Interrogating the Plasmodium Sporozoite Surface: Identification of Surface-Exposed Proteins and Demonstration of Glycosylation on CSP and TRAP by Mass Spectrometry-Based Proteomics

PLoS Pathogens

Volumn 12, Issue 4, 2016, Pages

  Swearingen, Kristian E ^a   Lindner, Scott E ^b,c   Shi, Lirong ^d   Shears, Melanie J ^d   Harupa, Anke ^b   Hopp, Christine S ^d   Vaughan, Ashley M ^b   Springer, Timothy A ^e   Moritz, Robert L ^a   Kappe, Stefan H I ^b   Sinnis, Photini ^d  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

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

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; CIRCUMSPOROZOITE PROTEIN; HEPARIN; MALARIA VACCINE; MEMBRANE PROTEIN; PARASITE ANTIGEN; SPOROZOITE VACCINE; THROMBOSPONDIN RELATED ANONYMOUS PROTEIN; UNCLASSIFIED DRUG; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; PROTOZOAL PROTEIN; THROMBOSPONDIN-RELATED ADHESIVE PROTEIN, PROTOZOAN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; FLUORESCENCE MICROSCOPY; GLYCOSYLATION; IMMUNOFLUORESCENCE TEST; INNER MEMBRANE; LIQUID CHROMATOGRAPHY; MALARIA FALCIPARUM; MASS SPECTROMETRY; MOUSE; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIABILITY; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEOMICS; SPOROZOITE; ANIMAL; CHEMISTRY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MOSQUITO; PROCEDURES; TRANSGENIC ORGANISM;

ANIMALS; CULICIDAE; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLATION; MALARIA, FALCIPARUM; MASS SPECTROMETRY; MEMBRANE PROTEINS; ORGANISMS, GENETICALLY MODIFIED; PROTEOMICS; PROTOZOAN PROTEINS; SPOROZOITES;

EID: 84964810080     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005606     Document Type: Article

References (95)

1. Lindner SE, Miller JL, Kappe SH, Malaria parasite pre-erythrocytic infection: preparation meets opportunity. Cell Microbiol. 2012;14(3):316–24. Epub 2011/12/14. doi: 10.1111/j.1462-5822.2011.01734.x22151703; PubMed Central PMCID: PMC3907120.
2. Sinnis P, Zavala F, The skin: where malaria infection and the host immune response begin. Semin Immunopathol.2012;34(6):787–92. Epub 2012/10/12. doi: 10.1007/s00281-012-0345-523053392; PubMed Central PMCID: PMC3934925.
3. Winzeler EA, Manary MJ, Drug resistance genomics of the antimalarial drug artemisinin. Genome Biol. 2014;15(11):544. Epub 2014/12/04. doi: s13059-014-0544-6 [pii] doi: 10.1186/s13059-014-0544-625470531; PubMed Central PMCID: PMC4283579.
4. Kumpornsin K, Modchang C, Heinberg A, Ekland EH, Jirawatcharadech P, Chobson P, et al. Origin of robustness in generating drug-resistant malaria parasites. Mol Biol Evol. 2014;31(7):1649–60. Epub 2014/04/18. doi: msu140 [pii] doi: 10.1093/molbev/msu14024739308; PubMed Central PMCID: PMC4069624.
5. Vannice KS, Brown GV, Akanmori BD, Moorthy VS, MALVAC 2012 scientific forum: accelerating development of second-generation malaria vaccines. Malar J. 2012;11:372. Epub 2012/11/13. doi: 1475-2875-11-372 [pii] doi: 10.1186/1475-2875-11-37223140365; PubMed Central PMCID: PMC3519521.
6. Olotu A, Fegan G, Wambua J, Nyangweso G, Awuondo KO, Leach A, et al. Four-year efficacy of RTS,S/AS01E and its interaction with malaria exposure. N Engl J Med. 2013;368(12):1111–20. Epub 2013/03/22. doi: 10.1056/NEJMoa120756423514288.
7. Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BG, Kabwende AL, et al. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med. 2012;367(24):2284–95. Epub 2012/11/10. doi: 10.1056/NEJMoa120839423136909.
8. Olotu A, Lusingu J, Leach A, Lievens M, Vekemans J, Msham S, et al. Efficacy of RTS,S/AS01E malaria vaccine and exploratory analysis on anti-circumsporozoite antibody titres and protection in children aged 5–17 months in Kenya and Tanzania: a randomised controlled trial. Lancet Infect Dis. 2011;11(2):102–9. Epub 2011/01/18. doi: S1473-3099(10)70262-0 [pii] doi: 10.1016/S1473-3099(10)70262-021237715; PubMed Central PMCID: PMC3341451.
9. White MT, Bejon P, Olotu A, Griffin JT, Riley EM, Kester KE, et al. The relationship between RTS,S vaccine-induced antibodies, CD4(+) T cell responses and protection against Plasmodium falciparum infection. PLoS One. 2013;8(4):e61395. Epub 2013/04/25. doi: 10.1371/journal.pone.0061395 PONE-D-12-36899 [pii]. 23613845; PubMed Central PMCID: PMC3628884.
10. Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep. 2013;3:3549. Epub 2013/12/20. doi: srep03549 [pii] doi: 10.1038/srep0354924351974.
11. Trieu A, Kayala MA, Burk C, Molina DM, Freilich DA, Richie TL, et al. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol Cell Proteomics. 2011;10(9):M111 007948. Epub 2011/06/02. doi: M111.007948 [pii] doi: 10.1074/mcp.M111.00794821628511; PubMed Central PMCID: PMC3186199.
12. Duffy PE, Sahu T, Akue A, Milman N, Anderson C, Pre-erythrocytic malaria vaccines: identifying the targets. Expert Rev Vaccines. 2012;11(10):1261–80. Epub 2012/11/28. doi: 10.1586/erv.12.9223176657; PubMed Central PMCID: PMC3584156.
13. Hodgson SH, Ewer KJ, Bliss CM, Edwards NJ, Rampling T, Anagnostou NA, et al. Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. J Infect Dis. 2015;211(7):1076–86. Epub 2014/10/23. doi: jiu579 [pii] doi: 10.1093/infdis/jiu57925336730; PubMed Central PMCID: PMC4354983.
14. Tables of malaria vaccine projects globally. Available from: http://www.who.int/immunization/research/development/Rainbow_tables/en/.
15. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, et al. A proteomic view of the Plasmodium falciparum life cycle. Nature. 2002;419(6906):520–6. Epub 2002/10/09. doi: 10.1038/nature01107 [pii]. 12368866.
16. Lasonder E, Janse CJ, van Gemert GJ, Mair GR, Vermunt AM, Douradinha BG, et al. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog. 2008;4(10):e1000195. Epub 2008/11/01. doi: 10.1371/journal.ppat.100019518974882; PubMed Central PMCID: PMC2570797.
17. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science. 2005;307(5706):82–6. Epub 2005/01/08. doi: 307/5706/82 [pii] doi: 10.1126/science.110371715637271.
18. Lindner SE, Swearingen KE, Harupa A, Vaughan AM, Sinnis P, Moritz RL, et al. Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics. 2013;12(5):1127–43. Epub 2013/01/18. doi: M112.024505 [pii] doi: 10.1074/mcp.M112.02450523325771; PubMed Central PMCID: PMC3650326.
19. Kennedy M, Fishbaugher ME, Vaughan AM, Patrapuvich R, Boonhok R, Yimamnuaychok N, et al. A rapid and scalable density gradient purification method for Plasmodium sporozoites. Malaria journal. 2012;11:421. doi: 10.1186/1475-2875-11-42123244590; PubMed Central PMCID: PMC3543293.
20. Staros JV, N-hydroxysulfosuccinimide active esters: bis(N-hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers. Biochemistry. 1982;21(17):3950–5. Epub 1982/08/17. 7126526.
21. Deutsch EW, Mendoza L, Shteynberg D, Slagel J, Sun Z, Moritz RL, Trans-Proteomic Pipeline, a standardized data processing pipeline for large-scale reproducible proteomics informatics. Proteomics Clin Appl. 2015. Epub 2015/01/30. doi: 10.1002/prca.20140016425631240.
22. Wass MN, Stanway R, Blagborough AM, Lal K, Prieto JH, Raine D, et al. Proteomic analysis of Plasmodium in the mosquito: progress and pitfalls. Parasitology. 2012;139(9):1131–45. Epub 2012/02/18. doi: S0031182012000133 [pii] doi: 10.1017/S003118201200013322336136; PubMed Central PMCID: PMC3417538.
23. Choi H, Larsen B, Lin ZY, Breitkreutz A, Mellacheruvu D, Fermin D, et al. SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods. 2011;8(1):70–3. Epub 2010/12/07. doi: nmeth.1541 [pii] doi: 10.1038/nmeth.154121131968; PubMed Central PMCID: PMC3064265.
24. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP, Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res. 2006;5(9):2339–47. Epub 2006/09/02. doi: 10.1021/pr060161n16944946.
25. Schiapparelli LM, McClatchy DB, Liu HH, Sharma P, Yates JR, 3rdCline HT, Direct detection of biotinylated proteins by mass spectrometry. J Proteome Res. 2014;13(9):3966–78. Epub 2014/08/15. doi: 10.1021/pr500286225117199; PubMed Central PMCID: PMC4156236.
26. Ejigiri I, Ragheb DR, Pino P, Coppi A, Bennett BL, Soldati-Favre D, et al. Shedding of TRAP by a rhomboid protease from the malaria sporozoite surface is essential for gliding motility and sporozoite infectivity. PLoS Pathog. 2012;8(7):e1002725. Epub 2012/08/23. doi: 10.1371/journal.ppat.1002725 PPATHOGENS-D-11-01012 [pii]. 22911675; PubMed Central PMCID: PMC3406075.
27. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37(Database issue):D539-43. Epub 2008/10/30. doi: gkn814 [pii] doi: 10.1093/nar/gkn81418957442; PubMed Central PMCID: PMC2686598.
28. Henderson B, Martin A, Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun. 2011;79(9):3476–91. Epub 2011/06/08. doi: IAI.00179-11 [pii] doi: 10.1128/IAI.00179-1121646455; PubMed Central PMCID: PMC3165470.
29. Pancholi V, Chhatwal GS, Housekeeping enzymes as virulence factors for pathogens. Int J Med Microbiol. 2003;293(6):391–401. Epub 2004/02/06. doi: S1438-4221(04)70173-3 [pii] doi: 10.1078/1438-4221-0028314760970.
30. Kumar N, Koski G, Harada M, Aikawa M, Zheng H, Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol. 1991;48(1):47–58. Epub 1991/09/01. doi: 0166-6851(91)90163-Z [pii]. 1779989.
31. Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI, Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol. 2006;61(3):614–30. Epub 2006/06/22. doi: MMI5244 [pii] doi: 10.1111/j.1365-2958.2006.05244.x16787449.
32. Mouray E, Moutiez M, Girault S, Sergheraert C, Florent I, Grellier P, Biochemical properties and cellular localization of Plasmodium falciparum protein disulfide isomerase. Biochimie. 2007;89(3):337–46. Epub 2006/12/15. doi: S0300-9084(06)00281-1 [pii] doi: 10.1016/j.biochi.2006.11.00117166645.
33. Zhang Y, Liu R, Ni M, Gill P, Lee AS, Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J Biol Chem. 2010;285(20):15065–75. Epub 2010/03/09. doi: M109.087445 [pii] doi: 10.1074/jbc.M109.08744520208072; PubMed Central PMCID: PMC2865300.
34. Robert J, Menoret A, Cohen N, Cell surface expression of the endoplasmic reticular heat shock protein gp96 is phylogenetically conserved. J Immunol. 1999;163(8):4133–9. Epub 1999/10/08. doi: ji_v163n8p4133 [pii]. 10510348.
35. Ghosh AK, Coppens I, Gardsvoll H, Ploug M, Jacobs-Lorena M, Plasmodium ookinetes coopt mammalian plasminogen to invade the mosquito midgut. Proc Natl Acad Sci U S A. 2011;108(41):17153–8. Epub 2011/09/29. doi: 1103657108 [pii] doi: 10.1073/pnas.110365710821949403; PubMed Central PMCID: PMC3193258.
36. Ghosh AK, Jacobs-Lorena M, Surface-expressed enolases of Plasmodium and other pathogens. Mem Inst Oswaldo Cruz. 2011;106Suppl 1:85–90. Epub 2011/09/09. doi: S0074-02762011000900011 [pii]. 21881761; PubMed Central PMCID: PMC4153683.
37. Hernandez-Romano J, Rodriguez MH, Pando V, Torres-Monzon JA, Alvarado-Delgado A, Lecona Valera AN, et al. Conserved peptide sequences bind to actin and enolase on the surface of Plasmodium berghei ookinetes. Parasitology. 2011;138(11):1341–53. Epub 2011/08/06. doi: S0031182011001296 [pii] doi: 10.1017/S003118201100129621816124.
38. Montagna GN, Buscaglia CA, Munter S, Goosmann C, Frischknecht F, Brinkmann V, et al. Critical role for heat shock protein 20 (HSP20) in migration of malarial sporozoites. J Biol Chem. 2012;287(4):2410–22. Epub 2011/12/06. doi: M111.302109 [pii] doi: 10.1074/jbc.M111.30210922139844; PubMed Central PMCID: PMC3268402.
39. Katris NJ, van Dooren GG, McMillan PJ, Hanssen E, Tilley L, Waller RF, The apical complex provides a regulated gateway for secretion of invasion factors in Toxoplasma. PLoS Pathog. 2014;10(4):e1004074. Epub 2014/04/20. doi: 10.1371/journal.ppat.1004074 PPATHOGENS-D-13-02653 [pii]. 24743791; PubMed Central PMCID: PMC3990729.
40. Carruthers VB, Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol Int. 1999;48(1):1–10. Epub 2001/03/28. doi: S1383576998000427 [pii]. 11269320.
41. Carruthers VB, Sibley LD, Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol. 1997;73(2):114–23. Epub 1997/06/01. 9208224.
42. Vanderberg JP, Studies on the motility of Plasmodium sporozoites. J Protozool. 1974;21(4):527–37. Epub 1974/10/01. 4138523.
43. Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P, The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem. 2001;276(29):26784–91. Epub 2001/05/16. doi: 10.1074/jbc.M104038200 [pii]. 11352923; PubMed Central PMCID: PMC3941197.
44. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, et al. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2007;2(5):316–27. Epub 2007/11/17. doi: S1931-3128(07)00248-X [pii] doi: 10.1016/j.chom.2007.10.00218005753; PubMed Central PMCID: PMC2117360.
45. ApiLoc—A database of published protein sub-cellular localisation in Apicomplexa. Available from: http://apiloc.biochem.unimelb.edu.au/apiloc/apiloc.
46. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003;301(5639):1503–8. Epub 2003/08/02. doi: 10.1126/science.1087025 [pii]. 12893887.
47. Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF, Apicomplexan cytoskeleton and motors: key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol. 2009;39(2):153–62. Epub 2008/11/26. doi: S0020-7519(08)00390-1 [pii] doi: 10.1016/j.ijpara.2008.10.00719028497.
48. Harding CR, Meissner M, The inner membrane complex through development of Toxoplasma gondii and Plasmodium. Cell Microbiol. 2014;16(5):632–41. Epub 2014/03/13. doi: 10.1111/cmi.1228524612102; PubMed Central PMCID: PMC4286798.
49. Lal K, Prieto JH, Bromley E, Sanderson SJ, Yates JR, 3rdWastling JM, et al. Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics. 2009;9(5):1142–51. Epub 2009/02/12. doi: 10.1002/pmic.20080040419206106; PubMed Central PMCID: PMC2706521.
50. Bergman LW, Kaiser K, Fujioka H, Coppens I, Daly TM, Fox S, et al. Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J Cell Sci. 2003;116(Pt 1):39–49. Epub 2002/11/29. 12456714.
51. Gaskins E, Gilk S, DeVore N, Mann T, Ward G, Beckers C, Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol. 2004;165(3):383–93. Epub 2004/05/05. doi: 10.1083/jcb.200311137 jcb.200311137 [pii]. 15123738; PubMed Central PMCID: PMC2172186.
52. Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, Soldati-Favre D, Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe. 2010;8(4):343–57. Epub 2010/10/19. doi: S1931-3128(10)00304-5 [pii] doi: 10.1016/j.chom.2010.09.00220951968.
53. Tucker RP, The thrombospondin type 1 repeat superfamily. Int J Biochem Cell Biol. 2004;36(6):969–74. Epub 2004/04/20. doi: 10.1016/j.biocel.2003.12.011 S135727250300428X [pii]. 15094110.
54. Shao L, Haltiwanger RS, O-fucose modifications of epidermal growth factor-like repeats and thrombospondin type 1 repeats: unusual modifications in unusual places. Cell Mol Life Sci. 2003;60(2):241–50. Epub 2003/04/08. 12678489.
55. Hofsteenge J, Huwiler KG, Macek B, Hess D, Lawler J, Mosher DF, et al. C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J Biol Chem. 2001;276(9):6485–98. Epub 2000/11/09. doi: 10.1074/jbc.M008073200 [pii]. 11067851.
56. Sato T, Sato M, Kiyohara K, Sogabe M, Shikanai T, Kikuchi N, et al. Molecular cloning and characterization of a novel human beta1,3-glucosyltransferase, which is localized at the endoplasmic reticulum and glucosylates O-linked fucosylglycan on thrombospondin type 1 repeat domain. Glycobiology. 2006;16(12):1194–206. Epub 2006/08/11. doi: cwl035 [pii] doi: 10.1093/glycob/cwl03516899492.
57. Kozma K, Keusch JJ, Hegemann B, Luther KB, Klein D, Hess D, et al. Identification and characterization of abeta1,3-glucosyltransferase that synthesizes the Glc-beta1,3-Fuc disaccharide on thrombospondin type 1 repeats. J Biol Chem. 2006;281(48):36742–51. Epub 2006/10/13. doi: M605912200 [pii] doi: 10.1074/jbc.M60591220017032646.
58. Hofsteenge J, Muller DR, de Beer T, Loffler A, Richter WJ, Vliegenthart JF, New type of linkage between a carbohydrate and a protein: C-glycosylation of a specific tryptophan residue in human RNase Us. Biochemistry. 1994;33(46):13524–30. Epub 1994/11/22. 7947762.
59. Julenius K, NetCGlyc 1.0: prediction of mammalian C-mannosylation sites. Glycobiology. 2007;17(8):868–76. Epub 2007/05/12. doi: cwm050 [pii] doi: 10.1093/glycob/cwm05017494086.
60. Song G, Koksal AC, Lu C, Springer TA, Shape change in the receptor for gliding motility in Plasmodium sporozoites. Proc Natl Acad Sci U S A. 2012;109(52):21420–5. Epub 2012/12/14. doi: 1218581109 [pii] doi: 10.1073/pnas.121858110923236185; PubMed Central PMCID: PMC3535621.
61. Doud MB, Koksal AC, Mi LZ, Song G, Lu C, Springer TA, Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci U S A. 2012;109(20):7817–22. Epub 2012/05/02. doi: 1205737109 [pii] doi: 10.1073/pnas.120573710922547819; PubMed Central PMCID: PMC3356675.
62. Song G, Springer TA, Structures of the Toxoplasma gliding motility adhesin. Proc Natl Acad Sci U S A. 2014;111(13):4862–7. Epub 2014/03/19. doi: 1403059111 [pii] doi: 10.1073/pnas.140305911124639528; PubMed Central PMCID: PMC3977308.
63. Macek B, Hofsteenge J, Peter-Katalinic J, Direct determination of glycosylation sites in O-fucosylated glycopeptides using nano-electrospray quadrupole time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2001;15(10):771–7. Epub 2001/05/10. doi: 10.1002/rcm.29811344537.
64. Wang LW, Leonhard-Melief C, Haltiwanger RS, Apte SS, Post-translational modification of thrombospondin type-1 repeats in ADAMTS-like 1/punctin-1 by C-mannosylation of tryptophan. J Biol Chem. 2009;284(44):30004–15. Epub 2009/08/13. doi: M109.038059 [pii] doi: 10.1074/jbc.M109.03805919671700; PubMed Central PMCID: PMC2781554.
65. Copley SD, Moonlighting is mainstream: paradigm adjustment required. Bioessays. 2012;34(7):578–88. Epub 2012/06/15. doi: 10.1002/bies.20110019122696112.
66. Henderson B, Martin A, Bacterial moonlighting proteins and bacterial virulence. Curr Top Microbiol Immunol. 2013;358:155–213. Epub 2011/12/07. doi: 10.1007/82_2011_18822143554.
67. Collingridge PW, Brown RW, Ginger ML, Moonlighting enzymes in parasitic protozoa. Parasitology. 2010;137(9):1467–75. Epub 2010/03/18. doi: S0031182010000259 [pii] doi: 10.1017/S003118201000025920233494.
68. Moorthy VS, Imoukhuede EB, Milligan P, Bojang K, Keating S, Kaye P, et al. A randomised, double-blind, controlled vaccine efficacy trial of DNA/MVA ME-TRAP against malaria infection in Gambian adults. PLoS Med. 2004;1(2):e33. Epub 2004/11/05. doi: 10.1371/journal.pmed.001003315526058; PubMed Central PMCID: PMC524376.
69. Gowda DC, Gupta P, Davidson EA, Glycosylphosphatidylinositol anchors represent the major carbohydrate modification in proteins of intraerythrocytic stage Plasmodium falciparum. J Biol Chem. 1997;272(10):6428–39. Epub 1997/03/07. 9045667.
70. Samuelson J, Banerjee S, Magnelli P, Cui J, Kelleher DJ, Gilmore R, et al. The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci U S A. 2005;102(5):1548–53. Epub 2005/01/25. doi: 0409460102 [pii] doi: 10.1073/pnas.040946010215665075; PubMed Central PMCID: PMC545090.
71. Bushkin GG, Ratner DM, Cui J, Banerjee S, Duraisingh MT, Jennings CV, et al. Suggestive evidence for Darwinian Selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii. Eukaryot Cell. 2010;9(2):228–41. Epub 2009/09/29. doi: EC.00197-09 [pii] doi: 10.1128/EC.00197-0919783771; PubMed Central PMCID: PMC2823003.
72. Sanz S, Bandini G, Ospina D, Bernabeu M, Marino K, Fernandez-Becerra C, et al. Biosynthesis of GDP-fucose and other sugar nucleotides in the blood stages of Plasmodium falciparum. J Biol Chem. 2013;288(23):16506–17. Epub 2013/04/26. doi: M112.439828 [pii] doi: 10.1074/jbc.M112.43982823615908; PubMed Central PMCID: PMC3675586.
73. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, Wang SK, et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science. 2011;334(6059):1097–103. Epub 2011/10/15. doi: science.1213256 [pii] doi: 10.1126/science.121325621998254; PubMed Central PMCID: PMC3280215.
74. Florens L, Liu X, Wang Y, Yang S, Schwartz O, Peglar M, et al. Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol Biochem Parasitol. 2004;135(1):1–11. Epub 2004/08/04. 15287581.
75. Buettner FF, Ashikov A, Tiemann B, Lehle L, Bakker H, C. elegans DPY-19 is a C-mannosyltransferase glycosylating thrombospondin repeats. Mol Cell. 2013;50(2):295–302. Epub 2013/04/09. doi: S1097-2765(13)00206-2 [pii] doi: 10.1016/j.molcel.2013.03.00323562325.
76. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 2015;43(Database issue):D213-21. Epub 2014/11/28. doi: gku1243 [pii] doi: 10.1093/nar/gku124325428371; PubMed Central PMCID: PMC4383996.
77. Luca VC, Jude KM, Pierce NW, Nachury MV, Fischer S, Garcia KC, Structural biology. Structural basis for Notch1 engagement of Delta-like 4. Science. 2015;347(6224):847–53. Epub 2015/02/24. doi: 347/6224/847 [pii] doi: 10.1126/science.126109325700513; PubMed Central PMCID: PMC4445638.
78. Reece WH, Pinder M, Gothard PK, Milligan P, Bojang K, Doherty T, et al. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat Med. 2004;10(4):406–10. Epub 2004/03/23. doi: 10.1038/nm1009 [pii]. 15034567.
79. Jalloh A, Jalloh M, Matsuoka H, T-cell epitope polymorphisms of the Plasmodium falciparum circumsporozoite protein among field isolates from Sierra Leone: age-dependent haplotype distribution?Malar J. 2009;8:120. Epub 2009/06/09. doi: 1475-2875-8-120 [pii] doi: 10.1186/1475-2875-8-12019500348; PubMed Central PMCID: PMC2698914.
80. Lindner SE, Mikolajczak SA, Vaughan AM, Moon W, Joyce BR, Sullivan WJ, Jr.et al. Perturbations of Plasmodium Puf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility. Cellular microbiology. 2013;15(7):1266–83. doi: 10.1111/cmi.1211623356439; PubMed Central PMCID: PMC3815636.
81. Harupa A, Sack BK, Lakshmanan V, Arang N, Douglass AN, Oliver BG, et al. SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility. Infection and immunity. 2014;82(11):4643–53. doi: 10.1128/IAI.01800-1425156733; PubMed Central PMCID: PMC4249349.
82. Lindner SE, Sartain MJ, Hayes K, Harupa A, Moritz RL, Kappe SH, et al. Enzymes involved in plastid-targeted phosphatidic acid synthesis are essential for Plasmodium yoelii liver-stage development. Mol Microbiol. 2014;91(4):679–93. Epub 2013/12/18. doi: 10.1111/mmi.1248524330260; PubMed Central PMCID: PMC3925071.
83. Sack BK, Miller JL, Vaughan AM, Douglass A, Kaushansky A, Mikolajczak S, et al. Model for in vivo assessment of humoral protection against malaria sporozoite challenge by passive transfer of monoclonal antibodies and immune serum. Infect Immun. 2014;82(2):808–17. Epub 2014/01/31. doi: IAI.01249-13 [pii] doi: 10.1128/IAI.01249-1324478094; PubMed Central PMCID: PMC3911395.
84. Kaiser K, Matuschewski K, Camargo N, Ross J, Kappe SH, Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol Microbiol. 2004;51(5):1221–32. Epub 2004/02/26. doi: 10.1046/j.1365-2958.2003.03909.x [pii]. 14982620.
85. Green JL, Rees-Channer RR, Howell SA, Martin SR, Knuepfer E, Taylor HM, et al. The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase. J Biol Chem. 2008;283(45):30980–9. Epub 2008/09/05. doi: M803129200 [pii] doi: 10.1074/jbc.M80312920018768477; PubMed Central PMCID: PMC2576532.
86. Kessner D, Chambers M, Burke R, Agus D, Mallick P, ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics. 2008;24(21):2534–6. Epub 2008/07/09. doi: 10.1093/bioinformatics/btn32318606607; PubMed Central PMCID: PMC2732273.
87. Craig R, Beavis RC, TANDEM: matching proteins with tandem mass spectra. Bioinformatics. 2004;20(9):1466–7. 14976030.
88. Eng JK, Jahan TA, Hoopmann MR, Comet: an open-source MS/MS sequence database search tool. Proteomics. 2013;13(1):22–4. Epub 2012/11/14. doi: 10.1002/pmic.20120043923148064.
89. Anker R, Zavala F, Pollok BA, VH and VL region structure of antibodies that recognize the (NANP)3 dodecapeptide sequence in the circumsporozoite protein of Plasmodium falciparum. Eur J Immunol. 1990;20(12):2757–61. Epub 1990/12/01. doi: 10.1002/eji.18302012332125276.
90. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74(20):5383–92. Epub 2002/10/31. 12403597.
91. Deutsch EW, Mendoza L, Shteynberg D, Slagel J, Sun Z, Moritz RL, Trans-Proteomic Pipeline, a standardized data processing pipeline for large-scale reproducible proteomics informatics. Proteomics Clin Appl. 2015;9(7–8):745–54. Epub 2015/01/30. doi: 10.1002/prca.20140016425631240.
92. Shteynberg D, Deutsch EW, Lam H, Eng JK, Sun Z, Tasman N, et al. iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates. Mol Cell Proteomics. 2011;10(12):M111 007690. Epub 2011/08/31. doi: 10.1074/mcp.M111.00769021876204; PubMed Central PMCID: PMC3237071.
93. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75(17):4646–58. Epub 2003/11/25. 14632076.
94. Hendrickson EL, Xia Q, Wang T, Leigh JA, Hackett M, Comparison of spectral counting and metabolic stable isotope labeling for use with quantitative microbial proteomics. Analyst. 2006;131(12):1335–41. Epub 2006/11/25. doi: 10.1039/b610957h17124542; PubMed Central PMCID: PMC2660848.
95. Karpievitch YV, Dabney AR, Smith RD, Normalization and missing value imputation for label-free LC-MS analysis. BMC Bioinformatics. 2012;13Suppl 16:S5. Epub 2012/11/28. doi: 1471-2105-13-S16-S5 [pii] doi: 10.1186/1471-2105-13-S16-S523176322; PubMed Central PMCID: PMC3489534.