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New roles for perforins and proteases in apicomplexan egress

dc.contributor.authorRoiko, Marijo S.en_US
dc.contributor.authorCarruthers, Vern B.en_US
dc.date.accessioned2010-06-01T22:05:33Z
dc.date.available2010-06-01T22:05:33Z
dc.date.issued2009-10en_US
dc.identifier.citationRoiko, Marijo S.; Carruthers, Vern B. (2009). "New roles for perforins and proteases in apicomplexan egress." Cellular Microbiology 11(10): 1444-1452. <http://hdl.handle.net/2027.42/75116>en_US
dc.identifier.issn1462-5814en_US
dc.identifier.issn1462-5822en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/75116
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=19614666&dopt=citationen_US
dc.description.abstractEgress is a pivotal step in the life cycle of intracellular pathogens initiating the transition from an expiring host cell to a fresh target cell. While much attention has been focused on understanding cell invasion by intracellular pathogens, recent work is providing a new appreciation of mechanisms and therapeutic potential of microbial egress. This review highlights recent insight into cell egress by apicomplexan parasites and emerging contributions of membranolytic and proteolytic secretory products, along with host proteases. New findings suggest that Toxoplasma gondii secretes a pore-forming protein, TgPLP1, during egress that facilitates parasite escape from the cell by perforating the parasitophorous membrane. Also, in a cascade of proteolytic events, Plasmodium falciparum late-stage schizonts activate and secrete a subtilisin, PfSUB1, which processes enigmatic putative proteases called serine-repeat antigens that contribute to merozoite egress. A new report also suggests that calcium-activated host proteases called calpains aid parasite exit, possibly by acting upon the host cytoskeleton. Together these discoveries reveal important new molecular players involved in the principal steps of egress by apicomplexans.en_US
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dc.publisherBlackwell Publishing Ltden_US
dc.rights© 2009 Blackwell Publishing Ltden_US
dc.titleNew roles for perforins and proteases in apicomplexan egressen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.identifier.pmid19614666en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/75116/1/j.1462-5822.2009.01357.x.pdf
dc.identifier.doi10.1111/j.1462-5822.2009.01357.xen_US
dc.identifier.sourceCellular Microbiologyen_US
dc.identifier.citedreferenceAly, A.S., Mikolajczak, S.A., Rivera, H.S., Camargo, N., Jacobs-Lorena, V., Labaied, M., et al. ( 2008 ) Targeted deletion of SAP1 abolishes the expression of infectivity factors necessary for successful malaria parasite liver infection. Mol Microbiol 69: 152 – 163.en_US
dc.identifier.citedreferenceArastu-Kapur, S., Ponder, E.L., Fonovic, U.P., Yeoh, S., Yuan, F., Fonovic, M., et al. ( 2008 ) Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 4: 203 – 213.en_US
dc.identifier.citedreferenceArrizabalaga, G., Ruiz, F., Moreno, S., and Boothroyd, J.C. ( 2004 ) Ionophore-resistant mutant of Toxoplasma gondii reveals involvement of a sodium/hydrogen exchanger in calcium regulation. J Cell Biol 5: 653 – 662.en_US
dc.identifier.citedreferenceBaer, K., Klotz, C., Kappe, S.H., Schnieder, T., and Frevert, U. ( 2007 ) Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog 3: e171.en_US
dc.identifier.citedreferenceBlack, M.W., and Boothroyd, J.C. ( 2000 ) Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 64: 607 – 623.en_US
dc.identifier.citedreferenceBlack, M.W., Arrizabalaga, G., and Boothroyd, J.C. ( 2000 ) Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol Cell Biol 20: 9399 – 9408.en_US
dc.identifier.citedreferenceBlackman, M.J. ( 2008 ) Malarial proteases and host cell egress: an ‘emerging’ cascade. Cell Microbiol 10: 1925 – 1934.en_US
dc.identifier.citedreferenceBlocker, A., Gounon, P., Larquet, E., Niebuhr, K., Cabiaux, V., Parsot, C., and Sansonetti, P. ( 1999 ) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147: 683 – 693.en_US
dc.identifier.citedreferenceCaldas, L.A., de Souza, W., and Attias, M. ( 2007 ) Calcium ionophore-induced egress of Toxoplasma gondii shortly after host cell invasion. Vet Parasitol 3–4: 210 – 220.en_US
dc.identifier.citedreferenceCarruthers, V., and Boothroyd, J.C. ( 2007 ) Pulling together: an integrated model of Toxoplasma cell invasion. Curr Opin Microbiol 10: 83 – 89.en_US
dc.identifier.citedreferenceCarruthers, V., Moreno, S.N.J., and Sibley, L.D. ( 1999 ) Ethanol and acetaldehyde elevate intracellular calcium and stimulate microneme discharge in Toxoplasma gondii. Biochem J 2: 379 – 386.en_US
dc.identifier.citedreferenceChandramohanadas, R., Davis, P.H., Beiting, D.P., Harbut, M.B., Darling, C., Velmourougane, G., et al. ( 2009 ) Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 5928: 794 – 797.en_US
dc.identifier.citedreferenceCowman, A.F., and Crabb, B.S. ( 2006 ) Invasion of red blood cells by malaria parasites. Cell 124: 755 – 766.en_US
dc.identifier.citedreferenceDramsi, S., and Cossart, P. ( 2002 ) Listeriolysin O: a genuine cytolysin optimized for an intracellular parasite. J Cell Biol 156: 943 – 946.en_US
dc.identifier.citedreferenceEcker, A., Pinto, S.B., Baker, K.W., Kafatos, F.C., and Sinden, R.E. ( 2007 ) Plasmodium berghei: Plasmodium perforin-like protein 5 is required for mosquito midgut invasion in anopheles stephensi. Exp Parasitol 116: 504 – 508.en_US
dc.identifier.citedreferenceEngelmann, S., Silvie, O., and Matuschewski, K. ( 2009 ) Disruption of Plasmodium sporozoite transmission by depletion of sporozoite invasion-associated protein 1. Eukaryot Cell 4: 640 – 648.en_US
dc.identifier.citedreferenceFairlie, W.D., Spurck, T.P., McCoubrie, J.E., Gilson, P.R., Miller, S.K., McFadden, G.I., et al. ( 2008 ) Inhibition of malaria parasite development by a cyclic peptide that targets the vital parasite protein SERA5. Infect Immun 76: 4332 – 4344.en_US
dc.identifier.citedreferenceFruth, I.A., and Arrizabalaga, G. ( 2007 ) Toxoplasma gondii: induction of egress by the potassium ionophore nigericin. Int J Parasitol 14: 1559 – 1567.en_US
dc.identifier.citedreferenceGlushakova, 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.en_US
dc.identifier.citedreferenceGlushakova, S., Mazar, J., Hohmann-Marriott, M.F., Hama, E., and Zimmerberg, J. ( 2009 ) Irreversible effect of cysteine protease inhibitors on the release of malaria parasites from infected erythrocytes. Cell Microbiol 11: 95 – 105.en_US
dc.identifier.citedreferenceGoll, D.E., Thompson, V.F., Li, H., Wei, W., and Cong, J. ( 2003 ) The calpain system. Physiol Rev 83: 731 – 801.en_US
dc.identifier.citedreferenceHadders, M.A., Beringer, D.X., and Gros, P. ( 2007 ) Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317: 1552 – 1554.en_US
dc.identifier.citedreferenceIshino, T., Chinzei, Y., and Yuda, M. ( 2005 ) A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 7: 199 – 208.en_US
dc.identifier.citedreferenceKadota, K., Ishino, T., Matsuyama, T., Chinzei, Y., and Yuda, M. ( 2004 ) Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci USA 101: 16310 – 16315.en_US
dc.identifier.citedreferenceKafsack, B.F., Pena, J.D., Coppens, I., Ravindran, S., Boothroyd, J.C., and Carruthers, V.B. ( 2009 ) Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323: 530 – 533.en_US
dc.identifier.citedreferenceKieschnick, H., Wakefield, T., Narducci, C.A., and Beckers, C. ( 2001 ) Toxoplasma gondii attachment to host cells is regulated by a calmodulin- like domain protein kinase. J Biol Chem 15: 12369 – 12377.en_US
dc.identifier.citedreferenceKoussis, K., Withers-Martinez, C., Yeoh, S., Child, M., Hackett, F., Knuepfer, E., et al. ( 2009 ) A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J 28: 725 – 735.en_US
dc.identifier.citedreferenceKumar, K.A., Garcia, C.R., Chandran, V.R., Van Rooijen, N., Zhou, Y., Winzeler, E., and Nussenzweig, V. ( 2007 ) Exposure of Plasmodium sporozoites to the intracellular concentration of potassium enhances infectivity and reduces cell passage activity. Mol Biochem Parasitol 156: 32 – 40.en_US
dc.identifier.citedreferenceLavine, M.D., and Arrizabalaga, G. ( 2007 ) Invasion and egress by the obligate intracellular parasite Toxoplasma gondii: potential targets for the development of new antiparasitic drugs. Curr Pharm Des 13: 641 – 651.en_US
dc.identifier.citedreferenceLavine, M.D., and Arrizabalaga, G. ( 2008 ) Exit from host cells by the pathogenic parasite Toxoplasma gondii does not require motility. Eukaryot Cell 7: 131 – 140.en_US
dc.identifier.citedreferenceLe Bonniec, S., Deregnaucourt, C., Redeker, V., Banerjee, R., Grellier, P., Goldberg, D.E., and Schrevel, J. ( 1999 ) Plasmepsin II, an acidic hemoglobinase from the Plasmodium falciparum food vacuole, is active at neutral pH on the host erythrocyte membrane skeleton. J Biol Chem 274: 14218 – 14223.en_US
dc.identifier.citedreferenceLukoyanova, N., and Saibil, H.R. ( 2008 ) Friend or foe: The same fold for attack and defense. Trends Immunol 29: 51 – 53.en_US
dc.identifier.citedreferenceMartin, A.M., Liu, T., Lynn, B.C., and Sinai, A.P. ( 2007 ) The Toxoplasma gondii parasitophorous vacuole membrane: transactions across the border. J Eukaryot Microbiol 54: 25 – 28.en_US
dc.identifier.citedreferenceMeissner, M., Brecht, S., Bujard, H., and Soldati, D. ( 2001 ) Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res 22: E115, 1 – 10.en_US
dc.identifier.citedreferenceMota, L.J. ( 2006 ) Type III secretion gets an LcrV tip. Trends Microbiol 14: 197 – 200.en_US
dc.identifier.citedreferenceMoudy, 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.en_US
dc.identifier.citedreferenceNagamune, K., Moreno, S.N., Chini, E.N., and Sibley, L.D. ( 2008a ) Calcium regulation and signaling in apicomplexan parasites. Subcell Biochem 47: 70 – 81.en_US
dc.identifier.citedreferenceNagamune, K., Hicks, L.M., Fux, B., Brossier, F., Chini, E.N., and Sibley, L.D. ( 2008b ) Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451: 207 – 210.en_US
dc.identifier.citedreferenceOmara-Opyene, A.L., Moura, P.A., Sulsona, C.R., Bonilla, J.A., Yowell, C.A., Fujioka, H., et al. ( 2004 ) Genetic disruption of the Plasmodium falciparum digestive vacuole plasmepsins demonstrates their functional redundancy. J Biol Chem 279: 54088 – 54096.en_US
dc.identifier.citedreferencePersson, C.M., Lambert, H., Vutova, P.P., Dellacasa-Lindberg, I., Nederby, J., Yagita, H., et al. ( 2009 ) Transmission of Toxoplasma gondii from infected dendritic cells to natural killer cells. Infect Immun 77: 970 – 976.en_US
dc.identifier.citedreferencePersson, K.E., McCallum, F.J., Reiling, L., Lister, N.A., Stubbs, J., Cowman, A.F., et al. ( 2008 ) Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 118: 342 – 351.en_US
dc.identifier.citedreferencePlattner, F., Yarovinsky, F., Romero, S., Didry, D., Carlier, M.F., Sher, A., and Soldati-Favre, D. ( 2008 ) Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3: 77 – 87.en_US
dc.identifier.citedreferencePonzi, M., Siden-Kiamos, I., Bertuccini, L., Curra, C., Kroeze, H., Camarda, G., et al. ( 2009 ) Egress of Plasmodium berghei gametes from their host erythrocyte is mediated by the MDV-1/PEG3 protein. Cell Microbiol 11: 1272 – 1288.en_US
dc.identifier.citedreferenceQue, X., Engel, J.C., Ferguson, D., Wunderlich, A., Tomavo, S., and Reed, S.L. ( 2007 ) Cathepsin cs are key for the intracellular survival of the protozoan parasite, Toxoplasma gondii. J Biol Chem 282: 4994 – 5003.en_US
dc.identifier.citedreferenceRosado, C.J., Buckle, A.M., Law, R.H., Butcher, R.E., Kan, W.T., Bird, C.H., et al. ( 2007 ) A common fold mediates vertebrate defense and bacterial attack. Science 317: 1548 – 1551.en_US
dc.identifier.citedreferenceRosado, C.J., Kondos, S., Bull, T.E., Kuiper, M.J., Law, R.H., Buckle, A.M., et al. ( 2008 ) The MACPF/CDC family of pore-forming toxins. Cell Microbiol 9: 1765 – 1774.en_US
dc.identifier.citedreferenceSalmon, 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.en_US
dc.identifier.citedreferenceSchmidt-Christensen, A., Sturm, A., Horstmann, S., and Heussler, V.T. ( 2008 ) Expression and processing of Plasmodium berghei SERA3 during liver stages. Cell Microbiol 10: 1723 – 1734.en_US
dc.identifier.citedreferenceSchwartzman, J.D., and Pfefferkorn, E.R. ( 1983 ) Immunofluorescent localization of myosin at the anterior pole of the coccidian, Toxoplasma gondii. J Protozool 4: 657 – 661.en_US
dc.identifier.citedreferenceSijwali, 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.en_US
dc.identifier.citedreferenceSijwali, 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.en_US
dc.identifier.citedreferenceSinai, A.P. ( 2008 ) Biogenesis of and activities at the Toxoplasma gondii parasitophorous vacuole membrane. Subcell Biochem 47: 155 – 164.en_US
dc.identifier.citedreferenceSoni, S., Dhawan, S., Rosen, K.M., Chafel, M., Chishti, A.H., and Hanspal, M. ( 2005 ) Characterization of events preceding the release of malaria parasite from the host red blood cell. Blood Cells Mol Dis 35: 201 – 211.en_US
dc.identifier.citedreferenceStommel, E.W., Ely, K.H., Schwartzman, J.D., and Kasper, L.H. ( 1997 ) Toxoplasma gondii: dithiol-induced Ca2+ flux causes egress of parasites from the parasitophorous vacuole. Exp Parasitol 2: 88 – 97.en_US
dc.identifier.citedreferenceSturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., et al. ( 2006 ) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313: 1287 – 1290.en_US
dc.identifier.citedreferenceSturm, A., Graewe, S., Franke-Fayard, B., Retzlaff, S., Bolte, S., Roppenser, B., et al. ( 2009 ) Alteration of the parasite plasma membrane and the parasitophorous vacuole membrane during exo-erythrocytic development of malaria parasites. Protist 160: 51 – 63.en_US
dc.identifier.citedreferenceTweten, R.K. ( 2005 ) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73: 6199 – 6209.en_US
dc.identifier.citedreferenceWickham, 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.en_US
dc.identifier.citedreferenceYeoh, S., O'Donnell, R.A., Koussis, K., Dluzewski, A.R., Ansell, K.H., Osborne, S.A., et al. ( 2007 ) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131: 1072 – 1083.en_US
dc.identifier.citedreferenceZhou, X.W., Kafsack, B.F., Cole, R.N., Beckett, P., Shen, R.F., and Carruthers, V.B. ( 2005 ) The opportunistic pathogen Toxoplasma gondii deploys a diverse legion of invasion and survival proteins. J Biol Chem 280: 34233 – 34244.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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