Gender-associated genes in filarial nematodes are important for reproduction and potential intervention targets

PLoS Neglected Tropical Diseases

Volumn 5, Issue 1, 2011, Pages

  Li, Ben Wen ^a   Rush, Amy C ^a   Jiang, Dao Jun ^a   Mitreva, Makedonka ^a   Abubucker, Sahar ^a   Weil, Gary J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CARBOHYDRATE; CYTOKINE; LIGASE; LIPID; PENTOSE PHOSPHATE; PEPTIDASE; PHOSPHOTRANSFERASE; RIBOSOME RNA; TETRACYCLINE; TRANSFERASE;

ARTICLE; BINDING SITE; BIOINFORMATICS; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; CARBOHYDRATE METABOLISM; CELL COMMUNICATION; CELL GROWTH; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENERGY YIELD; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; IMMUNOMODULATION; MALE; MICROARRAY ANALYSIS; NONHUMAN; ONCHOCERCA VOLVULUS; OOCYTE DEVELOPMENT; PHENOTYPE; PHOSPHATE METABOLISM; PROTEIN SYNTHESIS; REPRODUCTIVE SUCCESS; RNA INTERFERENCE; SEQUENCE HOMOLOGY; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SPERMATOGENESIS; WOLBACHIA; WUCHERERIA BANCROFTI; ANIMAL; BIOLOGY; GENETICS; METHODOLOGY; PHYSIOLOGY; REPRODUCTION; SEX;

ANIMALS; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; COMPUTATIONAL BIOLOGY; FEMALE; GENE EXPRESSION PROFILING; MALE; MICROARRAY ANALYSIS; REPRODUCTION; SEX;

EID: 79851501772     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000947     Document Type: Article

References (74)

1. WHO, (2006) Global program to eliminate lymphatic filariasis. Wkly Epidemiol Rec 81: 221-232.
2. Geary TG, Woo K, McCarthy JS, Mackenzie CD, Horton J, et al. (2010) Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int J Parasitol 40: 1-13.
3. Boakye DA, Baidoo HA, Glah E, Brown C, Appawu M, et al. (2007) Monitoring lymphatic filariasis interventions: Adult mosquito sampling, and improved PCR- based pool screening method for Wuchereria bancrofti infection in Anopheles mosquitoes. Filaria J 6: 13.
4. Prichard RK, (2005) Is anthelmintic resistance a concern for heartworm control? What can we learn from the human filariasis control programs? Vet Parasitol 133: 243-253.
5. Nisbet AJ, Cottee P, Gasser RB, (2004) Molecular biology of reproduction and development in parasitic nematodes: progress and opportunities. Int J Parasitol 34: 125-138.
6. Reinke V, Gil IS, Ward S, Kazmer K, (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311-323.
7. Fitzpatrick JM, Johansen MV, Johnston DA, Dunne DW, Hoffmann KF, (2004) Gender-associated gene expression in two related strains of Schistosoma japonicum. Mol Biochem Parasitol 136: 191-209.
8. Li BW, Rush AC, Crosby SD, Warren WC, Williams SA, et al. (2005) Profiling of gender-regulated gene transcripts in the filarial nematode Brugia malayi by cDNA oligonucleotide array analysis. Mol Biochem Parasitol 143: 49-57.
9. Michalski ML, Weil GJ, (1999) Gender-specific gene expression in Brugia malayi. Mol Biochem Parasitol 104: 247-257.
10. Tellam RL, Kemp D, Riding G, Briscoe S, Smith D, et al. (2002) Reduced oviposition of Boophilus microplus feeding on sheep vaccinated with vitellin. Vet Parasitol 103: 141-156.
11. Fu G, Condon KC, Epton MJ, Gong P, Jin L, et al. (2007) Female-specific insect lethality engineered using alternative splicing. Nat Biotechnol 25: 353-357.
12. Barnes TM, Hekimi S, (1997) The Caenorhabditis elegans avermectin resistance and anesthetic response gene unc-9 encodes a member of a protein family implicated in electrical coupling of excitable cells. J Neurochem 69: 2251-2260.
13. Lok JB, Knight DH, Selavka CM, Eynard J, Zhang Y, et al. (1995) Studies of reproductive competence in male Dirofilaria immitis treated with milbemycin oxime. Trop Med Parasitol 46: 235-240.
14. Ghedin E, Hailemariam T, DePasse JV, Zhang X, Oksov Y, et al. (2009) Brugia malayi gene expression in response to the targeting of the Wolbachia endosymbiont by tetracycline treatment. PLoS Negl Trop Dis 3: e525.
15. Aragon AD, Imani RA, Blackburn VR, Cunningham C, (2008) Microarray based analysis of temperature and oxidative stress induced messenger RNA in Schistosoma mansoni. Mol Biochem Parasitol 162: 134-141.
16. Li BW, Rush AC, Mitreva M, Yin Y, Spiro D, et al. (2009) Transcriptomes and pathways associated with infectivity, survival and immunogenicity in Brugia malayi L3. BMC Genomics 10: 267.
17. Butchar JP, Cremer TJ, Clay CD, Gavrilin MA, Wewers MD, et al. (2008) Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS One 3: e2924.
18. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, et al. (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462-469.
19. Waisberg M, Lobo FP, Cerqueira GC, Passos LK, Carvalho OS, et al. (2007) Microarray analysis of gene expression induced by sexual contact in Schistosoma mansoni. BMC Genomics 8: 181.
20. Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, et al. (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Negl Trop Dis 3: e410.
21. Michalski ML, Monsey JD, Cistola DP, Weil GJ, (2002) An embryo-associated fatty acid-binding protein in the filarial nematode Brugia malayi. Mol Biochem Parasitol 124: 1-10.
22. Moreno Y, Geary TG, (2008) Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Negl Trop Dis 2: e326.
23. Kumar S, Chaudhary K, Foster JM, Novelli JF, Zhang Y, et al. (2007) Mining predicted essential genes of Brugia malayi for nematode drug targets. PLoS One 2: e1189.
24. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.
25. Cleveland WS, Devlin S, (1988) Locally-weighted regression: an approach to regression analysis by local fitting. J American Statistic J American Statistic Association 83: 596-610.
26. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
28. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
29. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330.
30. Simmer F, Moorman C, van der Linden AM, Kuijk E, van den Berghe PV, et al. (2003) Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 1: E12.
31. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, et al. (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-120.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
33. Bono H, Ogata H, Goto S, Kanehisa M, (1998) Reconstruction of amino acid biosynthesis pathways from the complete genome sequence. Genome Res 8: 203-210.
34. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
35. Mao X, Cai T, Olyarchuk J, Wei L, (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21: 3787-3793.
36. Li BW, Rush AC, Tan J, Weil GJ, (2004) Quantitative analysis of gender-regulated transcripts in the filarial nematode Brugia malayi by real-time RT-PCR. Mol Biochem Parasitol 137: 329-337.
37. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
38. Jiang D, Li BW, Fischer PU, Weil GJ, (2008) Localization of gender-regulated gene expression in the filarial nematode Brugia malayi. Int J Parasitol 38: 503-512.
39. Campbell BE, Nagaraj SH, Hu M, Zhong W, Sternberg PW, et al. (2008) Gender-enriched transcripts in Haemonchus contortus-predicted functions and genetic interactions based on comparative analyses with Caenorhabditis elegans. Int J Parasitol 38: 65-83.
40. Copley RR, Ponting CP, Schultz J, Bork P, (2002) Sequence analysis of multidomain proteins: past perspectives and future directions. Adv Protein Chem 61: 75-98.
41. Nisbet AJ, Cottee PA, Gasser RB, (2008) Genomics of reproduction in nematodes: prospects for parasite intervention? Trends Parasitol 24: 89-95.
42. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, et al. (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6: 605-616.
43. Boag PR, Newton SE, Gasser RB, (2001) Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Adv Parasitol 50: 153-198.
44. Boag PR, Ranganathan S, Newton SE, Gasser RB, (2002) A male-specific (cysteine-rich) protein of Oesophagostomum dentatum (Strongylida) with structural characteristics of a serine protease inhibitor containing two trypsin inhibitor-like domains. Parasitology 125: 445-455.
45. Martin J, Abubucker S, Wylie T, Yin Y, Wang Z, et al. (2009) Nematode.net update 2008: improvements enabling more efficient data mining and comparative nematode genomics. Nucleic Acids Res 37: D571-578.
46. McDonnell DP, Vegeto E, Gleeson MA, (1993) Nuclear hormone receptors as targets for new drug discovery. Biotechnology (N Y) 11: 1256-1261.
47. Henderson PJ, (1990) The homologous glucose transport proteins of prokaryotes and eukaryotes. Res Microbiol 141: 316-328.
48. Kaback HR, Wu J, (1997) From membrane to molecule to the third amino acid from the left with a membrane transport protein. Q Rev Biophys 30: 333-364.
49. Croce JC, Wu SY, Byrum C, Xu R, Duloquin L, et al. (2006) A genome-wide survey of the evolutionarily conserved Wnt pathways in the sea urchin Strongylocentrotus purpuratus. Dev Biol 300: 121-131.
50. Lee JY, Marston DJ, Walston T, Hardin J, Halberstadt A, et al. (2006) Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr Biol 16: 1986-1997.
51. Blaxter M, (1998) Caenorhabditis elegans is a nematode. Science 282: 2041-2046.
52. Ashton FT, Li J, Schad GA, (1999) Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Vet Parasitol 84: 297-316.
53. Stohard P, Pilgrim D, (2003) Sex-determination gene and pathway evolution in nematodes. Bioassy 25: 105-107.
54. Piano F, Schetter AJ, Morton DG, Gunsalus KC, Reinke V, et al. (2002) Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr Biol 12: 1959-1964.
55. Maeda I, Kohara Y, Yamamoto M, Sugimoto A, (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11: 171-176.
56. Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJ, et al. (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408: 331-336.
57. Reinke V, (2004) Sex and the genome. Nat Genet 36: 548-549.
58. Cottee PA, Nisbet AJ, Abs El-Osta YG, Webster TL, Gasser RB, (2006) Construction of gender-enriched cDNA archives for adult Oesophagostomum dentatum by suppressive-subtractive hybridization and a microarray analysis of expressed sequence tags. Parasitology 132: 691-708.
59. Parker JS, Roe SM, Barford D, (2004) Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J 23: 4727-4737.
60. Piano F, Schetter AJ, Mangone M, Stein L, Kemphues KJ, (2000) RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans. Curr Biol 10: 1619-1622.
61. Knox DP, Geldhof P, Visser A, Britton C, (2007) RNA interference in parasitic nematodes of animals: a reality check? Trends Parasitol 23: 105-107.
62. Miller S, Schreuer D, Hammerberg B, (1991) Inhibition of antigen-driven proliferative responses and enhancement of antibody production during infection with Brugia pahangi. J Immunol 147: 1007-1013.
63. Allen JE, MacDonald AS, (1998) Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite Immunol 20: 241-247.
64. Hewitson JP, Harcus YM, Curwen RS, Dowle AA, Atmadja AK, et al. (2008) The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Mol Biochem Parasitol 160: 8-21.
65. Kearney R, Blondeau F, McPherson P, Bell A, Servant F, et al. (2005) Elimination of redundant protein identifications in high throughput proteomics. Conf Proc IEEE Eng Med Biol Soc 5: 4803-4806.
66. Tang L, Ou X, Henkle-Duhrsen K, Selkirk ME, (1994) Extracellular and cytoplasmic CuZn superoxide dismutases from Brugia lymphatic filarial nematode parasites. Infect Immun 62: 961-967.
67. Maizels RM, Gregory WF, Kwan-Lim GE, Selkirk ME, (1989) Filarial surface antigens: the major 29 kilodalton glycoprotein and a novel 17-200 kilodalton complex from adult Brugia malayi parasites. Mol Biochem Parasitol 32: 213-227.
68. Cookson E, Blaxter ML, Selkirk ME, (1992) Identification of the major soluble cuticular glycoprotein of lymphatic filarial nematode parasites (gp29) as a secretory homolog of glutathione peroxidase. Proc Natl Acad Sci U S A 89: 5837-5841.
69. Zang X, Taylor P, Wang JM, Meyer DJ, Scott AL, et al. (2002) Homologues of human macrophage migration inhibitory factor from a parasitic nematode. Gene cloning, protein activity and crystal structure. J Biol Chem 277: 44261-44267.
70. Bell A, Monaghan P, Page AP, (2006) Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int J Parasitol 36: 261-276.
71. Bandi C, McCall JW, Genchi C, Corona S, Venco L, et al. (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29: 357-364.
72. Hoerauf A, Nissen-Pahle K, Schmetz C, Henkle-Duhrsen K, Blaxter ML, et al. (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103: 11-18.
73. Ford L, Zhang J, Liu J, Hashmi S, Fuhrman JA, et al. (2009) Functional analysis of the cathepsin-like cysteine protease genes in adult Brugia malayi using RNA interference. PLoS Negl Trop Dis 3: e377.
74. Guiliano DB, Hong X, McKerrow JH, Blaxter ML, Oksov Y, et al. (2004) A gene family of cathepsin L-like proteases of filarial nematodes are associated with larval molting and cuticle and eggshell remodeling. Mol Biochem Parasitol 136: 227-242.