Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Leykauf, Kerstin ^a   Treeck, Moritz ^b   Gilson, Paul R ^a   Nebl, Thomas ^c   Braulke, Thomas ^d   Cowman, Alan F ^c   Gilberger, Tim W ^b,e   Crabb, Brendan S ^a,f,g  

^a MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e MCMASTER UNIVERSITY   (Canada)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; APICAL MEMBRANE ANTIGEN 1; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; SERINE; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CELL INVASION; CYTOSOL; ERYTHROCYTE; GENE MUTATION; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SCHIZONT; AMINO ACID SEQUENCE; HUMAN; IMMUNOPRECIPITATION; MALARIA FALCIPARUM; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; PHOSPHORYLATION; SEQUENCE HOMOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

PLASMODIUM FALCIPARUM;

AMINO ACID SEQUENCE; ANTIGENS, PROTOZOAN; BLOTTING, WESTERN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ERYTHROCYTES; HUMANS; IMMUNOPRECIPITATION; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77954665296     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000941     Document Type: Article

References (36)

1. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434: 214-217.
2. Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124: 755-766.
3. Bannister L, Mitchell G (2003) The ins, outs and roundabouts of malaria. Trends Parasitol 19: 209-213.
4. Healer J, Crawford S, Ralph S, McFadden G, Cowman AF (2002) Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect Immun 70: 5751-5758.
5. Hodder A, Crewther P, Matthew M, Reid G, Moritz R, et al. (1996) The disulfide bond structure of Plasmodium apical membrane antigen-1. J Biol Chem 271: 29446-29452.
6. Peterson MG, Marshall VM, Smythe JA, Crewther PE, Lew A, et al. (1989) Integral membrane protein located in the apical complex of Plasmodium falciparum. Mol Cell Biol 9: 3151-3154.
7. 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.
8. 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.
9. 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.
10. 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.
11. Mitchell GH, Thomas AW, Margos G, Dluzewski AR, Bannister LH (2004) Apical membrane antigen 1, a major malaria vaccine candidate, mediates the close attachment of invasive merozoites to host red blood cells. Infect Immun 72: 154-158.
12. Urquiza M, Suarez JE, Cardenas C, Lopez R, Puentes A, et al. (2000) Plasmodium falciparum AMA-1 erythrocyte binding peptides implicate AMA-1 as erythrocyte binding protein. Vaccine 19: 508-513.
13. Bai T, Becker M, Gupta A, Strike P, Murphy VJ, et al. (2005) Structure of AMA1 from Plasmodium falciparum reveals a clustering of polymorphisms that surround a conserved hydrophobic pocket. Proc Natl Acad Sci U S A 102: 12736-12741.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Nagamune K, Moreno SN, Chini EN, Sibley LD (2008) Calcium regulation and signaling in apicomplexan parasites. Subcell Biochem 47: 70-81.
20. Beraldo FH, Almeida FM, da Silva AM, Garcia CR (2005) Cyclic AMP and calcium interplay as second messengers in melatonin-dependent regulation of Plasmodium falciparum cell cycle. J Cell Biol 170: 551-557.
21. Syin C, Parzy D, Traincard F, Boccaccio I, Joshi MB, et al. (2001) The H89 cAMP-dependent protein kinase inhibitor blocks Plasmodium falciparum development in infected erythrocytes. Eur J Biochem 268: 4842-4849.
22. Bozdech Z, Zhu J, Joachimiak MP, Cohen FE, Pulliam B, et al. (2003) Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biol 4: R9.
23. Ward P, Equinet L, Packer J, Doerig C (2004) Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5: 79.
24. Murray AJ (2008) Pharmacological PKA inhibition: all may not be what it seems. Sci Signal 1: re4.
25. Steinberg RA, Cauthron RD, Symcox MM, Shuntoh H (1993) Autoactivation of catalytic (C alpha) subunit of cyclic AMP-dependent protein kinase by phosphorylation of threonine 197. Mol Cell Biol 13: 2332-2341.
26. Tang Y, McLeod M (2004) In vivo activation of protein kinase A in Schizosaccharomyces pombe requires threonine phosphorylation at its activation loop and is dependent on PDK1. Genetics 168: 1843-1853.
27. Healer J, Triglia T, Hodder AN, Gemmill AW, Cowman AF (2005) Functional analysis of Plasmodium falciparum apical membrane antigen 1 utilizing interspecies domains. Infect Immun 73: 2444-2451.
28. 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.
29. Coley AM, Parisi K, Masciantonio R, Hoeck J, Casey JL, et al. (2006) The most polymorphic residue on Plasmodium falciparum apical membrane antigen 1 determines binding of an invasion-inhibitory antibody. Infect Immun 74: 2628-2636.
30. 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.
31. Green JL, Rees-Channer RR, Howell SA, Martin SR, Knuepfer E, et al. (2008) The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase. J Biol Chem 283: 30980-30989.
32. Ono T, Cabrita-Santos L, Leitao R, Bettiol E, Purcell LA, et al. (2008) Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLoS Pathog 4: e1000008.
33. Baker DA (2004) Adenylyl and guanylyl cyclases from the malaria parasite Plasmodium falciparum. IUBMB Life 56: 535-540.
34. Besteiro S, Michelin A, Poncet J, Dubremetz JF, Lebrun M (2009) Export of a Toxoplasma gondii rhoptry neck protein complex at the host cell membrane to form the moving junction during invasion. PLoS Pathog 5: e1000309.
35. Borodinsky LN, Spitzer NC (2006) Second messenger pas de deux: the coordinated dance between calcium and cAMP. Sci STKE 2006: pe22.
36. Rabilloud T, Blisnick T, Heller M, Luche S, Aebersold R, et al. (1999) Analysis of membrane proteins by two-dimensional electrophoresis: comparison of the proteins extracted from normal or Plasmodium falciparum-infected erythrocyte ghosts. Electrophoresis 20: 3603-3610.