Intramembrane proteolysis of Toxoplasma apical membrane antigen 1 facilitates host-cell invasion but is dispensable for replication

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 19, 2012, Pages 7463-7468

  Parussini, Fabiola ^a   Tang, Qing ^a   Moin, Syed M ^b   Mital, Jeffrey ^a,c   Urban, Sinisa ^b   Ward, Gary E ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cell signaling; Malaria; Microneme; Regulated intramembrane proteolysis

Indexed keywords

APICAL MEMBRANE ANTIGEN 1;

ALLELE; ARTICLE; CELL DIVISION; CELL INVASION; CONTROLLED STUDY; GROWTH DISORDER; HOST CELL; MUTATION; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TOXOPLASMA GONDII; TRANSGENICS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; BLOTTING, WESTERN; CELL DIVISION; CELL MEMBRANE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; GREEN FLUORESCENT PROTEINS; HOST-PARASITE INTERACTIONS; HUMANS; MALE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEOLYSIS; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TOXOPLASMA;

TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84860798774     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114661109     Document Type: Article

References (33)

1. Carruthers V, Boothroyd JC (2007) Pulling together: An integrated model of Toxoplasma cell invasion. Curr Opin Microbiol 10:83-89. (Pubitemid 46223639)
2. Waters AP, et al. (1990) A merozoite receptor protein from Plasmodium knowlesi is highly conserved and distributed throughout Plasmodium. J Biol Chem265:17974-17979.
3. Donahue CG, Carruthers VB, Gilk SD, Ward GE (2000) The Toxoplasma homolog of Plasmodium apical membrane antigen-1 (AMA-1) is a microneme protein secreted in response to elevated intracellular calcium levels. Mol Biochem Parasitol 111:15-30.
4. Hehl AB, et al. (2000) Toxoplasma gondii homologue of plasmodium apical membrane antigen 1 is involved in invasion of host cells. Infect Immun 68:7078-7086. (Pubitemid 32463422)
5. 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. (Pubitemid 41262901)
6. Giovannini D, et al. (2011) Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa. Cell Host Microbe 10:591-602.
7. Tonkin ML, et al. (2011) Host cell invasion by apicomplexan parasites: Insights from the co-structure of AMA1 with a RON2 peptide. Science 333:463-467.
8. Srinivasan P, et al. (2011) Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci USA 108:13275-13280.
9. 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.
10. Cao J, et al. (2009) Rhoptry neck protein RON2 forms a complex with microneme protein AMA1 in Plasmodium falciparum merozoites. Parasitol Int 58:29-35.
11. 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. (Pubitemid 44100714)
12. Alexander DL, Mital J, Ward GE, Bradley P, Boothroyd JC (2005) Identification of the moving junction complex of Toxoplasma gondii: A collaboration between distinct secretory organelles. PLoS Pathog 1:e17.
13. Lebrun M, et al. (2005) The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cell Microbiol 7:1823-1833. (Pubitemid 41685274)
14. Straub KW, Cheng SJ, Sohn CS, Bradley PJ (2009) Novel components of the Apicomplexan moving junction reveal conserved and coccidia-restricted elements. Cell Microbiol 11:590-603.
15. 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. (Pubitemid 24287311)
16. Urban S, Freeman M (2003) Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain. Mol Cell 11:1425-1434. (Pubitemid 36776530)
17. Howell SA, et al. (2005) Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens. Mol Microbiol 57:1342-1356. (Pubitemid 41176527)
18. 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. (Pubitemid 38878516)
19. Opitz C, et al. (2002) Intramembrane cleavage of microneme proteins at the surface of the apicomplexan parasite Toxoplasma gondii. EMBO J 21:1577-1585. (Pubitemid 34614614)
20. 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.
21. Brossier F, Jewett TJ, Sibley LD, Urban S (2005) A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc Natl Acad Sci USA 102:4146-4151. (Pubitemid 40388570)
22. Dowse TJ, Pascall JC, Brown KD, Soldati D (2005) Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. Int J Parasitol 35:747-756. (Pubitemid 40733613)
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. Carruthers VB, Blackman MJ (2005) A new release on life: Emerging concepts in proteolysis and parasite invasion. Mol Microbiol 55:1617-1630. (Pubitemid 40445201)
25. Santos JM, Ferguson DJP, 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.
26. Strisovsky K, Sharpe HJ, Freeman M (2009) Sequence-specific intramembrane proteolysis: Identification of a recognition motif in rhomboid substrates. Mol Cell 36:1048-1059.
27. Olivieri A, et al. (2011) Juxtamembrane shedding of Plasmodium falciparum AMA1 is sequence independent and essential, and helps evade invasion-inhibitory antibodies. PLoS Pathog 7:e1002448.
28. Meissner M, Brecht S, Bujard H, Soldati D (2001) Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res 29:E115.
29. Sheiner L, et al. (2010) Toxoplasma gondii transmembrane microneme proteins and their modular design. Mol Microbiol 77:912-929.
30. Gaji RY, Behnke MS, Lehmann MM, White MW, Carruthers VB (2011) Cell cycle-dependent, intercellular transmission of Toxoplasma gondii is accompanied by marked changes in parasite gene expression. Mol Microbiol 79:192-204.
31. Baker RP, Young K, Feng L, Shi Y, Urban S (2007) Enzymatic analysis of a rhomboid intramembrane protease implicates transmembrane helix 5 as the lateral substrate gate. Proc Natl Acad Sci USA 104:8257-8262. (Pubitemid 47175475)
32. Mital J, Schwarz J, Taatjes DJ, Ward GE (2006) Laser scanning cytometer-based assays for measuring host cell attachment and invasion by the human pathogen Toxoplasma gondii. Cytometry A 69:13-19. (Pubitemid 43062692)
33. Ward GE, Carey KL (1999) 96-Well plates providing high optical resolution for high-throughput, immunofluorescence-based screening of monoclonal antibodies against Toxoplasma gondii. J Immunol Methods 230:11-18.