Ca2+-mediated exocytosis of subtilisin-like protease 1: A key step in egress of Plasmodium falciparum merozoites

Cellular Microbiology

Volumn 15, Issue 6, 2013, Pages 910-921

  Agarwal, Shalini ^a   Singh, Maneesh Kumar ^a   Garg, Swati ^a   Chitnis, Chetan E ^a   Singh, Shailja ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; CALCIUM; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PROTEIN; PROTEINASE; SERINE; SERINE REPEAT ANTIGEN 5; SUBTILISIN; SUBTILISIN LIKE PROTEASE 1; UNCLASSIFIED DRUG;

ARTICLE; CELL VACUOLE; CHELATION; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; EXOCYTOSIS; EXON; MEROZOITE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN SECRETION; SCHIZONT; TIME-LAPSE VIDEO MICROSCOPY; TONOPLAST;

ANIMALS; CALCIUM; CELLS, CULTURED; CHELATING AGENTS; DISEASE MODELS, ANIMAL; EGTAZIC ACID; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; EXOCYTOSIS; FEMALE; MALARIA, FALCIPARUM; MEROZOITES; MICE; MICE, INBRED BALB C; MICROSCOPY, VIDEO; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SUBTILISINS;

PLASMODIUM FALCIPARUM;

EID: 84877794605     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12086     Document Type: Article

References (44)

1. Alleva, L.M., and Kirk, K. (2001) Calcium regulation in the intraerythrocytic malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 117: 121-128.
2. 2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J Biol Chem 286: 5905-5912.
3. Ansorge, I., Benting, J., Bhakdi, S., and Lingelbach, K. (1996) Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem J 315: 307-314.
4. Aoki, S., Li, J., Itagaki, S., Okech, B.A., Egwang, T.G., Matsuuoka, 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. Nature Chem Biol 4: 203-213.
6. Beraldo, F.H., and Garcia, C.R.S. (2005) Products of tryptophan catabolism induce Calcium release and modulate the cell cycle of Plasmodium falciparum malaria parasites. J Pineal Res 39: 224-230.
7. Blackman, M.J. (2008) Malarial proteases and host cell egress: an 'emerging' cascade. Cell Microbiol 10: 1925-1934.
8. Carruthers, V.B., and Sibley, L.D. (1999) Mobilization of intracellular Calcium stimulates microneme discharge in Toxoplasma gondii. Mol Microbiol 31: 421-428.
9. Carruthers, V.B., Giddings, O.K., and Sibley, L.D. (1999) Secretion of micronemal proteins is associated with Toxoplasma invasion of host cells. Cell Microbiol 1: 225-236.
10. Chandra, B.R., Olivieri, A., Silvestrini, F., Alano, P., and Sharma, A. (2005) Biochemical characterization of the two nucleosome assembly proteins from Plasmodium falciparum. Mol Biochem Parasitol 142: 237-247.
11. Chandramohanadas, R., Davis, P.H., Beiting, D.P., Harbut, M.B., Darling, C., Velmourougane, G., etal. (2009) Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 314: 794-797.
12. Cowman, A.F., and Crabb, B.S. (2006) Invasion of red blood cells by malaria parasites. Cell 124: 755-766.
13. 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.
14. Dhawan, S., Dua, M., Chishti, A.H., and Hanspal, M. (2003) Ankyrin peptide blocks falcipain-2-mediated malaria parasite release from red blood cells. J Biol Chem 278: 30180-30186.
15. Dluzewski, A.R., Mitchell, G.H., Fryer, P.R., Griffiths, S., Wilson, R.J., and Gratzer, W.B. (1992) Origins of the parasitophorous vacuole membrane of the malaria parasite, Plasmodium falciparum, in human red blood cells. J Cell Sci 102: 527-532.
16. Dvorin, J.D., Martyn, D.C., Patel, S.D., Grimley, J.S., Collins, C.R., Hopp, C.S., etal. (2010) A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science 328: 910-912.
17. Gazarini, M.L., Thomas, A.P., Pozzan, T., and Garcia, C.R.S. (2003) Calcium signaling in a low Calcium environment: how the intracellular malaria parasite solves the problem. J Cell Biol 161: 103-110.
18. Glushakova, S., Yin, D., Li, T., and Zimmerberg, J. (2005) Membrane transformation during malaria parasite release from human red blood cells. Curr Biol 15: 1645-1650.
19. Glushakova, S., Humphrey, G., Leikina, E., Balaban, A., Miller, J., and Zimmerberg, J. (2010) New stages in the program of malaria parasite egress imaged in normal and sickle erythrocytes. Curr Biol 20: 1117-1121.
20. Lew, V.L. (2005) Malaria: endless fascination with merozoite release. Curr Biol 15: R760-R761.
21. Lew, V.L. (2011) Malaria: surprising mechanism of merozoite egress revealed. Curr Biol 21: R314-R316.
22. Li, J., Matsuoka, H., Mitamura, T., and Horii, T. (2002) Characterization of proteases involved in the processing of Plasmodium falciparum serine repeat antigen (SERA). Mol Biochem Parasitol 120: 177-186.
23. Lingelbach, K., and Joiner, K.A. (1998) The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci 111: 1467-1475.
24. Liu, J., Gluzman, I.Y., Drew, M.E., and Goldberg, D.E. (2005) The role of Plasmodium falciparum food vacuole plasmepsins. J Biol Chem 280: 1432-1437.
25. Miller, L.H., Baruch, D.I., Marsh, K., and Doumbo, O.K. (2002a) The pathogenic basis of malaria. Nature 415: 673-679.
26. Miller, S.K., Good, R.T., Drew, D.R., Delorenzi, M., Sanders, P.R., Hodder, A.N., etal. (2002b) 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.
27. Moudy, R., Manning, T.J., and Beckers, C.J. (2001) The loss of cytoplasmic potassium upon host cell breakdown triggers egress of Toxoplasma gondii. J Biol Chem 276: 41492-41501.
28. Nagamune, K., Moreno, S.N., Chini, E.N., and Sibley, L.D. (2008) Calcium regulation and signaling in apicomplexan parasites. Subcell Biochem 47: 70-81.
29. Ono, T., Cabrita-Santos, L., Leitao, R., Bettiol, E., Purcell, L.A., Diaz-Pulido, O., etal. (2008) Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLoS Pathog 4: e1000008.
30. Richards, J.S., and Beeson, J.G. (2009) The future fo blood-stage vaccines against malaria. Immunol Cell Biol 87: 377-390.
31. Ross, C.A., Meldolesi, J., Milner, T.A., Satoh, T., Supattapone, S., and Synder, S.H. (1989) Inositol 1, 4, 5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons. Nature 339: 468-470.
32. Sajid, M., Withers-Martinez, C., and Blackman, M.J. (2000) Maturation and specificity of Plasmodium falciparum subtilisin-like protease-1, a malaria merozoite subtilisin-like serine protease. J Biol Chem 275: 631-641.
33. Salmon, B.L., Oksman, A., and Goldberg, D.E. (2001) Malaria parasite exit from the host erythrocyte: a two-step process requiring extraerythrocytic proteolysis. Proc Natl Acad Sci USA 98: 271-276.
34. Sijwali, P.S., and Rosenthal, P.J. (2004) Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum. Proc Natl Acad Sci USA 101: 4384-4389.
35. Sijwali, P.S., Koo, J., Singh, N., and Rosenthal, P.J. (2006) Gene disruptions demonstrate independent roles for the four falcipain cysteine proteases of Plasmodium falciparum. Mol Biochem Parasitol 150: 96-106.
36. Sim, B.K., Toyoshima, T., Haynes, J.D., and Aikawa, M. (1992) Localization of the 175-kilodalton erythrocyte binding antigen in micronemes of Plasmodium falciparum merozoites. Mol Biochem Parasitol 51: 157-159.
37. Singh, S., and Chitnis, C.E. (2013) Flow cytometry-based methods for measurement of cytosolic calcium and surface protein expression in Plasmodium falciparum merozoites. Methods Mol Biol 923: 281-290.
38. Singh, S., Alam, M.M., Pal-Bhowmick, I., Brzostowski, J.A., and Chitnis, C.E. (2010) Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog 6: e1000746.
39. Taylor, H.M., McRobert, L., Grainger, M., Sicard, A., Dluzewski, A.R., Hopp, C.S., etal. (2010) The malaria parasite cyclic GMP-dependent protein kinase plays a central role in blood-stage schizogony. Eukaryot Cell 9: 37-45.
40. Trager, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
41. 2+/CaM-PfPKB signaling pathway in erythrocyte invasion by Plasmodium falciparum. J Biol Chem 283: 5589-5597.
42. Wickham, M.E., Culvenor, J.G., and Cowman, A.F. (2003) Selective inhibition of a two step egress of malaria parasites from the host erythrocyte. J Biol Chem 278: 37658-37663.
43. Winograd, E., Clavijo, C.A., Bustamante, L.Y., and Jaramillo, M. (1999) Release of merozoites from Plasmodium falciparum-infected erythrocytes could be mediated by a non-explosive event. Parasitol Res 85: 621-624.
44. Yeoh, S., O'Donnell, R.A., Koussis, K., Dluzewski, A.R., Ansell, K.H., Osborne, S.A., etal. (2009) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131: 1072-1083.