Loss-of-function analyses defines vital and redundant functions of the Plasmodium rhomboid protease family

Molecular Microbiology

Volumn 88, Issue 2, 2013, Pages 318-338

  Lin, Jing wen ^a   Meireles, Patrícia ^b   Prudêncio, Miguel ^b   Engelmann, Sabine ^c   Annoura, Takeshi ^a   Sajid, Mohammed ^a   Chevalley Maurel, Séverine ^a   Ramesar, Jai ^a   Nahar, Carolin ^d   Avramut, Cristina M C ^a   Koster, Abraham J ^a   Matuschewski, Kai ^c,d   Waters, Andrew P ^e   Janse, Chris J ^a   Mair, Gunnar R ^b   Khan, Shahid M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ROM1; PROTEIN ROM10; PROTEIN ROM3; PROTEIN ROM4; PROTEIN ROM6; PROTEIN ROM7; PROTEIN ROM8; PROTEIN ROM9; PROTEINASE; RHOMBOID PROTEASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASEXUAL REPRODUCTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; ENZYME DEFICIENCY; FEMALE; GENE DELETION; HEPATITIS; LIVER DEVELOPMENT; MALE; MOSQUITO; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE VIRULENCE; PHENOTYPE; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN FAMILY; RODENT;

ANIMALS; BLOOD; CULICIDAE; FEMALE; GENE DELETION; LIFE CYCLE STAGES; LIVER; MALARIA; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PEPTIDE HYDROLASES; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; SPOROZOITES; VIRULENCE;

RODENTIA;

EID: 84876164304     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12187     Document Type: Article

References (64)

1. Amani, V., Boubou, M.I., Pied, S., Marussig, M., Walliker, D., Mazier, D., and Renia, L. (1998) Cloned lines of Plasmodium berghei ANKA differ in their abilities to induce experimental cerebral malaria. Infect Immun 66: 4093-4099.
2. Annoura, T., Ploemen, I.H., van Schaijk, B.C., Sajid, M., Vos, M.W., van Gemert, G.J., etal. (2012) Assessing the adequacy of attenuation of genetically modified malaria parasite vaccine candidates. Vaccine 30: 2662-2670.
3. Baker, R.P., Wijetilaka, R., and Urban, S. (2006) Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathog 2: e113.
4. Beetsma, A.L., van de Wiel, T.J., Sauerwein, R.W., and Eling, W.M. (1998) Plasmodium berghei ANKA: purification of large numbers of infectious gametocytes. Exp Parasitol 88: 69-72.
5. Ben-Shem, A., Fass, D., and Bibi, E. (2007) Structural basis for intramembrane proteolysis by rhomboid serine proteases. Proc Natl Acad Sci USA 104: 462-466.
6. Brossier, F., Jewett, T.J., Sibley, L.D., and 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.
7. Brossier, F., Starnes, G.L., Beatty, W.L., and Sibley, L.D. (2008) Microneme rhomboid protease TgROM1 is required for efficient intracellular growth of Toxoplasma gondii. Eukaryot Cell 7: 664-674.
8. Buguliskis, J.S., Brossier, F., Shuman, J., and Sibley, L.D. (2010) Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii. PLoS Pathog 6: e1000858.
9. Charneau, S., Bastos, I.M., Mouray, E., Ribeiro, B.M., Santana, J.M., Grellier, P., and Florent, I. (2007) Characterization of PfDYN2, a dynamin-like protein of Plasmodium falciparum expressed in schizonts. Microbes Infect 9: 797-805.
10. Cipolat, S., Rudka, T., Hartmann, D., Costa, V., Serneels, L., Craessaerts, K., etal. (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126: 163-175.
11. van Dijk, M.R., Janse, C.J., Thompson, J., Waters, A.P., Braks, J.A., Dodemont, H.J., etal. (2001) A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153-164.
12. van Dijk, M.R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M.W., van Schaijk, B., etal. (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 102: 12194-12199.
13. Dowse, T.J., and Soldati, D. (2005) Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature. Trends Parasitol 21: 254-258.
14. Ecker, A., Bushell, E.S., Tewari, R., and Sinden, R.E. (2008) Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol Microbiol 70: 209-220.
15. Ejigiri, I., Ragheb, D.R.T., Pino, P., Coppi, A., Bennett, B.L., Soldati-Favre, D., and Sinnis, P. (2012) Shedding of TRAP by a rhomboid protease from the malaria sporozoite surface is essential for gliding motility and sporozoite infectivity. PLoS Pathog 8: e1002725.
16. Franke-Fayard, B., Djokovic, D., Dooren, M.W., Ramesar, J., Waters, A.P., Falade, M.O., etal. (2008) Simple and sensitive antimalarial drug screening in vitro and in vivo using transgenic luciferase expressing Plasmodium berghei parasites. Int J Parasitol 38: 1651-1662.
17. Freeman, M. (2004) Proteolysis within the membrane: rhomboids revealed. Nat Rev Mol Cell Biol 5: 188-197.
18. Freeman, M. (2009) Rhomboids: 7 years of a new protease family. Semin Cell Dev Biol 20: 231-239.
19. Garnham, P.C., Bird, R.G., and Baker, J.R. (1962) Electron microscope studies of motile stages of malaria parasites. III. The ookinetes of Haemamoeba and Plasmodium. Trans R Soc Trop Med Hyg 56: 116-120.
20. Garnham, P.C., Bird, R.G., Baker, J.R., Desser, S.S., and el-Nahal, H.M. (1969) Electron microscope studies on motile stages of malaria parasites. VI. The ookinete of Plasmodium berghei yoelii and its transformation into the early oocyst. Trans R Soc Trop Med Hyg 63: 187-194.
21. Janse, C.J., and Waters, A.P. (1995) Plasmodium berghei: the application of cultivation and purification techniques to molecular studies of malaria parasites. Parasitol Today 11: 138-143.
22. Janse, C.J., Boorsma, E.G., Ramesar, J., van Vianen, P., van der Meer, R., Zenobi, P., etal. (1989) Plasmodium berghei: gametocyte production, DNA content, and chromosome-size polymorphisms during asexual multiplication in vivo. Exp Parasitol 68: 274-282.
23. Janse, C.J., Haghparast, A., Speranca, M.A., Ramesar, J., Kroeze, H., del Portillo, H.A., and Waters, A.P. (2003) Malaria parasites lacking eef1a have a normal S/M phase yet grow more slowly due to a longer G1 phase. Mol Microbiol 50: 1539-1551.
24. Janse, C.J., Franke-Fayard, B., Mair, G.R., Ramesar, J., Thiel, C., Engelmann, S., etal. (2006a) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 145: 60-70.
25. Janse, C.J., Ramesar, J., and Waters, A.P. (2006b) High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356.
26. Khan, S.M., Franke-Fayard, B., Mair, G.R., Lasonder, E., Janse, C.J., Mann, M., and Waters, A.P. (2005) Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121: 675-687.
27. Koonin, E.V., Makarova, K.S., Rogozin, I.B., Davidovic, L., Letellier, M.C., and Pellegrini, L. (2003) The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol 4: R19.
28. Lasonder, E., Janse, C.J., van Gemert, G.J., Mair, G.R., Vermunt, A.M., Douradinha, B.G., etal. (2008) Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog 4: e1000195.
29. Lavazec, C., Moreira, C.K., Mair, G.R., Waters, A.P., Janse, C.J., and Templeton, T.J. (2009) Analysis of mutant Plasmodium berghei parasites lacking expression of multiple PbCCp genes. Mol Biochem Parasitol 163: 1-7.
30. Lemberg, M.K., and Freeman, M. (2007) Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases. Genome Res 17: 1634-1646.
31. Levander, O.A., Fontela, R., Morris, V.C., and Ager, A.L., Jr (1995) Protection against murine cerebral malaria by dietary-induced oxidative stress. J Parasitol 81: 99-103.
32. Lin, J.W., Annoura, T., Sajid, M., Chevalley-Maurel, S., Ramesar, J., Klop, O., etal. (2011) A novel 'Gene Insertion/Marker Out' (GIMO) method for transgene expression and gene complementation in rodent malaria parasites. PLoS ONE 6: e29289.
33. Lin, J.W., Sajid, M., Ramesar, J., Khan, S.M., Janse, C.J., and Franke-Fayard, B. (2013) Screening inhibitors of P.berghei blood stages using bioluminescent reporter parasites. Methods Mol Biol 923: 507-522.
34. McQuibban, G.A., Saurya, S., and Freeman, M. (2003) Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423: 537-541.
35. Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M., Carret, C.K., Wiegant, J.C., etal. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog 6: e1000767.
36. Menard, R., Sultan, A.A., Cortes, C., Altszuler, R., van Dijk, M.R., Janse, C.J., etal. (1997) Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 385: 336-340.
37. Mota, M.M., Pradel, G., Vanderberg, J.P., Hafalla, J.C.R., Frevert, U., Nussenzweig, R.S., etal. (2001) Migration of Plasmodium sporozoites through cells before infection. Science 291: 141-144.
38. Mueller, A.K., Camargo, N., Kaiser, K., Andorfer, C., Frevert, U., Matuschewski, K., and Kappe, S.H. (2005) Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA 102: 3022-3027.
39. O'Donnell, R.A., Hackett, F., Howell, S.A., Treeck, M., Struck, N., Krnajski, Z., etal. (2006) Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 174: 1023-1033.
40. Olivieri, A., Collins, C.R., Hackett, F., Withers-Martinez, C., Marshall, J., Flynn, H.R., etal. (2011) Juxtamembrane shedding of Plasmodium falciparum AMA1 is sequence independent and essential, and helps evade invasion-inhibitory antibodies. PLoS Pathog 7: e1002448.
41. Otsuki, H., Kaneko, O., Thongkukiatkul, A., Tachibana, M., Iriko, H., Takeo, S., etal. (2009) Single amino acid substitution in Plasmodium yoelii erythrocyte ligand determines its localization and controls parasite virulence. Proc Natl Acad Sci USA 106: 7167-7172.
42. Parussini, F., Tang, Q., Moin, S.M., Mital, J., Urban, S., and Ward, G.E. (2012) Intramembrane proteolysis of Toxoplasma apical membrane antigen 1 facilitates host-cell invasion but is dispensable for replication. Proc Natl Acad Sci USA 109: 7463-7468.
43. Ploemen, I.H., Prudencio, M., Douradinha, B.G., Ramesar, J., Fonager, J., van Gemert, G.J., etal. (2009) Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS ONE 4: e7881.
44. Potocnjak, P., Yoshida, N., Nussenzweig, R.S., and Nussenzweig, V. (1980) Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med 151: 1504-1513.
45. Raine, J.D., Ecker, A., Mendoza, J., Tewari, R., Stanway, R.R., and Sinden, R.E. (2007) Female inheritance of malarial lap genes is essential for mosquito transmission. PLoS Pathog 3: e30.
46. Saeed, S., Carter, V., Tremp, A.Z., and Dessens, J.T. (2010) Plasmodium berghei crystalloids contain multiple LCCL proteins. Mol Biochem Parasitol 170: 49-53.
47. Santos, J.M., Ferguson, D.J., Blackman, M.J., and Soldati-Favre, D. (2011a) Intramembrane cleavage of AMA1 triggers Toxoplasma to switch from an invasive to a replicative mode. Science 331: 473-477.
48. Santos, M., Graindorge, A., and Soldati-Favre, D. (2011b) New insights into parasite rhomboid proteases. Mol Biochem Parasitol 182: 27-36.
49. Sinden, R.E. (1997) Infection of mosquitoes with rodent malaria. In Molecular Biology of Insect Disease Vectors: A Method Manual. Crampton, J.M., Beard, C.B., and Louis, C. (eds). London: Chapman and Hall, pp. 67-91.
50. Spaccapelo, R., Janse, C.J., Caterbi, S., Franke-Fayard, B., Bonilla, J.A., Syphard, L.M., etal. (2010) Plasmepsin 4-deficient Plasmodium berghei are virulence attenuated and induce protective immunity against experimental malaria. Am J Pathol 176: 205-217.
51. van Spaendonk, R.M., Ramesar, J., van Wigcheren, A., Eling, W., Beetsma, A.L., van Gemert, G.J., etal. (2001) Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. J Biol Chem 276: 22638-22647.
52. Srinivasan, P., Coppens, I., and Jacobs-Lorena, M. (2009) Distinct roles of Plasmodium rhomboid 1 in parasite development and malaria pathogenesis. PLoS Pathog 5: e1000262.
53. Stevenson, L.G., Strisovsky, K., Clemmer, K.M., Bhatt, S., Freeman, M., and Rather, P.N. (2007) Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc Natl Acad Sci USA 104: 1003-1008.
54. Sturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., etal. (2006) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313: 1287-1290.
55. Sundaram, M.V. (2004) Vulval development: the battle between Ras and Notch. Curr Biol 14: R311-R313.
56. Thathy, V., Fujioka, H., Gantt, S., Nussenzweig, R., Nussenzweig, V., and Menard, R. (2002) Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology. EMBO J 21: 1586-1596.
57. Urban, S., Lee, J.R., and Freeman, M. (2001) Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107: 173-182.
58. Urban, S., Lee, J.R., and Freeman, M. (2002a) A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J 21: 4277-4286.
59. Urban, S., Schlieper, D., and Freeman, M. (2002b) Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids. Curr Biol 12: 1507-1512.
60. Vera, I.M., Beatty, W.L., Sinnis, P., and Kim, K. (2011) Plasmodium protease ROM1 is important for proper formation of the parasitophorous vacuole. PLoS Pathog 7: e1002197.
61. Verma, R., Varshney, G.C., and Raghava, G.P. (2010) Prediction of mitochondrial proteins of malaria parasite using split amino acid composition and PSSM profile. Amino Acids 39: 101-110.
62. Wang, Y., Zhang, Y., and Ha, Y. (2006) Crystal structure of a rhomboid family intramembrane protease. Nature 444: 179-180.
63. Wu, Z., Yan, N., Feng, L., Oberstein, A., Yan, H., Baker, R.P., etal. (2006) Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry. Nat Struct Mol Biol 13: 1084-1091.
64. Yoshida, N., Nussenzweig, R.S., Potocnjak, P., Nussenzweig, V., and Aikawa, M. (1980) Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71-73.