Dual RNA-seq of Parasite and Host Reveals Gene Expression Dynamics during Filarial Worm-Mosquito Interactions

PLoS Neglected Tropical Diseases

Volumn 8, Issue 5, 2014, Pages

  Choi, Young Jun ^a,b,c,d   Aliota, Matthew T ^a   Mayhew, George F ^a,b,c,d   Erickson, Sara M ^a,b,c,d   Christensen, Bruce M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Roche NimbleGen Inc   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES AEGYPTI; ANIMAL MODEL; ARTICLE; BRUGIA MALAYI; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; HOST PARASITE INTERACTION; LIFE CYCLE; MOLECULAR INTERACTION; MULTIDIMENSIONAL SCALING; NONHUMAN; NUCLEOTIDE SEQUENCE; PREVALENCE; QUANTITATIVE TRAIT LOCUS; RNA ISOLATION; RNA SEQUENCE; AEDES; ANIMAL; CLUSTER ANALYSIS; ENVIRONMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; PARASITOLOGY; SEQUENCE ANALYSIS;

TRANSCRIPTOME;

AEDES; ANIMALS; BRUGIA MALAYI; CLUSTER ANALYSIS; ENVIRONMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS; MALE; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84901748068     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002905     Document Type: Article

References (72)

1. 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.
2. Global programme to eliminate lymphatic filariasis: progress report for 2012 (2013). Relevé Épidémiologique Hebd Sect Hygiène Secrétariat Société Nations Wkly Epidemiol Rec Health Sect Secr Leag Nations 88: 389-399.
3. Aliota MT, Fuchs JF, Rocheleau TA, Clark AK, Hillyer JF, et al. (2010) Mosquito transcriptome profiles and filarial worm susceptibility in Armigeres subalbatus. PLoS Negl Trop Dis 4: e666.
4. Erickson SM, Xi Z, Mayhew GF, Ramirez JL, Aliota MT, et al. (2009) Mosquito infection responses to developing filarial worms. PLoS Negl Trop Dis 3: e529.
5. Erickson SM, Thomsen EK, Keven JB, Vincent N, Koimbu G, et al. (2013) Mosquito-parasite interactions can shape filariasis transmission dynamics and impact elimination programs. PLoS Negl Trop Dis 7: e2433.
6. Chellappah WT, (1968) Observations on the survival rate of Armigeres subalbatus after being fed on hosts with different levels of micro-filariae of Brugia pahangi. Med J Malaya 22: 240.
7. Yamamoto H, Kobayashi M, Ogura N, Tsuruoka H, Chigusa Y, (1985) Studies on filariasis VI: The encapsulation of Brugia malayi and B. pahangi larvae in the mosquito, Armigeres subalbatus. Jpn J Sanit Zool 36: 1-6.
8. Pichon G, (2002) Limitation and facilitation in the vectors and other aspects of the dynamics of filarial transmission: the need for vector control against Anopheles-transmitted filariasis. Ann Trop Med Parasitol 96 (Suppl 2):: S143-152.
9. Bartholomay LC, Christensen BM, (2002) Vector-Parasite Interactions in Mosquito-Borne Filariasis. The Filaria. World Class Parasites 5: 9-19.
10. Beckett EB, (1971) Histological changes in mosquito flight muscle fibres associated with parasitization by filarial larvae. Parasitology 63: 365-372.
11. Beckett EB, (1973) Some quantitative aspects of flight muscle damage in mosquitoes infected with filarial larvae. Ann Trop Med Parasitol 67: 455-466.
12. Matthews KR, (2011) Controlling and coordinating development in vector-transmitted parasites. Science 331: 1149-1153.
13. Lefèvre T, Thomas F, (2008) Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 8: 504-519.
14. Castillo JC, Reynolds SE, Eleftherianos I, (2011) Insect immune responses to nematode parasites. Trends Parasitol 27: 537-547.
15. Pfarr KM, Debrah AY, Specht S, Hoerauf A, (2009) Filariasis and lymphoedema. Parasite Immunol 31: 664-672.
16. Bennuru S, Nutman TB, (2009) Lymphatics in human lymphatic filariasis: in vitro models of parasite-induced lymphatic remodeling. Lymphat Res Biol 7: 215-219.
17. Aliota MT, Fuchs JF, Mayhew GF, Chen C-C, Christensen BM, (2007) Mosquito transcriptome changes and filarial worm resistance in Armigeres subalbatus. BMC Genomics 8: 463.
18. Westermann AJ, Gorski SA, Vogel J, (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10: 618-630.
19. Christensen BM, Sutherland DR, (1984) Brugia pahangi: Exsheathment and Midgut Penetration in Aedes aegypti. Trans Am Microsc Soc 103: 423-433.
20. Macdonald WW, Ramachandran CP, (1965) The influence of the gene Fm (Filarial Susceptibility, Brugia malayi) on the susceptibility of Aedes aegypti to seven strains of Brugia, Wuchereria and Dirofilaria. Ann Trop Med Parasitol 59: 64-73.
21. Hickey WA, Craig GB Jr, (1966) Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53: 1177-1196.
22. Severson DW, Mori A, Zhang Y, Christensen BM, (1994) Chromosomal mapping of two loci affecting filarial worm susceptibility in Aedes aegypti. Insect Mol Biol 3: 67-72.
23. Christensen BM, Sutherland DR, Gleason LN, (1984) Defense reactions of mosquitoes to filarial worms: comparative studies on the response of three different mosquitoes to inoculated Brugia pahangi and Dirofilaria immitis microfilariae. J Invertebr Pathol 44: 267-274.
24. Efron B, Tibshirani R (1993). An introduction to the bootstrap. London, U.K.: Chapman & Hall. p. 436.
25. Auer PL, Doerge RW, (2010) Statistical design and analysis of RNA sequencing data. Genetics 185: 405-416.
26. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinforma Oxf Engl 25: 1105-1111.
27. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
28. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinforma Oxf Engl 25: 2078-2079.
29. Li H, Ruan J, Durbin R, (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851-1858.
30. Choi Y-J, Ghedin E, Berriman M, McQuillan J, Holroyd N, et al. (2011) A deep sequencing approach to comparatively analyze the transcriptome of lifecycle stages of the filarial worm, Brugia malayi. PLoS Negl Trop Dis 5: e1409.
31. Robinson MD, Smyth GK, (2007) Moderated statistical tests for assessing differences in tag abundance. Bioinforma Oxf Engl 23: 2881-2887.
32. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma Oxf Engl 26: 139-140.
33. McCarthy DJ, Chen Y, Smyth GK, (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40: 4288-4297.
34. Robinson MD, Oshlack A, (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11: R25.
35. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc 57: 289-300.
36. Yeung KY, Haynor DR, Ruzzo WL, (2001) Validating clustering for gene expression data. Bioinforma Oxf Engl 17: 309-318.
37. Young MD, Wakefield MJ, Smyth GK, Oshlack A, (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11: R14.
38. Camon E, Magrane M, Barrell D, Lee V, Dimmer E, et al. (2004) The Gene Ontology Annotation (GOA) Database: sharing knowledge in Uniprot with Gene Ontology. Nucleic Acids Res 32: D262-266.
39. Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, et al. (2007) VectorBase: a home for invertebrate vectors of human pathogens. Nucleic Acids Res 35: D503-505.
40. Murthy PK, Sen AB, (1981) Sequential development changes in microfilariae of subperiodic Brugia malayi to infective larvae in susceptible strain of Aedes aegypti (Macdonald). J Commun Dis 13: 102-109.
41. Yosef N, Regev A, (2011) Impulse control: temporal dynamics in gene transcription. Cell 144: 886-896.
42. Frand AR, Russel S, Ruvkun G, (2005) Functional genomic analysis of C. elegans molting. PLoS Biol 3: e312.
43. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Dimon MT, et al. (2011) RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti. BMC Genomics 12: 82.
44. Lehane MJ, Laurence BR, (1977) Flight muscle ultrastructure of susceptible and refractory mosquitoes parasitized by larval Brugia pahangi. Parasitology 74: 87-92.
45. Razin SV, Borunova VV, Maksimenko OG, Kantidze OL, (2012) Cys2His2 zinc finger protein family: classification, functions, and major members. Biochem Biokhimiiâ 77: 217-226.
46. Laurence BR, Simpson MG, (1971) The microfilaria of Brugia: a first stage nematode larva. J Helminthol 45: 23-40.
47. 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.
48. Monsalve GC, Frand AR, (2012) Toward a unified model of developmental timing: A "molting" approach. Worm 1: 221-230.
49. Kafsack BFC, Llinás M, (2010) Eating at the table of another: metabolomics of host-parasite interactions. Cell Host Microbe 7: 90-99.
50. Ranson H, Hemingway J, (2005) Mosquito glutathione transferases. Methods Enzymol 401: 226-241.
51. Beckett EB, Boothroyd B, (1970) Mode of nutrition of the larvae of the filarial nematode Brugia pahangi. Parasitology 60: 21-26.
52. Beckett EB, (1990) Species variation in mosquito flight-muscle damage resulting from a single filarial infection and its repercussions on a second infection. Parasitol Res 76: 606-609.
53. Moreno Y, Geary TG, (2008) Stage- and gender-specific proteomic analysis of Brugia malayi excretory-secretory products. PLoS Negl Trop Dis 2: e326.
54. Martínez O, Reyes-Valdés MH, (2008) Defining diversity, specialization, and gene specificity in transcriptomes through information theory. Proc Natl Acad Sci U S A 105: 9709-9714.
55. Fulda S, Gorman AM, Hori O, Samali A, (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010: 214074.
56. Beckett EB, (1990) The non-specific nature of the response of mosquito flight muscle to filarial parasitization. Parasitol Res 76: 360-366.
57. Berry WJ, Rowley WA, Christensen BM, (1986) Influence of developing Brugia pahangi on spontaneous flight activity of Aedes aegypti (Diptera: Culicidae). J Med Entomol 23: 441-445.
58. Hockmeyer WT, Schiefer BA, Redington BC, Eldridge BF, (1975) Brugia pahangi: effects upon the flight capability of Aedes aegypti. Exp Parasitol 38: 1-5.
59. Hammarlund M, Davis WS, Jorgensen EM, (2000) Mutations in beta-spectrin disrupt axon outgrowth and sarcomere structure. J Cell Biol 149: 931-942.
60. Wilson D, Charoensawan V, Kummerfeld SK, Teichmann SA, (2008) DBD-taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res 36: D88-92.
61. Golstein P, Kroemer G, (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32: 37-43.
62. 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.
63. Gregory WF, Maizels RM, (2008) Cystatins from filarial parasites: evolution, adaptation and function in the host-parasite relationship. Int J Biochem Cell Biol 40: 1389-1398.
64. Köhler P, (1991) The pathways of energy generation in filarial parasites. Parasitol Today Pers Ed 7: 21-25.
65. Behm C (2002) Metabolism. The Biology of Nematodes. London: Taylor and Francis. pp. 261-290.
66. Barrett J, Mendis AH, Butterworth PE, (1986) Carbohydrate metabolism in Brugia pahangi (Nematoda: Filarioidea). Int J Parasitol 16: 465-469.
67. Barrett J (2011) Biochemistry of Survival. Molecular and Physiological Basis of Nematode Survival. Wallingford: CABI. pp. 282-304.
68. Bennuru S, Semnani R, Meng Z, Ribeiro JMC, 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.
69. Griffiths KG, Mayhew GF, Zink RL, Erickson SM, Fuchs JF, et al. (2009) Use of microarray hybridization to identify Brugia genes involved in mosquito infectivity. Parasitol Res 106: 227-235.
70. Li B-W, Rush AC, Jiang D-J, Mitreva M, Abubucker S, et al. (2011) Gender-associated genes in filarial nematodes are important for reproduction and potential intervention targets. PLoS Negl Trop Dis 5: e947.
71. Li B-W, Wang Z, Rush AC, Mitreva M, Weil GJ, (2012) Transcription profiling reveals stage- and function-dependent expression patterns in the filarial nematode Brugia malayi. BMC Genomics 13: 184.
72. Li B-W, 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.