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Activity-Based Protein Profiling for the Study of Parasite Biology

  • Henry J. Benns
  • Edward W. Tate
  • Matthew A. ChildEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 420)

Abstract

Parasites exist within most ecological niches, often transitioning through biologically and chemically complex host environments over the course of their parasitic life cycles. While the development of technologies for genetic engineering has revolutionised the field of functional genomics, parasites have historically been less amenable to such modification. In light of this, parasitologists have often been at the forefront of adopting new small-molecule technologies, repurposing drugs into biological tools and probes. Over the last decade, activity-based protein profiling (ABPP) has evolved into a powerful and versatile chemical proteomic platform for characterising the function of enzymes. Central to ABPP is the use of activity-based probes (ABPs), which covalently modify the active sites of enzyme classes ranging from serine hydrolases to glycosidases. The application of ABPP to cellular systems has contributed vastly to our knowledge on the fundamental biology of a diverse range of organisms and has facilitated the identification of potential drug targets in many pathogens. In this chapter, we provide a comprehensive review on the different forms of ABPP that have been successfully applied to parasite systems, and highlight key biological insights that have been enabled through their application.

References

  1. Abdulla MH, O’Brien T, Mackey ZB, Sajid M, Grab DJ, McKerrow JH (2008) RNA interference of Trypanosoma brucei cathepsin B and L affects disease progression in a mouse model. PLoS Negl Trop Dis 2(9):e298.  https://doi.org/10.1371/journal.pntd.0000298CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abo M, Li C, Weerapana E (2018) Isotopically-labeled iodoacetamide-alkyne probes for quantitative cysteine-reactivity profiling. Mol Pharm 15(3):743–749.  https://doi.org/10.1021/acs.molpharmaceut.7b00832CrossRefPubMedGoogle Scholar
  3. Advisory Committee on the Microbiological Safety of Food (2012) Ad Hoc group on vulnerable groups. Risk profile in relation to Toxoplasma in the food chainGoogle Scholar
  4. Anderson KE, To M, Olzmann JA, Nomura DK (2017) Chemoproteomics-enabled covalent ligand screening reveals a thioredoxin-caspase 3 interaction disruptor that impairs breast cancer pathogenicity. ACS Chem Biol 12(10):2522–2528.  https://doi.org/10.1021/acschembio.7b00711CrossRefPubMedPubMedCentralGoogle Scholar
  5. Arastu-Kapur S, Ponder EL, Fonovic UP, Yeoh S, Yuan F, Fonovic M, Grainger M, Phillips CI, Powers JC, Bogyo M (2008) Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 4(3):203–213.  https://doi.org/10.1038/nchembio.70CrossRefPubMedGoogle Scholar
  6. Banerjee R, Liu J, Beatty W, Pelosof L, Klemba M, Goldberg DE (2002) Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc Natl Acad Sci U S A 99(2):990–995.  https://doi.org/10.1073/pnas.022630099CrossRefPubMedPubMedCentralGoogle Scholar
  7. Caffrey CR, Hansell E, Lucas KD, Brinen LS, Alvarez Hernandez A, Cheng J, Gwaltney SL 2nd, Roush WR, Stierhof YD, Bogyo M, Steverding D, McKerrow JH (2001) Active site mapping, biochemical properties and subcellular localization of rhodesain, the major cysteine protease of Trypanosoma brucei rhodesiense. Mol Biochem Parasitol 118(1):61–73CrossRefGoogle Scholar
  8. Chandramohanadas R, Davis PH, Beiting DP, Harbut MB, Darling C, Velmourougane G, Lee MY, Greer PA, Roos DS, Greenbaum DC (2009) Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 324(5928):794–797.  https://doi.org/10.1126/science.1171085CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chaparro JD, Cheng T, Tran UP, Andrade RM, Brenner SBT, Hwang G, Cohn S, Hirata K, McKerrow JH, Reed SL (2018) Two key cathepsins, TgCPB and TgCPL, are targeted by the vinyl sulfone inhibitor K11777 in in vitro and in vivo models of toxoplasmosis. PLoS ONE 13(3):e0193982.  https://doi.org/10.1371/journal.pone.0193982CrossRefPubMedPubMedCentralGoogle Scholar
  10. Child MA, Hall CI, Beck JR, Ofori LO, Albrow VE, Garland M, Bowyer PW, Bradley PJ, Powers JC, Boothroyd JC, Weerapana E, Bogyo M (2013) Small-molecule inhibition of a depalmitoylase enhances Toxoplasma host-cell invasion. Nat Chem Biol 9(10):651–656.  https://doi.org/10.1038/nchembio.1315CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chuh KN, Pratt MR (2015) Chemical methods for the proteome-wide identification of posttranslationally modified proteins. Curr Opin Chem Biol 24:27–37.  https://doi.org/10.1016/j.cbpa.2014.10.020CrossRefPubMedGoogle Scholar
  12. Chuh KN, Batt AR, Pratt MR (2016) Chemical methods for encoding and decoding of posttranslational modifications. Cell Chem Biol 23(1):86–107.  https://doi.org/10.1016/j.chembiol.2015.11.006CrossRefPubMedPubMedCentralGoogle Scholar
  13. Collins CR, Hackett F, Atid J, Tan MSY, Blackman MJ (2017) The Plasmodium falciparum pseudoprotease SERA5 regulates the kinetics and efficiency of malaria parasite egress from host erythrocytes. PLoS Pathog 13(7):e1006453.  https://doi.org/10.1371/journal.ppat.1006453CrossRefPubMedPubMedCentralGoogle Scholar
  14. Coombs GH, Goldberg DE, Klemba M, Berry C, Kay J, Mottram JC (2001) Aspartic proteases of Plasmodium falciparum and other parasitic protozoa as drug targets. Trends Parasitol 17(11):532–537CrossRefGoogle Scholar
  15. Cravatt BF, Wright AT, Kozarich JW (2008) Activity-based protein profiling: from enzyme chemistry to proteomic chemistry. Annu Rev Biochem 77:383–414.  https://doi.org/10.1146/annurev.biochem.75.101304.124125CrossRefPubMedGoogle Scholar
  16. Croft SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19(1):111–126.  https://doi.org/10.1128/CMR.19.1.111-126.2006CrossRefPubMedPubMedCentralGoogle Scholar
  17. Deng X, Weerapana E, Ulanovskaya O, Sun F, Liang H, Ji Q, Ye Y, Fu Y, Zhou L, Li J, Zhang H, Wang C, Alvarez S, Hicks LM, Lan L, Wu M, Cravatt BF, He C (2013) Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe 13(3):358–370.  https://doi.org/10.1016/j.chom.2013.02.004CrossRefPubMedPubMedCentralGoogle Scholar
  18. Doerig C (2004) Protein kinases as targets for anti-parasitic chemotherapy. Biochim Biophys Acta 1697(1–2):155–168.  https://doi.org/10.1016/j.bbapap.2003.11.021CrossRefPubMedGoogle Scholar
  19. Dou Z, Coppens I, Carruthers VB (2013) Non-canonical maturation of two papain-family proteases in Toxoplasma gondii. J Biol Chem 288(5):3523–3534.  https://doi.org/10.1074/jbc.M112.443697CrossRefPubMedGoogle Scholar
  20. Doyle PS, Zhou YM, Hsieh I, Greenbaum DC, McKerrow JH, Engel JC (2011) The Trypanosoma cruzi protease cruzain mediates immune evasion. PLoS Pathog 7(9):e1002139.  https://doi.org/10.1371/journal.ppat.1002139CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dvořák J, Mashiyama ST, Braschi S, Sajid M, Knudsen GM, Hansell E, Lim KC, Hsieh I, Bahgat M, Mackenzie B, Medzihradszky KF, Babbitt PC, Caffrey CR, McKerrow JH (2008) Differential use of protease families for invasion by Schistosome cercariae. Biochimie 90(2):345–358.  https://doi.org/10.1016/j.biochi.2007.08.013CrossRefPubMedGoogle Scholar
  22. Eksi S, Czesny B, Greenbaum DC, Bogyo M, Williamson KC (2004) Targeted disruption of Plasmodium falciparum cysteine protease, falcipain 1, reduces oocyst production, not erythrocytic stage growth. Mol Microbiol 53(1):243–250.  https://doi.org/10.1111/j.1365-2958.2004.04108.xCrossRefPubMedGoogle Scholar
  23. Flegr J, Prandota J, Sovickova M, Israili ZH (2014) Toxoplasmosis–a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE 9(3):e90203.  https://doi.org/10.1371/journal.pone.0090203CrossRefPubMedPubMedCentralGoogle Scholar
  24. G. B. D. Causes of Death Collaborators (2017) Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390(10100):1151–1210.  https://doi.org/10.1016/s0140-6736(17)32152-9CrossRefGoogle Scholar
  25. Garland M, Schulze CJ, Foe IT, van der Linden WA, Child MA, Bogyo M (2018) Development of an activity-based probe for acyl-protein thioesterases. PLoS ONE 13(1):e0190255.  https://doi.org/10.1371/journal.pone.0190255CrossRefPubMedPubMedCentralGoogle Scholar
  26. Goupil LS, Ivry SL, Hsieh I, Suzuki BM, Craik CS, O’Donoghue AJ, McKerrow JH (2016) Cysteine and aspartyl proteases contribute to protein digestion in the gut of freshwater planaria. PLoS Negl Trop Dis 10(8):e0004893.  https://doi.org/10.1371/journal.pntd.0004893CrossRefPubMedPubMedCentralGoogle Scholar
  27. Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M (2000) Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem Biol 7(8):569–581CrossRefGoogle Scholar
  28. Greenbaum DC, Baruch A, Grainger M, Bozdech Z, Medzihradszky KF, Engel J, DeRisi J, Holder AA, Bogyo M (2002) A role for the protease falcipain 1 in host cell invasion by the human malaria parasite. Science 298(5600):2002–2006.  https://doi.org/10.1126/science.1077426CrossRefPubMedGoogle Scholar
  29. Hacker SM, Backus KM, Lazear MR, Forli S, Correia BE, Cravatt BF (2017) Global profiling of lysine reactivity and ligandability in the human proteome. Nat Chem 9(12):1181–1190.  https://doi.org/10.1038/nchem.2826CrossRefPubMedPubMedCentralGoogle Scholar
  30. Haldar K, Bhattacharjee S, Safeukui I (2018) Drug resistance in Plasmodium. Nat Rev Microbiol 16(3):156–170.  https://doi.org/10.1038/nrmicro.2017.161CrossRefPubMedGoogle Scholar
  31. Hall CI, Reese ML, Weerapana E, Child MA, Bowyer PW, Albrow VE, Haraldsen JD, Phillips MR, Sandoval ED, Ward GE, Cravatt BF, Boothroyd JC, Bogyo M (2011) Chemical genetic screen identifies Toxoplasma DJ-1 as a regulator of parasite secretion, attachment, and invasion. Proc Natl Acad Sci U S A 108(26):10568–10573.  https://doi.org/10.1073/pnas.1105622108CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hammoudi PM, Jacot D, Mueller C, Di Cristina M, Dogga SK, Marq JB, Romano J, Tosetti N, Dubrot J, Emre Y, Lunghi M, Coppens I, Yamamoto M, Sojka D, Pino P, Soldati-Favre D (2015) Fundamental roles of the golgi-associated Toxoplasma aspartyl protease, ASP5, at the host-parasite interface. PLoS Pathog 11(10):e1005211.  https://doi.org/10.1371/journal.ppat.1005211CrossRefPubMedPubMedCentralGoogle Scholar
  33. Harbut MB, Velmourougane G, Dalal S, Reiss G, Whisstock JC, Onder O, Brisson D, McGowan S, Klemba M, Greenbaum DC (2011) Bestatin-based chemical biology strategy reveals distinct roles for malaria M1- and M17-family aminopeptidases. Proc Natl Acad Sci U S A 108(34):E526–E534.  https://doi.org/10.1073/pnas.1105601108CrossRefPubMedPubMedCentralGoogle Scholar
  34. He YX, Salafsky B, Ramaswamy K (2005) Comparison of skin invasion among three major species of Schistosoma. Trends Parasitol 21(5):201–203.  https://doi.org/10.1016/j.pt.2005.03.003CrossRefPubMedGoogle Scholar
  35. Kemp LE, Rusch M, Adibekian A, Bullen HE, Graindorge A, Freymond C, Rottmann M, Braun-Breton C, Baumeister S, Porfetye AT, Vetter IR, Hedberg C, Soldati-Favre D (2013) Characterization of a serine hydrolase targeted by acyl-protein thioesterase inhibitors in Toxoplasma gondii. J Biol Chem 288(38):27002–27018.  https://doi.org/10.1074/jbc.M113.460709CrossRefPubMedPubMedCentralGoogle Scholar
  36. Klemba M, Beatty W, Gluzman I, Goldberg DE (2004) Trafficking of plasmepsin II to the food vacuole of the malaria parasite Plasmodium falciparum. J Cell Biol 164(1):47–56.  https://doi.org/10.1083/jcb200307147CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kolb HC, Finn MG, Sharpless KB (2001) Click chemistry: diverse chemical function from a few good reactions. Angew Chem Int Ed Engl 40(11):2004–2021.  https://doi.org/10.1002/15213773(20010601)40:11CrossRefPubMedGoogle Scholar
  38. Larson ET, Parussini F, Huynh MH, Giebel JD, Kelley AM, Zhang L, Bogyo M, Merritt EA, Carruthers VB (2009) Toxoplasma gondii cathepsin L is the primary target of the invasion-inhibitory compound morpholinurea-leucyl-homophenyl-vinyl sulfone phenyl. J Biol Chem 284(39):26839–26850.  https://doi.org/10.1074/jbc.M109.003780CrossRefPubMedPubMedCentralGoogle Scholar
  39. Li H, van der Linden WA, Verdoes M, Florea BI, McAllister FE, Govindaswamy K, Elias JE, Bhanot P, Overkleeft HS, Bogyo M (2014) Assessing subunit dependency of the Plasmodium proteasome using small molecule inhibitors and active site probes. ACS Chem Biol 9(8):1869–1876.  https://doi.org/10.1021/cb5001263CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li H, O’Donoghue AJ, van der Linden WA, Xie SC, Yoo E, Foe IT, Tilley L, Craik CS, da Fonseca PC, Bogyo M (2016) Structure- and function-based design of Plasmodium-selective proteasome inhibitors. Nature 530(7589):233–236.  https://doi.org/10.1038/nature16936CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liu K, Shi H, Xiao H, Chong AG, Bi X, Chang YT, Tan KS, Yada RY, Yao SQ (2009) Functional profiling, identification, and inhibition of plasmepsins in intraerythrocytic malaria parasites. Angew Chem Int Ed Engl 48(44):8293–8297.  https://doi.org/10.1002/anie.200903747CrossRefPubMedGoogle Scholar
  42. Long JZ, Cravatt BF (2011) The metabolic serine hydrolases and their functions in mammalian physiology and disease. Chem Rev 111(10):6022–6063.  https://doi.org/10.1021/cr200075yCrossRefPubMedPubMedCentralGoogle Scholar
  43. López-Otín C, Bond JS (2008) Proteases: multifunctional enzymes in life and disease. J Biol Chem 283(45):30433–30437.  https://doi.org/10.1074/jbc.R800035200CrossRefPubMedPubMedCentralGoogle Scholar
  44. Martell J, Seo Y, Bak DW, Kingsley SF, Tissenbaum HA, Weerapana E (2016) Global cysteine-reactivity profiling during impaired insulin/IGF-1 signaling in C. elegans identifies uncharacterized mediators of longevity. Cell Chem Biol 23(8):955–966.  https://doi.org/10.1016/j.chembiol.2016.06.015CrossRefPubMedPubMedCentralGoogle Scholar
  45. McCall LI, Siqueira-Neto JL, McKerrow JH (2016) Location, location, location: five facts about tissue tropism and pathogenesis. PLoS Pathog 12(5):e1005519.  https://doi.org/10.1371/journal.ppat.1005519CrossRefPubMedPubMedCentralGoogle Scholar
  46. McGowan S (2013) Working in concert: the metalloaminopeptidases from Plasmodium falciparum. Curr Opin Struct Biol 23(6):828–835.  https://doi.org/10.1016/j.sbi.2013.07.015CrossRefPubMedGoogle Scholar
  47. McKerrow JH, Caffrey C, Kelly B, Loke P, Sajid M (2006) Proteases in parasitic diseases. Annu Rev Pathol 1:497–536.  https://doi.org/10.1146/annurev.pathol.1.110304.100151CrossRefPubMedGoogle Scholar
  48. Montero E, Gonzalez LM, Rodriguez M, Oksov Y, Blackman MJ, Lobo CA (2006) A conserved subtilisin protease identified in Babesia divergens merozoites. J Biol Chem 281(47):35717–35726.  https://doi.org/10.1074/jbc.M604344200CrossRefPubMedGoogle Scholar
  49. Monzote L, Siddiq A (2011) Drug development to protozoan diseases. Open Med Chem J 5:1–3.  https://doi.org/10.2174/1874104501105010001CrossRefPubMedPubMedCentralGoogle Scholar
  50. Munoz C, San Francisco J, Gutierrez B, Gonzalez J (2015) Role of the ubiquitin-proteasome systems in the biology and virulence of protozoan parasites. Biomed Res Int 2015:141526.  https://doi.org/10.1155/2015/141526CrossRefPubMedPubMedCentralGoogle Scholar
  51. Nasamu AS, Glushakova S, Russo I, Vaupel B, Oksman A, Kim AS, Fremont DH, Tolia N, Beck JR, Meyers MJ, Niles JC, Zimmerberg J, Goldberg DE (2017) Plasmepsins IX and X are essential and druggable mediators of malaria parasite egress and invasion. Science 358(6362):518–522.  https://doi.org/10.1126/science.aan1478CrossRefPubMedPubMedCentralGoogle Scholar
  52. Naughton JA, Nasizadeh S, Bell A (2010) Downstream effects of haemoglobinase inhibition in Plasmodium falciparum-infected erythrocytes. Mol Biochem Parasitol 173(2):81–87.  https://doi.org/10.1016/j.molbiopara.2010.05.007CrossRefPubMedGoogle Scholar
  53. Nazif T, Bogyo M (2001) Global analysis of proteasomal substrate specificity using positional-scanning libraries of covalent inhibitors. Proc Natl Acad Sci U S A 98(6):2967–2972.  https://doi.org/10.1073/pnas.061028898CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ndao M, Nath-Chowdhury M, Sajid M, Marcus V, Mashiyama ST, Sakanari J, Chow E, Mackey Z, Land KM, Jacobson MP, Kalyanaraman C, McKerrow JH, Arrowood MJ, Caffrey CR (2013) A cysteine protease inhibitor rescues mice from a lethal Cryptosporidium parvum infection. Antimicrob Agents Chemother 57(12):6063–6073.  https://doi.org/10.1128/AAC.00734-13CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nett IR, Martin DM, Miranda-Saavedra D, Lamont D, Barber JD, Mehlert A, Ferguson MA (2009) The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol Cell Proteomics 8(7):1527–1538.  https://doi.org/10.1074/mcp.M800556-MCP200CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nikolskaia OV, de ALAP, Kim YV, Lonsdale-Eccles JD, Fukuma T, Scharfstein J, Grab DJ (2006) Blood-brain barrier traversal by African trypanosomes requires calcium signaling induced by parasite cysteine protease. J Clin Invest 116(10):2739–2747.  https://doi.org/10.1172/jci27798CrossRefGoogle Scholar
  57. Nishino M, Choy JW, Gushwa NN, Oses-Prieto JA, Koupparis K, Burlingame AL, Renslo AR, McKerrow JH, Taunton J (2013) Hypothemycin, a fungal natural product, identifies therapeutic targets in Trypanosoma brucei [corrected]. Elife 2:e00712.  https://doi.org/10.7554/eLife.00712CrossRefPubMedPubMedCentralGoogle Scholar
  58. Parsons M, Worthey EA, Ward PN, Mottram JC (2005) Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genom 6:127.  https://doi.org/10.1186/1471-2164-6-127CrossRefGoogle Scholar
  59. Parussini F, Coppens I, Shah PP, Diamond SL, Carruthers VB (2010) Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii. Mol Microbiol 76(6):1340–1357.  https://doi.org/10.1111/j.1365-2958.2010.07181.xCrossRefPubMedPubMedCentralGoogle Scholar
  60. Que X, Wunderlich A, Joiner KA, Reed SL (2004) Toxopain-1 is critical for infection in a novel chicken embryo model of congenital toxoplasmosis. Infect Immun 72(5):2915–2921CrossRefGoogle Scholar
  61. Rathore S, Sinha D, Asad M, Bottcher T, Afrin F, Chauhan VS, Gupta D, Sieber SA, Mohmmed A (2010) A cyanobacterial serine protease of Plasmodium falciparum is targeted to the apicoplast and plays an important role in its growth and development. Mol Microbiol 77(4):873–890.  https://doi.org/10.1111/j.1365-2958.2010.07251.xCrossRefPubMedGoogle Scholar
  62. Rosenblum JS, Nomanbhoy TK, Kozarich JW (2013) Functional interrogation of kinases and other nucleotide-binding proteins. FEBS Lett 587(13):1870–1877.  https://doi.org/10.1016/j.febslet.2013.05.008CrossRefPubMedGoogle Scholar
  63. Russo I, Babbitt S, Muralidharan V, Butler T, Oksman A, Goldberg DE (2010) Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. Nature 463(7281):632–636.  https://doi.org/10.1038/nature08726CrossRefPubMedPubMedCentralGoogle Scholar
  64. Salmon BL, Oksman A, Goldberg DE (2001) Malaria parasite exit from the host erythrocyte: a two-step process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci U S A 98(1):271–276.  https://doi.org/10.1073/pnas.011413198CrossRefPubMedGoogle Scholar
  65. Schirmer A, Kennedy J, Murli S, Reid R, Santi DV (2006) Targeted covalent inactivation of protein kinases by resorcylic acid lactone polyketides. Proc Natl Acad Sci U S A 103(11):4234–4239.  https://doi.org/10.1073/pnas.0600445103CrossRefPubMedPubMedCentralGoogle Scholar
  66. Simner PJ (2017) Medical parasitology taxonomy update: january 2012 to december 2015. J Clin Microbiol 55(1):43–47.  https://doi.org/10.1128/JCM.01020-16CrossRefPubMedGoogle Scholar
  67. Suarez CE, Bishop RP, Alzan HF, Poole WA, Cooke BM (2017) Advances in the application of genetic manipulation methods to apicomplexan parasites. Int J Parasitol 47(12):701–710.  https://doi.org/10.1016/j.ijpara.2017.08.002CrossRefPubMedGoogle Scholar
  68. Teo CF, Zhou XW, Bogyo M, Carruthers VB (2007) Cysteine protease inhibitors block Toxoplasma gondii microneme secretion and cell invasion. Antimicrob Agents Chemother 51(2):679–688.  https://doi.org/10.1128/AAC.01059-06CrossRefPubMedGoogle Scholar
  69. Wang CC, Bozdech Z, Liu CL, Shipway A, Backes BJ, Harris JL, Bogyo M (2003) Biochemical analysis of the 20 S proteasome of Trypanosoma brucei. J Biol Chem 278(18):15800–15808.  https://doi.org/10.1074/jbc.M300195200CrossRefPubMedGoogle Scholar
  70. Weerapana E, Speers AE, Cravatt BF (2007) Tandem orthogonal proteolysis-activity-based protein profiling (TOP-ABPP)–a general method for mapping sites of probe modification in proteomes. Nat Protoc 2(6):1414–1425.  https://doi.org/10.1038/nprot.2007.194CrossRefPubMedGoogle Scholar
  71. Weerapana E, Wang C, Simon GM, Richter F, Khare S, Dillon MB, Bachovchin DA, Mowen K, Baker D, Cravatt BF (2010) Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468(7325):790–795.  https://doi.org/10.1038/nature09472CrossRefPubMedPubMedCentralGoogle Scholar
  72. World Health Organization (2017) World Malaria Report 2017. World Health Organization, GenevaCrossRefGoogle Scholar
  73. Yang P, Liu K (2015) Activity-based protein profiling: recent advances in probe development and applications. ChemBioChem 16(5):712–724.  https://doi.org/10.1002/cbic.201402582CrossRefPubMedGoogle Scholar
  74. Yang J, Gupta V, Tallman KA, Porter NA, Carroll KS, Liebler DC (2015) Global, in situ, site-specific analysis of protein S-sulfenylation. Nat Protoc 10(7):1022–1037.  https://doi.org/10.1038/nprot.2015.062CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yeoh S, O’Donnell RA, Koussis K, Dluzewski AR, Ansell KH, Osborne SA, Hackett F, Withers-Martinez C, Mitchell GH, Bannister LH, Bryans JS, Kettleborough CA, Blackman MJ (2007) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131(6):1072–1083.  https://doi.org/10.1016/j.cell.2007.10.049CrossRefPubMedGoogle Scholar
  76. Zhou Y, Wynia-Smith SL, Couvertier SM, Kalous KS, Marletta MA, Smith BC, Weerapana E (2016) Chemoproteomic strategy to quantitatively monitor transnitrosation uncovers functionally relevant S-nitrosation sites on Cathepsin D and HADH2. Cell Chem Biol 23(6):727–737.  https://doi.org/10.1016/j.chembiol.2016.05.008CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Henry J. Benns
    • 1
  • Edward W. Tate
    • 1
  • Matthew A. Child
    • 2
    Email author
  1. 1.Department of ChemistryImperial College LondonSouth Kensington, LondonUK
  2. 2.Life SciencesImperial College LondonSouth Kensington, LondonUK

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