Hodgkinson, Anne Lespine, Aaron R Jex, John S Gilleard, Robin N Beech, Adrian J Wolstenholme, Janina Demeler, Alan P Robertson, Claude L Charvet, Cedric Neveu, Ronald Kaminsky, Lucien Rufener, Melanie Alberich, Cecile Menez, Roger K Prichard

Affiliations

  1. CSIRO Animal, Food and Health Sciences, Brisbane, QLD, Australia.
  2. CSIRO Animal, Food and Health Sciences, Armidale, NSW, Australia.
  3. Parasitology Division, Moredun Research Institute, Penicuik, Midlothian, UK.
  4. Institute for Parasitology and Tropical Veterinary Medicine, Freie Universitat Berlin, Berlin, Germany.
  5. Department of Biomedical Sciences, Iowa State University, Ames, IA, USA.
  6. Novartis Centre de Recherche Sante Animale, St. Aubin, Switzerland.
  7. Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
  8. INRA, Toxalim, Research Centre in Food Toxicology, Toulouse, France.
  9. Faculty of Veterinary Science, University of Melbourne, Parkville, VIC, Australia.
  10. Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, Canada.
  11. Institute of Parasitology, McGill University, QC, Canada.
  12. Department of Infectious Diseases & Center for Tropical and Emerging Global Disease, University of Georgia, Athens, GA, USA.
  13. INRA, Infectiologie et Santé Publique, Nouzilly, France ; Université François Rabelais de Tours, Infectiologie et Santé Publique, Tours, France.

PMID: 25516826 PMCID: PMC4266812 DOI: 10.1016/j.ijpddr.2014.07.007

Abstract

Anthelmintic resistance has a great impact on livestock production systems worldwide, is an emerging concern in companion animal medicine, and represents a threat to our ongoing ability to control human soil-transmitted helminths. The Consortium for Anthelmintic Resistance and Susceptibility (CARS) provides a forum for scientists to meet and discuss the latest developments in the search for molecular markers of anthelmintic resistance. Such markers are important for detecting drug resistant worm populations, and indicating the likely impact of the resistance on drug efficacy. The molecular basis of resistance is also important for understanding how anthelmintics work, and how drug resistant populations arise. Changes to target receptors, drug efflux and other biological processes can be involved. This paper reports on the CARS group meeting held in August 2013 in Perth, Australia. The latest knowledge on the development of molecular markers for resistance to each of the principal classes of anthelmintics is reviewed. The molecular basis of resistance is best understood for the benzimidazole group of compounds, and we examine recent work to translate this knowledge into useful diagnostics for field use. We examine recent candidate-gene and whole-genome approaches to understanding anthelmintic resistance and identify markers. We also look at drug transporters in terms of providing both useful markers for resistance, as well as opportunities to overcome resistance through the targeting of the transporters themselves with inhibitors. Finally, we describe the tools available for the application of the newest high-throughput sequencing technologies to the study of anthelmintic resistance.

Keywords: Anthelmintic drugs; Anthelmintic resistance; Anthelmintic targets; Molecular markers; Receptors

References

  1. Genome Biol. 2013 Aug 28;14(8):R89 - PubMed
  2. Int J Parasitol. 2013 May;43(6):465-75 - PubMed
  3. J Neurosci. 1985 Apr;5(4):956-64 - PubMed
  4. Mol Biochem Parasitol. 2003 Oct;131(2):137-45 - PubMed
  5. Int J Parasitol Drugs Drug Resist. 2011 Nov 07;2:58-75 - PubMed
  6. Vet Parasitol. 2012 Dec 21;190(3-4):608-12 - PubMed
  7. Exp Parasitol. 2013 Jun;134(2):171-7 - PubMed
  8. Parasitology. 2009 Aug;136(9):1081-8 - PubMed
  9. Nat Methods. 2010 Nov;7(11):909-12 - PubMed
  10. Trends Parasitol. 2011 Apr;27(4):176-81 - PubMed
  11. Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):14802-7 - PubMed
  12. Mol Biochem Parasitol. 2010 Apr;170(2):105-7 - PubMed
  13. Int J Parasitol. 2011 Jul;41(8):881-94 - PubMed
  14. Biotechnol Adv. 2013 Dec;31(8):1109-19 - PubMed
  15. Parasitology. 2005 Oct;131(Pt 4):501-10 - PubMed
  16. Genome Res. 2002 Apr;12(4):656-64 - PubMed
  17. Pharmacogenet Genomics. 2010 Jul;20(7):414-25 - PubMed
  18. Genetics. 2004 Jan;166(1):161-9 - PubMed
  19. PLoS Pathog. 2009 Apr;5(4):e1000380 - PubMed
  20. Nat Methods. 2012 Mar 04;9(4):357-9 - PubMed
  21. Mol Biochem Parasitol. 2002 Apr 9;120(2):297-300 - PubMed
  22. Mol Biochem Parasitol. 2013 Apr;188(2):79-86 - PubMed
  23. Science. 2012 Feb 3;335(6068):574-8 - PubMed
  24. WormBook. 2013 Aug 13;:1-106 - PubMed
  25. Vet Parasitol. 2014 Feb 24;200(1-2):90-6 - PubMed
  26. Parasitol Res. 2004 Feb;92(3):205-10 - PubMed
  27. Bioinformatics. 2012 Jun 15;28(12):1647-9 - PubMed
  28. Parasitology. 2010 Apr;137(4):705-17 - PubMed
  29. PLoS Negl Trop Dis. 2009;3(3):e397 - PubMed
  30. Int J Parasitol. 2010 Nov;40(13):1477-81 - PubMed
  31. Int J Parasitol Drugs Drug Resist. 2012 Dec 03;3:20-7 - PubMed
  32. Vet Parasitol. 2010 Sep 20;172(3-4):291-8 - PubMed
  33. Mol Biochem Parasitol. 1994 Feb;63(2):299-303 - PubMed
  34. PLoS One. 2013 Apr 24;8(4):e61635 - PubMed
  35. PLoS Pathog. 2009 Jul;5(7):e1000517 - PubMed
  36. PLoS Negl Trop Dis. 2008 Jul 09;2(7):e260 - PubMed
  37. Pharmacogenomics. 2011 Jan;12(1):59-85 - PubMed
  38. Chem Biol Interact. 2006 Feb 25;159(3):169-79 - PubMed
  39. Mol Biochem Parasitol. 2013 Mar;188(1):10-9 - PubMed
  40. Nature. 2008 Mar 13;452(7184):176-80 - PubMed
  41. Int J Parasitol Drugs Drug Resist. 2014 Mar 13;4(2):77-84 - PubMed
  42. Genome Res. 2008 May;18(5):821-9 - PubMed
  43. Nat Rev Genet. 2009 Dec;10(12):833-44 - PubMed
  44. Parasitology. 2011 Feb;138(2):160-74 - PubMed
  45. Nat Rev Genet. 2010 Jan;11(1):31-46 - PubMed
  46. Int J Parasitol Drugs Drug Resist. 2013 Feb 01;3:51-8 - PubMed
  47. PLoS Pathog. 2010 Sep 09;6(9):e1001091 - PubMed
  48. Trends Pharmacol Sci. 2012 Aug;33(8):432-41 - PubMed
  49. PLoS Pathog. 2014 Jan 30;10(1):e1003870 - PubMed
  50. Nat Rev Genet. 2011 Feb;12(2):87-98 - PubMed
  51. Trends Genet. 2008 Nov;24(11):539-51 - PubMed
  52. Trans R Soc Trop Med Hyg. 2007 Dec;101(12):1223-32 - PubMed
  53. Mol Biochem Parasitol. 2014 Jan;193(1):66-70 - PubMed
  54. Eur J Pharmacol. 2000 Apr 14;394(2-3):163-70 - PubMed
  55. Mol Biochem Parasitol. 2008 May;159(1):73-8 - PubMed
  56. PLoS Negl Trop Dis. 2014 Feb 20;8(2):e2698 - PubMed
  57. Int J Parasitol. 2012 Jul;42(8):761-70 - PubMed
  58. Asp Appl Biol. 2011 Apr 15;107:79-87 - PubMed
  59. Mol Biochem Parasitol. 2009 Nov;168(1):120-2 - PubMed
  60. Annu Rev Biochem. 1993;62:385-427 - PubMed
  61. Int J Parasitol. 2008 Feb;38(2):149-55 - PubMed
  62. Nucleic Acids Res. 2011 Jul;39(Web Server issue):W13-7 - PubMed
  63. Mol Biochem Parasitol. 2012 Nov;186(1):69-72 - PubMed
  64. PLoS Genet. 2012;8(3):e1002570 - PubMed
  65. Mol Pharmacol. 2009 Jun;75(6):1347-55 - PubMed
  66. Int J Parasitol. 2000 Jan;30(1):105-11 - PubMed
  67. Curr Drug Targets. 2006 Jul;7(7):861-79 - PubMed
  68. Nat Biotechnol. 2010 May;28(5):511-5 - PubMed
  69. Mol Biochem Parasitol. 1997 Oct;89(1):97-107 - PubMed
  70. Genome Res. 2010 Sep;20(9):1297-303 - PubMed
  71. Int J Parasitol Drugs Drug Resist. 2014 Jul 12;4(3):143-51 - PubMed
  72. Trends Parasitol. 2008 Jul;24(7):293-8 - PubMed
  73. Bioinformatics. 2014 Aug 1;30(15):2114-20 - PubMed
  74. Int J Parasitol. 2013 Dec;43(14):1133-9 - PubMed
  75. Genome Res. 2012 Mar;22(3):549-56 - PubMed
  76. Parasitology. 2007 May;134(Pt 5):609-19 - PubMed
  77. Emerg Infect Dis. 2012 Jun;18(6):1028-9 - PubMed
  78. EMBO J. 2005 Jul 20;24(14):2566-78 - PubMed
  79. Vet Rec. 2011 Jun 11;168(23):623-4 - PubMed
  80. Bioinformatics. 2009 Aug 15;25(16):2078-9 - PubMed
  81. Vet Parasitol. 2013 Dec 6;198(3-4):325-35 - PubMed
  82. Nat Biotechnol. 2011 May 15;29(7):644-52 - PubMed
  83. FASEB J. 2012 Nov;26(11):4650-61 - PubMed
  84. Int J Parasitol Drugs Drug Resist. 2011 Oct 14;1(1):14-27 - PubMed
  85. J Pharm Sci. 2011 Jan;100(1):94-7 - PubMed
  86. Int J Parasitol Drugs Drug Resist. 2013 Dec 11;4(1):48-54 - PubMed
  87. Bioinformatics. 2010 Mar 1;26(5):589-95 - PubMed
  88. Drug Metab Dispos. 2006 Mar;34(3):457-63 - PubMed
  89. Front Mol Neurosci. 2012 May 07;5:60 - PubMed
  90. PLoS Negl Trop Dis. 2012;6(11):e1883 - PubMed
  91. Science. 2007 Sep 21;317(5845):1756-60 - PubMed
  92. Nature. 1994 Oct 20;371(6499):707-11 - PubMed
  93. Mol Biochem Parasitol. 2005 Jan;139(1):51-64 - PubMed
  94. FASEB J. 2006 Dec;20(14):2606-8 - PubMed
  95. Vet Parasitol. 2007 Feb 28;143(3-4):299-304 - PubMed
  96. Lancet. 2007 Jun 16;369(9578):2021-9 - PubMed
  97. Vet Parasitol. 2011 Feb 28;176(1):1-8 - PubMed
  98. J Gen Physiol. 1993 Feb;101(2):271-96 - PubMed
  99. Parasitol Res. 1996;82(2):97-101 - PubMed
  100. J Neurochem. 2004 Jun;89(5):1137-47 - PubMed
  101. J Neurosci. 1997 Aug 1;17(15):5843-57 - PubMed
  102. Nat Biotechnol. 2008 Aug;26(8):909-15 - PubMed
  103. Int J Parasitol Drugs Drug Resist. 2012 Mar 03;2:92-7 - PubMed
  104. Nature. 2011 Oct 26;479(7374):529-33 - PubMed
  105. Am J Trop Med Hyg. 2013 Jun;88(6):1052-61 - PubMed
  106. Mol Biochem Parasitol. 2010 May;171(1):1-7 - PubMed
  107. Vet Parasitol. 1995 Sep;59(2):139-56 - PubMed
  108. Mol Biochem Parasitol. 2010 May;171(1):8-16 - PubMed
  109. Parasitol Res. 2012 Nov;111(5):1871-7 - PubMed
  110. Parasitology. 2013 Oct;140(12):1523-33 - PubMed
  111. Parasitology. 2013 Sep;140(10):1287-303 - PubMed
  112. Nat Protoc. 2012 Jun 07;7(7):1260-84 - PubMed
  113. Vet Parasitol. 2012 Apr 19;185(1):2-8 - PubMed
  114. Nat Methods. 2012 Jan 30;9(2):145-51 - PubMed
  115. Br J Pharmacol. 2011 Sep;164(2b):453-70 - PubMed
  116. Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2674-9 - PubMed
  117. Drug Metab Dispos. 2010 Apr;38(4):573-80 - PubMed
  118. Vet Parasitol. 2013 Jan 31;191(3-4):264-75 - PubMed
  119. Exp Parasitol. 2012 Sep;132(1):40-6 - PubMed
  120. Parasitol Int. 2013 Oct;62(5):464-70 - PubMed
  121. Curr Protoc Bioinformatics. 2003 Feb;Chapter 10:Unit 10.3 - PubMed
  122. Parasitol Res. 2008 Sep;103(4):931-9 - PubMed
  123. Nucleic Acids Res. 2012 Jan;40(1):37-52 - PubMed
  124. Invert Neurosci. 2012 Jun;12(1):29-36 - PubMed
  125. Nat Methods. 2013 Dec;10(12):1185-91 - PubMed
  126. Vet Parasitol. 2012 Dec 21;190(3-4):519-29 - PubMed
  127. Parasitology. 2007;134(Pt 8):1111-21 - PubMed
  128. Int J Parasitol. 1999 Dec;29(12):1979-85 - PubMed
  129. Br J Pharmacol. 2011 Nov;164(5):1421-32 - PubMed
  130. Nat Genet. 2011 Mar;43(3):228-35 - PubMed
  131. Nature. 2012 Oct 25;490(7421):566-9 - PubMed
  132. Vet Parasitol. 2012 May 25;186(3-4):344-9 - PubMed
  133. Nat Genet. 2013 May;45(5):495-500 - PubMed
  134. PLoS Negl Trop Dis. 2013 May 30;7(5):e2247 - PubMed
  135. Parasitology. 2013 Apr;140(4):499-508 - PubMed
  136. Int J Parasitol. 2014 Mar;44(3-4):235-41 - PubMed
  137. Mol Pharmacol. 2011 Jun;79(6):1031-43 - PubMed
  138. PLoS One. 2013 Aug 12;8(8):e70212 - PubMed
  139. Hum Genomics. 2010 Apr;4(4):271-7 - PubMed
  140. Nat Neurosci. 2013 Dec;16(12):1794-801 - PubMed
  141. Pharmacogenetics. 2001 Nov;11(8):727-33 - PubMed
  142. Vet Parasitol. 2012 Jul 6;187(3-4):464-72 - PubMed
  143. Mol Biochem Parasitol. 2006 Aug;148(2):181-9 - PubMed
  144. Vet Parasitol. 2013 Nov 15;198(1-2):159-65 - PubMed
  145. PLoS Pathog. 2013;9(8):e1003524 - PubMed
  146. Nat Protoc. 2012 Mar 01;7(3):562-78 - PubMed
  147. Trends Parasitol. 2012 Sep;28(9):385-94 - PubMed
  148. PLoS Negl Trop Dis. 2011 Mar 29;5(3):e998 - PubMed
  149. Int J Parasitol. 2011 Aug 1;41(9):951-7 - PubMed
  150. Genome Res. 2011 Sep;21(9):1462-77 - PubMed
  151. Aust Vet J. 1995 Jul;72(7):275-6 - PubMed
  152. Nat Rev Genet. 2012 Dec;13(12):840-52 - PubMed
  153. Parasitology. 2009 Mar;136(3):349-58 - PubMed
  154. Top Companion Anim Med. 2011 Nov;26(4):186-92 - PubMed
  155. Int J Parasitol. 2011 Aug 1;41(9):935-42 - PubMed
  156. Mol Biochem Parasitol. 2011 Dec;180(2):99-105 - PubMed
  157. Eur J Pharm Sci. 2007 Jan;30(1):84-94 - PubMed
  158. Vet Parasitol. 2007 Mar 31;144(3-4):313-20 - PubMed
  159. Exp Parasitol. 1998 Sep;90(1):42-8 - PubMed
  160. Nucleic Acids Res. 2012 Jan;40(Database issue):D720-8 - PubMed
  161. Vet Parasitol. 2011 Sep 27;181(2-4):388-92 - PubMed
  162. Nature. 2011 Jun 2;474(7349):54-60 - PubMed
  163. Genome Biol. 2006;7 Suppl 1:S2.1-31 - PubMed
  164. J Neurochem. 2002 Nov;83(4):870-8 - PubMed
  165. Curr Protoc Bioinformatics. 2010 Sep;Chapter 11:Unit 11.5 - PubMed
  166. Int J Parasitol. 2008 Jan;38(1):111-22 - PubMed
  167. PLoS Pathog. 2012 Feb;8(2):e1002534 - PubMed
  168. Mol Biochem Parasitol. 2000 Sep;110(1):69-77 - PubMed
  169. Vet Parasitol. 2013 Nov 15;198(1-2):166-71 - PubMed
  170. Genome Biol. 2013 Aug 28;14(8):R88 - PubMed
  171. Exp Parasitol. 1998 Jun;89(2):169-79 - PubMed
  172. Vet Parasitol. 2009 Mar 23;160(3-4):251-7 - PubMed
  173. Vet Parasitol. 2014 Aug 29;204(3-4):411-5 - PubMed
  174. Int J Parasitol Drugs Drug Resist. 2012 Apr 17;2:154-61 - PubMed
  175. Int J Parasitol. 2009 Mar;39(4):435-41 - PubMed
  176. Chem Res Toxicol. 2012 Aug 20;25(8):1571-3 - PubMed
  177. Int J Parasitol. 2009 Jan;39(2):213-20 - PubMed
  178. Vet Rec. 1998 Mar 7;142(10):255-6 - PubMed
  179. Vet Parasitol. 2013 Jan 31;191(3-4):240-51 - PubMed
  180. Parasitol Res. 2012 Nov;111(5):2205-7 - PubMed
  181. J Biol Chem. 2011 Dec 23;286(51):43913-24 - PubMed
  182. Trends Parasitol. 2004 Oct;20(10):477-81 - PubMed
  183. Exp Parasitol. 2010 Jun;125(2):172-8 - PubMed
  184. Cell Struct Funct. 1997 Feb;22(1):213-8 - PubMed
  185. Parasitology. 2012 Apr;139(5):613-29 - PubMed

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