A bioinformatics approach for integrated transcriptomic and proteomic comparative analyses of model and non-sequenced anopheline vectors of human malaria parasites

Molecular and Cellular Proteomics

Volumn 12, Issue 1, 2013, Pages 120-131

  Mohien, Ceereena Ubaida ^a,b   Colquhoun, David R ^a,b   Mathias, Derrick K ^a,b   Gibbons, John G ^c   Armistead, Jennifer S ^a   Rodriguez, Maria C ^d   Rodriguez, Mario Henry ^d   Edwards, Nathan J ^e   Hartler, Jürgen ^f   Thallinger, Gerhard G ^f   Graham, David R ^b   Martinez Barnetche, Jesus ^d   Rokas, Antonis ^c   Dinglasan, Rhoel R ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^e GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^f GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; TRANSCRIPTOME;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ANOPHELES; ANOPHELES ALBIMANUS; ANOPHELES GAMBIAE; ARTICLE; BIOINFORMATICS; COMPARATIVE STUDY; CONTROLLED STUDY; DATA PROCESSING; DISEASE CARRIER; FUNCTIONAL PROTEOMICS; LIQUID CHROMATOGRAPHY; MIDGUT; MODEL; NONHUMAN; PEPTIDE MAPPING; PLASMODIUM VIVAX; PRIORITY JOURNAL; PROTEIN DATABASE; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; TRANSCRIPTOMICS;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; HOST-PARASITE INTERACTIONS; HUMANS; INSECT PROTEINS; INSECT VECTORS; MALARIA; MICROVILLI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROTEOME; PROTEOMICS; RNA; TANDEM MASS SPECTROMETRY; TRANSCRIPTOME;

ANOPHELES (GENUS); ANOPHELES ALBIMANUS; ANOPHELES GAMBIAE; DIPTERA; PLASMODIUM FALCIPARUM; PLASMODIUM PARASITES; PLASMODIUM VIVAX;

EID: 84871859805     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.019596     Document Type: Article

References (56)

1. Mueller, I., Galinski, M. R., Baird, J. K., Carlton, J. M., Kochar, D. K., Alonso, P. L., and del Portillo, H. A. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect. Dis. 9, 555-566
2. Alonso, P. L., Brown, G., Arevalo-Herrera, M., Binka, F., Chitnis, C., Collins, F., Doumbo, O. K., Greenwood, B., Hall, B. F., Levine, M. M., Mendis, K., Newman, R. D., Plowe, C. V., Rodriguez, M. H., Sinden, R., Slutsker, L., and Tanner, M. (2011) A research agenda to underpin malaria eradication. PLoS Med. 8, e1000406
3. Rodriguez, M. H., Gonzalez-Ceron, L., Hernandez, J. E., Nettel, J. A., Villarreal, C., Kain, K. C., and Wirtz, R. A. (2000) Different prevalences of Plasmodium vivax phenotypes VK210 and VK247 associated with the distribution of Anopheles albimanus and Anopheles pseudopunctipennis in Mexico. Am. J. Trop. Med. Hyg. 62, 122-127 (Pubitemid 30180362)
4. Joy, D. A., Gonzalez-Ceron, L., Carlton, J. M., Gueye, A., Fay, M., McCutchan, T. F., and Su, X. Z. (2008) Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Mol. Biol. Evol. 25, 1245-1252
5. Collins, W. E., Warren, M., Skinner, J. C., Richardson, B. B., and Kearse, T. S. (1977) Infectivity of the Santa Lucia (El Salvador) strain of Plasmodium falciparum to different anophelines. J. Parasit. 63, 57-61 (Pubitemid 8077804)
6. Olano, V. A., Carrillo, M. P., Delavega, P., and Espinal, C. A. (1985) Vector competence of Cartagena strain of Anopheles albimanus for Plasmodium falciparum and Plasmodium vivax. Trans. R. Soc. Trop. Med. Hyg. 79, 685-686
7. Collins, W. E., McClure, H., Strobert, E., Skinner, J. C., Richardson, B. B., Roberts, J. M., Galland, G. G., Sullivan, J., Morris, C. L., and Adams, S. R. (1993) Experimental infection of Anopheles gambiae s.s., Anopheles freeborni and Anopheles stephensi with Plasmodium malariae and Plasmodium brasilianum. J. Am. Mosq. Control Assoc. 9, 68-71
8. Kiszewski, A., Mellinger, A., Spielman, A., Malaney, P., Sachs, S. E., and Sachs, J. (2004) A global index representing the stability of malaria transmission. Am. J. Trop. Med. Hyg. 70, 486-498 (Pubitemid 38658142)
9. Parish, L. A., Colquhoun, D. R., Mohien, C. U., Lyashkov, A. E., Graham, D. R., and Dinglasan, R. R. (2011) Ookinete-interacting proteins on the microvillar surface are partitioned into detergent resistant membranes of Anopheles gambiae midguts. J. Proteome Res. 10, 5150-5162
10. Lavazec, C., Boudin, C., Lacroix, R., Bonnet, S., Diop, A., Thiberge, S., Boisson, B., Tahar, R., and Bourgouin, C. (2007) Carboxypeptidases B of Anopheles gambiae as targets for a Plasmodium falciparum transmission-blocking vaccine. Infect. Immun. 75, 1635-1642 (Pubitemid 46559427)
11. Mathias, D. K., Plieskatt, J. L., Armistead, J. S., Bethony, J. M., Abdul-Majid, K. B., McMillan, A., Angov, E., Aryee, M. J., Zhan, B., Gillespie, P., Keegan, B., Jariwala, A. R., Rezende, W., Bottazzi, M. E., Scorpio, D. G., Hotez, P. J., and Dinglasan, R. R. (2012) Expression, immunogenicity, histopathology, and potency of a mosquito-based malaria transmissionblocking recombinant vaccine. Infect. Immun. 80, 1606-1614
12. Dinglasan, R. R., Kalume, D. E., Kanzok, S. M., Ghosh, A. K., Muratova, O., Pandey, A., and Jacobs-Lorena, M. (2007) Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc. Natl. Acad. Sci. U.S.A. 104, 13461-13466 (Pubitemid 47293967)
13. Dinglasan, R. R., and Jacobs-Lorena, M. (2008) Flipping the paradigm on malaria transmission-blocking vaccines. Trends Parasitol. 24, 364-370
14. Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., de Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober- Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J. J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H., and Hoffman, S. L. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129-149
15. Hittinger, C. T., Johnston, M., Tossberg, J. T., and Rokas, A. (2010) Leveraging skewed transcript abundance by RNA-Seq to increase the genomic depth of the tree of life. Proc. Natl. Acad. Sci. U.S.A. 107, 1476-1481
16. Krzywinski, J., and Besansky, N. J. (2003) Molecular systematics of Anopheles: from subgenera to subpopulations. Annu. Rev. Entomol. 48, 111-139 (Pubitemid 37365388)
17. Zdobnov, E. M., von Mering, C., Letunic, I., Torrents, D., Suyama, M., Copley, R. R., Christophides, G. K., Thomasova, D., Holt, R. A., Subramanian, G. M., Mueller, H. M., Dimopoulos, G., Law, J. H., Wells, M. A., Birney, E., Charlab, R., Halpern, A. L., Kokoza, E., Kraft, C. L., Lai, Z., Lewis, S., Louis, C., Barillas-Mury, C., Nusskern, D., Rubin, G. M., Salzberg, S. L., Sutton, G. G., Topalis, P., Wides, R., Wincker, P., Yandell, M., Collins, F. H., Ribeiro, J., Gelbart, W. M., Kafatos, F. C., and Bork, P. (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298, 149-159
18. Hurd, H., Taylor, P., Adams, D., Underhill, A., and Eggleston, P. (2005) Measuring the costs of mosquito resistance to malaria infection. Evolution 12, 2560-2572 (Pubitemid 43069938)
19. Abdul-Rauf, M., and Ellar, D. J. (1999) Isolation and characterization of brush border membrane vesicles from whole Aedes aegypti larvae. J. Invertebr. Pathol. 73, 45-51 (Pubitemid 129498851)
20. Hauser, H., Howell, K., Dawson, R. M. C., and Bowyer, D. E. (1980) Rabbit small intestinal brush-border membrane preparation and lipid-composition. Biochim. Biophys. Acta 602, 567-577 (Pubitemid 11218316)
21. Gibbons, J. G., Beauvais, A., Beau, R., McGary, K. L., Latge, J. P., and Rokas, A. (2012) Global transcriptome changes underlying colony growth in the opportunistic human pathogen Aspergillus fumigatus. Eukaryot. Cell 11, 68-78
22. Gibbons, J. G., Janson, E. M., Hittinger, C. T., Johnston, M., Abbot, P., and Rokas, A. (2009) Benchmarking next-generation transcriptome sequencing for functional and evolutionary genomics. Mol. Biol. Evol. 26, 2731-2744
23. Martinez-Barnetche, J., Gomez-Barreto, R. E., Ovilla-Munoz, M., Tellez-Sosa, J., Garcia-Lopez, D. E., Dinglasan, R. R., Ubaida Mohien, C., Maccallum, R. M., Redmond, S. N., Gibbons, J. G., Rokas, A., Machado, C. M., Cazares-Raga, F., Gonzalez-Ceron, L., Hernandez-Martinez, S., and Rodriguez-Lopez, M. H. (2012) Transcriptome of the adult female malaria mosquito vector Anopheles albimanus. BMC Genomics 13, 207
24. Zerbino, D. R., and Birney, E. (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (Pubitemid 351645072)
25. Schulz, M. H., Zerbino, D. R., Vingron, M., and Birney, E. (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086-1092
26. Surget-Groba, Y., and Montoya-Burgos, J. I. (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res. 20, 1432-1440
27. Edwards, N., Wu, X., and Tseng, C. W. (2009) An unsupervised, model-free, machine-learning combiner for peptide identifications from tandem mass spectra. Clin. Proteomics 5, 23-36
28. Perkins, D. N., Pappin, D. J. C., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (Pubitemid 30007252)
29. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., Yang, X. Y., Shi, W. Y., and Bryant, S. H. (2004) Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964 (Pubitemid 39425651)
30. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467 (Pubitemid 38931421)
31. MacLean, B., Eng, J. K., Beavis, R. C., and McIntosh, M. (2006) General framework for developing and evaluating database scoring algorithms using the TANDEM search engine. Bioinformatics 22, 2830-2832 (Pubitemid 44742409)
32. Tabb, D. L., Fernando, C. G., and Chambers, M. C. (2007) MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661 (Pubitemid 46340169)
33. Tanner, S., Shu, H., Frank, A., Wang, L. C., Zandi, E., Mumby, M., Pevzner, P. A., and Bafna, V. (2005) InsPecT: identification of posttranslationally modified peptides from tandem mass spectra. Anal. Chem. 77, 4626-4639 (Pubitemid 41542287)
34. Kim, S., Gupta, N., and Pevzner, P. A. (2008) Spectral probabilities and generating functions of tandem mass spectra: a strike against decoy databases. J. Proteome Res. 7, 3354-3363
35. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214 (Pubitemid 46358868)
36. Mohien, C. U., Hartler, J., Breitwieser, F., Rix, U., Rix, L. R., Winter, G. E., Thallinger, G. G., Bennett, K. L., Superti-Furga, G., Trajanoski, Z., and Colinge, J. (2010) MASPECTRAS 2: an integration and analysis platform for proteomic data. Proteomics 10, 2719-2722
37. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M., and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (Pubitemid 41264107)
38. Pitts, R. J., Rinker, D. C., Jones, P. L., Rokas, A., and Zwiebel, L. J. (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 12, 271
39. Collins, L. J., Biggs, P. J., Voelckel, C., and Joly, S. (2008) An approach to transcriptome analysis of non-model organisms using short-read sequences. Genome Inform. 21, 3-14
40. DiGuistini, S., Liao, N. Y., Platt, D., Robertson, G., Seidel, M., Chan, S. K., Docking, T. R., Birol, I., Holt, R. A., Hirst, M., Mardis, E., Marra, M. A., Hamelin, R. C., Bohlmann, J., Breuil, C., and Jones, S. J. M. (2009) De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biol. 10, R94
41. Eisen, N. S., Fernandes, V. F., Harvey, W. R., Spaeth, D. D., and Wolfersberger, M. G. (1988) Comparison of brush border membrane vesicles prepared by three methods from larval Manduca sexta midgut. Insect Biochem. 9, 337-342
42. Horth, P., Miller, C. A., Preckel, T., and Wenz, C. (2006) Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol. Cell. Proteomics 5, 1968-1974 (Pubitemid 44688204)
43. Wang, X., Slebos, R. J. C., Wang, D., Halvey, P. J., Tabb, D. L., Liebler, D. C., and Zhang, B. (2012) Protein identification using customized protein sequence databases derived from RNA-Seq data. J. Proteome Res. 11, 1009-1017
44. Desgagne-Penix, I., Khan, M. F., Schriemer, D. C., Cram, D., Nowak, J., and Facchini, P. J. (2010) Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol. 10, 252
45. Adamidi, C., Wang, Y., Gruen, D., Mastrobuoni, G., You, X., Tolle, D., Dodt, M., Mackowiak, S. D., Gogol-Doering, A., Oenal, P., Rybak, A., Ross, E., Sanchez Alvarado, A., Kempa, S., Dieterich, C., Rajewsky, N., and Chen, W. (2011) De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics. Genome Res. 21, 1193-1200
46. Nesvizhskii, A. I., and Aebersold, R. (2005) Interpretation of shotgun proteomic data: the protein inference problem. Mol. Cell. Proteomics 4, 1419-1440 (Pubitemid 41555469)
47. Tharakan, R., Edwards, N., and Graham, D. R. (2010) Data maximization by multipass analysis of protein mass spectra. Proteomics 10, 1160-1171
48. Wang, H., Tang, H. Y., Tan, G. C., and Speicher, D. W. (2011) Data analysis strategy for maximizing high-confidence protein identifications in complex proteomes such as human tumor secretomes and human serum. J. Proteome Res. 10, 4993-5005
49. Tabb, D. L., Vega-Montoto, L., Rudnick, P. A., Variyath, A. M., Ham, A. J. L., Bunk, D. M., Kilpatrick, L. E., Billheimer, D. D., Blackman, R. K., Cardasis, H. L., Carr, S. A., Clauser, K. R., Jaffe, J. D., Kowalski, K. A., Neubert, T. A., Regnier, F. E., Schilling, B., Tegeler, T. J., Wang, M., Wang, P., Whiteaker, J. R., Zimmerman, L. J., Fisher, S. J., Gibson, B. W., Kinsinger, C. R., Mesri, M., Rodriguez, H., Stein, S. E., Tempst, P., Paulovich, A. G., Liebler, D. C., and Spiegelman, C. (2010) Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry. J. Proteome Res. 9, 761-776
50. Salichos, L., and Rokas, A. (2011) Evaluating ortholog prediction algorithms in a yeast model clade. PLoS One 6, e18755
51. Garver, L. S., Xi, Z. Y., and Dimopoulos, G. (2008) Immunoglobulin superfamily members play an important role in the mosquito immune system. Dev. Comp. Immunol. 32, 519-531 (Pubitemid 351172447)
52. Rodriguez, M. D., Martinez-Barnetche, J., Alvarado-Delgado, A., Batista, C., Argotte-Ramos, R. S., Hernandez-Martinez, S., Ceron, L. G., Torres, J. A., Margos, G., and Rodriguez, M. H. (2007) The surface protein Pvs25 of Plasmodium vivax ookinetes interacts with calreticulin on the midgut apical surface of the malaria vector Anopheles albimanus. Mol. Biochem. Parasitol. 153, 167-177 (Pubitemid 46667170)
53. Sattabongkot, J., Tsuboi, T., Hisaeda, H., Tachibana, M., Suwanabun, N., Rungruang, T., Cao, Y. M., Stowers, A. W., Sirichaisinthop, J., Coleman, R. E., and Torii, M. (2003) Blocking of transmission to mosquitoes by antibody to Plasmodium vivax malaria vaccine candidates Pvs25 and Pvs28 despite antigenic polymorphism in field isolates. Am. J. Trop. Med. Hyg. 69, 536-541 (Pubitemid 38248256)
54. Gonzalez-Lazaro, M., Dinglasan, R. R., Hernandez-Hernandez Fde, L., Rodriguez, M. H., Laclaustra, M., Jacobs-Lorena, M., and Flores-Romo, L. (2009) Anopheles gambiae Croquemort SCRBQ2, expression profile in the mosquito and its potential interaction with the malaria parasite Plasmodium berghei. Insect Biochem. Mol. Biol. 39, 395-402
55. Kotsyfakis, M., Ehret-Sabatier, L., Siden-Kiamos, I., Mendoza, J., Sinden, R. E., and Louis, C. (2005) Plasmodium berghei ookinetes bind to Anopheles gambiae and Drosophila melanogaster annexins. Mol. Microbiol. 57, 171-179 (Pubitemid 40896606)
56. Lavazec, C., Bonnet, S., Thiery, I., Boisson, B., and Bourgouin, C. (2005) cpbAg1 encodes an active carboxypeptidase B expressed in the midgut of Anopheles gambiae. Insect Mol. Biol. 14, 163-174 (Pubitemid 40534282)