Comparative genomic and phylogenetic analyses of calcium ATPases and calcium-regulated proteins in the Apicomplexa

Molecular Biology and Evolution

Volumn 23, Issue 8, 2006, Pages 1613-1627

  Nagamune, Kisaburo ^a   Sibley, L David ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apicomplexan; Calcium; Calmodulin; Centrin; EF hand; Kinase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ANTIPORTER; CALCIUM CHANNEL P TYPE; CALMODULIN; CENTRIN; PROTEIN; PROTEIN KINASE; RYANODINE; VOLTAGE GATED CALCIUM CHANNEL;

APICOMPLEXA; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CELL MOTILITY; CRYPTOSPORIDIUM; DIFFERENTIATION; ENDOPLASMIC RETICULUM; GENOME ANALYSIS; GOLGI COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; PHYLOGENY; PLASMODIUM; PROTEIN MOTIF; SARCOPLASMIC RETICULUM; SECRETION; SEQUENCE HOMOLOGY; TOXOPLASMA GONDII;

AMINO ACID SEQUENCE; ANIMALS; APICOMPLEXA; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM CHANNELS; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CALCIUM-TRANSPORTING ATPASES; CRYPTOSPORIDIUM; GENOME, PROTOZOAN; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMODIUM; SEQUENCE HOMOLOGY, AMINO ACID; TOXOPLASMA;

ANIMALIA; APICOMPLEXA; CILIOPHORA; CRYPTOSPORIDIUM; EUKARYOTA; PLASMODIUM (APICOMPLEXA); TOXOPLASMA GONDII; VERTEBRATA;

EID: 33748079101     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl026     Document Type: Article

References (91)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-402.
2. Aravind L, Iyer LM, Wellems TE, Miller LH. 2003. Plasmodium biology: genomic gleanings. Cell 115:771-85.
3. Baldauf SL. 2003. The deep roots of eukaryotes. Science 300:1703-6.
4. Bastien O, Lespinats S, Roy S, Metayer K, Fertil B, Codani J-J, Marechal E. 2004. Analysis of the compositional biases in Plasmodium falciparum genome and proteome using Arabidopsis thaliana as a reference. Gene 336:163-73.
5. Bedard K, Szabo E, Michalak M, Opas M. 2005. Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and ERp57. Int Rev Cytol 245:91-121.
6. Berridge MJ. 1993. Inositol triphosphate and calcium signalling. Nature 361:315-25.
7. Berridge MJ. 1995. Capacitative calcium entry. Biochem J 312:1-11.
8. Berridge MJ, Lipp P, Bootman MD. 2000a. Signal transduction. The calcium entry pas de deux. Science 287:1604-5.
9. Berridge MJ, Lipp P, Bootman MD. 2000b. The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol 1:11-21.
10. Billker O, Lindo V, Panico M, Etienne AE, Paxton T, Dell A, Rogers M, Sinden RE, Morris HR. 1998. Identification of xanthurenic acid as a putative inducer of malaria development in the mosquito. Nature (Lond) 392:289-92.
11. Billker O, Tewari R, Franke-Fayard B, Brinkman V. 2004. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117:503-14.
12. Carruthers VB, Giddings OK, Sibley LD. 1999. Secretion of micronemal proteins is associated with Toxoplasma invasion of host cells. Cell Microbiol 1:225-36.
13. 2+] calcium and stimulate microneme discharge in Toxoplasma gondii. Biochem J 342:379-86.
14. Carvalho TG, Menard R. 2005. Manipulating the Plasmodium genome. Curr Issues Mol Biol 7:39-55.
15. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J. 2005. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57:411-25.
16. Cellebaut I, Prat K, Meurice E, Mornon J-P, Tomavo S. 2005. Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: conserved features and differences relative to other eukaryotes. BMC Genomics 6:100.
17. Chen XM, O'Hara SP, Huang BQ, Nelson JB, Lin JJC, Zhu G, Ward HD, LaRusso NF. 2004. Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infect Immun 72:6806-16.
18. Chini EN, De Toledo FGS. 2002. Nicotinic acid adenine dinucleotide phosphate: a new intracellular second messenger? Am J Physiol 282:C1191-8.
19. Chini EN, Nagamune K, Wetzel DM, Sibley LD. 2005. Evidence that the cADPR signaling pathway controls calcium-mediated secretion in Toxoplasma gondii. Biochem J 389:269-77.
20. Clapham DE. 1995. Calcium signaling. Cell 80:259-68.
21. Docampo R, Souza W, Miranda K, Rohloff P, Moreno SN. 2005. Acidocalcisomes - conserved from bacteria to man. Nat Rev Microbiol 3:251-61.
22. Doerig C, Billker O, Pratt D, Endicott J. 2005. Protein kinases as targets for antimalarial intervention: kinomics, structure-based design, transmission-blockade, and targeting host cell enzymes. Biochim Biophys Acta 1754:132-50.
23. Dyer M, Jackson M, McWhinney C, Zhao G, Mikkelsen R. 1996. Analysis of a cation-transporting ATPase of Plasmodium falciparum. Mol Biochem Parasitol 78:1-12.
24. Eckstein-Ludwig U, Webb RJ, van Goethem IDA, East JM, Lee AG, Kimura M, O'Neill PM, Bray PG, Ward SA, Krishna S. 2003. Artemisinins target the SERCA of Plasmodium falciparum. Nature 424:957-61.
25. Eddy S. 1995. Multiple alignment using hidden Markov models. Proceedings Third International Conference on Intelligent Systems for Molecular Biology. Menlo Park, CA: AAAI Press. p 114-20.
26. Eddy SR. 1998. Profile hidden Markov models. Bioinformatics 14:755-63.
27. Facanha AL, Appelgren H, Tabish M, Okorokov L, Ekwall K. 2002. The endoplasmic reticulum cation P-type ATPase Cta4p is required for control of cell shape and microtubule dynamics. J Cell Biol 157:1029-39.
28. Fang J, Marchesini N, Moreno SNJ. 2005. A Toxoplasma gondii phosphoinositde phospholipase C (TgPI-PLC) with high affinity for phosphatidylinositol. Biochem J 394:417-25.
29. Gantt S, Persson C, Rose K, Birkett AJ, Abagyan B, Nussenzweig V. 2000. Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect Immun 68:3667-73.
30. 2+ channels. Biochem Biophys Res Commun 323:891-7.
31. Guerra C, Wada Y, Leick V, Bell A, Satir P. 2003. Cloning, localization, and axonemal function of Tetrahymena centrin. Mol Biol Cell 14:251-61.
32. Hannah AL. 2005. Kinases as drug discovery targets in hematologic malignancies. Curr Mol Med 5:625-42.
33. 2+ signal? Trends Plant Sci 5:154-9.
34. Harper JF, Harmon AC. 2005. Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6:555-66.
35. Hartmann J, Hu K, He CY, Pelletier L, Roos DS, Warren GL. 2006. Golgi and centrosome cycles in Toxoplasma gondii. Mol Biochem Parasitol 145:125-7.
36. Haynes RK, Krishna S. 2004. Artemisinins: activities and actions. Microbes Infect 6:1339-46.
37. Higgins DG, Thompson JD, Gibson TJ. 1996. Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:382-402.
38. 2+/CaM-dependent kinases: from activation to function. Annu Rev Pharmacol Toxicol 41:471-505.
39. Hu K, Johnson J, Florens L, Franholz M, Suravajjala S, Dilullo C, Yates JR, Roos DS, Murray JM. 2006. Cytoskeletal components of an invasion machine - the apical complex of Toxoplasma gondii. PLoS Pathog 2:121-38.
40. Huang J, Mullapudi N, Sicheritz-Ponten T, Kissinger JC. 2004. A first glimpse into the pattern and scale of gene transfer in the Apicomplexa. Int J Parasitol 34:265-74.
41. Ishibashi K, Suzuki M, Imai M. 2000. Molecular cloning of a novel form (two repeat) protein related to voltage-gated sodium and calcium channels. Biochim Biophys Res Commun 270:370-6.
42. Ishino T, Orito Y, Chinzei Y, Yuda M. 2006. A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59:1175-84.
43. 2+ channels. J Exp Biol 203:841-56.
44. Khan A, Taylor S, Su C, et al. (17 co-authors). 2005. Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res 33:2980-92.
45. Khan SM, Franke-Fayard B, Mair GR, Lasonder E, Janse CJ, Mann M, Waters AP. 2005. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121:675-87.
46. Kieschnick H, Wakefield T, Narducci CA, Beckers C. 2001. Toxoplasma gondii attachment to host cells is regulated by a calmodulin-like domain protein kinase. J Biol Chem 276:12369-77.
47. 2+-dependent protein kinases. J Cell Sci 115:1973-84.
48. 2+-ATPases. J Cell Sci 104:1129-36.
49. 2+-ATPase (PfATP4) belonging to a subclass unique to apicomplexan organisms. J Biol Chem 276:10782-7.
50. Kuhlbrandt W. 2004. Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282-95.
51. 3 / ryanodine sensitive stores. J Biol Chem 277:25870-6.
52. Lovett JL, Sibley LD. 2003. Intracellular calcium stores in Toxoplasma gondii govern invasion of host cells. J Cell Sci 116:3009-16.
53. 2+ ATPase (TgA1) of Toxoplasma gondii is required for polyphosphate storage, intracellular calcium homeostasis and virulence. Mol Microbiol 55:1034-45.
54. +-pyrophosphatase to acidocalcisomes of Toxoplasma gondii. EMBO J 20:55-64.
55. 2+ in a protist, Euglena gracilis. Comp Biochem Physiol 118:279-83.
56. Miller RJ, Fox AP. 1990. Voltage-sensitive calcium channels. In: Bronner F, editor. Intracellular calcium regulation. Wiley-Liss. p 97-138.
57. Molinier J, Ramos C, Fritsch O, Hohn B. 2004. CENTRIN2 modulates homologous recombination and nuclear excision repair in Arabidopsis. Plant Cell 16:1633-43.
58. Moreno SNJ, Docampo R. 2003. Calcium regulation in protozoan parasites. Curr Opin Microbiol 6:359-64.
59. Moreno SNJ, Zhong L. 1996. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem J 313:655-9.
60. Morrissette NS, Sibley LD. 2002. Cytoskeleton of apicomplexan parasites. Microbiol. Mol Biol Rev 66:21-38.
61. Musto H, Rodriguez-Maseda H, Bernardi G. 1995. Compositional properties of nuclear genes from Plasmodium falciparum. Gene 152:127-32.
62. Musto H, Romero H, Zavala A, Jabbari K, Bernardi G. 1999. Synonymous codon choices in the extremely GC-poor genome of Plasmodium falciparum: compositional constraints and translational selection. J Mol Evol 49:27-35.
63. Nagata T, Iizumi S, Satoh K, et al. (11 co-authors). 2004. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol Biol Evol 21:1855-70.
64. O'Neill PM. 2004. Medicinal chemistry: a worthy adversary for malaria. Nature 430:838-9.
65. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature (Lond) 434:404-8.
66. Plattner H. 2002. My favorite cell - Paramecium. Bioessays 24:649-58.
67. 2+ release channels). Trends Biochem Sci 22:193-4.
68. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. 2005. InterProScan: protein domains identifier. Nucleic Acids Res 33:W116-20.
69. Roos DS, Donald RGK, Morrissette NS, Moulton AL. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 45:28-61.
70. 2+ transport ATPase by thapsigargin at subnanomolar concentrations. J Biol Chem 266:13503-6.
71. Sagara Y, Wade JB, Inesi G. 1992. A conformational mechanism for formation of a dead-end complex by the sarcoplasmic reticulum ATPase with thapsigargin. J Biol Chem 267:1286-92.
72. Salisbury JL. 1995. Centrin, centrosomes, and mitotic spindle poles. Curr Opin Cell Biol 7:39-45.
73. Salisbury JL, Suino KM, Busby R, Springett M. 2002. Centrin-2 is required for centriole duplicaiton in mammalian cells. Curr Biol 12:1287-92.
74. Schwartz GK, Shah MA. 2005. Targeting the cell cycle: a new approach to cancer therapy. J Clin Oncol 23:9408-21.
75. 2+ release channels in evolution. Curr Opin Genet Devel 10:662-7.
76. Stemm-Wolf AJ, Morgan G, Gidddings TH Jr, White EA, Marchione R, McDonald HB, Winey M. 2005. Basal body duplication and maintenance require one member of the Tetrahymena thermophila centrin gene family. Mol Biol Cell 16:3606-19.
77. Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F, Roos DS. 2000. The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151:1423-34.
78. Su XZ, Wootton JC. 2004. Genetic mapping in the human malaria parasite Plasmodium falciparum. Mol Microbiol 53:1573-82.
79. Swofford DL. 1998. PAUP. Phylogenetic analysis using parsimony and other methods. Sunderland, MA: Sinauer Associates.
80. Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, Subramanian GM, Hoffman SL, Abrahamsen MS, Aravind L. 2004. Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14:1686-95.
81. Thiel G, MacRobbie EAC, Hanke DE. 1990. Raising the intracellular level of inositol 1,4,5-triphosphate changes plasma membrane ion transport in characean algae. EMBO J 9:1737-41.
82. Trottein F, Corman AF. 1995. Molecular cloning and sequence of two novel P-type adenosinetriphosphatases from Plasmodium falciparum. Eur J Biochem 227:214-25.
83. 2+ ATPases. Gene 158:133-7.
84. Tsien RW. 1990. Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715-60.
85. 2+ pool. Cell Calcium 33:137-44.
86. Wetzel DM, Chen LA, Ruiz FA, Moreno SNJ, Sibley LD. 2004. Calcium-mediated protein secretion potentiates motility by Toxoplasma gondii. J Cell Sci 117:5739-48.
87. White PJ. 2000. Calcium channels in higher plants. Biochim Biophys Acta 1465:171-89.
88. Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R, Chua NH. 1997. Abscisic acid signaling through cyclic ADP ribose in plants. Science 278:2126-30.
89. Wuytack F, Raeymaekers L, Missiaen L. 2002. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 35:279-305.
90. Yap KL, Ames JB, Swindells MB, Ikura M. 1999. Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins 37:499-507.
91. Zhu G, Keithly JS. 1997. Molecular analysis of a P-type ATPase from Cryptosporidium parvum. Mol Biochem Parasitol 90:307-16.