Abstract
Parasites including helminthes, protozoa, and medical arthropod vectors are a major cause of global infectious diseases, affecting one-sixth of the world’s population, which are responsible for enormous levels of morbidity and mortality important and remain impediments to economic development especially in tropical countries. Prevalent drug resistance, lack of highly effective and practical vaccines, as well as specific and sensitive diagnostic markers are proving to be challenging problems in parasitic disease control in most parts of the world. The impressive progress recently made in genome-wide analysis of parasites of medical importance, including trematodes of Clonorchis sinensis, Opisthorchis viverrini, Schistosoma haematobium, S. japonicum, and S. mansoni; nematodes of Brugia malayi, Loa loa, Necator americanus, Trichinella spiralis, and Trichuris suis; cestodes of Echinococcus granulosus, E. multilocularis, and Taenia solium; protozoa of Babesia bovis, B. microti, Cryptosporidium hominis, Eimeria falciformis, E. histolytica, Giardia intestinalis, Leishmania braziliensis, L. donovani, L. major, Plasmodium falciparum, P. vivax, Trichomonas vaginalis, Trypanosoma brucei and T. cruzi; and medical arthropod vectors of Aedes aegypti, Anopheles darlingi, A. sinensis, and Culex quinquefasciatus, have been systematically covered in this review for a comprehensive understanding of the genetic information contained in nuclear, mitochondrial, kinetoplast, plastid, or endosymbiotic bacterial genomes of parasites, further valuable insight into parasite-host interactions and development of promising novel drug and vaccine candidates and preferable diagnostic tools, thereby underpinning the prevention and control of parasitic diseases.
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References
Alemayehu S, Feghali KC, Cowden J et al (2013) Comparative evaluation of published real-time PCR assays for the detection of malaria following MIQE guidelines. Malar J 12:277
Alvarez VE, Niemirowicz GT, Cazzulo JJ (2012) The peptidases of Trypanosoma cruzi: digestive enzymes, virulence factors, and mediators of autophagy and programmed cell death. Biochim Biophys Acta 1824(1):195–206
Andersson JO, Sjögren AM, Davis LA et al (2013) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13(2):94–104
Arensburger P, Megy K, Waterhouse RM et al (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330(6000):86–88
Baig S, Damian RT, Morales-Montor J, Ghaleb A et al (2006) Protection from murine cysticercosis by immunization with a parasite cysteine protease. Microbes Infect 8(12–13):2733–2735
Baker N, de Koning HP, Mäser P et al (2013) Drug resistance in African trypanosomiasis: the melarsoprol and pentamidine story. Trends Parasitol 29(3):110–118
Barry JD, McCulloch R (2001) Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv Parasitol 49:1–70
Berriman M, Ghedin E, Hertz-Fowler C et al (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309(5733):416–422
Berriman M, Haas BJ, LoVerde PT et al (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460(7253):352–358
Blaxter ML, De Ley P, Garey JR et al (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392(6671):71–75
Botelho MC, Machado JC, da Costa JM (2010) Schistosoma haematobium and bladder cancer: what lies beneath? Virulence 1(2):84–87
Bouzid M, Hunter PR, Chalmers RM et al (2013) Cryptosporidium pathogenicity and virulence. Clin Microbiol Rev 26(1):115–134
Brayton KA, Lau AO, Herndon DR et al (2007) Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 3(10):1401–1413
Buscaglia CA, Campo VA, Frasch AC et al (2006) Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol 4(3):229–236
Cardoso FC, Pacífico RN, Mortara RA et al (2006) Human antibody responses of patients living in endemic areas for schistosomiasis to the tegumental protein Sm29 identified through genomic studies. Clin Exp Immunol 144(3):382–391
Cardoso FC, Macedo GC, Gava E et al (2008) Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2(10):e308
Carlton JM, Hirt RP, Silva JC et al (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315(5809):207–212
Carlton JM, Adams JH, Silva JC et al (2008) Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455(7214):757–763
Chantree P, Phatsara M, Meemon K et al (2013) Vaccine potential of recombinant cathepsin B against Fasciola gigantica. Exp Parasitol 135(1):102–109
Chilton NB, Huby-Chilton F, Gasser RB et al (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Mol Phylogenet Evol 40(1):118–128
Cornillot E, Hadj-Kaddour K, Dassouli A et al (2012) Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Res 40(18):9102–9114
Correa PR (2013) Genetic structure and expression of the surface glycoprotein GP82, the main adhesin of Trypanosoma cruzi metacyclic trypomastigotes. Sci World J 2013:156734
Dasgupta SS, Aghazadeh-Dibavar BM (2014) The role of toll-like receptor agonists in the immunotherapy of leishmaniosis. An update and proposal for a new form of anti-leishmanial therapy. Ann Parasitol 60(2):75–82
De Pablos LM, Osuna A (2012) Multigene families in Trypanosoma cruzi and their role in infectivity. Infect Immun 80(7):2258–2264
Desjardins CA, Cerqueira GC, Goldberg JM et al (2013) Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nat Genet 45(5):495–500
Downing T, Imamura H, Decuypere S et al (2011) Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res 21(12):2143–2156
El-Sayed NM, Myler PJ, Blandin G et al (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309(5733):404–409
Esteban JG, Muñoz-Antoli C, Toledo R et al (2014) Diagnosis of human trematode infections. Adv Exp Med Biol 766:293–327
Flegontov P, Gray MW, Burger G et al (2011) Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr Genet 57(4):225–232
Flick K, Chen Q (2004) var genes, PfEMP1 and the human host. Mol Biochem Parasitol 134(1):3–9
Frand AR, Russel S, Ruvkun G (2005) Functional genomic analysis of C. elegans molting. PLoS Biol 3(10):e312
Franzén O, Jerlström-Hultqvist J, Castro E et al (2009) Draft genome sequencing of Giardia intestinalis assemblage B Isolate GS: is human giardiasis caused by two different species? PLoS Pathog 5(8):e1000560
Gardner MJ, Hall N, Fung E et al (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419(6906):498–511
Ghedin E, Wang S, Spiro D et al (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317(5845):1756–1760
Gleeson MT (2000) The plastid in Apicomplexa: what use is it? Int J Parasitol 30(10):1053–1070
Greenberg RM (2013) New approaches for understanding mechanisms of drug resistance in schistosomes. Parasitology 140(12):1534–1546
Harnett W (2014) Secretory products of helminth parasites as immunomodulators. Mol Biochem Parasitol 195(2):130–136
Heitlinger E, Spork S, Lucius R et al (2014) The genome of Eimeria falciformis—reduction and specialization in a single host apicomplexan parasite. BMC Genomics 15(1):696
Hillyer GV (2005) Fasciola antigens as vaccines against fascioliasis and schistosomiasis. J Helminthol 79(3):241–247
Horn D, Duraisingh MT (2014) Duraisingh, antiparasitic chemotherapy: from genomes to mechanisms. Annu Rev Pharmacol Toxicol 54(1):71–94
Hu PJ (2007) Dauer. WormBook:1–19
Hu W, Yan Q, Shen DK et al (2003) Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nat Genet 35(2):139–147
Ivens AC, Peacock CS, Worthey EA et al (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309(5733):436–442
Jensen RE, Englund PT (2012) Network news: the replication of kinetoplast DNA. Annu Rev Microbiol 66:473–491
Jerlström-Hultqvist J, Franzén O, Ankarklev J et al (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11:543
Jex AR, Littlewood DT, Gasser RB (2010) Toward next-generation sequencing of mitochondrial genomes—focus on parasitic worms of animals and biotechnological implications. Biotechnol Adv 28(1):151–159
Jex AR, Nejsum P, Schwarz EM et al (2014) Genome and transcriptome of the porcine whipworm Trichuris suis. Nat Genet 46(7):701–706
Kissoon-Singh VL, Mortimer CK (2011) Entamoeba histolytica cathepsin-like enzymes: interactions with the host gut. Adv Exp Med Biol 712:62–83
Knapp J, Millon L, Mouzon L et al (2014) Real time PCR to detect the environmental faecal contamination by Echinococcus multilocularis from red fox stools. Vet Parasitol 201(1–2):40–47
Kolev NG, Tschudi C, Ullu E (2011) RNA interference in protozoan parasites: achievements and challenges. Eukaryot Cell 10(9):1156–1163
Kotewong R, Duangkaew P, Srisook E et al (2014) Structure–function relationships of inhibition of mosquito cytochrome P450 enzymes by flavonoids of Andrographis paniculata. Parasitol Res 113(9):3381–3392
Kumar A, Kumar K, Korde R et al (2007) Falcipain-1, a Plasmodium falciparum cysteine protease with vaccine potential. Infect Immun 75(4):2026–2034
Landmann F, Foster JM, Slatko BE et al (2012) Efficient in vitro RNA interference and immunofluorescence-based phenotype analysis in a human parasitic nematode, Brugia malayi. Parasit Vectors 5:16
Lee JS, Kim IS, Sohn WM et al (2006) A DNA vaccine encoding a fatty acid-binding protein of Clonorchis sinensis induces protective immune response in Sprague-Dawley rats. Scand J Immunol 63(3):169–176
Lee J, Kim JH, Sohn HJ et al (2014) Novel cathepsin B and cathepsin B-like cysteine protease of Naegleria fowleri excretory-secretory proteins and their biochemical properties. Parasitol Res 113(8):2765–2776
Loftus B, Anderson I, Davies R et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433(7028):865–868
Lorenzi H, Thiagarajan M, Haas B et al (2008) Genome wide survey, discovery and evolution of repetitive elements in three Entamoeba species. BMC Genomics 9:595
Lukes J, Hashimi H, Zíková A (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48(5):277–299
Marinotti O, Cerqueira GC, de Almeida LG et al (2013) The genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res 41(15):7387–7400
Mather MW, Henry KW, Vaidya AB (2007) Mitochondrial drug targets in apicomplexan parasites. Curr Drug Targets 8(1):49–60
McNulty SN, Mullin AS, Vaughan JA et al (2012) Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species. BMC Genomics 13:145
Mendes TA, Reis Cunha JL, de Almeida LR et al (2013) Identification of strain-specific B-cell epitopes in Trypanosoma cruzi using genome-scale epitope prediction and high-throughput immunoscreening with peptide arrays. PLoS Negl Trop Dis 7(10):e2524
Mitreva M, Jasmer DP, Zarlenga DS et al (2011) The draft genome of the parasitic nematode Trichinella spiralis. Nat Genet 43(3):228–235
Naya H, Romero H, Zavala A et al (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55(3):260–264
Nene V, Wortman JR, Lawson D et al (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316(5832):1718–1823
Nixon JE, Wang A, Field J et al (2002) Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 1(2):181–190
Opperdoes FR, Coombs GH (2007) Metabolism of Leishmania: proven and predicted. Trends Parasitol 23(4):149–158
Pakpour N, Camp L, Smithers HM et al (2013) Protein kinase C-dependent signaling controls the midgut epithelial barrier to malaria parasite infection in anopheline mosquitoes. PLoS One 8(10):e76535
Peacock CS, Seeger K, Harris D et al (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39(7):839–847
Poulin R, Randhawa HS (2013) Evolution of parasitism along convergent lines: from ecology to genomics. Parasitology 1–10
Povelones ML (2014) Beyond replication: division and segregation of mitochondrial DNA in kinetoplastids. Mol Biochem Parasitol 196(1):53–60
Rana AK, Misra-Bhattacharya S (2013) Current drug targets for helminthic diseases. Parasitol Res 112(5):1819–1831
Ricciardi A, Ndao M (2014) Diagnosis of parasitic infections: What’s going on? J Biomol Screen
Robertson AP, Martin RJ (2007) Ion-channels on parasite muscle: pharmacology and physiology. Invert Neurosci 7(4):209–217
Robinson MW, Dalton JP, Donnelly S (2008) Helminth pathogen cathepsin proteases: it’s a family affair. Trends Biochem Sci 33(12):601–608
Rocha DA, de Andrade RI, de Souza W et al (2014) Evaluation of the effect of miltefosine on Trichomonas vaginalis. Parasitol Res 113(3):1041–1047
Rollend L, Bent SJ, Krause PJ et al (2013) Quantitative PCR for detection of Babesia microti in Ixodes scapularis ticks and in human blood. Vector Borne Zoonotic Dis 13(11):784–790
Ruppel A, Chlichlia K, Bahgat M (2004) Invasion by schistosome cercariae: neglected aspects in Schistosoma japonicum. Trends Parasitol 20(9):397–400
Scott AL, Ghedin E, Nutman TB et al (2012) Filarial and Wolbachia genomics. Parasite Immunol 34:121–129
Sistrom M, Evans B, Bjornson R et al (2014) Comparative genomics reveals multiple genetic backgrounds of human pathogenicity in the Trypanosoma brucei complex. Genome Biol Evol 6(10):2811–2819
Skuce PJ, Redmond DL, Liddell S et al (1999) Molecular cloning and characterization of gut-derived cysteine proteinases associated with a host protective extract from Haemonchus contortus. Parasitology 119(Pt4):405–412
Sor-Suwan S, Jariyapan N, Roytrakul S et al (2013) Salivary gland proteome of the human malaria vector, Anopheles campestris-like (Diptera: Culicidae). Parasitol Res 112(3):1065–1075
Tang YT, Gao X, Rosa BA et al (2014) Genome of the human hookworm Necator americanus. Nat Genet 46(3):261–269
Taylor MJ, Bandi C, Hoerauf A (2005) Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 60:245–284
Taylor CM, Fischer K, Abubucker S et al (2011) Targeting protein-protein interactions for parasite control. PLoS One 6(4):e18381
Tendler M, Vilar MM, Brito CA et al (1995) Vaccination against schistosomiasis and fascioliasis with the new recombinant antigen Sm14: potential basis of a multi-valent anti-helminth vaccine? Mem Inst Oswaldo Cruz 90(2):255–256
Tiengwe C, Marques CA, McCulloch R (2014) Nuclear DNA replication initiation in kinetoplastid parasites: new insights into an ancient process. Trends Parasitol 30(1):227–236
Toubarro D, Lucena-Robles M, Nascimento G et al (2010) Serine protease-mediated host invasion by the parasitic nematode Steinernema carpocapsae. J Biol Chem 285(40):30666–30675
Tsai IJ, Zarowiecki M, Holroyd N et al (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496(7443):57–63
Tschoeke DA, Nunes GL, Jardim R et al (2014) The comparative genomics and phylogenomics of Leishmania amazonensis parasite. Evol Bioinform Online 10:131–153
Vaidya AB, Mather MW (2009) Mitochondrial evolution and functions in malaria parasites. Annu Rev Microbiol 63:249–267
van Dijk MR, Douradinha B, Franke-Fayard B et al (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci U S A 102(34):12194–12199
Verweij JJ, Blangé RA, Templeton K et al (2004) Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 42(3):1220–1223
Villa-Mancera A, Reynoso-Palomar A, Utrera-Quintana F et al (2014) Cathepsin L1 mimotopes with adjuvant Quil A induces a Th1/Th2 immune response and confers significant protection against Fasciola hepatica infection in goats. Parasitol Res 113(1):243–250
Walker AJ, Ressurreição M, Rothermel R (2014) Exploring the function of protein kinases in schistosomes: perspectives from the laboratory and from comparative genomics. Front Genet 5:229
Wang X, Chen W, Huang Y et al (2011a) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol 12(10):R107
Wang J, Czech B, Crunk A et al (2011b) Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res 21(9):1462–1477
Wijayawardena BK, Minchella DJ, DeWoody JA (2013) Hosts, parasites, and horizontal gene transfer. Trends Parasitol 29(7):329–338
Winston WM, Molodowitch C, Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295(5564):2456–2459
Wongsrichanalai C, Sibley CH (2013) Fighting drug-resistant Plasmodium falciparum: the challenge of artemisinin resistance. Clin Microbiol Infect 19(10):908–916
Xu P, Widmer G, Wang Y et al (2004) The genome of Cryptosporidium hominis. Nature 431(7012):1107–1112
Yan HB, Lou ZZ, Li L et al (2014) Genome-wide analysis of regulatory proteases sequences identified through bioinformatics data mining in Taenia solium. BMC Genomics 15:428
Young ND, Jex AR, Li B et al (2012) Whole-genome sequence of Schistosoma haematobium. Nat Genet 44(2):221–225
Young ND, Nagarajan N, Lin SJ et al (2014) The Opisthorchis viverrini genome provides insights into life in the bile duct. Nat Commun 5:4378
Zhang H, Pompey JM, Singh U (2011) RNA interference in Entamoeba histolytica: implications for parasite biology and gene silencing. Future Microbiol 6(1):103–117
Zhang C, Wang L, Wang H et al (2014) Identification and characterization of functional Smad8 and Smad4 homologues from Echinococcus granulosus. Parasitol Res 113(10):3745–3757
Zheng H, Zhang W, Zhang L et al (2013) The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet 45(10):1168–1175
Zhou Y, Zheng H, Chen Y et al (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460(7253):345–351
Zhou D, Zhang D, Ding G et al (2014) Genome sequence of Anopheles sinensis provides insight into genetics basis of mosquito competence for malaria parasites. BMC Genomics 15:42
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This work was supported by grants from the National Basic Research Program of China (grant no. 2010CB530004), the National Natural Science Foundation of China (grant no. 81371836, 30771888, 81271855, and 30800966), the 111 Project (grant no. B12003), the Undergraduates Innovation Training Program of Guangdong Province (201410558274), and the Research Fund for Students of Sun Yat-sen University (2012–2014).
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Zhiyue Lv, Zhongdao Wu, and Limei Zhang are joint first authors.
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Lv, Z., Wu, Z., Zhang, L. et al. Genome mining offers a new starting point for parasitology research. Parasitol Res 114, 399–409 (2015). https://doi.org/10.1007/s00436-014-4299-5
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DOI: https://doi.org/10.1007/s00436-014-4299-5