An essential role of the basal body protein SAS-6 in Plasmodium male gamete development and malaria transmission

Cellular Microbiology

Volumn 17, Issue 2, 2015, Pages 191-206

  Marques, Sara R ^a   Ramakrishnan, Chandra ^b   Carzaniga, Raffaella ^c   Blagborough, Andrew M ^a   Delves, Michael J ^a   Talman, Arthur M ^d   Sinden, Robert E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SAS 6; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APICOMPLEXA; ARTICLE; AXONEME; CELL ORGANELLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; FEMALE; FERTILIZATION IN VITRO; FLAGELLUM; GAMETE; GAMETOCYTE; GAMETOGENESIS; GENE INACTIVATION; HOST PARASITE INTERACTION; KINETOSOME; MALARIA; MALE; MICROTUBULE; MOSQUITO; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIRULENCE; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN MOTIF; REPRODUCTION; SEQUENCE ALIGNMENT; SPOROZOITE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PARASITOLOGY; PHYSIOLOGY; TRANSMISSION;

EUKARYOTA; PLASMODIUM (APICOMPLEXA); PLASMODIUM PARASITES; VERTEBRATA;

ANIMALS; BASAL BODIES; CULICIDAE; GENE KNOCKOUT TECHNIQUES; MALARIA; MICE; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS;

EID: 84921491375     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12355     Document Type: Article

References (48)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Bettencourt-Dias, M., and Glover, D.M. (2009) SnapShot: centriole biogenesis. Cell 136: 188-188.e1.
3. Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B., and Brinkmann, V. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503-514.
4. van Breugel, M., Hirono, M., Andreeva, A., Yanagisawa, H.A., Yamaguchi, S., Nakazawa, Y., etal. (2011) Structures of SAS-6 suggest its organization in centrioles. Science 331: 1196-1199.
5. van Breugel, M., Wilcken, R., McLaughlin, S.H., Rutherford, T.J., and Johnson, C.M. (2014) Structure of the SAS-6 cartwheel hub from Leishmania major. eLife 3: e01812.
6. Briggs, L.J., Davidge, J.A., Wickstead, B., Ginger, M.L., and Gull, K. (2004) More than one way to build a flagellum: comparative genomics of parasitic protozoa. Curr Biol 14: R611-R612.
7. Carvalho-Santos, Z., Machado, P., Branco, P., Tavares-Cadete, F., Rodrigues-Martins, A., Pereira-Leal, J.B., and Bettencourt-Dias, M. (2010) Stepwise evolution of the centriole-assembly pathway. J Cell Sci 123: 1414-1426.
8. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
9. Cheadle, M.A., Toivio-Kinnucan, M., and Blagburn, B.L. (1999) The ultrastructure of gametogenesis of Cryptosporidium baileyi (Eimeriorina; Cryptosporidiidae) in the respiratory tract of broiler chickens (Gallus domesticus). J Parasitol 85: 609-615.
10. Collins, F.H., Sakai, R.K., Vernick, K.D., Paskewitz, S., Seeley, D.C., Miller, L.H., etal. (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234: 607-610.
11. Culver, B.P., Meehl, J.B., Giddings, T.H., Jr, and Winey, M. (2009) The two SAS-6 homologs in Tetrahymena thermophila have distinct functions in basal body assembly. Mol Biol Cell 20: 1865-1877.
12. Delves, M.J., Ruecker, A., Straschil, U., Lelievre, J., Marques, S., Lopez-Barragan, M.J., etal. (2013) Male and female Plasmodium falciparum mature gametocytes show different responses to antimalarial drugs. Antimicrob Agents Chemother 57: 3268-3274.
13. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., etal. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
14. Dimopoulos, G., Seeley, D., Wolf, A., and Kafatos, F.C. (1998) Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J 17: 6115-6123.
15. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
16. Fidock, D.A. (2010) Drug discovery: priming the antimalarial pipeline. Nature 465: 297-298.
17. Guttery, D.S., Holder, A.A., and Tewari, R. (2012) Sexual development in Plasmodium: lessons from functional analyses. PLoS Pathog 8: e1002404.
18. Han, Y.G., Kwok, B.H., and Kernan, M.J. (2003) Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr Biol 13: 1679-1686.
19. Heitman, J. (2010) Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8: 86-99.
20. Hodges, M.E., Scheumann, N., Wickstead, B., Langdale, J.A., and Gull, K. (2010) Reconstructing the evolutionary history of the centriole from protein components. J Cell Sci 123: 1407-1413.
21. Janse, C.J., van der Klooster, P.F., van der Kaay, H.J., van der Ploeg, M., and Overdulve, J.P. (1986a) DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol Biochem Parasitol 20: 173-182.
22. Janse, C.J., Van der Klooster, P.F., Van der Kaay, H.J., Van der Ploeg, M., and Overdulve, J.P. (1986b) Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. Trans R Soc Trop Med Hyg 80: 154-157.
23. 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.
24. Kitagawa, D., Vakonakis, I., Olieric, N., Hilbert, M., Keller, D., Olieric, V., etal. (2011) Structural basis of the 9-fold symmetry of centrioles. Cell 144: 364-375.
25. Kobayashi, T., and Dynlacht, B.D. (2011) Regulating the transition from centriole to basal body. J Cell Biol 193: 435-444.
26. Kumar, N., and Carter, R. (1985) Biosynthesis of two stage-specific membrane proteins during transformation of Plasmodium gallinaceum zygotes into ookinetes. Mol Biochem Parasitol 14: 127-139.
27. Leidel, S., Delattre, M., Cerutti, L., Baumer, K., and Gonczy, P. (2005) SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat Cell Biol 7: 115-125.
28. de Leon, J.C., Scheumann, N., Beatty, W., Beck, J.R., Tran, J.Q., Yau, C., etal. (2013) A SAS-6-like prote in suggests that the toxoplasma conoid complex evolved from flagellar components. Eukaryot Cell 12: 1009-1019.
29. Liu, Y., Tewari, R., Ning, J., Blagborough, A.M., Garbom, S., Pei, J., etal. (2008) The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 22: 1051-1068.
30. Mair, G.R., Braks, J.A., Garver, L.S., Wiegant, J.C., Hall, N., Dirks, R.W., etal. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313: 667-669.
31. Marshall, W.F. (2008) Basal bodies platforms for building cilia. Curr Top Dev Biol 85: 1-22.
32. Nakazawa, Y., Hiraki, M., Kamiya, R., and Hirono, M. (2007) SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr Biol 17: 2169-2174.
33. Ostrovska, K. and Paperna, I. (1990) Cryptosporidium sp. of the starred lizard Agama stellio: ultrastructure and life cycle. Parasitol Res 76: 712-720.
34. Reininger, L., Billker, O., Tewari, R., Mukhopadhyay, A., Fennell, C., Dorin-Semblat, D., etal. (2005) A NIMA-related protein kinase is essential for completion of the sexual cycle of malaria parasites. J Biol Chem 280: 31957-31964.
35. Rodrigues-Martins, A., Bettencourt-Dias, M., Riparbelli, M., Ferreira, C., Ferreira, I., Callaini, G., and Glover, D.M. (2007) DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 17: 1465-1472.
36. Rodriguez, M.C., Margos, G., Compton, H., Ku, M., Lanz, H., Rodriguez, M.H., and Sinden, R.E. (2002) Plasmodium berghei: routine production of pure gametocytes, extracellular gametes, zygotes, and ookinetes. Exp Parasitol 101: 73-76.
37. Sarpal, R., Todi, S.V., Sivan-Loukianova, E., Shirolikar, S., Subramanian, N., Raff, E.C., etal. (2003) Drosophila KAP interacts with the kinesin II motor subunit KLP64D to assemble chordotonal sensory cilia, but not sperm tails. Curr Biol 13: 1687-1696.
38. Schrevel, J., Asfaux-Foucher, G., and Bafort, J. (1977) Etude ultrastructurale des mitoses multiples au cours de la sporogonie du Plasmodium b berghei. J Ultrastruct Res 59: 332-350.
39. Sinden, R. (1978) Cell Biology. In Rodent Malaria. New York. London: Academic Press.
40. Sinden, R.E., Canning, E.U., and Spain, B. (1976) Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proc R Soc Lond B Biol Sci 193: 55-76.
41. Sinden, R.E., Canning, E.U., Bray, R.S., and Smalley, M.E. (1978) Gametocyte and gamete development in Plasmodium falciparum. Proc R Soc Lond B Biol Sci 201: 375-399.
42. Sinden, R.E., Butcher, G.A., and Beetsma, A.L. (2002) Maintenance of the Plasmodium berghei life cycle. Methods Mol Med 72: 25-40.
43. Sinden, R.E., Talman, A., Marques, S.R., Wass, M.N., and Sternberg, M.J. (2010) The flagellum in malarial parasites. Curr Opin Microbiol 13: 491-500.
44. Talman, A.M., Lacroix, C., Marques, S.R., Blagborough, A.M., Carzaniga, R., Menard, R., and Sinden, R.E. (2011) PbGEST mediates malaria transmission to both mosquito and vertebrate host. Mol Microbiol 82: 462-474.
45. Tewari, R., Dorin, D., Moon, R., Doerig, C., and Billker, O. (2005) An atypical mitogen-activated protein kinase controls cytokinesis and flagellar motility during male gamete formation in a malaria parasite. Mol Microbiol 58: 1253-1263.
46. Vladar, E.K., and Stearns, T. (2007) Molecular characterization of centriole assembly in ciliated epithelial cells. J Cell Biol 178: 31-42.
47. Wilson, L.G., Carter, L.M., and Reece, S.E. (2013) High-speed holographic microscopy of malaria parasites reveals ambidextrous flagellar waveforms. Proc Natl Acad Sci USA 110: 18769-18774.
48. Yoeli, M., and Upmanis, R.S. (1968) Plasmodium berghei ookinete formation in vitro. Exp Parasitol 22: 122-128.