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cAMP-dependent protein kinase from Plasmodium falciparum: an update

  • NATHALIE WURTZ (a1), CHARLES CHAPUS (a1), JEROME DESPLANS (a1) and DANIEL PARZY (a1)
Summary

One of the most important public health problems in the world today is the emergence and dissemination of drug-resistant malaria parasites. Plasmodium falciparum is the causative agent of the most lethal form of human malaria. New anti-malarial strategies are urgently required, and their design and development require the identification of potential therapeutic targets. However, the molecular mechanisms controlling the life cycle of the malaria parasite are still poorly understood. The published genome sequence of P. falciparum and previous studies have revealed that several homologues of eukaryotic signalling proteins, such as protein kinases, are relatively conserved. Protein kinases are now widely recognized as important drug targets in protozoan parasites. Cyclic AMP-dependent protein kinase (PKA) is implicated in numerous processes in mammalian cells, and the regulatory mechanisms of the cAMP pathway have been characterized. P. falciparum cAMP-dependent protein kinase plays an important role in the parasite's life cycle and thus represents an attractive target for the development of anti-malarial drugs. In this review, we focus on the P. falciparum cAMP/PKA pathway to provide new insights and an improved understanding of this signalling cascade.

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*Corresponding author: Tel: +334 91 15 01 14. Fax: +334 91 15 01 64. E-mail: d.parzy@free.fr
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Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 21042105. doi: 10.1093/bioinformatics/bti263.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403410. doi: 10.1006/jmbi.1990.9999.
Anamika, , Srinivasan, N. and Krupa, A. (2005). A genomic perspective of protein kinases in Plasmodium falciparum. Proteins 58, 180189. doi: 10.1002/prot.20278.
Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195201. doi: 10.1093/bioinformatics/bti770.
Ashby, C. D. and Walsh, D. A. (1972). Characterization of the interaction of a protein inhibitor with adenosine 3′,5′-monophosphate-dependent protein kinases. I. Interaction with the catalytic subunit of the protein kinase. The Journal of Biological Chemistry 247, 66376642.
Ashby, C. D. and Walsh, D. A. (1973). Characterization of the interaction of a protein inhibitor with adenosine 3′,5′-monophosphate-dependent protein kinases. II. Mechanism of action with the holoenzyme. The Journal of Biological Chemistry 248, 12551261.
Bahl, A., Brunk, B., Crabtree, J., Fraunholz, M. J., Gajria, B., Grant, G. R., Ginsburg, H., Gupta, D., Kissinger, J. C., Labo, P., Li, L., Mailman, M. D., Milgram, A. J., Pearson, D. S., Roos, D. S., Schug, J., Stoeckert, C. J. Jr. and Whetzel, P. (2003). PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Research 31, 212215.
Baker, D. A. (2004). Adenylyl and guanylyl cyclases from the malaria parasite Plasmodium falciparum. International Union of Biochemistry and Molecular Biology Life 56, 535540. doi: 10.1080/15216540400013937.
Baker, D. A. and Kelly, J. M. (2004). Purine nucleotide cyclases in the malaria parasite. Trends in Parasitology 20, 227232. doi: 10.1016/j.pt.2004.02.007.
Banky, P., Huang, L. J. and Taylor, S. S. (1998). Dimerization/docking domain of the type Ialpha regulatory subunit of cAMP-dependent protein kinase. Requirements for dimerization and docking are distinct but overlapping. The Journal of Biological Chemistry 273, 3504835055. doi: 10.1074/jbc.273.52.35048.
Barradeau, S., Imaizumi-Scherrer, T., Weiss, M. C. and Faust, D. M. (2002). Intracellular targeting of the type-I alpha regulatory subunit of cAMP-dependent protein kinase. Trends in Cardiovascular Medicine 12, 235241. doi: 10.1016/S1050-1738(02)00167-6.
Baum, J., Papenfuss, A. T., Mair, G. R., Janse, C. J., Vlachou, D., Waters, A. P., Cowman, A. F., Crabb, B. S. and de Koning-Ward, T. F. (2009). Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Research 37, 37883798. doi: 10.1093/nar/gkp239.
Beraldo, F. H., Almeida, F. M., da Silva, A. M. and Garcia, C. R. (2005). Cyclic AMP and calcium interplay as second messengers in melatonin-dependent regulation of Plasmodium falciparum cell cycle. The Journal of Cell Biology 170, 551557. doi: 10.1083/jcb.200505117.
Berman, H. M., Ten Eyck, L. F., Goodsell, D. S., Haste, N. M., Kornev, A. and Taylor, S. S. (2005). The cAMP binding domain: an ancient signaling module. Proceedings of the National Academy of Sciences, USA 102, 4550. doi: 10.1073/pnas.0408579102.
Blackwell, L. J., Birkos, S., Hallam, R., Van De Carr, G., Arroway, J., Suto, C. M. and Janzen, W. P. (2009). High-throughput screening of the cyclic AMP-dependent protein kinase (PKA) using the caliper microfluidic platform. Methods in Molecular Biology 565, 225237. doi: 10.1007/978-1-60327-258-2_11.
Bozdech, Z., Llina, M., Pulliam, B. L., Wong, E. D., Zhu, J. and DeRisi, J. L. (2003). The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. Public Library of Science Biology 1, 116. doi: 10.1371/journal.pbio.0000005.
Bradbury, A. W., Carter, D. C., Miller, W. R., Cho-Chung, Y. S. and Clair, T. (1994). Protein kinase A (PK-A) regulatory subunit expression in colorectal cancer and related mucosa. British Journal of Cancer 69, 738742.
Brockelman, C. R. (1982). Conditions favoring gametocytogenesis in the continuous culture of Plasmodium falciparum. Journal of Protozoology 29, 454458. doi: 10.1111/j.1550-7408.1982.tb05432.x.
Cabrera-Vera, T. M., Vanhauwe, J., Thomas, T. O., Medkova, M., Preininger, A., Mazzoni, M. R. and Hamm, H. E. (2003). Insights into G protein structure, function, and regulation. Endocrine Reviews 24, 765781.
Canaves, J. M. and Taylor, S. S. (2002). Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family. Journal of Molecular Evolution 54, 1729. doi: 10.1007/s00239-001-0013-1.
Carlson, G. L. and Nelson, D. L. (1996). The 44-kDa regulatory subunit of the Paramecium cAMP-dependent protein kinase lacks a dimerization domain and may have a unique autophosphorylation site sequence. Journal of Eukaryotic Microbiology 43, 347356. doi: 10.1111/j.1550-7408.1996.tb03999.x.
Carlton, J. M., Angiuoli, S. V., Suh, B. B., Kooij, T. W., Pertea, M., Silva, J. C., Ermolaeva, M. D., Allen, J. E., Selengut, J. D., Koo, H. L., Peterson, J. D., Pop, M., Kosack, D. S., Shumway, M. F., Bidwell, S. L., Shallom, S. J., van Aken, S. E., Riedmuller, S. B., Feldblyum, T. V., Cho, J. K., Quackenbush, J., Sedegah, M., Shoaibi, A., Cummings, L. M., Florens, L., Yates, J. R., Raine, J. D., Sinden, R. E., Harris, M. A., Cunningham, D. A., Preiser, P. R., Bergman, L. W., Vaidya, A. B., van Lin, L. H., Janse, C. J., Waters, A. P., Smith, H. O., White, O. R., Salzberg, S. L., Venter, J. C., Fraser, C. M., Hoffman, S. L., Gardner, M. J. and Carucci, D. J. (2002). Genome sequence and comparative analysis of the model rodent malaria parasite. Plasmodium yoelii yoelii. Nature, London 419, 512519. doi: 10.1038/nature01099.
Carruthers, V. B., Giddings, O. K. and Sibley, L. D. (1999). Secretion of micronemal proteins is associated with toxoplasma invasion of host cells. Cellular Microbiology 1, 225235. doi: 10.1046/j.1462-5822.1999.00023.x.
Chakrabarti, S. and Freedman, J. E. (2008). Dipyridamole, cerebrovascular disease, and the vasculature. Vascular Pharmacology 48, 143149. doi: 10.1016/j.vph.2007.12.004.
Cho-Chung, Y. S. and Nesterova, M. V. (2005). Tumor reversion: protein kinase A isozyme switching. Annals of the New York Academy of Sciences 1058, 7686. doi: 10.1196/annals.1359.014.
Chung, D. W., Ponts, N., Cervantes, S. and Le Roch, K. G. (2009). Post-translational modifications in Plasmodium: more than you think! Molecular and Biochemical Parasitology 168, 123134. doi: 10.1016/j.molbiopara.2009.08.001.
Cohen, P. and Knebel, A. (2006). KESTREL: a powerful method for identifying the physiological substrates of protein kinases. The Biochemical Journal 393, 16. doi: 10.1042/BJ20051545
Congiatu, C., McGuigan, C., Jiang, W. G., Davies, G. and Mason, M. D. (2005). Naphthyl phosphoramidate derivatives of BVdU as potential anticancer agents: design, synthesis and biological evaluation. Nucleosides, Nucleotides and Nucleic Acids 24, 485489. doi: 10.1081/NCN-200061774.
Dalton, G. D. and Dewey, W. L. (2006). Protein kinase inhibitor peptide (PKI): a family of endogenous neuropeptides that modulate neuronal cAMP-dependent protein kinase function. Neuropeptides 40, 2334. doi: 10.1016/j.npep.2005.10.002.
Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. The Biochemical Journal 351, 95105.
Davis, M. A., Hinerfeld, D., Joseph, S., Hui, Y. H., Huang, N. H., Leszyk, J., Rutherford, , Bethard, J. and Tam, S. W. (2006). Proteomic analysis of rat liver phosphoproteins after treatment with protein kinase inhibitor H89 (N-(2-[p-bromocinnamylamino-]ethyl)-5-isoquinolinesulfonamide). Journal of Pharmacology and Experimental Therapeutics 318, 589595. doi: 10.1124/jpet.105.100032.
De Rasmo, D., Panelli, D., Sardanelli, A. M. and Papa, S. (2008). cAMP-dependent protein kinase regulates the mitochondrial import of the nuclear encoded NDUFS4 subunit of complex I. Cellular Signalling 20, 989997. doi: 10.1016/j.cellsig.2008.01.017.
DeLano, W. L. (2008). The PyMOL Molecular Graphics System. DeLano Scientific LLC, Palo Alto, CA, USA.
Denault, A. Y., Lamarche, Y., Couture, P., Haddad, F., Lambert, J., Tardif, J. C. and Perrault, L. P. (2006). Inhaled milrinone: a new alternative in cardiac surgery? Seminars in Cardiothoracic and Vascular Anesthesia 10, 346360. doi: 10.1177/1089253206294400.
Diller, T. C., Madhusudan, , Xuong, N. H. and Taylor, S. S. (2001). Molecular basis for regulatory subunit diversity in cAMP-dependent protein kinase: crystal structure of the type II beta regulatory subunit. Structure 9, 7382. doi: 10.1016/S0969-2126(00)00556-6.
Diviani, D. (2008). Modulation of cardiac function by A-kinase anchoring proteins. Current Opinion in Pharmacology 8, 166173. doi: 10.1016/j.coph.2007.11.001.
Doerig, C., Abdi, A., Bland, N., Eschenlauer, S., Dorin-Semblat, D., Fennell, C., Halbert, J., Holland, Z., Nivez, M. P., Semblat, J. P., Sicard, A. and Reininger, L. (2010). Malaria: targeting parasite and host cell kinomes. Biochimica et Biophysica Acta 1804, 604612. doi:10.1016/j.bbapap.2009.10.009.
Doerig, C., Baker, D., Billker, O., Blackman, M. J., Chitnis, C., Dhar Kumar, S., Heussler, V., Holder, A. A., Kocken, C., Krishna, S., Langsley, G., Lasonder, E., Menard, R., Meissner, M., Pradel, G., Ranford-Cartwright, L., Sharma, A., Sharma, P., Tardieux, T., Tatu, U. and Alano, P. (2009). Signalling in malaria parasites. The MALSIG consortium. Parasite 16, 169182.
Doerig, C., Billker, O., Haystead, T., Sharma, P., Tobin, A. B. and Waters, N. C. (2008). Protein kinases of malaria parasites: an update. Trends in Parasitology 24, 570577. doi: 10.1016/j.pt.2008.08.007.
Doskeland, S. O., Maronde, E. and Gjertsen, B. T. (1993). The genetic subtypes of cAMP-dependent protein kinase--functionally different or redundant? Biochimica et Biophysica Acta 1178, 249258. doi: 10.1016/0167-4889(93)90201-Y
Druker, B. J. (2002). STI571 (Gleevec) as a paradigm for cancer therapy. Trends in Molecular Medicine 8, S1418. doi: 10.1016/S1471-4914(02)02305-5.
Duncan, F. E., Moss, S. B. and Williams, C. J. (2006). Knockdown of the cAMP-dependent protein kinase (PKA) Type Ialpha regulatory subunit in mouse oocytes disrupts meiotic arrest and results in meiotic spindle defects. Developmental Dynamics 235, 29612968. doi: 10.1002/dvdy.20930.
Dyer, M. and Day, K. (2000). Expression of Plasmodium falciparum trimeric G proteins and their involvement in switching to sexual development. Molecular and Biochemical Parasitology 110, 437448. doi: 10.1016/S0166-6851(00)00288-7.
Egee, S., Lapaix, F., Decherf, G., Staines, H. M., Ellory, J. C., Doerig, C. and Thomas, S. L. (2002). A stretch-activated anion channel is up-regulated by the malaria parasite Plasmodium falciparum. The Journal of Physiology 542, 795801. doi: 10.1113/jphysiol.2002.022970.
Ejigiri, I. and Sinnis, P. (2009). Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Current Opinion in Microbiology 12, 401407. doi: 10.1016/j.mib.2009.06.006.
Emadi, A. and Spivak, J. L. (2009). Anagrelide: 20 years later. Expert Review of Anticancer Therapy 9, 3750. doi: 10.1586/14737140.9.1.37.
Ferguson, S. S. (2001). Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacological Reviews 53, 124.
Fimia, G. M. and Sassone-Corsi, P. (2001). Cyclic AMP signalling. Journal of Cell Science 114, 19711972.
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, London 419, 498511. doi: 10.1038/nature01097.
Gibson, C., Schanen, B., Chakrabarti, D. and Chakrabarti, R. (2006). Functional characterisation of the regulatory subunit of cyclic AMP-dependent protein kinase A homologue of Giardia lamblia: Differential expression of the regulatory and catalytic subunits during encystation. International Journal for Parasitology 36, 791799. doi: 10.1016/j.ijpara.2005.11.008.
Gibson, R. M. and Taylor, S. S. (1997). Dissecting the cooperative reassociation of the regulatory and catalytic subunits of cAMP-dependent protein kinase. Role of Trp-196 in the catalytic subunit. The Journal of Biological Chemistry 272, 3199832005. doi: 10.1074/jbc.272.51.31998.
Gissot, M., Briquet, S., Refour, P., Boschet, C. and Vaquero, C. (2005). PfMyb1, a Plasmodium falciparum transcription factor, is required for intra-erythrocytic growth and controls key genes for cell cycle regulation. Journal of Molecular Biology 346, 2942. doi: 10.1016/j.jmb.2004.11.045.
Gjertsen, B. T., Mellgren, G., Otten, A., Maronde, E., Genieser, H. G., Jastorff, B., Vintermyr, O. K., McKnight, G. S. and Doskeland, S. O. (1995). Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture. Basal cAMP-kinase activity modulates interleukin-1 beta action. The Journal of Biological Chemistry 270, 2059920607. doi: 10.1074/jbc.270.35.20599.
Grant, S. K. (2009). Therapeutic protein kinase inhibitors. Cellular and Molecular Life Sciences 66, 11631177. doi: 10.1007/s00018-008-8539-7.
Green, J. L., Rees-Channer, R. R., Howell, S. A., Martin, S. R., Knuepfer, E., Taylor, H. M., Grainger, M. and Holder, A. A. (2008). The motor complex of Plasmodium falciparum: phosphorylation by a calcium-dependent protein kinase. The Journal of Biological Chemistry 283, 3098030989. doi: 10.1074/jbc.M803129200.
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi: 10.1080/10635150390235520.
Gunasekera, A. M., Patankar, S., Schug, J., Eisen, G., Kissinger, J., Roos, D. and Wirth, D. F. (2004). Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Molecular and Biochemical Parasitology 136, 3542. doi: 10.1016/j.molbiopara.2004.02.007.
Hamm, H. E. (1998). The many faces of G protein signaling. The Journal of Biological Chemistry 273, 669672. doi: 10.1074/jbc.273.2.669
Hanks, S. K. and Hunter, T. (1995). Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. The Federation of American Societies for Experimental Biology Journal 9, 576596.
Hanks, S. K., Quinn, A. M. and Hunter, T. (1988). The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 4252. doi: 10.1126/science.3291115.
Harrison, T., Samuel, B. U., Akompong, T., Hamm, H., Mohandas, N., Lomasney, J. W. and Haldar, K. (2003). Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 301, 17341736. doi: 10.1126/science.1089324.
Hendriks-Balk, M. C., Peters, S. L., Michel, M. C. and Alewijnse, A. E. (2008). Regulation of G protein-coupled receptor signalling: focus on the cardiovascular system and regulator of G protein signalling proteins. European Journal of Pharmacology 585, 278291. doi: 10.1016/j.ejphar.2008.02.088.
Hidaka, H., Inagaki, M., Kawamoto, S. and Sasaki, Y. (1984). Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23, 50365041. doi: 10.1021/bi00316a032.
Holton, S., Merckx, A., Burgess, D., Doerig, C., Noble, M. and Endicott, J. (2003). Structures of P. falciparum PfPK5 test the CDK regulation paradigm and suggest mechanisms of small molecule inhibition. Structure 11, 13291337. doi: 10.1016/j.str.2003.09.020.
Hordijk, W. and Gascuel, O. (2005). Improving the efficiency of SPR moves in phylogenetic tree search methods based on maximum likelihood. Bioinformatics 21, 43384347. doi: 10.1093/bioinformatics/bti713.
Hotta, C. T., Gazarini, M. L., Beraldo, F. H., Varotti, F. P., Lopes, C., Markus, R. P., Pozzan, T. and Garcia, C. R. (2000). Calcium-dependent modulation by melatonin of the circadian rhythm in malarial parasites. Nature Cell Biology 2, 466468. doi: 10.1038/35017112.
Johnson, D. A., Akamine, P., Radzio-Andzelm, E., Madhusudan, M. and Taylor, S. S. (2001). Dynamics of cAMP-dependent protein kinase. Chemical Reviews 101, 22432270. doi: 10.1021/cr000226k.
Johnson, L. (2007). Protein kinases and their therapeutic exploitation. Biochemical Society Transactions 35, 711.
Johnson, L. N. (2009). Protein kinase inhibitors: contributions from structure to clinical compounds. Quarterly Reviews of Biophysics 42, 140. doi: 10.1017/S0033583508004745.
Kase, H., Iwahashi, K., Nakanishi, S., Matsuda, Y., Yamada, K., Takahashi, M., Murakata, C., Sato, A. and Kaneko, M. (1987). K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochemical and Biophysical Research Communications 142, 436440. doi: 10.1016/0006-291X(87)90293-2.
Kaushal, D. C., Carter, R., Miller, L. H. and Krishna, G. (1980). Gametocytogenesis by malaria parasites in continuous culture. Nature, London 286, 490492. doi: 10.1038/286490a0.
Kebaier, C. and Vanderberg, J. P. (2009). Initiation of Plasmodium sporozoite motility by albumin is associated with induction of intracellular signalling. International Journal for Parasitology 40, 2533. doi: 10.1016/j.ijpara.2009.06.011.
Khan, Z. M., Ng, C. and Vanderberg, J. P. (1992). Early hepatic stages of Plasmodium berghei: release of circumsporozoite protein and host cellular inflammatory response. Infection and Immunity 60, 264270.
Kim, C., Xuong, N. H. and Taylor, S. S. (2005). Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307, 690696. doi: 10.1126/science.1104607.
Kirk, K. (2001). Membrane transport in the malaria-infected erythrocyte. Physiological Reviews 81, 495537.
Knighton, D. R., Zheng, J. H., Ten Eyck, L. F., Ashford, V. A., Xuong, N. H., Taylor, S. S. and Sowadski, J. M. (1991). Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 407414. doi: 10.1126/science.1862342.
Kornev, A. P. and Taylor, S. S. (2010). Defining the conserved internal architecture of a protein kinase. Biochimica et Biophysica Acta 1804, 440444. doi: 10.1016/j.bbapap.2009.10.017.
Koyama, F. C., Chakrabarti, D. and Garcia, C. R. (2009). Molecular machinery of signal transduction and cell cycle regulation in Plasmodium. Molecular and Biochemical Parasitology 165, 17. doi: 10.1016/j.molbiopara.2009.01.003.
Kumar, R., Adams, B., Oldenburg, A., Musiyenko, A. and Barik, S. (2002). Characterisation and expression of a PP1 serine/threonine protein phosphatase (PfPP1) from the malaria parasite, Plasmodium falciparum: demonstration of its essential role using RNA interference. Malaria Journal 1, 111. doi: 10.1186/1475-2875-1-5.
Lauer, S., VanWye, J., Harrison, T., McManus, H., Samuel, B. U., Hiller, N. L., Mohandas, N. and Haldar, K. (2000). Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. European Molecular Biology Organization Journal 19, 35563564. doi: 10.1093/emboj/19.14.3556.
Le Roch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., De laVega, P., Holder, A. A., Batalov, S., Carucci, D. J. and Winzeler, E. A. (2003). Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 15031508. doi: 10.1126/science.1087025.
Lefkowitz, R. J. (1998). G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. The Journal of Biological Chemistry 273, 1867718680. doi: 10.1074/jbc.273.30.18677.
Leon, D. A., Herberg, F. W., Banky, P. and Taylor, S. S. (1997). A stable alpha-helical domain at the N terminus of the RIalpha subunits of cAMP-dependent protein kinase is a novel dimerization/docking motif. The Journal of Biological Chemistry 272, 2843128437. doi: 10.1074/jbc.272.45.28431.
Leroy, D. and Doerig, C. (2008). Drugging the Plasmodium kinome: the benefits of academia-industry synergy. Trends in Pharmacological Sciences 29, 241249. doi: 10.1016/j.tips.2008.02.005.
Letunic, I. and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127128. doi: 10.1093/bioinformatics/btl529.
Li, F., Gangal, M., Jones, J. M., Deich, J., Lovett, K. E., Taylor, S. S. and Johnson, D. A. (2000). Consequences of cAMP and catalytic-subunit binding on the flexibility of the A-kinase regulatory subunit. Biochemistry 39, 1562615632. doi: 10.1021/bi002196l.
Li, J. and Cox, L. S. (2000). Isolation and characterisation of a cAMP-dependent protein kinase catalytic subunit gene from Plasmodium falciparum. Molecular and Biochemical Parasitology 109, 157163. doi: 10.1016/S0166-6851(00)00242-5.
Lugnier, C. (2006). Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacology & Therapeutics 109, 366398. doi: 10.1016/j.pharmthera.2005.07.003.
Madeira, L., Galante, P. A., Budu, A., Azevedo, M. F., Malnic, B. and Garcia, C. R. (2008). Genome-wide detection of serpentine receptor-like proteins in malaria parasites. Public Library of Science One 3, e1889. doi: 10.1371/journal.pone.0001889.
Malhotra, P., Dasaradhi, P. V., Kumar, A., Mohmmed, A., Agrawal, N., Bhatnagar, R. K. and Chauhan, V. S. (2002). Double-stranded RNA-mediated gene silencing of cysteine proteases (falcipain-1 and -2) of Plasmodium falciparum. Molecular Microbiology 45, 12451254. doi: 10.1046/j.1365-2958.2002.03105.x.
Manning, G., Plowman, G. D., Hunter, T. and Sudarsanam, S. (2002 a). Evolution of protein kinase signaling from yeast to man. Trends in Biochemical Sciences 27, 514520. doi: 10.1016/S0968-0004(02)02179-5.
Manning, G., Whyte, D. B., Martinez, R., Hunter, T. and Sudarsanam, S. (2002 b). The protein kinase complement of the human genome. Science 298, 19121934. doi: 10.1126/science.1075762.
McColm, A. A., Hommel, M. and Trigg, P. I. (1980). Inhibition of malaria parasite invasion into erythrocytes pretreated with membrane-active drugs. Molecular and Biochemical Parasitology 1, 119127. doi: 10.1016/0166-6851(80)90006-7.
McConnachie, G., Langeberg, L. K. and Scott, J. D. (2006). AKAP signaling complexes: getting to the heart of the matter. Trends in Molecular Medicine 12, 317323. doi: 10.1016/j.molmed.2006.05.008.
McRobert, L. and McConkey, G. A. (2002). RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Molecular and Biochemical Parasitology 119, 273278. doi: 10.1016/S0166-6851(01)00429-7.
McRobert, L., Taylor, C. J., Deng, W., Fivelman, Q. L., Cummings, R. M., Polley, S. D., Billker, O. and Baker, D. A. (2008). Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. Public Library of Science Biology 6, e139. doi: 10.1371/journal.pbio.0060139.
Meissner, M., Breinich, M. S., Gilson, P. R. and Crabb, B. S. (2007). Molecular genetic tools in Toxoplasma and Plasmodium: achievements and future needs. Current Opinion in Microbiology 10, 349356. doi: 10.1016/j.mib.2007.07.006.
Merckx, A., Bouyer, G., Thomas, S. L., Langsley, G. and Egee, S. (2009). Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A. Trends in Parasitology 25, 139144. doi: 10.1016/j.pt.2008.12.005.
Merckx, A., Echalier, A., Langford, K., Sicard, A., Langsley, G., Joore, J., Doerig, C., Noble, M. and Endicott, J. (2008 a). Structures of P. falciparum protein kinase 7 identify an activation motif and leads for inhibitor design. Structure 16, 228238. doi: 10.1016/j.str.2007.11.014.
Merckx, A., Nivez, M. P., Bouyer, G., Alano, P., Langsley, G., Deitsch, K., Thomas, S., Doerig, C. and Egee, S. (2008 b). Plasmodium falciparum regulatory subunit of cAMP-dependent PKA and anion channel conductance. Public Library of Science Pathogens 4, e19. doi: 10.1371/journal.ppat.0040019.
Miller, W. R. (2002). Regulatory subunits of PKA and breast cancer. Annals of the New York Academy of Sciences 968, 3748.
Modjtahedi, H. and Essapen, S. (2009). Epidermal growth factor receptor inhibitors in cancer treatment: advances, challenges and opportunities. Anticancer Drugs 20, 851855. doi: 10.1097/CAD.0b013e3283330590.
Mota, M. M., Hafalla, J. C. and Rodriguez, A. (2002). Migration through host cells activates Plasmodium sporozoites for infection. Nature Medicine 8, 13181322. doi: 10.1038/nm785.
Mota, M. M. and Rodriguez, A. (2002). Invasion of mammalian host cells by Plasmodium sporozoites. Bioessays 24, 149156. doi: 10.1002/bies.10050.
Muhia, D. K., Swales, C. A., Eckstein-Ludwig, U., Saran, S., Polley, S. D., Kelly, J. M., Schaap, P., Krishna, S. and Baker, D. A. (2003). Multiple splice variants encode a novel adenylyl cyclase of possible plastid origin expressed in the sexual stage of the malaria parasite Plasmodium falciparum. The Journal of Biological Chemistry 278, 2201422022. doi: 10.1074/jbc.M301639200.
Murray, A. J. (2008). Pharmacological PKA inhibition: all may not be what it seems. Science Signaling 1, re4. doi: 10.1126/scisignal.122re4.
Murtaugh, M. P., Steiner, A. L. and Davies, P. J. (1982). Localization of the catalytic subunit of cyclic AMP-dependent. Protein kinase in cultured cells using a specific antibody. The Journal of Cell Biology 95, 6472.
Mutzel, R., Lacombe, M. L., Simon, M. N., de Gunzburg, J. and Veron, M. (1987). Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum. Proceedings of the National Academy of Sciences, USA 84, 610.
Naviglio, S., Caraglia, M., Abbruzzese, A., Chiosi, E.,Di Gesto, D., Marra, M., Romano, M., Sorrentino, A., Sorvillo, L., Spina, A. and Illiano, G. (2009). Protein kinase A as a biological target in cancer therapy. Expert Opinion on Therapeutic Targets 13, 8392. doi: 10.1517/14728220802602349.
Neuberger, G., Schneider, G. and Eisenhaber, F. (2007). pkaPS: prediction of protein kinase A phosphorylation sites with the simplified kinase-substrate binding model. Biology Direct 2, 1. doi: 10.1186/1745-6150-2-1.
Newlon, M. G., Roy, M., Morikis, D., Carr, D. W., Westphal, R., Scott, J. D. and Jennings, P. A. (2001). A novel mechanism of PKA anchoring revealed by solution structures of anchoring complexes. European Molecular Biology Organization Journal 20, 16511662. doi: 10.1093/emboj/20.7.1651.
Noonpakdee, W., Pothikasikorn, J., Nimitsantiwong, W. and Wilairat, P. (2003). Inhibition of Plasmodium falciparum proliferation in vitro by antisense oligodeoxynucleotides against malarial topoisomerase II. Biochemical and Biophysical Research Communications 302, 659664. doi: 10.1016/S0006-291X(03)00246-8.
Notredame, C., Higgins, D. G. and Heringa, J. (2000). T-Coffee: A novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302, 205217. doi: 10.1006/jmbi.2000.4042.
Ogata, J., Segawa, K. and Minami, K. (2007). Effects of colforsin daropate hydrochloride on myocardium, smooth muscle and renal function. Masui 56, 896910.
Ono, T., Cabrita-Santos, L., Leitao, R., Bettiol, E., Purcell, L. A., Diaz-Pulido, O., Andrews, L. B., Tadakuma, T., Bhanot, P., Mota, M. M. and Rodriguez, A. (2008). Adenylyl cyclase alpha and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. Public Library of Science Pathogens 4, e1000008. doi: 10.1371/journal.ppat.1000008.
Orsatti, L., Forte, E., Tomei, L., Caterino, M., Pessi, A. and Talamo, F. (2009). 2-D Difference in gel electrophoresis combined with Pro-Q Diamond staining: a successful approach for the identification of kinase/phosphatase targets. Electrophoresis 30, 24692476. doi: 10.1002/elps.200800780.
Pavan, B., Biondi, C. and Dalpiaz, A. (2009). Adenylyl cyclases as innovative therapeutic goals. Drug Discovery Today 14, 982991. doi: 10.1016/j.drudis.2009.07.007.
Peng, C., Knebel, A., Morrice, N. A., Li, X., Barringer, K., Li, J., Jakes, S., Werneburg, B. and Wang, L. (2007). Pim kinase substrate identification and specificity. The Journal of Biochemistry 141, 353362. doi: 10.1093/jb/mvm040.
Perabo, F. G. and Muller, S. C. (2007). New agents for treatment of advanced transitional cell carcinoma. Annals of Oncology 18, 835843. doi: 10.1093/annonc/mdl331.
Philip, N. and Haystead, T. A. (2007). Characterization of a UBC13 kinase in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 104, 78457850. doi: 10.1073/pnas.0611601104.
Pierre, S., Eschenhagen, T., Geisslinger, G. and Scholich, K. (2009). Capturing adenylyl cyclases as potential drug targets. Nature Reviews Drug Discovery 8, 321335. doi: 10.1038/nrd2827.
Poirot, O., O'Toole, E. and Notredame, C. (2003). Tcoffee@igs: A web server for computing, evaluating and combining multiple sequence alignments. Nucleic Acids Research 31, 35033506.
Pradhan, A. and Tuteja, R. (2007). Bipolar, dual Plasmodium falciparum helicase 45 expressed in the intraerythrocytic developmental cycle is required for parasite growth. Journal of Molecular Biology 373, 268281. doi: 10.1016/j.jmb.2007.07.056.
Rangachari, K., Dluzewski, A., Wilson, R. J. and Gratzer, W. B. (1986). Control of malarial invasion by phosphorylation of the host cell membrane cytoskeleton. Nature 324, 364365. doi: 10.1038/324364a0.
Rathjen, T., Nicol, C., McConkey, G. and Dalmay, T. (2006). Analysis of short RNAs in the malaria parasite and its red blood cell host. Federation of European Biochemical Societies Letters 580, 51855188. doi: 10.1016/j.febslet.2006.08.063.
Ray, B. K., Chen, J. and Ray, A. (2001). Catalytic subunit of protein kinase A is an interacting partner of the inflammation-responsive transcription factor serum amyloid A-activating factor-1. The Journal of Immunology 167, 23432348.
Read, L. K. and Mikkelsen, R. B. (1990). Cyclic AMP- and Ca2(+)-dependent protein kinases in Plasmodium falciparum. Experimental Parasitology 71, 3948. doi: 10.1016/0014-4894(90)90006-X.
Read, L. K. and Mikkelsen, R. B. (1991 a). Comparison of adenylate cyclase and cAMP-dependent protein kinase in gametocytogenic and nongametocytogenic clones of Plasmodium falciparum. The Journal of Parasitology 77, 346352.
Read, L. K. and Mikkelsen, R. B. (1991 b). Plasmodium falciparum-infected erythrocytes contain an adenylate cyclase with properties which differ from those of the host enzyme. Molecular and Biochemical Parasitology 45, 109119. doi: 10.1016/0166-6851(91)90032-2.
Renslo, A. R. and McKerrow, J. H. (2006). Drug discovery and development for neglected parasitic diseases. Nature Chemical Biology 2, 701710. doi: 10.1038/nchembio837.
Sastri, M., Barraclough, D. M., Carmichael, P. T. and Taylor, S. S. (2005). A-kinase-interacting protein localizes protein kinase A in the nucleus. Proceedings of the National Academy of Sciences, USA 102, 349354. doi: 10.1073/pnas.0408608102.
Schulenberg, B., Goodman, T. N., Aggeler, R., Capaldi, R. A. and Patton, W. F. (2004). Characterization of dynamic and steady-state protein phosphorylation using a fluorescent phosphoprotein gel stain and mass spectrometry. Electrophoresis 25, 25262532. doi: 10.1002/elps.200406007.
Shabb, J. B. (2001). Physiological substrates of cAMP-dependent protein kinase. Chemical Reviews 101, 23812411. doi: 10.1021/cr0002361.
Shoji, S., Parmelee, D. C., Wade, R. D., Kumar, S., Ericsson, L. H., Walsh, K. A., Neurath, H., Long, G. L., Demaille, J. G., Fischer, E. H. and Titani, K. (1981). Complete amino acid sequence of the catalytic subunit of bovine cardiac muscle cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences, USA 78, 848851.
Smith, C. M., Radzio-Andzelm, E., Madhusudan, , Akamine, P. and Taylor, S. S. (1999). The catalytic subunit of cAMP-dependent protein kinase: prototype for an extended network of communication. Progress in Biophysics and Molecular Biology 71, 313341. doi: 10.1016/S0079-6107(98)00059-5.
Spaccapelo, R., Naitza, S., Robson, K. J. and Crisanti, A. (1997). Thrombospondin-related adhesive protein (TRAP) of Plasmodium berghei and parasite motility. The Lancet 350, 335. doi: 10.1016/S0140-6736(97)24031-6.
Sriwilaijaroen, N., Boonma, S., Attasart, P., Pothikasikorn, J., Panyim, S. and Noonpakdee, W. (2009). Inhibition of Plasmodium falciparum proliferation in vitro by double-stranded RNA directed against malaria histone deacetylase. Biochemical and Biophysical Research Communications 381, 144147. doi: 10.1016/j.bbrc.2009.01.165.
Su, Y., Dostmann, W. R., Herberg, F. W., Durick, K., Xuong, N. H., Ten Eyck, L., Taylor, S. S. and Varughese, K. I. (1995). Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science 269, 807813. doi: 10.1126/science.7638597.
Sudo, A., Kato, K., Kobayashi, K., Tohya, Y. and Akashi, H. (2008). Susceptibility of Plasmodium falciparum cyclic AMP-dependent protein kinase and its mammalian homologue to the inhibitors. Molecular and Biochemical Parasitology 160, 138142. doi: 10.1016/j.molbiopara.2008.03.011.
Syin, C., Parzy, D., Traincard, F., Boccaccio, I., Joshi, M. B., Lin, D. T., Yang, X. M., Assemat, K., Doerig, C. and Langsley, G. (2001). The H89 cAMP-dependent protein kinase inhibitor blocks Plasmodium falciparum development in infected erythrocytes. European Journal of Biochemistry 268, 48424849. doi: 10.1046/j.1432-1327.2001.02403.x.
Takeda, J., Adachi, K., Halprin, K. M., Itami, S., Levine, V. and Woodyard, C. (1983). Forskolin activates adenylate cyclase activity and inhibits mitosis in in vitro in pig epidermis. Journal of Investigative Dermatology 81, 236240. doi: 10.1111/1523-1747.ep12518219.
Takio, K., Smith, S. B., Krebs, E. G., Walsh, K. A. and Titani, K. (1984). Amino acid sequence of the regulatory subunit of bovine type II adenosine cyclic 3′,5′-phosphate dependent protein kinase. Biochemistry 23, 42004206. doi: 10.1021/bi00313a029.
Tasken, K. and Aandahl, E. M. (2004). Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiological Reviews 84, 137167. doi: 10.1152/physrev.00021.2003.
Taylor, C. J., McRobert, L. and Baker, D. A. (2008 a). Disruption of a Plasmodium falciparum cyclic nucleotide phosphodiesterase gene causes aberrant gametogenesis. Molecular Microbiology 69, 110118. doi: 10.1111/j.1365-2958.2008.06267.x.
Taylor, S. S., Buechler, J. A. and Yonemoto, W. (1990). cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annual Review of Biochemistry 59, 9711005. doi: 10.1146/annurev.bi.59.070190.004543.
Taylor, S. S., Kim, C., Cheng, C. Y., Brown, S. H., Wu, J. and Kannan, N. (2008 b). Signaling through cAMP and cAMP-dependent protein kinase: diverse strategies for drug design. Biochimica et Biophysica Acta 1784, 1626. doi: 10.1016/j.bbapap.2007.10.002.
Tham, W. H., Wilson, D. W., Reiling, L., Chen, L., Beeson, J. G. and Cowman, A. F. (2009). Antibodies to reticulocyte binding protein-like homologue 4 inhibit invasion of Plasmodium falciparum into human erythrocytes. Infection and Immunity 77, 24272435. doi: 10.1128/IAI.00048-09.
Tibes, R., Trent, J. and Kurzrock, R. (2005). Tyrosine kinase inhibitors and the dawn of molecular cancer therapeutics. Annual Review of Pharmacology and Toxicology 45, 357384. doi: 10.1146/annurev.pharmtox.45.120403.100124.
Torrentino-Madamet, M., Desplans, J., Travaille, C., James, Y. and Parzy, D. (2009). Microaerophilic respiratory metabolism of Plasmodium falciparum mitochondrion as a drug target. Current Molecular Medicine 10, 2946.
Tortora, G. and Ciardiello, F. (2002). Protein kinase A as target for novel integrated strategies of cancer therapy. Annals of the New York Academy of Sciences 968, 139147. doi: 10.1111/j.1749-6632.2002.tb04332.x.
Trager, W. and Gill, G. S. (1989). Plasmodium falciparum gametocyte formation in vitro: its stimulation by phorbol diesters and by 8-bromo cyclic adenosine monophosphate. Journal of Protozoology 36, 451454. doi: 10.1111/j.1550-7408.1989.tb01079.x.
Uhler, M. D., Carmichael, D. F., Lee, D. C., Chrivia, J. C., Krebs, E. G. and McKnight, G. S. (1986). Isolation of cDNA clones coding for the catalytic subunit of mouse cAMP-dependent protein kinase. Proceedings of the National Academy of Sciences, USA 83, 13001304.
Ullu, E., Tschudi, C. and Chakraborty, T. (2004). RNA interference in protozoan parasites. Cellular Microbiology 6, 509519. doi: 10.1111/j.1462-5822.2004.00399.x.
van Dooren, G. G., Stimmler, L. M. and McFadden, G. I. (2006). Metabolic maps and functions of the Plasmodium mitochondrion. Federation of European Microbiological Societies Microbiology Reviews 30, 596630. doi: 10.1111/j.1574-6976.2006.00027.x.
Walsh, D. A., Perkins, J. P. and Krebs, E. G. (1968). An adenosine 3′,5′-monophosphate-dependant protein kinase from rabbit skeletal muscle. The Journal of Biological Chemistry 243, 37633765.
Wang, H., Hang, J., Shi, Z., Li, M., Yu, D., Kandimalla, E. R., Agrawal, S. and Zhang, R. (2002). Antisense oligonucleotide targeted to RIalpha subunit of cAMP-dependent protein kinase (GEM231) enhances therapeutic effectiveness of cancer chemotherapeutic agent irinotecan in nude mice bearing human cancer xenografts: in vivo synergistic activity, pharmacokinetics and host toxicity. International Journal of Oncology 21, 7380.
Ward, P., Equinet, L., Packer, J. and Doerig, C. (2004). Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BioMed Central Genomics 5, 79. doi: 10.1186/1471-2164-5-79.
Weber, J. H., Vishnyakov, A., Hambach, K., Schultz, A., Schultz, J. E. and Linder, J. U. (2004). Adenylyl cyclases from Plasmodium, Paramecium and Tetrahymena are novel ion channel/enzyme fusion proteins. Cellular Signalling 16, 115125. doi: 10.1016/S0898-6568(03)00129-3.
Wellbrock, C., Karasarides, M. and Marais, R. (2004). The RAF proteins take centre stage. Nature Reviews Molecular Cell Biology 5, 875885. doi: 10.1038/nrm1498.
Wentzinger, L., Bopp, S., Tenor, H., Klar, J., Brun, R., Beck, H. P. and Seebeck, T. (2008). Cyclic nucleotide-specific phosphodiesterases of Plasmodium falciparum: PfPDEalpha, a non-essential cGMP-specific PDE that is an integral membrane protein. International Journal for Parasitology 38, 16251637. doi: 10.1016/j.ijpara.2008.05·016.
Wise, A., Gearing, K. and Rees, S. (2002). Target validation of G-protein coupled receptors. Drug Discovery Today 7, 235246. doi: 10.1016/S1359-6446(01)02131-6.
Wurtz, N., Desplans, J. and Parzy, D. (2009 a). Phenotypic and transcriptomic analyses of Plasmodium falciparum protein kinase A catalytic subunit inhibition. Parasitology Research 105, 16911699. doi: 10.1007/s00436-009-1615-6.
Wurtz, N., Pastorino, B., Almeras, L., Briolant, S., Villard, C. and Parzy, D. (2009 b). Expression and biochemical characterization of the Plasmodium falciparum protein kinase A catalytic subunit. Parasitology Research 104, 12991305. doi: 10.1007/s00436-008-1327-3.
Yuasa, K.,Mi-Ichi, F., Kobayashi, T., Yamanouchi, M., Kotera, J., Kita, K. and Omori, K. (2005). PfPDE1, a novel cGMP-specific phosphodiesterase from the human malaria parasite Plasmodium falciparum. The Biochemical Journal 392, 221229. doi: 10.1042/BJ20050425.
Zhang, C., Newsome, J. T., Mewani, R., Pei, J., Gokhale, P. C. and Kasid, U. N. (2009). Systemic delivery and pre-clinical evaluation of nanoparticles containing antisense oligonucleotides and siRNAs. Methods in Molecular Biology 480, 6583. doi: 10.1007/978-1-59745-429-2_5.
Zhang, K. Y., Ibrahim, P. N., Gillette, S. and Bollag, G. (2005). Phosphodiesterase-4 as a potential drug target. Expert Opinion on Therapeutic Targets 9, 12831305. doi: 10.1517/14728222.9.6.1283.
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