Juxtamembrane shedding of plasmodium falciparum AMA1 is sequence independent and essential, and helps evade invasion-inhibitory antibodies

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Olivieri, Anna ^a   Collins, Christine R ^a   Hackett, Fiona ^a   Withers Martinez, Chrislaine ^a   Marshall, Joshua ^a   Flynn, Helen R ^b   Skehel, J Mark ^b   Blackman, Michael J ^b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL MEMBRANE ANTIGEN 1; GENOMIC DNA; MALARIA VACCINE; PARASITE ANTIGEN; POLYCLONAL ANTIBODY; SUB2 PROTEIN; UNCLASSIFIED DRUG; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

AFFINITY CHROMATOGRAPHY; ANTIBODY RESPONSE; ARTICLE; GENE LOCUS; GENE REPLICATION; JUXTAMEMBRANE SHEDDING; MASS SPECTROMETRY; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; MUTAGENESIS; NONHUMAN; PARASITE CULTIVATION; PARASITOSIS; PLASMID; PLASMODIUM FALCIPARUM; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; HOMOLOGOUS RECOMBINATION; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOGENICITY;

PLASMODIUM FALCIPARUM;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; HOMOLOGOUS RECOMBINATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

EID: 84855282762     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002448     Document Type: Article

References (80)

1. Fraiture M, Baxter RH, Steinert S, Chelliah Y, Frolet C, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273-284.
2. Beeson JG, Osier FH, Engwerda CR, (2008) Recent insights into humoral and cellular immune responses against malaria. Trends Parasitol 24: 578-584.
3. O'Donnell RA, Blackman MJ, (2005) The role of malaria merozoite proteases in red blood cell invasion. Curr Opin Microbiol. 8: 422-427.
4. Soldati-Favre D, (2008) Molecular dissection of host cell invasion by the apicomplexans: the glideosome. Parasite 15: 197-205.
5. Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T, (1975) Invasion of erythrocytes by malaria merozoites. Science 187: 748-750.
6. Aikawa M, Miller LH, Johnson J, Rabbege J, (1978) Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J Cell Biol 77: 72-82.
7. Gilson PR, Crabb BS, (2009) Morphology and kinetics of the three distinct phases of red blood cell invasion by Plasmodium falciparum merozoites. Int J Parasitol 39: 91-96.
8. Howell SA, Hackett F, Jongco AM, Withers-Martinez C, Kim K, et al. (2005) Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens. Mol Microbiol 57: 1342-1356.
9. Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA, (1990) A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 172: 379-382.
10. Blackman MJ, Chappel JA, Shai S, Holder AA, (1993) A conserved parasite serine protease processes the Plasmodium falciparum merozoite surface protein-1. Mol Biochem Parasitol 62: 103-114.
11. Harris PK, Yeoh S, Dluzewski AR, O'Donnell RA, Withers-Martinez C, et al. (2005) Molecular identification of a malaria merozoite surface sheddase. PLoS Pathog 1: 241-251.
12. Howell SA, Well I, Fleck SL, Kettleborough C, Collins CR, et al. (2003) A single malaria merozoite serine protease mediates shedding of multiple surface proteins by juxtamembrane cleavage. J Biol Chem 278: 23890-23898.
13. Green JL, Hinds L, Grainger M, Knuepfer E, Holder AA, (2006) Plasmodium thrombospondin related apical merozoite protein (PTRAMP) is shed from the surface of merozoites by PfSUB2 upon invasion of erythrocytes. Mol Biochem Parasitol 150: 114-117.
14. Blackman MJ, Ling IT, Nicholls SC, Holder AA, (1991) Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Mol Biochem Parasitol 49: 29-33.
15. Schlondorff J, Blobel CP, (1999) Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci 112 (Pt 21): 3603-3617.
16. Wang X, He K, Gerhart M, Huang Y, Jiang J, et al. (2002) Metalloprotease-mediated GH receptor proteolysis and GHBP shedding. Determination of extracellular domain stem region cleavage site. J Biol Chem 277: 50510-50519.
17. Schwager SL, Chubb AJ, Woodman ZL, Yan L, Mentele R, et al. (2001) Cleavage of disulfide-bridged stalk domains during shedding of angiotensin-converting enzyme occurs at multiple juxtamembrane sites. Biochemistry 40: 15624-15630.
18. Pang S, Chubb AJ, Schwager SL, Ehlers MR, Sturrock ED, et al. (2001) Roles of the juxtamembrane and extracellular domains of angiotensin-converting enzyme in ectodomain shedding. Biochem J 358: 185-192.
19. Tanaka K, Chazenbalk GD, McLachlan SM, Rapoport B, (2000) Evidence that cleavage of the thyrotropin receptor involves a "molecular ruler" mechanism: deletion of amino acid residues 305-320 causes a spatial shift in cleavage site 1 independent of amino acid motif. Endocrinology 141: 3573-3577.
20. Maruyama K, Kametani F, Usami M, Yamao-Harigaya W, Tanaka K, (1991) "Secretase," Alzheimer amyloid protein precursor secreting enzyme is not sequence-specific. Biochem Biophys Res Commun 179: 1670-1676.
21. O'Donnell RA, Hackett F, Howell SA, Treeck M, Struck N, et al. (2006) Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 174: 1023-1033.
22. Baker RP, Wijetilaka R, Urban S, (2006) Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog 2: e113.
23. Buguliskis JS, Brossier F, Shuman J, Sibley LD, (2010) Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii. PLoS Pathog 6: e1000858.
24. Santos JM, Ferguson DJ, Blackman MJ, Soldati-Favre D, (2011) Intramembrane Cleavage of AMA1 Triggers Toxoplasma to Switch from an Invasive to a Replicative Mode. Science 331: 473-477.
25. Uzureau P, Barale JC, Janse CJ, Waters AP, Breton CB, (2004) Gene targeting demonstrates that the Plasmodium berghei subtilisin PbSUB2 is essential for red cell invasion and reveals spontaneous genetic recombination events. Cell Microbiol 6: 65-78.
26. Fleck SL, Birdsall B, Babon J, Dluzewski AR, Martin SR, et al. (2003) Suramin and suramin analogues inhibit merozoite surface protein-1 secondary processing and erythrocyte invasion by the malaria parasite Plasmodium falciparum. J Biol Chem 278: 47670-47677.
27. Blackman MJ, Scott-Finnigan TJ, Shai S, Holder AA, (1994) Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J Exp Med 180: 389-393.
28. Uthaipibull C, Aufiero B, Syed SE, Hansen B, Guevara Patino JA, et al. (2001) Inhibitory and blocking monoclonal antibody epitopes on merozoite surface protein 1 of the malaria parasite Plasmodium falciparum. J Mol Biol 307: 1381-1394.
29. Woehlbier U, Epp C, Hackett F, Blackman MJ, Bujard H, (2010) Antibodies against multiple merozoite surface antigens of the human malaria parasite Plasmodium falciparum inhibit parasite maturation and red blood cell invasion. Malar J 9: 77.
30. Dutta S, Haynes JD, Moch JK, Barbosa A, Lanar DE, (2003) Invasion-inhibitory antibodies inhibit proteolytic processing of apical membrane antigen 1 of Plasmodium falciparum merozoites. Proc Natl Acad Sci USA 100: 12295-12300.
31. Dutta S, Haynes JD, Barbosa A, Ware LA, Snavely JD, et al. (2005) Mode of action of invasion-inhibitory antibodies directed against apical membrane antigen 1 of Plasmodium falciparum. Infect Immun 73: 2116-2122.
32. Collins CR, Withers-Martinez C, Hackett F, Blackman MJ, (2009) An inhibitory antibody blocks interactions between components of the malarial invasion machinery. PLoS Pathog 5: e1000273.
33. Alexander DL, Arastu-Kapur S, Dubremetz JF, Boothroyd JC, (2006) Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryot Cell 5: 1169-1173.
34. Lamarque M, Besteiro S, Papoin J, Roques M, Vulliez-Le Normand B, et al. (2011) The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathog 7: e1001276.
35. Tonkin ML, Roques M, Lamarque MH, Pugniere M, Douguet D, et al. (2011) Host cell invasion by apicomplexan parasites: insights from the co-structure of AMA1 with a RON2 peptide. Science 333: 463-467.
36. Tyler JS, Boothroyd JC, (2011) The C-terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathog 7: e1001282.
37. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, et al. (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38: 706-718.
38. O'Donnell RA, Saul A, Cowman AF, Crabb BS, (2000) Functional conservation of the malaria vaccine antigen MSP-119across distantly related Plasmodium species. Nat Med 6: 91-95.
39. Drew DR, O'Donnell RA, Smith BJ, Crabb BS, (2004) A common cross-species function for the double epidermal growth factor-like modules of the highly divergent plasmodium surface proteins MSP-1 and MSP-8. J Biol Chem 279: 20147-20153.
40. Combe A, Giovannini D, Carvalho TG, Spath S, Boisson B, et al. (2009) Clonal conditional mutagenesis in malaria parasites. Cell Host Microbe 5: 386-396.
41. Mital J, Meissner M, Soldati D, Ward GE, (2005) Conditional Expression of Toxoplasma gondii Apical Membrane Antigen-1 (TgAMA1) Demonstrates That TgAMA1 Plays a Critical Role in Host Cell Invasion. Mol Biol Cell 16: 4341-4349.
42. Hehl AB, Lekutis C, Grigg ME, Bradley PJ, Dubremetz JF, et al. (2000) Toxoplasma gondii homologue of plasmodium apical membrane antigen 1 is involved in invasion of host cells. Infect Immun 68: 7078-7086.
43. Gaffar FR, Yatsuda AP, Franssen FF, de Vries E, (2004) Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infect Immun 72: 2947-2955.
44. Leykauf K, Treeck M, Gilson PR, Nebl T, Braulke T, et al. (2010) Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite. PLoS Pathog 6: e1000941.
45. Treeck M, Zacherl S, Herrmann S, Cabrera A, Kono M, et al. (2009) Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathog 5: e1000322.
46. Remarque EJ, Faber BW, Kocken CH, Thomas AW, (2008) Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol 24: 74-84.
47. Holder AA, (2009) The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136: 1445-1456.
48. Miura K, Zhou H, Diouf A, Moretz SE, Fay MP, et al. (2009) Anti-apical-membrane-antigen-1 antibody is more effective than anti-42-kilodalton-merozoite-surface-protein-1 antibody in inhibiting plasmodium falciparum growth, as determined by the in vitro growth inhibition assay. Clin Vaccine Immunol 16: 963-968.
49. Malkin EM, Diemert DJ, McArthur JH, Perreault JR, Miles AP, et al. (2005) Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. Infect Immun 73: 3677-3685.
50. Roestenberg M, Remarque E, de Jonge E, Hermsen R, Blythman H, et al. (2008) Safety and immunogenicity of a recombinant Plasmodium falciparum AMA1 malaria vaccine adjuvanted with Alhydrogel, Montanide ISA 720 or AS02. PLoS One 3: e3960.
51. Sagara I, Dicko A, Ellis RD, Fay MP, Diawara SI, et al. (2009) A randomized controlled phase 2 trial of the blood stage AMA1-C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 27: 3090-3098.
52. Spring MD, Cummings JF, Ockenhouse CF, Dutta S, Reidler R, et al. (2009) Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS One 4: e5254.
53. Thompson FM, Porter DW, Okitsu SL, Westerfeld N, Vogel D, et al. (2008) Evidence of blood stage efficacy with a virosomal malaria vaccine in a phase IIa clinical trial. PLoS One 3: e1493.
54. Ogutu BR, Apollo OJ, McKinney D, Okoth W, Siangla J, et al. (2009) Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS One 4: e4708.
55. Carruthers VB, Blackman MJ, (2005) A new release on life: emerging concepts in proteolysis and parasite invasion. Mol Microbiol 55: 1617-1630.
56. Brossier F, Jewett TJ, Lovett JL, Sibley LD, (2003) C-terminal processing of the toxoplasma protein MIC2 is essential for invasion into host cells. J Biol Chem 278: 6229-6234.
57. Saul A, (1987) Kinetic constraints on the development of a malaria vaccine. Parasite Immunol 9: 1-9.
58. Zhou XW, Blackman MJ, Howell SA, Carruthers VB, (2004) Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex. Mol Cell Proteomics. 3: 565-576.
59. Opitz C, Di Cristina M, Reiss M, Ruppert T, Crisanti A, et al. (2002) Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J 21: 1577-1585.
60. Schechter I, Berger A, (1967) On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 27: 157-162.
61. Strisovsky K, Sharpe HJ, Freeman M, (2009) Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates. Mol Cell 36: 1048-1059.
62. Akiyama Y, Maegawa S, (2007) Sequence features of substrates required for cleavage by GlpG, an Escherichia coli rhomboid protease. Mol Microbiol 64: 1028-1037.
63. Collins CR, Withers-Martinez C, Bentley GA, Batchelor AH, Thomas AW, et al. (2007) Fine Mapping of an Epitope Recognized by an Invasion-inhibitory Monoclonal Antibody on the Malaria Vaccine Candidate Apical Membrane Antigen 1. J Biol Chem 282: 7431-7441.
64. Pizarro JC, Normand BV, Chesne-Seck ML, Collins CR, Withers-Martinez C, et al. (2005) Crystal structure of the malaria vaccine candidate apical membrane antigen 1. Science 308: 408-411.
65. Narum DL, Thomas AW, (1994) Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol Biochem Parasitol 67: 59-68.
66. Howell SA, Withers-Martinez C, Kocken CH, Thomas AW, Blackman MJ, (2001) Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. J Biol Chem 276: 31311-31320.
67. O'Donnell RA, Freitas-Junior LH, Preiser PR, Williamson DH, Duraisingh M, et al. (2002) A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. EMBO J 21: 1231-1239.
68. Vanhoof G, Goossens F, De Meester I, Hendriks D, Scharpe S, (1995) Proline motifs in peptides and their biological processing. Faseb J 9: 736-744.
69. Chesne-Seck ML, Pizarro JC, Normand BV, Collins CR, Blackman MJ, et al. (2005) Structural comparison of apical membrane antigen 1 orthologues and paralogues in apicomplexan parasites. Mol Biochem Parasitol 144: 55-67.
70. Harris KS, Casey JL, Coley AM, Masciantonio R, Sabo JK, et al. (2005) Binding hot spot for invasion inhibitory molecules on Plasmodium falciparum apical membrane antigen 1. Infect Immun 73: 6981-6989.
71. Harris KS, Casey JL, Coley AM, Karas JA, Sabo JK, et al. (2009) Rapid optimization of a peptide inhibitor of malaria parasite invasion by comprehensive N-methyl scanning. J Biol Chem 284: 9361-9371.
72. Richard D, MacRaild CA, Riglar DT, Chan JA, Foley M, et al. (2010) Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. J Biol Chem 285: 14815-14822.
73. Kocken CH, van der Wel AM, Dubbeld MA, Narum DL, van de Rijke FM, et al. (1998) Precise timing of expression of a Plasmodium falciparum-derived transgene in Plasmodium berghei is a critical determinant of subsequent subcellular localization. J Biol Chem 273: 15119-15124.
74. Urban S, (2010) Taking the plunge: integrating structural, enzymatic and computational insights into a unified model for membrane-immersed rhomboid proteolysis. Biochem J 425: 501-512.
75. Waters AP, Thomas AW, Deans JA, Mitchell GH, Hudson DE, et al. (1990) A merozoite receptor protein from Plasmodium knowlesi is highly conserved and distributed throughout Plasmodium. J Biol Chem 265: 17974-17979.
76. Gantt S, Persson C, Rose K, Birkett AJ, Abagyan R, et al. (2000) Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect Immun 68: 3667-3673.
77. Blackman MJ, (1994) Purification of Plasmodium falciparum merozoites for analysis of the processing of merozoite surface protein-1. Methods Cell Biol 45: 213-220.
78. Delplace P, Dubremetz JF, Fortier B, Vernes A, (1985) A 50 kilodalton exoantigen specific to the merozoite release-reinvasion stage of Plasmodium falciparum. Mol Biochem Parasitol 17: 239-251.
79. Blackman MJ, Whittle H, Holder AA, (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.
80. Silmon de Monerri NC, Flynn HR, Campos MG, Hackett F, Koussis K, et al. (2011) Global Identification of Multiple Substrates for PfSUB1, an Essential Malarial Processing Protease. Infect Immun 79: 1086-1097.