Extracellular ATP triggers proteolysis and cytosolic Ca 2+ rise in Plasmodium berghei and Plasmodium yoelii malaria parasites

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Cruz, Laura Nogueira ^a   Juliano, Maria Aparecida ^b   Budu, Alexandre ^a   Juliano, Luiz ^b   Holder, Anthony A ^c   Blackman, Michael J ^c   Garcia, Célia R S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

ATP; Calcium modulation; Malaria; Merozoite surface protein 1; Plasmodium berghei; Plasmodium yoelii; Protease activity; Purinergic receptor

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MEROZOITE SURFACE PROTEIN 1; PROTEINASE; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SURAMIN; ANILINE DERIVATIVE; CALCIUM; FLUO 4; PEPTIDE; XANTHENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOUSE; NONHUMAN; PARASITE ISOLATION; PLASMODIUM BERGHEI; PLASMODIUM YOELII; PROTEIN DEGRADATION; TROPHOZOITE; WESTERN BLOTTING; DRUG EFFECT; METABOLISM; SIGNAL TRANSDUCTION; STAINING;

ADENOSINE TRIPHOSPHATE; ANILINE COMPOUNDS; CALCIUM; PEPTIDES; PLASMODIUM BERGHEI; PLASMODIUM YOELII; PROTEOLYSIS; SIGNAL TRANSDUCTION; STAINING AND LABELING; XANTHENES;

EID: 84858118765     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-69     Document Type: Article

References (67)

1. WHO Global Malaria Programme, World Malaria Report 2011 World Health Organization 2011
2. Imaging Plasmodium falciparum-infected ghost and parasite by atomic force microscopy. Garcia CR, Takeuschi M, Yoshioka K, Miyamoto H, J Struct Biol 1997 119 92 98 10.1006/jsbi.1997.3886 9245748 (Pubitemid 27325782)
3. Plasmodium in the postgenomic era: new insights into the molecular cell biology of malaria parasites. Garcia CR, de Azevedo MF, Wunderlich G, Budu A, Young JA, Bannister L, Int Rev Cell Mol Biol 2008 266 85 156 18544493
4. Moving in and renovating: exporting proteins from Plasmodium into host erythrocytes. Goldberg DE, Cowman AF, Nat Rev Microbiol 2010 8 617 621 10.1038/nrmicro2420 20706280
5. Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Banerjee R, Liu J, Beatty W, Pelosof L, Klemba M, Goldberg DE, Proc Natl Acad Sci USA 2002 99 990 995 10.1073/pnas.022630099 11782538 (Pubitemid 34106623)
6. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Billker O, Sinnis P, Cell Host Microbe 2007 2 316 327 10.1016/j.chom.2007.10.002 18005753 (Pubitemid 350056399)
7. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, Florens L, Janssen CS, Pain A, Christophides GK, et al. Science 2005 307 82 86 10.1126/science.1103717 15637271 (Pubitemid 40093481)
8. Molecular identification of a malaria merozoite surface sheddase. Harris PK, Yeoh S, Dluzewski AR, O'Donnell RA, Withers-Martinez C, Hackett F, Bannister LH, Mitchell GH, Blackman MJ, PLoS Pathog 2005 1 241 251 16322767
9. Cysteine proteases of malaria parasites. Rosenthal PJ, Int J Parasitol 2004 34 1489 1499 10.1016/j.ijpara.2004.10.003 15582526
10. Malaria: targeting parasite and host cell kinomes. Doerig C, Abdi A, Bland N, Eschenlauer S, Dorin-Semblat D, Fennell C, Halbert J, Holland Z, Nivez MP, Semblat JP, et al. Biochim Biophys Acta 2010 1804 604 612 19840874
11. Molecular machinery of signal transduction and cell cycle regulation in Plasmodium. Koyama FC, Chakrabarti D, Garcia CR, Mol Biochem Parasitol 2009 165 1 7 10.1016/j.molbiopara.2009.01.003 19393157
12. Exposure of Plasmodium sporozoites to the intracellular concentration of potassium enhances infectivity and reduces cell passage activity. Kumar KA, Garcia CR, Chandran VR, Van Rooijen N, Zhou Y, Winzeler E, Nussenzweig V, Mol Biochem Parasitol 2007 156 32 40 10.1016/j.molbiopara.2007.07.004 17714805 (Pubitemid 47354213)
13. Plasmodium falciparum subtilisin-like protease 2, a merozoite candidate for the merozoite surface protein 1-42 maturase. Barale JC, Blisnick T, Fujioka H, Alzari PM, Aikawa M, Braun-Breton C, Langsley G, Proc Natl Acad Sci USA 1999 96 6445 6450 10.1073/pnas.96.11.6445 10339607 (Pubitemid 29256685)
14. Calpain. Perrin BJ, Huttenlocher A, Int J Biochem Cell Biol 2002 34 722 725 10.1016/S1357-2725(02)00009-2 11950589 (Pubitemid 34304162)
15. FRET peptides reveal differential proteolytic activation in intraerythrocytic stages of the malaria parasites Plasmodium berghei and Plasmodium yoelii. Cruz LN, Alves E, Leal MT, Juliano MA, Rosenthal PJ, Juliano L, Garcia CR, Int J Parasitol 2011 41 363 372 10.1016/j.ijpara.2010.10.009 21168413
16. Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. Alves E, Bartlett PJ, Garcia CR, Thomas AP, J Biol Chem 2011 286 5905 5912 10.1074/jbc.M110.188474 21149448
17. Cyclic AMP and calcium interplay as second messengers in melatonin-dependent regulation of Plasmodium falciparum cell cycle. Beraldo FH, Almeida FM, da Silva AM, Garcia CR, J Cell Biol 2005 170 551 557 10.1083/jcb.200505117 16103224 (Pubitemid 41186930)
18. Thousands of chemical starting points for antimalarial lead identification. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, Lavandera JL, Vanderwall DE, Green DV, Kumar V, Hasan S, Brown JR, Peishoff CE, Cardon LR, Garcia-Bustos JF, Nature 2010 465 305 310 10.1038/nature09107 20485427
19. Artemisinins and the biological basis for the PfATP6/SERCA hypothesis. Krishna S, Pulcini S, Fatih F, Staines H, Trends Parasitol 2010 26 517 523 10.1016/j.pt.2010.06.014 20638904
20. Is invasion efficiency in malaria controlled by pre-invasion events? Lew VL, Tiffert T, Trends Parasitol 2007 23 481 484 10.1016/j.pt.2007.08.001 17804296 (Pubitemid 47465090)
21. Acidocalcisomes and a vacuolar H + -pyrophosphatase in malaria parasites. Marchesini N, Luo S, Rodrigues CO, Moreno SN, Docampo R, Biochem J 2000 347 243 253 10.1042/0264-6021:3470243 10727425 (Pubitemid 30199064)
22. Characterization of Ca2+ transport activity associated with a non-mitochondrial calcium pool in the rodent malaria parasite. Passos AP, Garcia CR, Chabaudi Biochem Mol Biol Int 1997 42 919 925 (Pubitemid 28297583)
23. Intracellular parasite invasion strategies. Sibley LD, Science 2004 304 248 253 10.1126/science.1094717 15073368 (Pubitemid 38452170)
24. PfPKB, a protein kinase B-like enzyme from Plasmodium falciparum: II. Identification of calcium/calmodulin as its upstream activator and dissection of a novel signaling pathway. Vaid A, Sharma P, J Biol Chem 2006 281 27126 27133 10.1074/jbc.M601914200 16809343 (Pubitemid 44401742)
25. Investigations into the role of the Plasmodium falciparum SERCA (PfATP6) L263E mutation in artemisinin action and resistance. Valderramos SG, Scanfeld D, Uhlemann AC, Fidock DA, Krishna S, Antimicrob Agents Chemother 2010 54 3842 3852 10.1128/AAC.00121-10 20566762
26. Plasmodium falciparum malaria parasites display a THG-sensitive Ca2+ pool. Varotti FP, Beraldo FH, Gazarini ML, Garcia CR, Cell Calcium 2003 33 137 144 10.1016/S0143-4160(02)00224-5 12531190 (Pubitemid 36221698)
27. Malaria: therapeutic implications of melatonin. Srinivasan V, Spence DW, Moscovitch A, Pandi-Perumal SR, Trakht I, Brown GM, Cardinali DP, J Pineal Res 2010 48 1 8 10.1111/j.1600-079X.2009.00728.x 20025640
28. Signal transduction in red blood cells of the lizards Ameiva ameiva and Tupinambis merianae (Squamata, Teiidae). Beraldo FH, Sartorello R, Lanari RD, Garcia CR, Cell Calcium 2001 29 439 445 10.1054/ceca.2001.0207 11352509 (Pubitemid 32496365)
29. N1-acetyl-N2-formyl-5-methoxykynuramine modulates the cell cycle of malaria parasites. Budu A, Peres R, Bueno VB, Catalani LH, Garcia CR, J Pineal Res 2007 42 261 266 10.1111/j.1600-079X.2006.00414.x 17349024 (Pubitemid 46365063)
30. Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem. Gazarini ML, Thomas AP, Pozzan T, Garcia CR, J Cell Biol 2003 161 103 110 10.1083/jcb.200212130 12682086 (Pubitemid 36459083)
31. Cysteine-protease activity elicited by Ca2+ stimulus in Plasmodium. Farias SL, Gazarini ML, Melo RL, Hirata IY, Juliano MA, Juliano L, Garcia CR, Mol Biochem Parasitol 2005 141 71 79 10.1016/j.molbiopara.2005.01.015 15811528 (Pubitemid 40461898)
32. Postjunctional synergism of noradrenaline and adenosine 5'-triphosphate in the mesenteric arterial bed of the rat. Ralevic V, Burnstock G, Eur J Pharmacol 1990 175 291 299 10.1016/0014-2999(90)90567-P 2157602 (Pubitemid 20035535)
33. Purinergic receptors: their role in nociception and primary afferent neurotransmission. Burnstock G, Wood JN, Curr Opin Neurobiol 1996 6 526 532 10.1016/S0959-4388(96)80060-2 8794102 (Pubitemid 26313056)
34. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA, Pharmacol Rev 2006 58 281 341 10.1124/pr.58.3.3 16968944 (Pubitemid 44394905)
35. The Plasmodium falciparum-induced anion channel of human erythrocytes is an ATP-release pathway. Akkaya C, Shumilina E, Bobballa D, Brand VB, Mahmud H, Lang F, Huber SM, Pflugers Arch 2009 457 1035 1047 10.1007/s00424-008-0572-8 18696103
36. Purinergic signalling is involved in the malaria parasite Plasmodium falciparum invasion to red blood cells. Levano-Garcia J, Dluzewski AR, Markus RP, Garcia CR, Purinergic Signal 2010 6 365 372 10.1007/s11302-010-9202-y 21437007
37. Suramin and suramin analogues inhibit merozoite surface protein-1 secondary processing and erythrocyte invasion by the malaria parasite Plasmodium falciparum. Fleck SL, Birdsall B, Babon J, Dluzewski AR, Martin SR, Morgan WD, Angov E, Kettleborough CA, Feeney J, Blackman MJ, Holder AA, J Biol Chem 2003 278 47670 47677 10.1074/jbc.M306603200 13679371 (Pubitemid 37523212)
38. Regulated maturation of malaria merozoite surface protein-1 is essential for parasite growth. Child MA, Epp C, Bujard H, Blackman MJ, Mol Microbiol 2010 78 187 202 20735778
39. CMCaCN: Internally quenched fluorogenic protease substrates: solid-phase synthesis and fluorescence spectroscopy of peptides containing ortho-aminobenzoyl/dinitrophenyl groups as donor-acceptor pairs. Hirata IY, Lett Pept Sci 1994 1 299 308
40. The use of Fluorescence Resonance Energy Transfer (FRET) peptides for measurement of clinically important proteolytic enzymes. Carmona AK, Juliano MA, Juliano L, An Acad Bras Cienc 2009 81 381 392 10.1590/S0001-37652009000300005 19722010
41. Internally quenched fluorogenic protease substrates: Solid-phase synthesis and fluorescence spectroscopy of peptides containing ortho-aminobenzoyl/dinitrophenyl groups as donor-acceptor pairs. Hirata IY, Cezari MH, Nakaie CR, Boschcov P, Ito AS, Juliano MA, Juliano L, Letters in Peptide Science 1994 1 299 308
42. Protective monoclonal antibodies recognising stage-specific merozoite antigens of a rodent malaria parasite. Freeman RR, Trejdosiewicz AJ, Cross GA, Nature 1980 284 366 368 10.1038/284366a0 7360274 (Pubitemid 10122195)
43. Characterization of a high molecular weight protective antigen of Plasmodium yoelii. Holder AA, Freeman RR, Parasitology 1984 88 Pt 2 211 219 6718053 (Pubitemid 14025320)
44. Immunization against blood-stage rodent malaria using purified parasite antigens. Holder AA, Freeman RR, Nature 1981 294 361 364 10.1038/294361a0 7312033 (Pubitemid 12202856)
45. The three major antigens on the surface of Plasmodium falciparum merozoites are derived from a single high molecular weight precursor. Holder AA, Freeman RR, J Exp Med 1984 160 624 629 10.1084/jem.160.2.624 6381636 (Pubitemid 14052523)
46. Calcium signaling in lizard red blood cells. Bagnaresi P, Rodrigues MT, Garcia CR, Comp Biochem Physiol A Mol Integr Physiol 2007 147 779 787 10.1016/j.cbpa.2006.09.015 17095273 (Pubitemid 46755609)
47. Divergent calcium signaling in RBCs from Tropidurus torquatus (Squamata-Tropiduridae) strengthen classification in lizard evolution. Beraldo FH, Garcia CR, BMC Physiol 2007 7 7 10.1186/1472-6793-7-7 17716375 (Pubitemid 47567290)
48. Red blood cells of the lizards Ameiva ameiva (Squamata, Teiidae) display multiple mechanisms to control cytosolic calcium. Beraldo FH, Sartorello R, Gazarini ML, Caldeira W, Garcia CR, Cell Calcium 2002 31 79 87 10.1054/ceca.2002.0258 11969248 (Pubitemid 34552447)
49. Evolutionary origins of the purinergic signalling system. Burnstock G, Verkhratsky A, Acta Physiol (Oxf) 2009 195 415 447 10.1111/j.1748-1716.2009. 01957.x
50. In vivo measurements of cytosolic calcium in Dictyostelium discoideum. Allan CY, Fisher PR, Methods Mol Biol 2009 571 291 308 10.1007/978-1-60761-198- 1-20 19763975
51. Acidic calcium stores of Saccharomyces cerevisiae. Cunningham KW, Cell Calcium 2011 50 129 138 10.1016/j.ceca.2011.01.010 21377728
52. Is there a basis for distinguishing two types of P2-purinoceptor? Burnstock G, Kennedy C, Gen Pharmacol 1985 16 433 440 10.1016/0306-3623(85) 90001-1 2996968 (Pubitemid 16250911)
53. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, Silva JC, Ermolaeva MD, Allen JE, Selengut JD, Koo HL, et al. Nature 2002 419 512 519 10.1038/nature01099 12368865
54. Genome sequence of the human malaria parasite Plasmodium falciparum. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. Nature 2002 419 498 511 10.1038/nature01097 12368864
55. Discovery of gene function by expression profiling of the malaria parasite life cycle. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA, Science 2003 301 1503 1508 10.1126/science.1087025 12893887 (Pubitemid 37128535)
56. High zinc sensitivity and pore formation in an invertebrate P2X receptor. Raouf R, Blais D, Seguela P, Biochim Biophys Acta 2005 1669 135 141 10.1016/j.bbamem.2005.01.009 15893516 (Pubitemid 40704731)
57. Genome-wide detection of serpentine receptor-like proteins in malaria parasites. Madeira L, Galante PA, Budu A, Azevedo MF, Malnic B, Garcia CR, PLoS One 2008 3 1889 10.1371/journal.pone.0001889 18365025 (Pubitemid 351943729)
58. Molecules targeting the purine salvage pathway in Apicomplexan parasites. Gherardi A, Sarciron ME, Trends Parasitol 2007 23 384 389 10.1016/j.pt.2007.06. 003 17574921 (Pubitemid 47069951)
59. Isolation and functional characterization of the PfNT1 nucleoside transporter gene from Plasmodium falciparu. Carter NS, Ben Mamoun C, Liu W, Silva EO, Landfear SM, Goldberg DE, Ullman B, J Biol Chem 2000 275 10683 10691 10.1074/jbc.275.14.10683 10744765 (Pubitemid 30202136)
60. Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for anti-malarial chemotherapy. Parker MD, Hyde RJ, Yao SY, McRobert L, Cass CE, Young JD, McConkey GA, Baldwin SA, Biochem J 2000 349 67 75 10.1042/0264-6021:3490067 10861212 (Pubitemid 30440166)
61. Localization of the Plasmodium falciparum PfNT1 nucleoside transporter to the parasite plasma membrane. Rager N, Mamoun CB, Carter NS, Goldberg DE, Ullman B, J Biol Chem 2001 276 41095 41099 10.1074/jbc.M107037200 11682491
62. Transport of nucleosides across the Plasmodium falciparum parasite plasma membrane has characteristics of PfENT1. Downie MJ, Saliba KJ, Howitt SM, Broer S, Kirk K, Mol Microbiol 2006 60 738 748 10.1111/j.1365-2958.2006.05125.x 16629674
63. The plasma membrane permease PfNT1 is essential for purine salvage in the human malaria parasite Plasmodium falciparum. El Bissati K, Zufferey R, Witola WH, Carter NS, Ullman B, Ben Mamoun C, Proc Natl Acad Sci USA 2006 103 9286 9291 10.1073/pnas.0602590103 16751273 (Pubitemid 43902570)
64. Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Murphy SC, Fernandez-Pol S, Chung PH, Prasanna Murthy SN, Milne SB, Salomao M, Brown HA, Lomasney JW, Mohandas N, Haldar K, Blood 2007 110 2132 2139 10.1182/blood-2007-04-083873 17526861 (Pubitemid 47443932)
65. How many functional transport pathways does Plasmodium falciparum induce in the membrane of its host erythrocyte? Ginsburg H, Stein WD, Trends Parasitol 2005 21 118 121 10.1016/j.pt.2005.01.004 15734658 (Pubitemid 40269775)
66. Selective killing of the human malaria parasite Plasmodium falciparum by a benzylthiazolium dye. Kelly JX, Winter RW, Braun TP, Osei-Agyemang M, Hinrichs DJ, Riscoe MK, Exp Parasitol 2007 116 103 110 10.1016/j.exppara.2006.12.001 17266952 (Pubitemid 46604814)
67. Targeting nutrient uptake mechanisms in Plasmodium. Kirk K, Saliba KJ, Curr Drug Targets 2007 8 75 88 10.2174/138945007779315560 17266532 (Pubitemid 46043899)