Stage-specific transcriptome and proteome analyses of the filarial parasite Onchocerca volvulus and its Wolbachia endosymbiont

mBio

Volumn 7, Issue 6, 2016, Pages

  Bennuru, Sasisekhar ^a   Cotton, James A ^b   Ribeiro, Jose M C ^a   Grote, Alexandra ^c   Harsha, Bhavana ^b   Holroyd, Nancy ^b   Mhashilkar, Amruta ^d   Molina, Douglas M ^e   Randall, Arlo Z ^e   Shandling, Adam D ^e   Unnasch, Thomas R ^d   Ghedin, Elodie ^c   Berriman, Matthew ^b   Lustigman, Sara ^f   Nutman, Thomas B ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e Antigen Discovery Inc   (United States)

^f NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PROTEOME; TRANSCRIPTOME;

ADAPTATION; ADULT; ARTICLE; CONTROLLED STUDY; ENDOSYMBIONT; FEMALE; GENE SEQUENCE; HOST PARASITE INTERACTION; MALE; MOLTING; NONHUMAN; ONCHOCERCA VOLVULUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; RNA ANALYSIS; RNA SEQUENCE; TRANSCRIPTOMICS; WOLBACHIA; ANIMAL; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; SYMBIOSIS;

ANIMALS; ONCHOCERCA VOLVULUS; PROTEOME; SYMBIOSIS; TRANSCRIPTOME; WOLBACHIA;

EID: 85007550882     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02028-16     Document Type: Article

References (65)

1. Hotez PJ, Alvarado M, Basáñez MG, Bolliger I, Bourne R, Boussinesq M, Brooker SJ, Brown AS, Buckle G, Budke CM, Carabin H, Coffeng LE, Fèvre EM, Fürst T, Halasa YA, Jasrasaria R, Johns NE, Keiser J, King CH, Lozano R, Murdoch ME, O’Hanlon S, Pion SD, Pullan RL, Ramaiah KD, Roberts T, Shepard DS, Smith JL, Stolk WA, Undurraga EA, Utzinger J, Wang M, Murray CJ, Naghavi M. 2014. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis 8: e2865. http://dx.doi.org/10.1371/journal.pntd.0002865.
2. WHO. 2016. Investing to overcome the global impact of neglected tropical diseases: thirdWHOreport on negelected tropical diseases. World Health Organization, Geneva, Switzerland.
3. Centers for Disease Control and Prevention (CDC). 2013. Progress toward elimination of onchocerciasis in the Americas-1993-2012. MMWR Morb Mortal Wkly Rep 62: 405-408. https://www.cdc.gov/ mmwr/preview/mmwrhtml/mm6220a4.htm.
4. WHO. 2014. African programme for onchocerciasis control: progress report, 2013-2014. Wkly Epidemiol Rec 89: 551-560.
5. Keenan JD, Hotez PJ, Amza A, Stoller NE, Gaynor BD, Porco TC, Lietman TM. 2013. Elimination and eradication of neglected tropical diseases with mass drug administrations: a survey of experts. PLoS Negl Trop Dis 7: e2562. http://dx.doi.org/10.1371/journal.pntd.0002562.
6. Kim YE, Remme JH, Steinmann P, Stolk WA, Roungou JB, Tediosi F. 2015. Control, elimination, and eradication of river blindness: scenarios, timelines, and ivermectin treatment needs in Africa. PLoS Negl Trop Dis 9: e0003664. http://dx.doi.org/10.1371/journal.pntd.0003664.
7. Gardon J, Gardon-Wendel N, Demanga-Ngangue N, Kamgno J, Chippaux JP, Boussinesq M. 1997. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350: 18-22. http://dx.doi.org/10.1016/S0140-6736(96)11094-1.
8. Lustigman S, McCarter JP. 2007. Ivermectin resistance in Onchocerca volvulus: toward a genetic basis. PLoS Negl Trop Dis 1: e76. http:// dx.doi.org/10.1371/journal.pntd.0000076.
9. Cotton JA, Bennuru S, Grote A, Harsha B, Tracey A, Beech R, Doyle SR, Dunn M, Hotopp JCD, Holroyd N, Kikuchi T, Lambert O, Mhashilkar AS, Mutowo P, Nursimulu N, Ribeiro JM, Rogers MB, Stanley E, Swapna LS, Tsai IJ, Unnasch TR, Voronin D, Parkinson J, Nutman TB, Ghedin E, Berriman M, Lustigman S. The genome of Onchocerca volvulus, agent of river blindness. Nat Microbiol, in press.
10. Neafie RC. 1972. Morphology of Onchocerca volvulus. Am J Clin Pathol 57: 574-586. http://dx.doi.org/10.1093/ajcp/57.5.574.
11. Ning K, Fermin D, Nesvizhskii AI. 2012. Comparative analysis of different label-free mass spectrometry based protein abundance estimates and their correlation with RNA-Seq gene expression data. J Proteome Res 11: 2261-2271. http://dx.doi.org/10.1021/pr201052x.
12. Vogel C, Marcotte EM. 2012. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13: 227-232. http://dx.doi.org/10.1038/nrg3185.
13. Ortiz MA, Noble D, Sorokin EP, Kimble J. 2014. A new dataset of spermatogenic vs. oogenic transcriptomes in the nematode Caenorhabditis elegans. G3 (Bethesda) 4: 1765-1772. http://dx.doi.org/10.1534/ g3.114.012351.
14. Depledge DP, Lower RP, Smith DF. 2007. RepSeq-a database of amino acid repeats present in lower eukaryotic pathogens. BMC Bioinformatics 8: 122. http://dx.doi.org/10.1186/1471-2105-8-122.
15. Brignull HR, Morley JF, Garcia SM, Morimoto RI. 2006. Modeling polyglutamine pathogenesis in C. elegans. Methods Enzymol 412: 256-282. http://dx.doi.org/10.1016/S0076-6879(06)12016-9.
16. Hess JA, Zhan B, Bonne-Année S, Deckman JM, Bottazzi ME, Hotez PJ, Klei TR, Lustigman S, Abraham D. 2014. Vaccines to combat river blindness: expression, selection and formulation of vaccines against infection with Onchocerca volvulus in a mouse model. Int J Parasitol 44: 637-646. http://dx.doi.org/10.1016/j.ijpara.2014.04.006.
17. Arumugam S, Wei J, Liu Z, Abraham D, Bell A, Bottazzi ME, Hotez PJ, Zhan B, Lustigman S, Klei TR. 2016. Vaccination of gerbils with Bm-103 and Bm-RAL-2 concurrently or as a fusion protein confers consistent and improved protection against Brugia malayi infection. PLoS Negl Trop Dis 10: e0004586. http://dx.doi.org/10.1371/journal.pntd.0004586.
18. Lustigman S, Zhang J, Liu J, Oksov Y, Hashmi S. 2004. RNA interference targeting cathepsin L and Z-like cysteine proteases of Onchocerca volvulus confirmed their essential function during L3 molting. Mol Biochem Parasitol 138: 165-170. http://dx.doi.org/10.1016/j.molbiopara.2004.08.003.
19. Lustigman S, McKerrow JH, Shah K, Lui J, Huima T, Hough M, Brotman B. 1996. Cloning of a cysteine protease required for the molting of Onchocerca volvulus third stage larvae. J Biol Chem 271: 30181-30189. http://dx.doi.org/10.1074/jbc.271.47.30181.
20. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335. http://dx.doi.org/10.1101/ gr.073585.107.
21. Wu Y, Egerton G, Underwood AP, Sakuda S, Bianco AE. 2001. Expression and secretion of a larval-specific chitinase (family 18 glycosyl hydrolase) by the infective stages of the parasitic nematode, Onchocerca volvulus. J Biol Chem 276: 42557-42564. http://dx.doi.org/10.1074/ jbc.M103479200.
22. Guiliano DB, Hong X, McKerrow JH, Blaxter ML, Oksov Y, Liu J, Ghedin E, Lustigman S. 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. http:// dx.doi.org/10.1016/j.molbiopara.2004.03.015.
23. Ford L, Zhang J, Liu J, Hashmi S, Fuhrman JA, Oksov Y, Lustigman S. 2009. Functional analysis of the cathepsin-like cysteine protease genes in adult Brugia malayi using RNA interference. PLoS Negl Trop Dis 3: e377. http://dx.doi.org/10.1371/journal.pntd.0000377.
24. Song C, Gallup JM, Day TA, Bartholomay LC, Kimber MJ. 2010. Development of an in vivo RNAi protocol to investigate gene function in the filarial nematode, Brugia malayi. PLoS Pathog 6: e1001239. http:// dx.doi.org/10.1371/journal.ppat.1001239.
25. Taylor CM, Martin J, Rao RU, Powell K, Abubucker S, Mitreva M. 2013. Using existing drugs as leads for broad spectrum anthelmintics targeting protein kinases. PLoS Pathog 9: e1003149. http://dx.doi.org/10.1371/journal.ppat.1003149.
26. Manning G. 2005. Genomic overview of protein kinases. WormBook 13: 1-19. http://dx.doi.org/10.1895/wormbook.1.60.1.
27. Sluder AE, Maina CV. 2001. Nuclear receptors in nematodes: themes and variations. Trends Genet 17: 206-213. http://dx.doi.org/10.1016/S0168-9525(01)02242-9.
28. Tzertzinis G, Egaña AL, Palli SR, Robinson-Rechavi M, Gissendanner CR, Liu C, Unnasch TR, Maina CV. 2010. Molecular evidence for a functional ecdysone signaling system in Brugia malayi. PLoS Negl Trop Dis 4: e625. http://dx.doi.org/10.1371/journal.pntd.0000625.
29. Mhashilkar AS, Adapa SR, Jiang RH, Williams SA, Zaky W, Slatko BE, Luck AN, Moorhead AR, Unnasch TR. 2016. Phenotypic and molecular analysis of the effect of 20-hydroxyecdysone on the human filarial parasite Brugia malayi. Int J Parasitol 46: 333-341 http://dx.doi.org/10.1016/ j.ijpara.2016.01.005.
30. Triteeraprapab S, Richie TL, Tuan RS, Shepley KJ, Dinman JD, Neubert TA, Scott AL. 1995. Molecular cloning of a gene expressed during early embryonic development in Onchocerca volvulus. Mol Biochem Parasitol 69: 161-171. http://dx.doi.org/10.1016/0166-6851(94)00187-R.
31. Tume C, Sun E, Titanji V, Bathurst I, Barr P, Hough M, Weiss N, Chakravarti B, Wahi M, Lackey A, Staunton C, Lustigman S, McKerrow JH. 1995. Onchocerca volvulus: identification and characterization of an immunogenic eggshell protein (Oveg1). Exp Parasitol 81: 445-452. http:// dx.doi.org/10.1006/expr.1995.1137.
32. Fisk Green R, Lorson M, Walhout AJ, Vidal M, van den Heuvel S. 2004. Identification of critical domains and putative partners for the Caenorhabditis elegans spindle component LIN-5. Mol Genet Genomics 271: 532-544. http://dx.doi.org/10.1007/s00438-004-1012-x.
33. Harnett W. 2014. Secretory products of helminth parasites as immunomodulators. Mol Biochem Parasitol 195: 130-136. http://dx.doi.org/10.1016/j.molbiopara.2014.03.007.
34. McKerrow JH, Caffrey C, Kelly B, Loke P, Sajid M. 2006. Proteases in parasitic diseases. Annu Rev Pathol 1: 497-536. http://dx.doi.org/10.1146/ annurev.pathol.1.110304.100151.
35. Hartmann S, Lucius R. 2003. Modulation of host immune responses by nematode cystatins. Int J Parasitol 33: 1291-1302. http://dx.doi.org/10.1016/S0020-7519(03)00163-2.
36. Ford L, Guiliano DB, Oksov Y, Debnath AK, Liu J, Williams SA, Blaxter ML, Lustigman S. 2005. Characterization of a novel filarial serine protease inhibitor, Ov-SPI-1, from Onchocerca volvulus, with potential multifunctional roles during development of the parasite. J Biol Chem 280: 40845-40856. http://dx.doi.org/10.1074/jbc.M504434200.
37. Maizels RM, Gomez-Escobar N, Gregory WF, Murray J, Zang X. 2001. Immune evasion genes from filarial nematodes. Int J Parasitol 31: 889-898. http://dx.doi.org/10.1016/S0020-7519(01)00213-2.
38. Gooyit M, Tricoche N, Lustigman S, Janda KD. 2014. Dual protonophore-chitinase inhibitors dramatically affect O. volvulus molting. J Med Chem 57: 5792-5799. http://dx.doi.org/10.1021/jm5006435.
39. Gloeckner C, Garner AL, Mersha F, Oksov Y, Tricoche N, Eubanks LM, Lustigman S, Kaufmann GF, Janda KD. 2010. Repositioning of an existing drug for the neglected tropical disease onchocerciasis. Proc Natl Acad Sci U S A 107: 3424-3429. http://dx.doi.org/10.1073/pnas.0915125107.
40. Gill AC, Darby AC, Makepeace BL. 2014. Iron necessity: the secret of Wolbachia’s success? PLoS Negl Trop Dis 8: e3224. http://dx.doi.org/10.1371/journal.pntd.0003224.
41. Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza Lima S, Bandi C, Wanji S, Diagne M, Casiraghi M. 2011. New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS One 6: e20843. http://dx.doi.org/10.1371/journal.pone.0020843.
42. Hoerauf A, Nissen-Pähle K, Schmetz C, Henkle-Dührsen K, Blaxter ML, Büttner DW, Gallin MY, Al-Qaoud KM, Lucius R, Fleischer B. 1999. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103: 11-18. http://dx.doi.org/10.1172/JCI4768.
43. Bandi C, McCall JW, Genchi C, Corona S, Venco L, Sacchi L. 1999. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29: 357-364. http://dx.doi.org/10.1016/S0020-7519(98)00200-8.
44. Langworthy NG, Renz A, Mackenstedt U, Henkle-Dührsen K, de Bronsvoort MB, Tanya VN, Donnelly MJ, Trees AJ. 2000. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc Biol Sci 267: 1063-1069. http://dx.doi.org/10.1098/rspb.2000.1110.
45. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, Kay SM, Koldkjær P, Rainbow L, Radford AD, Blaxter ML, Tanya VN, Trees AJ, Cordaux R, Wastling JM, Makepeace BL. 2012. Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 22: 2467-2477. http://dx.doi.org/10.1101/gr.138420.112.
46. Bennuru S, Meng Z, Ribeiro JM, Semnani RT, Ghedin E, Chan K, Lucas DA, Veenstra TD, Nutman TB. 2011. Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proc Natl Acad Sci U S A 108: 9649-9654. http:// dx.doi.org/10.1073/pnas.1011481108.
47. Slatko BE, Luck AN, Dobson SL, Foster JM. 2014. Wolbachia endosymbionts and human disease control. Mol Biochem Parasitol 195: 88-95. http://dx.doi.org/10.1016/j.molbiopara.2014.07.004.
48. Driguez P, Doolan DL, Loukas A, Felgner PL, McManus DP. 2010. Schistosomiasis vaccine discovery using immunomics. Parasit Vectors 3: 4. http://dx.doi.org/10.1186/1756-3305-3-4.
49. Gaze S, Driguez P, Pearson MS, Mendes T, Doolan DL, Trieu A, McManus DP, Gobert GN, Periago MV, Correa Oliveira R, Cardoso FC, Oliveira G, Nakajima R, Jasinskas A, Hung C, Liang L, Pablo J, Bethony JM, Felgner PL, Loukas A. 2014. An immunomics approach to schistosome antigen discovery: antibody signatures of naturally resistant and chronically infected individuals from endemic areas. PLoS Pathog 10: e1004033. http://dx.doi.org/10.1371/journal.ppat.1004033.
50. Tang YT, Gao X, Rosa BA, Abubucker S, Hallsworth-Pepin K, Martin J, Tyagi R, Heizer E, Zhang X, Bhonagiri-Palsikar V, Minx P, Warren WC, Wang Q, Zhan B, Hotez PJ, Sternberg PW, Dougall A, Gaze ST, Mulvenna J, Sotillo J, Ranganathan S, Rabelo EM, Wilson RK, Felgner PL, Bethony J, Hawdon JM, Gasser RB, Loukas A, Mitreva M. 2014. Genome of the human hookworm Necator americanus. Nat Genet 46: 261-269. http://dx.doi.org/10.1038/ng.2875.
51. Elson LH, Guderian RH, Araujo E, Bradley JE, Days A, Nutman TB. 1994. Immunity to onchocerciasis: identification of a putatively immune population in a hyperendemic area of Ecuador. J Infect Dis 169: 588-594. http://dx.doi.org/10.1093/infdis/169.3.588.
52. Ward DJ, Nutman TB, Zea-Flores G, Portocarrero C, Lujan A, Ottesen EA. 1988. Onchocerciasis and immunity in humans: enhanced T cell responsiveness to parasite antigen in putatively immune individuals. J Infect Dis 157: 536-543. http://dx.doi.org/10.1093/infdis/157.3.536.
53. MacDonald AJ, Turaga PS, Harmon-Brown C, Tierney TJ, Bennett KE, McCarthy MC, Simonek SC, Enyong PA, Moukatte DW, Lustigman S. 2002. Differential cytokine and antibody responses to adult and larval stages of Onchocerca volvulus consistent with the development of concomitant immunity. Infect Immun 70: 2796-2804. http://dx.doi.org/10.1128/ IAI.70.6.2796-2804.2002.
54. Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A. 2010. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 8: 814-826. http://dx.doi.org/10.1038/ nrmicro2438.
55. Makepeace BL, Babayan SA, Lustigman S, Taylor DW. 2015. The case for vaccine development in the strategy to eradicate river blindness (onchocerciasis) from Africa. Expert Rev Vaccines 14: 1163-1165. http:// dx.doi.org/10.1586/14760584.2015.1059281.
56. Weil GJ, Ogunrinade AF, Chandrashekar R, Kale OO. 1990. IgG4 subclass antibody serology for onchocerciasis. J Infect Dis 161: 549-554. http://dx.doi.org/10.1093/infdis/161.3.549.
57. Kurniawan-Atmadja A, Sartono E, Partono F, Yazdanbakhsh M, Maizels R. 1998. Specificity of predominant IgG4 antibodies to adult and microfilarial stages of Brugia malayi. Parasite Immunol 20: 155-162.
58. Armstrong SD, Xia D, Bah GS, Krishna R, Ngangyung HF, LaCourse EJ, McSorley HJ, Kengne-Ouafo JA, Chounna-Ndongmo PW, Wanji S, Enyong PA, Taylor DW, Blaxter ML, Wastling JM, Tanya VN, Makepeace BL. 2016. Stage-specific proteomes from Onchocerca ochengi, sister species of the human river blindness parasite, uncover adaptations to a nodular lifestyle. Mol Cell Proteomics 15: 2554-2575 http://dx.doi.org/10.1074/mcp.M115.055640.
59. +-dependent immunity to Onchocerca volvulus third-stage larvae in humans and the mouse vaccination model: common ground and distinctions. Int J Parasitol 33: 1161-1171. http://dx.doi.org/10.1016/S0020-7519(03)00170-X.
60. Turaga PS, Tierney TJ, Bennett KE, McCarthy MC, Simonek SC, Enyong PA, Moukatte DW, Lustigman S. 2000. Immunity to onchocerciasis: cells from putatively immune individuals produce enhanced levels of interleukin-5, gamma interferon, and granulocytemacrophage colony-stimulating factor in response to Onchocerca volvulus larval and male worm antigens. Infect Immun 68: 1905-1911. http:// dx.doi.org/10.1128/IAI.68.4.1905-1911.2000.
61. Lustigman S, Huima T, Brotman B, Miller K, Prince AM. 1990. Onchocerca volvulus: biochemical and morphological characteristics of the surface of third-and fourth-stage larvae. Exp Parasitol 71: 489-495. http://dx.doi.org/10.1016/0014-4894(90)90075-N.
62. Taylor DW, Goddard JM, McMahon JE. 1984. Isolation and purification of microfilariae from nodules of Onchocerca volvulus. Trans R Soc Trop Med Hyg 78: 707-708. http://dx.doi.org/10.1016/0035-9203(84)90255-4.
63. Medina-De la Garza CE, Brattig NW, Tischendorf FW. 1987. Rapid method for the purification of viable microfilariae from nodules of Onchocerca volvulus by Percoll gradient centrifugation. Trop Med Parasitol 38: 53-54.
64. Ribeiro JM, Schwarz A, Francischetti IM. 2015. A deep insight into the sialotranscriptome of the Chagas disease vector, Panstrongylus megistus (Hemiptera: Heteroptera). J Med Entomol 52: 351-358. http://dx.doi.org/10.1093/jme/tjv023.
65. Burbelo PD, Ching KH, Klimavicz CM, Iadarola MJ. 2009. Antibody profiling by luciferase immunoprecipitation systems (LIPS). J Vis Exp http://dx.doi.org/10.3791/1549.