New research tools for urogenital schistosomiasis

Journal of Infectious Diseases

Volumn 211, Issue 6, 2015, Pages 861-869

  Rinaldi, Gabriel ^a   Young, Neil D ^d   Honeycutt, Jared D ^b   Brindley, Paul J ^a   Gasser, Robin B ^d,e   Hsieh, Michael H ^c,f  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b STANFORD UNIVERSITY   (United States)

^c BIOMEDICAL RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e Inst Parasitol and Trop Vet Med   (Germany)

^f CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

bladder; genomics; Schistosoma; Schistosoma haematobium; Schistosomiasis; urogenital schistosomiasis.

Indexed keywords

VACCINE;

AFRICA SOUTH OF THE SAHARA; ANEMIA; ANIMAL MODEL; BLADDER CANCER; DRUG TARGETING; DYSURIA; FUNCTIONAL GENOMICS; GENETIC CONSERVATION; HEMATURIA; HOST PARASITE INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION CONTROL; MIXED INFECTION; NONHUMAN; PATHOGENESIS; PLATYHELMINTH; PREVALENCE; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMIASIS; SNAIL; STUNTING; UROGENITAL TRACT INFECTION; UROSEPSIS; ANIMAL; DISEASE MODEL; GENE; GENETICS; GENOMICS; MOLECULAR GENETICS; PARASITOLOGY; PATHOLOGY; SCHISTOSOMIASIS HAEMATOBIA;

ANIMALS; DISEASE MODELS, ANIMAL; GENES, HELMINTH; GENOMICS; HUMANS; MOLECULAR SEQUENCE ANNOTATION; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMIASIS HAEMATOBIA;

EID: 84924371197     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu527     Document Type: Review

References (61)

1. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest 2008; 118:1311-21
2. van der Werf MJ, de Vlas SJ, Brooker S, et al. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 2003; 86:125-139
3. Bedwani R, Renganathan E, El Kwhsky F, et al. Schistosomiasis and the risk of bladder cancer in Alexandria, Egypt. Br J Cancer 1998; 77:1186-9
4. Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 2012; 100:1-441
5. Kjetland EF, Ndhlovu PD, Mduluza T, et al. Simple clinical manifestations of genital Schistosoma haematobium infection in rural Zimbabwean women. Am J Trop Med Hyg 2005; 72:311-9
6. Young ND, Jex AR, Li B, et al. Whole-genome sequence of Schistosoma haematobium. Nat Genet 2012; 44:221-5
7. Rinaldi G, Okatcha TI, Popratiloff A, et al. Genetic manipulation of Schistosoma haematobium, the neglected schistosome. PLoS Negl Trop Dis 2011; 5:e1348
8. Celegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platformfor investigating biology. Science 1998; 282:2012-8
9. Li R, Fan W, Tian G, et al. The sequence and de novo assembly of the giant panda genome. Nature 2010; 463:311-7
10. Swain MT, Larkin DM, Caffrey CR, et al. Schistosoma comparative genomics: integrating genome structure, parasite biology and anthelmintic discovery. Trends Parasitol 2011; 27:555-64
11. Chuah C, Jones MK, Burke ML, et al. Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils. J Leukoc Biol 2013; 94:1-13
12. Defoin-Platel M, Hassani-Pak K, Rawlings C. Gaining confidence in cross-species annotation transfer: from simple molecular function to complex phenotypic traits. Asp Appl Biol 2011; 107:79-87
13. Zerlotini A, Aguiar ER, Yu F, et al. SchistoDB: an updated genome resource for the three key schistosomes of humans. Nucleic Acids Res 2013; 41:D728-31
14. Logan-Klumpler FJ, De Silva N, Boehme U, et al. GeneDB-an annotation database for pathogens. Nucleic Acids Res 2012; 40:D98-108
15. Mangiola S, Young ND, Korhonen P, et al. Getting the most out of parasitic helminth transcriptomes using HelmDB: implications for biology and biotechnology. Biotechnol Adv 2013; 31:1109-19
16. Caffrey CR, Rohwer A, Oellien F, et al. A comparative chemogenomics strategy to predict potential drug targets in the metazoan pathogen, Schistosoma mansoni. PLoS One 2009; 4:e4413
17. Robb SMC, Ross E, Alvarado AS. SmedGD: The Schmidtea mediterranea genome database. Nucleic Acids Res. 2008; 36
18. Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178-89
19. Kuzniar A, van Ham RC, Pongor S, Leunissen JA. The quest for orthologs: finding the corresponding gene across genomes. Trends Genet 2008; 24:539-51
20. Andrade LF, Nahum LA, Avelar LG, et al. Eukaryotic protein kinases (ePKs) of the helminth parasite Schistosoma mansoni. BMC Genomics 2011; 12:215
21. Zamanian M, Kimber MJ, McVeigh P, Carlson SA, Maule AG, Day TA. The repertoire of G protein-coupled receptors in the human parasite Schistosoma mansoni and the model organism Schmidtea mediterranea. BMC Genomics 2011; 12:596
22. Berriman M, Haas BJ, LoVerde PT, et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009; 460:352-8
23. Liu F, Zhou Y, Wang ZQ, et al. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009; 460:345-51
24. Mann VH, Suttiprapa S, Skinner DE, Brindley PJ, Rinaldi G. Pseudotyped murine leukemia virus for schistosome transgenesis: approaches, methods and perspectives. Transgenic Res 2014; 23:539-56
25. Morales ME, Mann VH, Kines KJ, et al. piggyBac transposon mediated transgenesis of the human blood fluke, Schistosoma mansoni. FASEB J 2007; 21:3479-89
26. Lok J. piggyBac: A vehicle for integrative DNA transformation of parasitic nematodes. Mob Genet Elements 2013; 3:e24417
27. Rinaldi G, Eckert SE, Tsai IJ, et al. Germline transgenesis and insertional mutagenesis in Schistosoma mansoni mediated by murine leukemia virus. PLoS Pathog 2012; 8:e1002820
28. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, Calarco JA. Heritable genome editing in C. elegans via a CRISPRCas9 system. Nat Methods 2013; 10:741-3
29. Suttiprapa S, Rinaldi G, Brindley PJ. Genetic manipulation of schistosomes-progress with integration competent vectors. Parasitology 2012; 139:641-50
30. Collins JJ, Wang B, Lambrus BG, Tharp ME, Iyer H, Newmark PA. Adult somatic stem cells in the human parasite Schistosoma mansoni. Nature 2013; 494:476-9
31. Hahnel S, Lu Z, Wilson RA, Grevelding CG, Quack T. Whole-Organ Isolation Approach as a Basis for Tissue-Specific Analyses in Schistosoma mansoni. PLoS Negl Trop Dis 2013; 7:e2336
32. Fu C-L, Odegaard JI, Herbert DR, Hsieh MH. A Novel Mouse Model of Schistosoma haematobium Egg-Induced Immunopathology. PLoS Pathog 2012; 8:e1002605
33. Boulanger D, Warter A, Sellin B, et al. Vaccine potential of a recombinant glutathione S-transferase cloned from Schistosoma haematobium in primates experimentally infected with an homologous challenge. Vaccine 1999; 17:319-26
34. Martins AV. Non-human vertebrate hosts of Schistosoma haematobium and Schistosoma mansoni. Bull World Heal Organ 1958; 18:931-44
35. Obuyu CK. Experimental Schistosoma haematobium infection in vervet monkeys (Ceropithecus aethiops centralis). Ann Trop Med Parasitol 1972; 66:75-82
36. Boulanger D, Warter A, Trottein F, et al. Vaccination of patas monkeys experimentally infected with Schistosoma haematobium using a recombinant glutathione S-transferase cloned from S. mansoni. Parasite Immunol 1995; 17:361-9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8552409
37. Soliman LA, Cheever AW, Kuntz RE, Myers BJ. Lesions of bladder muscle in baboons and monkeys infected with Schistosoma haematobium. Tropenmed Parasitol 1974; 25:327-33
38. Cheever AW, Kuntz RE, June B, Moore JA, Huang TAOC. Schistosomiasis haematobia in African, Hamadryas, and Gelada baboons. Am J Trop Med Hyg 1974; 23:429-48
39. Sulaiman SM, Hakim MA, Amin MA. The location of Schistosoma haematobium (Gezira strain, Sudan) in three experimental animal hosts. Trans R Soc Trop Med Hyg. 1982; 76:129
40. Cheever AW. Schistosoma haematobium: the pathology of experimental infection. Exp Parasitol 1985; 59:131-8
41. Kuntz RE, Malakatis GM. Susceptibility studies in schistosomiasis. III. Infection of various experimental hosts with Schistosoma haematobium in Egypt. Exp Parasitol 1955; 4:1-20
42. Niu Y, Shen B, Cui Y, et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 2014; 156:836-43
43. Hung YW, Remais J. Quantitative detection of Schistosoma japonicum Cercariae in water by real-time PCR. PLoS Negl Trop Dis 2008; 2:e337
44. Beaumier CM, Gillespie PM, Hotez PJ, Bottazzi ME. New vaccines for neglected parasitic diseases and dengue. Transl Res. 2013; 162:144-55
45. Kuntz RE, Malakatis GM. Susceptibility studies in schistosomiasis. IV. Susceptibility of wild mammals to infection by Schistosoma haematobium in Egypt, with emphasis on rodents. J Parasitol. 1955; 41:467-75
46. Rheinberg CE, Moné H, Caffrey CR, Imbert-Establet D, Jourdane J, Ruppel A. Schistosoma haematobium, S. intercalatum, S. japonicum, S. mansoni, and S. rodhaini in mice: relationship between patterns of lung migration by schistosomula and perfusion recovery of adult worms. Parasitol Res 1998; 84:338-42
47. Ray D, Nelson TA, Fu C-L, Patel S, Gong DN, Odegaard JI, et al. Transcriptional profiling of the bladder in urogenital schistosomiasis reveals pathways of inflammatory fibrosis and urothelial compromise. PLoS Negl Trop Dis 2012; 6:e1912
48. Hsieh Y-JH, Fu C-LL, Hsieh MH. Helminth-Induced Interleukin-4 Abrogates Invariant Natural Killer T Cell Activation-Associated Clearance of Bacterial Infection. Infect Immun 2014; 82:2087-97
49. Mann VH, Suttiprapa S, Rinaldi G, Brindley PJ. Establishing transgenic schistosomes. PLoS Negl Trop Dis 2011; 5:e1230
50. Skelly PJ, Dadara A, Harn DA. Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. Int J Parasitol. 2003; 33:363-9
51. Boyle JP, Wu X-J, Shoemaker CB, Yoshino TP. Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol Biochem Parasitol. 2003; 128:205-15
52. Davis RE, Parra A, LoVerde PT, Ribeiro E, Glorioso G, Hodgson S. Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proc Natl Acad Sci USA 1999; 96:8687-92
53. Wippersteg V, Kapp K, Kunz W, Jackstadt WP, Zahner H, Grevelding CG. HSP70-controlled GFP expression in transiently transformed schistosomes. Mol Biochem Parasitol 2002; 120:141-50
54. Correnti JM, Pearce EJ. Transgene expression in Schistosoma mansoni: Introduction of RNA into schistosomula by electroporation. Mol Biochem Parasitol 2004; 137:75-9
55. Beckmann S, Wippersteg V, El-Bahay A, Hirzmann J, Oliveira G, Grevelding CG. Schistosoma mansoni: Germ-line transformation approaches and actin-promoter analysis. Exp. Parasitol 2007. p. 292-303
56. Yang S, Brindley PJ, Zeng Q, et al. Transduction of Schistosoma japonicum schistosomules with vesicular stomatitis virus glycoprotein pseudotyped murine leukemia retrovirus and expression of reporter human telomerase reverse transcriptase in the transgenic schistosomes. Mol Biochem Parasitol. 2010; 174:109-16
57. Kines KJ, Morales ME, Mann VH, Gobert GN, Brindley PJ. Integration of reporter transgenes into Schistosoma mansoni chromosomes mediated by pseudotyped murine leukemia virus. FASEB J. 2008; 22:2936-48
58. Zhao ZR, Lei L, Liu M, et al. Schistosoma japonicum: Inhibition of Mago nashi gene expression by shRNA-mediated RNA interference. Exp Parasitol. 2008; 119:379-84
59. Tchoubrieva EB, Ong PC, Pike RN, Brindley PJ, Kalinna BH. Vectorbased RNA interference of cathepsin B1 in Schistosoma mansoni. Cell Mol Life Sci. 2010; 67:3739-48
60. Duvoisin R, Ayuk MA, Rinaldi G, et al. Human U6 promoter drives stronger shRNA activity than its schistosome orthologue in Schistosoma mansoni and human fibrosarcoma cells. Transgenic Res. 2012; 21: 511-21
61. Chamberlin HM. C. elegans select. Nat Methods 2010; 7:693-5