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TRP Channels in Parasites

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Book cover Transient Receptor Potential Channels

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 704))

Abstract

A wide range of single- and multi-cellular parasites infect humans and other animals, causing some of the most prevalent and debilitating diseases on the planet. There have been virtually no published studies on the TRP channels of this diverse group of organisms. However, since many parasite genomes have been sequenced, it is simple to demonstrate that they are present in all parasitic metazoans and that sequences related to the yeast trp are present in many protozoans, including all the kinetoplastids. We compared the TRP genes of three species of animal and plant parasitic nematode to those of C. elegans and found that the parasitic species all had fewer such genes. These differences may reflect the phylogenetic distance between the species studied, or may be due to loss of specific gene functions following the evolution of the parasitic lifestyle. Other helminth groups, the trematodes and cestodes, seem to possess many TRPC and TRPM genes, but lack TRPV and TRPN. Most ectoparasites are insects or arachnids. We compared the TRP genes of a plant parasitic aphid and an animal parasite louse and tick with those of Drosophila. Again, all the parasitic species seemed to have fewer types of TRP channel, though the difference was less marked than for the nematodes. The aphid lacks TRPP and TRPML channel genes, whereas the tick lacked those encoding TRPVs. Again, these differences may reflect adaptation to parasitism, and could enable TRP channels to be targeted in the development of novel antiparasitic drugs.

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References

  1. C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018

    Google Scholar 

  2. Kumari S, Kumar A, Samant M, Singh N, Dube A (2008) Discovery of Novel Vaccine Candidates and Drug Targets Against Visceral Leishmaniasis Using Proteomics and Transcriptomics. Curr Drug Targets 9:938–947

    Article  CAS  PubMed  Google Scholar 

  3. Martin RJ, Murray I, Robertson AP, Bjorn H, Sangster N (1998) Anthelmintics and ion-channels: after a puncture, use a patch. Int J Parasitol 28:849–862

    Article  CAS  PubMed  Google Scholar 

  4. Wolstenholme AJ, Rogers AT (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131:S85–S95

    Article  CAS  PubMed  Google Scholar 

  5. Harder A, Holden-Dye L, Walker RJ, Wunderlich F (2005) Mechanisms of action of emodepside. Parasitol Res 97:S1–S10

    Article  PubMed  Google Scholar 

  6. Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, Bouvier J, Schorderet Weber S, Wenger A, Wieland-Berghausen S, Goebel T, Gauvry N, Pautrat F, Skripsky T, Froelich O, Komoin-Oka C, Westlund B, Sluder A, Maser P (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452:176–180

    Article  CAS  PubMed  Google Scholar 

  7. Escalante AA, Smith DL, Kim Y (2009) The dynamics of mutations associated with anti-malarial drug resistance in Plasmodium falciparum. Trends Parasitol 25:557–563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Geary TG, Woo K, McCarthy JS, Mackenzie CD, Horton J, Prichard RK, de Silva NR, Olliaro PL, Lazdins-Helds JK, Engels DA, Bundy DA (2010) Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int J Parasitol 40:1–13

    Article  CAS  PubMed  Google Scholar 

  9. Wilkinson SR, Kelly JM (2009) Trypanocidal drugs: mechanisms, resistance and new targets. Expert Revs Mol Med 11:e31

    Article  Google Scholar 

  10. Clayton CE (1999) Genetic manipulation of kinetoplastida. Parasitology Today 15:372–378

    Article  CAS  PubMed  Google Scholar 

  11. Thathy V, Menard R (2002) Gene targeting in Plasmodium berghei. Methods Mol Med 72:317–331

    CAS  PubMed  Google Scholar 

  12. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193: 673–675

    Article  CAS  PubMed  Google Scholar 

  13. Wu Y, Sifri CD, Lei HH, Wellems TE (1995) Transfection of Plasmodium falciparum within human red blood cells. Proc Natl Acad Sci USA 92:973–977

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Benton R (2008) Chemical sensing in Drosophila. Curr Opin Neurobiol 18:357–363

    Article  CAS  PubMed  Google Scholar 

  15. Kahn-Kirby AH, Bargmann CI (2006) TRP channels in C. elegans. Ann Rev Physiol 68: 719–736

    Article  CAS  Google Scholar 

  16. Montell C (1999) Visual transduction in Drosophila. Ann Rev Cell Dev Biol 15:231–268

    Article  CAS  Google Scholar 

  17. Xiao R, Xu XZ (2009) Function and regulation of TRP family channels in C. elegans. Pflugers Arch 458:851–860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Ardelli BF, Stitt LE, Tompkins JB (2010) Inventory and analysis of ATP-binding cassette (ABC) systems in Brugia malayi. Parasitology 137:1195–1212

    Article  CAS  PubMed  Google Scholar 

  19. Williamson SM, Walsh TK, Wolstenholme AJ (2007) The cys-loop ligand-gated ion channel gene family of Brugia malayi and Trichinella spiralis: a comparison with Caenorhabditis elegans. Inv Neurosci 7:219–226

    Article  CAS  Google Scholar 

  20. Mathers CD, Ezzati M, Lopez AD (2007) Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis 1:e114

    Article  PubMed Central  PubMed  Google Scholar 

  21. Obornik M, Janouskovec J, Chrudimsky T, Liukes J (2009) Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again. Int J Parasitol 39:1–12

    Article  CAS  PubMed  Google Scholar 

  22. Blackman MJ, Bannister LH (2001) Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol Biochem Parasitol 117:11–25

    Article  CAS  PubMed  Google Scholar 

  23. de Souza W, Attias M, Rodrigues JC (2009) Particularities of mitochondrial structure in parasitic protists (Apicomplexa and Kinetoplastida). Int J Biochem Cell Biol 41:2069–2080

    Article  PubMed  Google Scholar 

  24. Chenik M, Douagi F, Ben Achour Y, Ben Khalef N, Ouakad M, Louzir H, Dellagi K (2005) Characterization of two different mucolipin-like genes from Leishmania major. Parasitol Res 98:5–13

    Article  PubMed  Google Scholar 

  25. Palmer CP, Zhou XL, Lin J, Loukin SH, Kung C, Saimi Y:A (2001) TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca(2+)-permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci USA 98:7801–7805

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Fares H, Greenwald I (2001) Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 28:64–68

    CAS  PubMed  Google Scholar 

  27. Nagamune K, Moreno SN, Chini EN, Sibley LD (2008) Calcium regulation and signaling in apicomplexan parasites. Subcell Biochem 47:70–81

    Article  PubMed  Google Scholar 

  28. Pryor PR, Reimann F, Gribble FM, Luzio JP (2006) Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 7:1388–1398

    Article  CAS  PubMed  Google Scholar 

  29. Martina JA, Lelouvier B, Puertollano R (2009) The calcium channel mucolipin-3 is a novel regulator of trafficking along the endosomal pathway. Traffic 10:1143–1156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Cesbron-Delauw MF, Gendrin C, Travier L, Ruffiot P, Mercier C (2008) Apicomplexa in mammalian cells: trafficking to the parasitophorous vacuole. Traffic 9:657–664

    Article  CAS  PubMed  Google Scholar 

  31. Ravindran S, Boothroyd JC (2008) Secretion of proteins into host cells by Apicomplexan parasites. Traffic 9:647–656

    Article  CAS  PubMed  Google Scholar 

  32. Rohloff P, Docampo R (2008) A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi. Exp Parasitol 118:17–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Andrade LF, Andrews NW (2004) Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. J Exp Med 200:1135–1143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Wilson J, Huynh C, Kennedy KA, Ward DM, Kaplan J, Aderem A, Andrews NW (2008) Control of parasitophorous vacuole expansion by LYST/Beige restricts the intracellular growth of Leishmania amazonensis. PLoS Pathogens 4:e100179

    Google Scholar 

  35. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, Angiuoli SV, Creasy T, Amedeo P, Haas B, El-Sayed NM, Wortman JR, Feldblyum T, Tallon L, Schatz M, Shumway M, Koo H, Salzberg SL, Schobel S, Pertea M, Pop M, White O, Barton GJ, Carlow CKS, Crawford MJ, Daub J, Dimmic MW, Estes CF, Foster JM, Ganatra M, Gregory WF, Johnson NM, Jin J, Komuniecki R, Korf I, Kumar S, Laney S, Li B-W, Li W, Lindblom TH, Lustigman S, Ma D, Maina CV, Martin DMA, McCarter JP, McReynolds L, Mitreva M, Nutman TB, Parkinson J, Peregrin-Alvarez JM, Poole C, Ren Q, Saunders L, Sluder AE, Smith K, Stanke M, Unnasch TR, Ware J, Wei AD, Weil G, Williams DJ, Zhang Y, Williams SA, Fraser-Liggett C, Slatko B, Blaxter ML, Scott AL (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317:1756–1760

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Segurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915

    Article  CAS  PubMed  Google Scholar 

  37. Wylie T, Martin JC, Dante M, Mitreva MD, Clifton SW, Chinwalla A, Waterston RH, Wilson RK, McCarter JP (2004) Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res 32:D423–D426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstrate A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolution framework for the phylum Nematoda. Nature 392:71–75

    Article  CAS  PubMed  Google Scholar 

  39. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW (2001) The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr Biol 11:1341–1346

    Article  CAS  PubMed  Google Scholar 

  40. Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386–389

    CAS  PubMed  Google Scholar 

  41. Xu XZS, Sternberg PW (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285–297

    Article  CAS  PubMed  Google Scholar 

  42. Jose AM, Bany IA, Chase DL, Koelle MR (2006) A specific subset of TRPV channels in Caenorhabditis elegans endocrine cells function as mixed heteromers to promote neurotransmitter release. Genetics 175:93–105

    Article  PubMed  Google Scholar 

  43. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D, Macedo CD, McVeigh P, Ning ZM, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu WJ, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Teramoto T, Lambie EJ, Iwasaki K (2005) Differential regulation of TRPM channels governs electrolyte homeostasis in the C. elegans intestine. Cell Metab 1:343–354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Teramoto T, Sternick LA, Kage-Nakadai E, Sajjadi S, Siembida J, Mitani S, Iwasaki K, Lambie EJ (2010) Magnesium excretion in C. elegans requires the activity of the GTL-2 TRPM channel. PLoS One 5:e9589

    Article  PubMed Central  PubMed  Google Scholar 

  46. Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114:191–200

    Article  CAS  PubMed  Google Scholar 

  47. The International Aphid Genomics Consortium (2010) Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biol 8:e1000313

    Google Scholar 

  48. Dale RP, Jones AK, Tamborindeguy C, Davies TGE, Amey JS, Williamson S, Wolstenholme A, Field LM, Williamson MS, Walsh TK, Sattelle DB (2010) Identification of ion channel genes in the Acyrthosiphon pisum genome. Insect Mol Biol 19(Suppl 2):141–153

    Article  CAS  PubMed  Google Scholar 

  49. Chentsova NA, Gruntenko NE, Bogomolova EV, Adonyeva NV, Karpova EK, Rauschenbach IY (2002) Stress response in Drosophila melanogaster strain inactive with decreased tyramine and octopamine contents. J Comp Physiol B 172:643–650

    Article  CAS  PubMed  Google Scholar 

  50. Rosenzweig M, Brennan KM, Taylor TD, Phelps PO, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419–424

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Lee Y, Lee Y, Lee J, Bang S, Hyun S, Kang J, Hong ST, Bae E, Kaang BK, Kim J (2005) Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet 37:305–310

    Article  CAS  PubMed  Google Scholar 

  52. Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259–8269

    CAS  PubMed  Google Scholar 

  53. Feng ZY, Li W, Ward A, Piggott BJ, Larkspur ER, Sternberg PW, Xu XZS (2006) A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels. Cell 127:621–633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. White JQ, Nicholas TJ, Gritton J, Truong L, Davidson ER, Jorgensen EM (2007) The sensory circuitry for sexual attraction in C. elegans males. Curr Biol 17:1847–1857

    Article  CAS  PubMed  Google Scholar 

  55. Tobin D, Madsen D, Kahn-Kirby AH, Peckol E, Moulder G, Barstead R, Maricq A, Bargmann C (2002) Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307–318

    Article  CAS  PubMed  Google Scholar 

  56. West RJ, Sun AY, Church DL, Lambie EJ (2001) The C. elegans gon-2 gene encodes a putative TRP cation channel protein required for mitotic cell progression. Gene 266:103–110

    Article  CAS  PubMed  Google Scholar 

  57. Kwan CS, Vazquez-Manrique RP, Ly S, Goyal K, Baylis HA (2008) TRPM channels are required for rhythmicity in the ultradian defecation rhythm of C. elegans. BMC Physiol 8:11

    Article  PubMed Central  PubMed  Google Scholar 

  58. Xing J, Yan XH, Estevez A, Strange K (2008) Highly Ca2+-selective TRPM channels regulate IP3-dependent oscillatory Ca2+ signaling in the C. elegans intestine. J Gen Physiol 131: 245–255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schafer WR (2007) Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat Neurosci 10:568–577

    Article  CAS  PubMed  Google Scholar 

  60. Kindt KS, Quast KB, Giles AC, De S, Hendrey D, Nicastro I, Rankin CH, Schafer WR (2007) Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 55:662–676

    Article  CAS  PubMed  Google Scholar 

  61. Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84

    Article  CAS  PubMed  Google Scholar 

  62. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454: 217–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Tracey WD, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila gene essential for nociception. Cell 113:261–273

    Article  CAS  PubMed  Google Scholar 

  64. Gopfert MC, Robert D (2003) Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci USA 100:5514–5519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Gao Z, Ruden DM, Lu X (2003) PKD2 cation channel is required for directional sperm movement and male fertility. Curr Biol 13:2175–2178

    Article  CAS  PubMed  Google Scholar 

  66. Venkatachalam K, Long AA, Elsaesser R, Nikolaeva D, Broadie K, Montell C (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell 135:838–851

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank all of those who make their sequence information publically available. The T. spiralis sequence data were produced by the Genome Sequencing Center at Washington University School of Medicine in St Louis and can be obtained from http://genome.wustl.edu. Funding for the sequence characterization of the Trichinella genome is being provided by the National Human Genome Research Institute (NHGRI), National Institutes of Health (NIH). The E. multilocularis data were produced by the Sanger Centre, Hinxton UK and funded by the Wellcome Tust. The P. humanus and I. scapularis data were obtained from Vectorbase (http://www.vectorbase.org), an NIAID Bioinformatics Resource Center for Invertebrate Vectors of Human Pathogens.

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Authors and Affiliations

  1. Department of Infectious Diseases, University of Georgia, Athens, GA, 30602, USA

    Adrian J. Wolstenholme, Sally M. Williamson & Barbara J. Reaves

  2. Center for Tropical and Emerging Global Disease, University of Georgia, Athens, GA, 30602, USA

    Adrian J. Wolstenholme

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  1. Adrian J. Wolstenholme
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Correspondence to Adrian J. Wolstenholme .

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  1. Dept. Clinical Research & Education, Södersjukhuset, Karolinska Institutet, Stockholm, 118 83, Sweden

    Md. Shahidul Islam

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Wolstenholme, A.J., Williamson, S.M., Reaves, B.J. (2011). TRP Channels in Parasites. In: Islam, M. (eds) Transient Receptor Potential Channels. Advances in Experimental Medicine and Biology, vol 704. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0265-3_20

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