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Computational and experimental analysis of the glycophosphatidylinositol-anchored proteome of the human parasitic nematode Brugia malayi


Autoři: Fana B. Mersha aff001;  Leslie K. Cortes aff001;  Ashley N. Luck aff001;  Colleen M. McClung aff001;  Cristian I. Ruse aff001;  Christopher H. Taron aff001;  Jeremy M. Foster aff001
Působiště autorů: New England Biolabs, Ipswich MA, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0216849

Souhrn

Further characterization of essential systems in the parasitic filarial nematode Brugia malayi is needed to better understand its biology, its interaction with its hosts, and to identify critical components that can be exploited to develop novel treatments. The production of glycophosphatidylinositol-anchored proteins (GPI-APs) is essential for eukaryotic cellular and physiological function. In addition, GPI-APs perform many important roles for cells. In this study, we characterized the B. malayi GPI-anchored proteome using both computational and experimental approaches. We used bioinformatic strategies to show the presence or absence of B. malayi GPI-AP biosynthetic pathway genes and to compile a putative B. malayi GPI-AP proteome using available prediction programs. We verified these in silico analyses using proteomics to identify GPI-AP candidates prepared from the surface of intact worms and from membrane enriched extracts. Our study represents the first description of the GPI-anchored proteome in B. malayi and lays the groundwork for further exploration of this essential protein modification as a target for novel anthelmintic therapeutic strategies.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Invertebrates – Nematoda – Brugia – Brugia malayi – Caenorhabditis – Caenorhabditis elegans – Biochemistry – Proteins – Proteomes – Protein domains – Transferases – Lipids – Proteomics – Proteomic databases – Enzymology – Enzymes – Cell biology – Cellular structures and organelles – Cell membranes – Membrane proteins – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Animal models – Database and informatics methods – Biological databases


Zdroje

1. Molyneux DH. Advancing toward the Elimination of Lymphatic Filariasis. New England Journal of Medicine. 2018;379(19):1871–2. doi: 10.1056/NEJMe1811455 30403953

2. Lymphatic filariasis: World Health Organization; March 2017 [updated March 2017. Available from: http://www.who.int/mediacentre/factsheets/fs102/en/.

3. Taylor MJ, Hoerauf A, Bockarie M. Lymphatic filariasis and onchocerciasis. The Lancet. 2010;376(9747):1175–85.

4. King CL, Suamani J, Sanuku N, Cheng Y-C, Satofan S, Mancuso B, et al. A Trial of a Triple-Drug Treatment for Lymphatic Filariasis. New England Journal of Medicine. 2018;379(19):1801–10. doi: 10.1056/NEJMoa1706854 30403937

5. Osei-Atweneboana MY, Awadzi K, Attah SK, Boakye DA, Gyapong JO, Prichard RK. Phenotypic evidence of emerging ivermectin resistance in Onchocerca volvulus. PLoS neglected tropical diseases. 2011;5(3):e998–e. doi: 10.1371/journal.pntd.0000998 21468315

6. Schwab AE, Boakye DA, Kyelem D, Prichard RK. Detection of Benzimidazole Resistance–Associated Mutations in the Filarial Nematode Wuchereria bancrofti and Evidence for Selection by Albendazole and Ivermectin Combination Treatment. The American Journal of Tropical Medicine and Hygiene. 2005;73(2):234–8. 16103581

7. Kinoshita T, Fujita M. Biosynthesis of GPI-anchored proteins: special emphasis on GPI lipid remodeling. Journal of Lipid Research. 2016;57(1):6–24. doi: 10.1194/jlr.R063313 26563290

8. Kinoshita T, Ohish K, Takeda J. GPI-Anchor Synthesis in Mammalian Cells: Genes, Their Products, and a Deficiency. The Journal of Biochemistry. 1997;122(2):251–7. doi: 10.1093/oxfordjournals.jbchem.a021746 9378699

9. Orlean P, Menon AK. Thematic review series: Lipid Posttranslational Modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. Journal of Lipid Research. 2007;48(5):993–1011. doi: 10.1194/jlr.R700002-JLR200 17361015

10. Gillmor CS, Lukowitz W, Brininstool G, Sedbrook JC, Hamann T, Poindexter P, et al. Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in Arabidopsis. Plant Cell. 2005;17(4):1128–40. doi: 10.1105/tpc.105.031815 15772281

11. Ferguson MAJ, Kinoshita T, Hart GW. Glycosylphosphatidylinositol Anchors. In: Varki A CR, Esko JD, et al., editor. Essentials of Glycobiology 2nd edition. Chapter 11. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009.

12. Ferguson MA, Homans SW, Dwek RA, Rademacher TW. Glycosyl-phosphatidylinositol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science. 1988;239(4841):753.

13. Paulick MG, Bertozzi CR. The Glycosylphosphatidylinositol Anchor: A Complex Membrane-Anchoring Structure for Proteins. Biochemistry. 2008;47(27):6991–7000. doi: 10.1021/bi8006324 18557633

14. Nozaki M, Ohishi K, Yamada N, Kinoshita T, Nagy A, Takeda J. Developmental abnormalities of glycosylphosphatidylinositol-anchor-deficient embryos revealed by Cre/loxP system. Lab Invest. 1999;79(3):293–9. 10092065

15. Pittet M, Conzelmann A. Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae. Biochimica et biophysica acta. 2007;1771(3):405–20. doi: 10.1016/j.bbalip.2006.05.015 16859984

16. Smith TK, Crossman A, Brimacombe JS, Ferguson MAJ. Chemical validation of GPI biosynthesis as a drug target against African sleeping sickness. The EMBO Journal. 2004;23(23):4701–8. doi: 10.1038/sj.emboj.7600456 15526036

17. Murata D, Nomura KH, Dejima K, Mizuguchi S, Kawasaki N, Matsuishi-Nakajima Y, et al. GPI-anchor synthesis is indispensable for the germline development of the nematode Caenorhabditis elegans. Molecular Biology of the Cell. 2012;23(6):982–95. doi: 10.1091/mbc.E10-10-0855 22298425

18. Budirahardja Y, Doan TD, Zaidel-Bar R. Glycosyl phosphatidylinositol anchor biosynthesis is essential for maintaining epithelial integrity during Caenorhabditis elegans embryogenesis. PLoS Genetics. 2015;11(3):e1005082. doi: 10.1371/journal.pgen.1005082 25807459

19. Ferguson MA, Low MG, Cross GA. Glycosyl-sn-1,2-dimyristylphosphatidylinositol is covalently linked to Trypanosoma brucei variant surface glycoprotein. Journal of Biological Chemistry. 1985;260(27):14547–55. 4055788

20. Gilson PR, Nebl T, Vukcevic D, Moritz RL, Sargeant T, Speed TP, et al. Identification and Stoichiometry of Glycosylphosphatidylinositol-anchored Membrane Proteins of the Human Malaria Parasite Plasmodium falciparum. Molecular & Cellular Proteomics. 2006;5(7):1286.

21. Jäschke A, Coulibaly B, Remarque EJ, Bujard H, Epp C. Merozoite Surface Protein 1 from Plasmodium falciparum Is a Major Target of Opsonizing Antibodies in Individuals with Acquired Immunity against Malaria. Clinical and Vaccine Immunology. 2017;24(11):e00155–17. doi: 10.1128/CVI.00155-17 28877929

22. Lee RY N, Howe KL, Harris TW, Arnaboldi V, Cain S, Chan J, et al. WormBase 2017: molting into a new stage. Nucleic Acids Research. 2018;46(D1):D869–D74. doi: 10.1093/nar/gkx998 29069413

23. KEGG: Kyoto Encyclopedia of Genes and Genomes [Internet]. Release 84.1, December 1, 2017 Available from: http://www.kegg.jp/kegg/.

24. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research. 2016;44(D1):D279–D85. doi: 10.1093/nar/gkv1344 26673716

25. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic acids research. 2017;45(D1):D200–D3. doi: 10.1093/nar/gkw1129 27899674

26. Database resources of the National Center for Biotechnology Information. Nucleic acids research. 2018;46(D1):D8–D13. doi: 10.1093/nar/gkx1095 29140470

27. Stiernagle T. Maintenance of C. elegans: WormBook; [updated February 11, 2006; cited 10.1895/wormbook.1.101.1. Available from: http://www.wormbook.org.

28. Vainauskas S, Cortes LK, Taron CH. In vivo incorporation of an azide-labeled sugar analog to detect mammalian glycosylphosphatidylinositol molecules isolated from the cell surface. Carbohydr Res. 2012;362:62–9. doi: 10.1016/j.carres.2012.09.012 23085221

29. Fankhauser N, Mäser P. Identification of GPI anchor attachment signals by a Kohonen self-organizing map. Bioinformatics. 2005;21(9):1846–52. doi: 10.1093/bioinformatics/bti299 15691858

30. Pierleoni A, Martelli PL, Casadio R. PredGPI: a GPI-anchor predictor. BMC Bioinformatics. 2008;9(1):392.

31. Eisenhaber B, Bork P, Eisenhaber F. Prediction of Potential GPI-modification Sites in Proprotein Sequences. Journal of Molecular Biology. 1999;292(3):741–58. doi: 10.1006/jmbi.1999.3069 10497036

32. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods. 2011;8:785. doi: 10.1038/nmeth.1701 21959131

33. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. Journal of Molecular Biology. 2001;305(3):567–80. doi: 10.1006/jmbi.2000.4315 11152613

34. Graham JM. Preparation of crude subcellular fractions by differential centrifugation. ScientificWorldJournal. 2002;2:1638–42. doi: 10.1100/tsw.2002.851 12806153

35. Nakayasu ES, Yashunsky DV, Nohara LL, Torrecilhas ACT, Nikolaev AV, Almeida IC. GPIomics: global analysis of glycosylphosphatidylinositol-anchored molecules of Trypanosoma cruzi. Molecular Systems Biology. 2009;5:261–. doi: 10.1038/msb.2009.13 19357640

36. Schleicher TR, VerBerkmoes NC, Shah M, Nyholm SV. Colonization State Influences the Hemocyte Proteome in a Beneficial Squid–Vibrio Symbiosis. Molecular & Cellular Proteomics. 2014;13(10):2673.

37. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Research. 2018;47(D1):D442–D50.

38. The UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Research. 2017;45(D1):D158–D69. doi: 10.1093/nar/gkw1099 27899622

39. Hong Y, Kinoshita T. Trypanosome glycosylphosphatidylinositol biosynthesis. Korean J Parasitol. 2009;47(3):197–204. doi: 10.3347/kjp.2009.47.3.197 19724691

40. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, et al. Proteine Database Searches Using Compositionally Adjusted Substitution Matrices. The FEBS journal. 2005;272(20):5101–9. doi: 10.1111/j.1742-4658.2005.04945.x 16218944

41. Murakami Y, Siripanyaphinyo U, Hong Y, Tashima Y, Maeda Y, Kinoshita T. The Initial Enzyme for Glycosylphosphatidylinositol Biosynthesis Requires PIG-Y, a Seventh Component. Molecular Biology of the Cell. 2005;16(11):5236–46. doi: 10.1091/mbc.E05-08-0743 16162815

42. Maeda Y, Tanaka S, Hino J, Kangawa K, Kinoshita T. Human dolichol-phosphate-mannose synthase consists of three subunits, DPM1, DPM2 and DPM3. The EMBO Journal. 2000;19(11):2475–82. doi: 10.1093/emboj/19.11.2475 10835346

43. Colussi PA, Taron CH, Mack JC, Orlean P. Human and Saccharomyces cerevisiae dolichol phosphate mannose synthases represent two classes of the enzyme, but both function in Schizosaccharomyces pombe. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(15):7873–8. doi: 10.1073/pnas.94.15.7873 9223280

44. Taron BW, Colussi PA, Wiedman JM, Orlean P, Taron CH. Human Smp3p Adds a Fourth Mannose to Yeast and Human Glycosylphosphatidylinositol Precursors in Vivo. Journal of Biological Chemistry. 2004;279(34):36083–92. doi: 10.1074/jbc.M405081200 15208306

45. Cortes LK, Scarcelli JJ, Taron CH. Complementation of essential yeast GPI mannosyltransferase mutations suggests a novel specificity for certain Trypanosoma and Plasmodium PigB proteins. PloS one. 2014;9(1):e87673–e. doi: 10.1371/journal.pone.0087673 24489949

46. Dzung B. Diep KLN, Srikumar M. Raja, Erin N. Pleshak, and J. Thomas Buclkley. <J. Biol. Chem.-1998-Diep-2355-60.pdf>. The Journal of Biological Chemistry. 1998;273(4):2355–60. doi: 10.1074/jbc.273.4.2355

47. Abrami L, Velluz M-C, Hong Y, Ohishi K, Mehlert A, Ferguson M, et al. The glycan core of GPI-anchored proteins modulates aerolysin binding but is not sufficient: the polypeptide moiety is required for the toxin–receptor interaction. FEBS Letters. 2002;512(1–3):249–54. doi: 10.1016/s0014-5793(02)02274-3 11852090

48. Goel TC, Goel A. Etiology. Lymphatic Filariasis. Singapor: Springer; 2018. p. 19–25.

49. Fenn K, Blaxter M. Quantification of Wolbachia bacteria in Brugia malayi through the nematode lifecycle. Molecular and Biochemical Parasitology. 2004;137(2):361–4. doi: 10.1016/j.molbiopara.2004.06.012 15383308

50. Corsi AK, Wightman B, Chalfie M. A Transparent window into biology: A primer on Caenorhabditis elegans: WormBook; [updated June 18, 2015; cited 10.1895/wormbook.1.177.1. Available from: http://www.wormbook.org.

51. Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H. UpSet: Visualization of Intersecting Sets. IEEE transactions on visualization and computer graphics. 2014;20(12):1983–92. doi: 10.1109/TVCG.2014.2346248 26356912

52. Cortes LK, Vainauskas S, Dai N, McClung CM, Shah M, Benner JS, et al. Proteomic identification of mammalian cell surface derived glycosylphosphatidylinositol-anchored proteins through selective glycan enrichment. Proteomics. 2014;14(21–22):2471–84. doi: 10.1002/pmic.201400148 25262930

53. Caro LHP, Tettelin H, Vossen JH, Ram AFJ, Van Den Ende H, Klis FM. In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast. 1997;13(15):1477–89. doi: 10.1002/(SICI)1097-0061(199712)13:15<1477::AID-YEA184>3.0.CO;2-L 9434352

54. Harischandra H, Yuan W, Loghry HJ, Zamanian M, Kimber MJ. Profiling extracellular vesicle release by the filarial nematode Brugia malayi reveals sex-specific differences in cargo and a sensitivity to ivermectin. PLoS Neglected Tropical Diseases. 2018;12(4):e0006438. doi: 10.1371/journal.pntd.0006438 29659599

55. Moreno Y, Geary TG. Stage- and Gender-Specific Proteomic Analysis of Brugia malayi Excretory-Secretory Products. PLOS Neglected Tropical Diseases. 2008;2(10):e326. doi: 10.1371/journal.pntd.0000326 18958170

56. Bennuru S, Semnani R, Meng Z, Ribeiro JMC, Veenstra TD, Nutman TB. Brugia malayi Excreted/Secreted Proteins at the Host/Parasite Interface: Stage- and Gender-Specific Proteomic Profiling. PLoS Neglected Tropical Diseases. 2009;3(4):e410. doi: 10.1371/journal.pntd.0000410 19352421

57. Morris CP, Bennuru S, Kropp LE, Zweben JA, Meng Z, Taylor RT, et al. A Proteomic Analysis of the Body Wall, Digestive Tract, and Reproductive Tract of Brugia malayi. PLoS Neglected Tropical Diseases. 2015;9(9):e0004054. doi: 10.1371/journal.pntd.0004054 26367142

58. Bennuru S, Meng Z, Ribeiro JMC, Semnani RT, Ghedin E, Chan K, et al. Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proceedings of the National Academy of Sciences. 2011;108(23):9649.

59. Arumugam S, Wei J, Liu Z, Abraham D, Bell A, Bottazzi ME, et al. 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 Neglected Tropical Diseases. 2016;10(4):e0004586. doi: 10.1371/journal.pntd.0004586 27045170

60. Low MG, Finean JB. The action of phosphatidylinositol-specific phospholipases C on membranes. Biochemical Journal. 1976;154(1):203–8. doi: 10.1042/bj1540203 1275908

61. Low MG, Finean JB. Release of alkaline phosphatase from membranes by a phosphatidylinositol-specific phospholipase C. Biochemical Journal. 1977;167(1):281–4. doi: 10.1042/bj1670281 588258

62. Rao W, Isaac RE, Keen JN. An analysis of the Caenorhabditis elegans lipid raft proteome using geLC-MS/MS. J Proteomics. 2011;74(2):242–53. doi: 10.1016/j.jprot.2010.11.001 21070894

63. Roberts WL, Kim BH, Rosenberry TL. Differences in the glycolipid membrane anchors of bovine and human erythrocyte acetylcholinesterases. Proceedings of the National Academy of Sciences of the United States of America. 1987;84(22):7817–21. doi: 10.1073/pnas.84.22.7817 3479767

64. Stieger A, de Almeida MLC, Blatter MC, Brodbeck U, Bordier C. The membrane-anchoring systems of vertebrate acetylcholinesterase and variant surface glycoproteins of African trypanosomes share a common antigenic determinant. FEBS Letters. 1986;199(2):182–6. doi: 10.1016/0014-5793(86)80476-8 2422055

65. Low MG, Finean JB. Non-lytic release of acetylcholinesterase from erythrocytes by A phosphatidylinositol-specific phospholipase C. FEBS Letters. 1977;82(1):143–6. doi: 10.1016/0014-5793(77)80905-8 913568

66. Rathaur S D. Robertson B, Selkirk M, M. Maizels R. Secretory acetylcholinesterases from Brugia malayi and microfilarial parasites. 1988;26:257–65.

67. Veeranki S, Kim B, Kim L. The GPI-anchored superoxide dismutase SodC is essential for regulating basal Ras activity and for chemotaxis of Dictyostelium discoideum. Journal of Cell Science. 2008;121(18):3099.

68. Frand AR, Russel S, Ruvkun G. Functional genomic analysis of C. elegans molting. PLoS biology. 2005;3(10):e312–e. doi: 10.1371/journal.pbio.0030312 16122351

69. Tordai H, Bányai L, Patthy L. The PAN module: the N-terminal domains of plasminogen and hepatocyte growth factor are homologous with the apple domains of the prekallikrein family and with a novel domain found in numerous nematode proteins. FEBS Letters. 1999;461(1–2):63–7. doi: 10.1016/s0014-5793(99)01416-7 10561497


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