Plasmodium falciparum SERA5 plays a non-enzymatic role in the malarial asexual blood-stage lifecycle

Molecular Microbiology

Volumn 96, Issue 2, 2015, Pages 368-387

  Stallmach, Robert ^a   Kavishwar, Manoli ^a   Withers Martinez, Chrislaine ^a   Hackett, Fiona ^a   Collins, Christine R ^a   Howell, Steven A ^a   Yeoh, Sharon ^a   Knuepfer, Ellen ^a   Atid, Avshalom J ^a   Holder, Anthony A ^a   Blackman, Michael J ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; CYSTEINE; CYSTEINE PROTEINASE; PROTEIN SERA5; RECOMBINANT ENZYME; SERINE; UNCLASSIFIED DRUG; PARASITE ANTIGEN; PEPTIDE HYDROLASE; SERINE REPEAT ANTIGEN 5, PLASMODIUM FALCIPARUM;

AMINO ACID SUBSTITUTION; APICOMPLEXAN LIFE CYCLE STAGE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; HOMOLOGOUS RECOMBINATION; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SERA5 GENE; ASEXUAL REPRODUCTION; BLOOD; CHEMISTRY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LIFE CYCLE STAGE; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PROTEIN MOTIF;

PLASMODIUM FALCIPARUM;

AMINO ACID MOTIFS; ANTIGENS, PROTOZOAN; HUMANS; LIFE CYCLE STAGES; MALARIA, FALCIPARUM; PEPTIDE HYDROLASES; PLASMODIUM FALCIPARUM; REPRODUCTION, ASEXUAL;

EID: 84926407704     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12941     Document Type: Article

References (72)

1. Adrain, C., and Freeman, M. (2012) New lives for old: evolution of pseudoenzyme function illustrated by iRhoms. Nat Rev Mol Cell Biol 13: 489-498.
2. Adrain, C., Zettl, M., Christova, Y., Taylor, N., and Freeman, M. (2012) Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science 335: 225-228.
3. Alam, A., and Chauhan, V.S. (2012) Inhibitory potential of prodomain of Plasmodium falciparum protease serine repeat antigen 5 for asexual blood stages of parasite. PLoS ONE 7: e30452.
4. Aoki, S., Li, J., Itagaki, S., Okech, B.A., Egwang, T.G., Matsuoka, H., etal. (2002) Serine repeat antigen (SERA5) is predominantly expressed among the SERA multigene family of Plasmodium falciparum, and the acquired antibody titers correlate with serum inhibition of the parasite growth. J Biol Chem 277: 47533-47540.
5. Arastu-Kapur, S., Ponder, E.L., Fonovic, U.P., Yeoh, S., Yuan, F., Fonovic, M., etal. (2008) Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 4: 203-213.
6. Arisue, N., Hirai, M., Arai, M., Matsuoka, H., and Horii, T. (2007) Phylogeny and evolution of the SERA multigene family in the genus Plasmodium. J Mol Evol 65: 82-91.
7. Arisue, N., Kawai, S., Hirai, M., Palacpac, N.M., Jia, M., Kaneko, A., etal. (2011) Clues to evolution of the SERA multigene family in 18 Plasmodium species. PLoS ONE 6: e17775.
8. Ashley, E.A., Dhorda, M., Fairhurst, R.M., Amaratunga, C., Lim, P., Suon, S., etal. (2014) Spread of artemisinin resistance in plasmodium falciparum malaria. N Engl J Med 371: 411-423.
9. Barr, P.J., Inselburg, J., Green, K.M., Kansopon, J., Hahm, B.K., Gibson, H.L., etal. (1991) Immunogenicity of recombinant Plasmodium falciparum SERA proteins in rodents. Mol Biochem Parasitol 45: 159-170.
10. Bartlett, G.J., Borkakoti, N., and Thornton, J.M. (2003) Catalysing new reactions during evolution: economy of residues and mechanism. J Mol Biol 331: 829-860.
11. Bergbold, N., and Lemberg, M.K. (2013) Emerging role of rhomboid family proteins in mammalian biology and disease. Biochim Biophys Acta 1828: 2840-2848.
12. Bergmann-Leitner, E.S., Duncan, E.H., Mullen, G.E., Burge, J.R., Khan, F., Long, C.A., etal. (2006) Critical evaluation of different methods for measuring the functional activity of antibodies against malaria blood stage antigens. Am J Trop Med Hyg 75: 437-442.
13. Blackman, M.J. (1994) Purification of Plasmodium falciparum merozoites for analysis of the processing of merozoite surface protein-1. Methods Cell Biol 45: 213-220.
14. Blackman, M.J. (2008) Malarial proteases and host cell egress: an 'emerging' cascade. Cell Microbiol 10: 1925-1934.
15. Blackman, M.J., Whittle, H., and Holder, A.A. (1991) Processing of the Plasmodium falciparum major merozoite surface protein-1: identification of a 33-kilodalton secondary processing product which is shed prior to erythrocyte invasion. Mol Biochem Parasitol 49: 35-44.
16. Blackman, M.J., Corrie, J.E., Croney, J.C., Kelly, G., Eccleston, J.F., and Jameson, D.M. (2002) Structural and biochemical characterization of a fluorogenic rhodamine-labeled malarial protease substrate. Biochemistry 41: 12244-12252.
17. Bourgon, R., Delorenzi, M., Sargeant, T., Hodder, A.N., Crabb, B.S., and Speed, T.P. (2004) The serine repeat antigen (SERA) gene family phylogeny in Plasmodium: the impact of GC content and reconciliation of gene and species trees. Mol Biol Evol 21: 2161-2171.
18. Burrows, J.N., van Huijsduijnen, R.H., Mohrle, J.J., Oeuvray, C., and Wells, T.N. (2013) Designing the next generation of medicines for malaria control and eradication. Malar J 12: 187.
19. Cha, J.N., Shimizu, K., Zhou, Y., Christiansen, S.C., Chmelka, B.F., Stucky, G.D., and Morse, D.E. (1999) Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proc Natl Acad Sci USA 96: 361-365.
20. Christova, Y., Adrain, C., Bambrough, P., Ibrahim, A., and Freeman, M. (2013) Mammalian iRhoms have distinct physiological functions including an essential role in TACE regulation. EMBO Rep 14: 884-890.
21. Clark, P.I., and Lowe, G. (1978) Conversion of the active-site cysteine residue of papain into a dehydro-serine, a serine and a glycine residue. Eur J Biochem 84: 293-299.
22. Collins, C.R., Withers-Martinez, C., Hackett, F., and Blackman, M.J. (2009) An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog 5: e1000273.
23. Collins, C.R., Hackett, F., Strath, M., Penzo, M., Withers-Martinez, C., Baker, D.A., and Blackman, M.J. (2013a) Malaria parasite cGMP-dependent protein kinase regulates blood stage merozoite secretory organelle discharge and egress. PLoS Pathog 9: e1003344.
24. Collins, C.R., Das, S., Wong, E.H., Andenmatten, N., Stallmach, R., Hackett, F., etal. (2013b) Robust inducible Cre recombinase activity in the human malaria parasite Plasmodium falciparum enables efficient gene deletion within a single asexual erythrocytic growth cycle. Mol Microbiol 88: 687-701.
25. Coulombe, R., Grochulski, P., Sivaraman, J., Menard, R., Mort, J.S., and Cygler, M. (1996) Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J 15: 5492-5503.
26. Debrabant, A., Maes, P., Delplace, P., Dubremetz, J.F., Tartar, A., and Camus, D. (1992) Intramolecular mapping of Plasmodium falciparum P126 proteolytic fragments by N-terminal amino acid sequencing. Mol Biochem Parasitol 53: 89-95.
27. Delplace, P., Dubremetz, J.F., Fortier, B., and Vernes, A. (1985) A 50 kilodalton exoantigen specific to the merozoite release-reinvasion stage of Plasmodium falciparum. Mol Biochem Parasitol 17: 239-251.
28. Delplace, P., Bhatia, A., Cagnard, M., Camus, D., Colombet, G., Debrabant, A., etal. (1988) Protein p126: a parasitophorous vacuole antigen associated with the release of Plasmodium falciparum merozoites. Biol Cell 64: 215-221.
29. Devedjiev, Y., Popov, A., Atanasov, B., and Bartunik, H.D. (1997) X-ray structure at 1.76 A resolution of a polypeptide phospholipase A2 inhibitor. J Mol Biol 266: 160-172.
30. Drenth, J., Kalk, K.H., and Swen, H.M. (1976) Binding of chloromethyl ketone substrate analogues to crystalline papain. Biochemistry 15: 3731-3738.
31. Dvorak, J.A., Miller, L.H., Whitehouse, W.C., and Shiroishi, T. (1975) Invasion of erythrocytes by malaria merozoites. Science 187: 748-750.
32. Enders, B., Hundt, E., and Knapp, B. (1992) Protection of Aotus monkeys after immunization with recombinant antigens of Plasmodium falciparum. Mem Inst Oswaldo Cruz 87 (Suppl. 3): 413-422.
33. Fairlie, W.D., Spurck, T.P., McCoubrie, J.E., Gilson, P.R., Miller, S.K., McFadden, G.I., etal. (2008) Inhibition of malaria parasite development by a cyclic peptide that targets the vital parasite protein SERA5. Infect Immun 76: 4332-4344.
34. Fox, B.A., Xing-Li, P., Suzue, K., Horii, T., and Bzik, D.J. (1997) Plasmodium falciparum: an epitope within a highly conserved region of the 47-kDa amino-terminal domain of the serine repeat antigen is a target of parasite-inhibitory antibodies. Exp Parasitol 85: 121-134.
35. Harris, P.K., Yeoh, S., Dluzewski, A.R., O'Donnell, R.A., Withers-Martinez, C., Hackett, F., etal. (2005) Molecular identification of a malaria merozoite surface sheddase. PLoS Pathog 1: 241-251.
36. Hata, S., Kitamura, F., and Sorimachi, H. (2013) Efficient expression and purification of recombinant human mu-calpain using an Escherichia coli expression system. Genes Cells 18: 753-763.
37. Hayashi, R., Moore, S., and Stein, W.H. (1973) Carboxypeptidase from yeast. Large scale preparation and the application to COOH-terminal analysis of peptides and proteins. J Biol Chem 248: 2296-2302.
38. Hodder, A.N., Drew, D.R., Epa, V.C., Delorenzi, M., Bourgon, R., Miller, S.K., etal. (2003) Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. J Biol Chem 278: 48169-48177.
39. Hodder, A.N., Malby, R.L., Clarke, O.B., Fairlie, W.D., Colman, P.M., Crabb, B.S., and Smith, B.J. (2009) Structural insights into the protease-like antigen Plasmodium falciparum SERA5 and its noncanonical active-site serine. J Mol Biol 392: 154-165.
40. Holder, A.A., and Freeman, R.R. (1982) Biosynthesis and processing of a Plasmodium falciparum schizont antigen recognized by immune serum and a monoclonal antibody. J Exp Med 156: 1528-1538.
41. Horii, T., Shirai, H., Jie, L., Ishii, K.J., Palacpac, N.Q., Tougan, T., etal. (2010) Evidences of protection against blood-stage infection of Plasmodium falciparum by the novel protein vaccine SE36. Parasitol Int 59: 380-386.
42. Inselburg, J., Bzik, D.J., Li, W.B., Green, K.M., Kansopon, J., Hahm, B.K., etal. (1991) Protective immunity induced in Aotus monkeys by recombinant SERA proteins of Plasmodium falciparum. Infect Immun 59: 1247-1250.
43. Janse, C.J., Ramesar, J., and Waters, A.P. (2006) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356.
44. Jean, L., Hackett, F., Martin, S.R., and Blackman, M.J. (2003) Functional characterization of the propeptide of Plasmodium falciparum subtilisin-like protease-1. J Biol Chem 278: 28572-28579.
45. Kanodia, S., Kumar, G., Rizzi, L., Pedretti, A., Hodder, A.N., Romeo, S., and Malhotra, P. (2014) Synthetic peptides derived from the C-terminal 6kDa region of Plasmodium falciparum SERA5 inhibit the enzyme activity and malaria parasite development. Biochim Biophys Acta 1840: 2765-2775.
46. Li, J., Mitamura, T., Fox, B.A., Bzik, D.J., and Horii, T. (2002) Differential localization of processed fragments of Plasmodium falciparum serine repeat antigen and further processing of its N-terminal 47kDa fragment. Parasitol Int 51: 343-352.
47. Liu, Y., Patricelli, M.P., and Cravatt, B.F. (1999) Activity-based protein profiling: the serine hydrolases. Proc Natl Acad Sci USA 96: 14694-14699.
48. McCoubrie, J.E., Miller, S.K., Sargeant, T., Good, R.T., Hodder, A.N., Speed, T.P., etal. (2007) Evidence for a common role for the serine-type Plasmodium falciparum serine repeat antigen proteases: implications for vaccine and drug design. Infect Immun 75: 5565-5574.
49. Miller, S.K., Good, R.T., Drew, D.R., Delorenzi, M., Sanders, P.R., Hodder, A.N., etal. (2002) A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem 277: 47524-47532.
50. Moss, D.K., Remarque, E.J., Faber, B.W., Cavanagh, D.R., Arnot, D.E., Thomas, A.W., and Holder, A.A. (2012) Plasmodium falciparum 19-kilodalton merozoite surface protein 1 (MSP1)-specific antibodies that interfere with parasite growth in vitro can inhibit MSP1 processing, merozoite invasion, and intracellular parasite development. Infect Immun 80: 1280-1287.
51. Muller, W.E., Schroder, H.C., Burghard, Z., Pisignano, D., and Wang, X. (2013) Silicateins-a novel paradigm in bioinorganic chemistry: enzymatic synthesis of inorganic polymeric silica. Chemistry (Easton) 19: 5790-5804.
52. O'Farrell, P.A., Gonzalez, F., Zheng, W., Johnston, S.A., and Joshua-Tor, L. (1999) Crystal structure of human bleomycin hydrolase, a self-compartmentalizing cysteine protease. Structure 7: 619-627.
53. Okech, B., Mujuzi, G., Ogwal, A., Shirai, H., Horii, T., and Egwang, T.G. (2006) High titers of IgG antibodies against Plasmodium falciparum serine repeat antigen 5 (SERA5) are associated with protection against severe malaria in Ugandan children. Am J Trop Med Hyg 74: 191-197.
54. Pang, X.L., Mitamura, T., and Horii, T. (1999) Antibodies reactive with the N-terminal domain of Plasmodium falciparum serine repeat antigen inhibit cell proliferation by agglutinating merozoites and schizonts. Infect Immun 67: 1821-1827.
55. Pils, B., and Schultz, J. (2004) Inactive enzyme-homologues find new function in regulatory processes. J Mol Biol 340: 399-404.
56. Proto, W.R., Castanys-Munoz, E., Black, A., Tetley, L., Moss, C.X., Juliano, L., etal. (2011) Trypanosoma brucei metacaspase 4 is a pseudopeptidase and a virulence factor. J Biol Chem 286: 39914-39925.
57. Putrianti, E.D., Schmidt-Christensen, A., Arnold, I., Heussler, V.T., Matuschewski, K., and Silvie, O. (2010) The Plasmodium serine-type SERA proteases display distinct expression patterns and non-essential in vivo roles during life cycle progression of the malaria parasite. Cell Microbiol 12: 725-739.
58. Reese, M.L., and Boyle, J.P. (2012) Virulence without catalysis: how can a pseudokinase affect host cell signaling? Trends Parasitol 28: 53-57.
59. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
60. Ruecker, A., Shea, M., Hackett, F., Suarez, C., Hirst, E.M., Milutinovic, K., etal. (2012) Proteolytic activation of the essential parasitophorous vacuole cysteine protease SERA6 accompanies malaria parasite egress from its host erythrocyte. J Biol Chem 287: 37949-37963.
61. Stallmach, R., and Gloor, S.M. (2008) Neurobin/TMPRSS11c, a novel type II transmembrane serine protease that cleaves fibroblast growth factor-2 in vitro. Biochem J 412: 81-91.
62. Sugiyama, T., Suzue, K., Okamoto, M., Inselburg, J., Tai, K., and Horii, T. (1996) Production of recombinant SERA proteins of Plasmodium falciparum in Escherichia coli by using synthetic genes. Vaccine 14: 1069-1076.
63. Turkenburg, J.P., Lamers, M.B., Brzozowski, A.M., Wright, L.M., Hubbard, R.E., Sturt, S.L., and Williams, D.H. (2002) Structure of a Cys25→Ser mutant of human cathepsin S. Acta Crystallogr D Biol Crystallogr 58: 451-455.
64. Van Criekinge, W., Beyaert, R., Van de Craen, M., Vandenabeele, P., Schotte, P., De Valck, D., and Fiers, W. (1996) Functional characterization of the prodomain of interleukin-1beta-converting enzyme. J Biol Chem 271: 27245-27248.
65. White, N.J., Pukrittayakamee, S., Hien, T.T., Faiz, M.A., Mokuolu, O.A., and Dondorp, A.M. (2014) Malaria. Lancet 383: 723-735.
66. Willert, E.K., Fitzpatrick, R., and Phillips, M.A. (2007) Allosteric regulation of an essential trypanosome polyamine biosynthetic enzyme by a catalytically dead homolog. Proc Natl Acad Sci USA 104: 8275-8280.
67. Withers-Martinez, C., Saldanha, J.W., Ely, B., Hackett, F., O'Connor, T., and Blackman, M.J. (2002) Expression of recombinant Plasmodium falciparum subtilisin-like protease-1 in insect cells. Characterization, comparison with the parasite protease, and homology modeling. J Biol Chem 277: 29698-29709.
68. Withers-Martinez, C., Suarez, C., Fulle, S., Kher, S., Penzo, M., Ebejer, J.P., etal. (2012) Plasmodium subtilisin-like protease 1 (SUB1): insights into the active-site structure, specificity and function of a pan-malaria drug target. Int J Parasitol 42: 597-612.
69. Withers-Martinez, C., Strath, M., Hackett, F., Haire, L.F., Howell, S.A., Walker, P.A., etal. (2014) The malaria parasite egress protease SUB1 is a calcium-dependent redox switch subtilisin. Nat Commun 5: 3726.
70. Yahata, K., Treeck, M., Culleton, R., Gilberger, T.W., and Kaneko, O. (2012) Time-lapse imaging of red blood cell invasion by the rodent malaria parasite Plasmodium yoelii. PLoS ONE 7: e50780.
71. Yeoh, S., O'Donnell, R.A., Koussis, K., Dluzewski, A.R., Ansell, K.H., Osborne, S.A., etal. (2007) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131: 1072-1083.
72. Zettl, M., Adrain, C., Strisovsky, K., Lastun, V., and Freeman, M. (2011) Rhomboid family pseudoproteases use the ER quality control machinery to regulate intercellular signaling. Cell 145: 79-91.