Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Evidences of G Coupled-Protein Receptor (GPCR) Signaling in the human Malaria Parasite Plasmodium falciparum for Sensing its Microenvironment and the Role of Purinergic Signaling in Malaria Parasites

Author(s): Pedro H.S. Pereira, Lucas Borges-Pereira and Célia R.S. Garcia*

Volume 21, Issue 3, 2021

Published on: 26 August, 2020

Page: [171 - 180] Pages: 10

DOI: 10.2174/1568026620666200826122716

Abstract

The nucleotides were discovered in the early 19th century and a few years later, the role of such molecules in energy metabolism and cell survival was postulated. In 1972, a pioneer work by Burnstock and colleagues suggested that ATP could also work as a neurotransmitter, which was known as the “purinergic hypothesis”. The idea of ATP working as a signaling molecule faced initial resistance until the discovery of the receptors for ATP and other nucleotides, called purinergic receptors. Among the purinergic receptors, the P2Y family is of great importance because it comprises of G proteincoupled receptors (GPCRs). GPCRs are widespread among different organisms. These receptors work in the cells' ability to sense the external environment, which involves: to sense a dangerous situation or detect a pheromone through smell; the taste of food that should not be eaten; response to hormones that alter metabolism according to the body's need; or even transform light into an electrical stimulus to generate vision. Advances in understanding the mechanism of action of GPCRs shed light on increasingly promising treatments for diseases that have hitherto remained incurable, or the possibility of abolishing side effects from therapies widely used today.

Keywords: Malaria, Receptors, Plasmodium falciparum, E-NTPDase, GPCRs, Side effects.

« Previous Next »
Graphical Abstract

[1]
Fredriksson, R.; Lagerström, M.C.; Lundin, L.G.; Schiöth, H.B. The g-protein-coupled receptors in the human genome form five main families. phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol., 2003, 63(6), 1256-1272.
[2]
Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci., 2004, 5(4), 263-278.
[http://dx.doi.org/10.1038/nrn1365] [PMID: 15034552]
[3]
Overington, J.P.; Al-Lazikani, B.; Hopkins, A.L. How many drug targets are there? Nat. Rev. Drug Discov., 2006, 5(12), 993-996.
[http://dx.doi.org/10.1038/nrd2199] [PMID: 17139284]
[4]
Rask-Andersen, M.; Masuram, S.; Schiöth, H.B. The druggable genome: evaluation of drug targets in clinical trials suggests major shifts in molecular class and indication. Annu. Rev. Pharmacol. Toxicol., 2014, 54, 9-26.
[PMID: 24016212]
[5]
Schiöth, H.B.; Fredriksson, R. The grafs classification system of g-protein coupled receptors in comparative perspective. Gen. Comp. Endocrinol., 2005, 142(1-2), 94-101.
[http://dx.doi.org/10.1016/j.ygcen.2004.12.018]
[6]
Manglik, A.; Kobilka, B. The role of protein dynamics in GPCR function: insights from the β2AR and rhodopsin. Curr. Opin. Cell Biol., 2014, 27, 136-143.
[http://dx.doi.org/10.1016/j.ceb.2014.01.008] [PMID: 24534489]
[7]
Park, P.S-H. Rhodopsin oligomerization and aggregation. J. Membr. Biol., 2019, 252(4-5), 413-423.
[http://dx.doi.org/10.1007/s00232-019-00078-1] [PMID: 31286171]
[8]
Kobilka, B.K. Structural insights into adrenergic receptor function and pharmacology. Trends Pharmacol. Sci., 2011, 32(4), 213-218.
[http://dx.doi.org/10.1016/j.tips.2011.02.005] [PMID: 21414670]
[9]
Fredriksson, R.; Lagerström, M.C.; Höglund, P.J.; Schiöth, H.B. Novel human G protein-coupled receptors with long N-terminals containing GPS domains and Ser/Thr-rich regions. FEBS Lett., 2002, 531(3), 407-414.
[http://dx.doi.org/10.1016/S0014-5793(02)03574-3] [PMID: 12435584]
[10]
Prömel, S.; Langenhan, T.; Araç, D. Matching structure with function: the GAIN domain of adhesion-GPCR and PKD1-like proteins. Trends Pharmacol. Sci., 2013, 34(8), 470-478.
[http://dx.doi.org/10.1016/j.tips.2013.06.002] [PMID: 23850273]
[11]
Langenhan, T.; Aust, G.; Hamann, J. Sticky signaling--adhesion class G protein-coupled receptors take the stage. Sci. Signal., 2013, 6(276), re3.
[http://dx.doi.org/10.1126/scisignal.2003825] [PMID: 23695165]
[12]
Paavola, K.J.; Sidik, H.; Zuchero, J.B.; Eckart, M.; Talbot, W.S.; Type, I.V. Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126. Sci. Signal., 2014, 7(338), ra76.
[http://dx.doi.org/10.1126/scisignal.2005347] [PMID: 25118328]
[13]
Scholz, N.; Gehring, J.; Guan, C.; Ljaschenko, D.; Fischer, R.; Lakshmanan, V.; Kittel, R.J.; Langenhan, T. The adhesion GPCR latrophilin/CIRL shapes mechanosensation. Cell Rep., 2015, 11(6), 866-874.
[http://dx.doi.org/10.1016/j.celrep.2015.04.008] [PMID: 25937282]
[14]
Poyner, D.R.; Hay, D.L. Secretin family (Class B) G protein-coupled receptors - from molecular to clinical perspectives. Br. J. Pharmacol., 2012, 166(1), 1-3.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01810.x] [PMID: 22489621]
[15]
Harmar, A.J. Family-B G-protein-coupled receptors. Genome Biol., 2001, 2(12), S3013.
[http://dx.doi.org/10.1186/gb-2001-2-12-reviews3013] [PMID: 11790261]
[16]
Miller, L.J.; Dong, M.; Harikumar, K.G. Ligand binding and activation of the secretin receptor, a prototypic family B G protein-coupled receptor. Br. J. Pharmacol., 2012, 166(1), 18-26.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01463.x] [PMID: 21542831]
[17]
Zhang, H.; Qiao, A.; Yang, L.; Van Eps, N.; Frederiksen, K.S.; Yang, D.; Dai, A.; Cai, X.; Zhang, H.; Yi, C.; Cao, C.; He, L.; Yang, H.; Lau, J.; Ernst, O.P.; Hanson, M.A.; Stevens, R.C.; Wang, M.W.; Reedtz-Runge, S.; Jiang, H.; Zhao, Q.; Wu, B. Structure of the glucagon receptor in complex with a glucagon analogue. Nature, 2018, 553(7686), 106-110.
[http://dx.doi.org/10.1038/nature25153] [PMID: 29300013]
[18]
Slusarski, D.C.; Corces, V.G.; Moon, R.T. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature, 1997, 390(6658), 410-413.
[http://dx.doi.org/10.1038/37138] [PMID: 9389482]
[19]
Dzitoyeva, S.; Dimitrijevic, N.; Manev, H. Gamma-aminobutyric acid B receptor 1 mediates behavior-impairing actions of alcohol in Drosophila: adult RNA interference and pharmacological evidence. Proc. Natl. Acad. Sci. USA, 2003, 100(9), 5485-5490.
[http://dx.doi.org/10.1073/pnas.0830111100] [PMID: 12692303]
[20]
Latorraca, N.R.; Venkatakrishnan, A.J.; Dror, R.O. GPCR dynamics: structures in motion. Chem. Rev., 2017, 117(1), 139-155.
[http://dx.doi.org/10.1021/acs.chemrev.6b00177] [PMID: 27622975]
[21]
Venkatakrishnan, A.J.; Deupi, X.; Lebon, G.; Heydenreich, F.M.; Flock, T.; Miljus, T.; Balaji, S.; Bouvier, M.; Veprintsev, D.B.; Tate, C.G.; Schertler, G.F.X.; Babu, M.M. Diverse activation pathways in class A GPCRs converge near the G-protein-coupling region. Nature, 2016, 536(7617), 484-487.
[http://dx.doi.org/10.1038/nature19107] [PMID: 27525504]
[22]
Rosenbaum, D.M.; Rasmussen, S.G.F.; Kobilka, B.K. The structure and function of G-protein-coupled receptors. Nature, 2009, 459(7245), 356-363.
[http://dx.doi.org/10.1038/nature08144] [PMID: 19458711]
[23]
Kenakin, T. New concepts in pharmacological efficacy at 7TM receptors: IUPHAR review 2. Br. J. Pharmacol., 2013, 168(3), 554-575.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02223.x] [PMID: 22994528]
[24]
Mizuno, T.M.; Makimura, H.; Mobbs, C.V. The physiological function of the agouti-related peptide gene: the control of weight and metabolic rate. Ann. Med., 2003, 35(6), 425-433.
[http://dx.doi.org/10.1080/07853890310012076] [PMID: 14572167]
[25]
Downes, G.B.; Gautam, N. The G protein subunit gene families. Genomics, 1999, 62(3), 544-552.
[http://dx.doi.org/10.1006/geno.1999.5992] [PMID: 10644457]
[26]
Lokits, A.D.; Indrischek, H.; Meiler, J.; Hamm, H.E.; Stadler, P.F. Tracing the evolution of the heterotrimeric G protein α subunit in Metazoa. BMC Evol. Biol., 2018, 18(1), 51.
[http://dx.doi.org/10.1186/s12862-018-1147-8] [PMID: 29642851]
[27]
Kristiansen, K. Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of g-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharm. Thera., 2004, 103(1), 21-80.
[28]
Hilger, D.; Masureel, M.; Kobilka, B.K. Structure and dynamics of GPCR signaling complexes. Nat. Struct. Mol. Biol., 2018, 25(1), 4-12.
[http://dx.doi.org/10.1038/s41594-017-0011-7] [PMID: 29323277]
[29]
Oldham, W.M.; Hamm, H.E.; Heterotrimeric, G. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol., 2008, 9(1), 60-71.
[http://dx.doi.org/10.1038/nrm2299] [PMID: 18043707]
[30]
Khan, S.M.; Sleno, R.; Gora, S.; Zylbergold, P.; Laverdure, J-P.; Labbé, J-C.; Miller, G.J.; Hébert, T.E. The expanding roles of Gβγ subunits in G protein-coupled receptor signaling and drug action. Pharmacol. Rev., 2013, 65(2), 545-577.
[http://dx.doi.org/10.1124/pr.111.005603] [PMID: 23406670]
[31]
Rajagopal, S.; Shenoy, S.K. GPCR desensitization: Acute and prolonged phases. Cell. Signal., 2018, 41, 9-16.
[http://dx.doi.org/10.1016/j.cellsig.2017.01.024] [PMID: 28137506]
[32]
kuhn, H. Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry, 1978, 17(21), 4389-4395.
[33]
Benovic, J.L.; Strasser, R.H.; Caron, M.G.; Lefkowitz, R.J. β-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc. Natl. Acad. Sci. USA, 1986, 83(9), 2797-2801.
[http://dx.doi.org/10.1073/pnas.83.9.2797] [PMID: 2871555]
[34]
Gurevich, E.V.; Tesmer, J.J.G.; Mushegian, A.; Gurevich, V.V.G. G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther., 2012, 133(1), 40-69.
[http://dx.doi.org/10.1016/j.pharmthera.2011.08.001] [PMID: 21903131]
[35]
Liang, Y.L.; Khoshouei, M.; Radjainia, M.; Zhang, Y.; Glukhova, A.; Tarrasch, J.; Thal, D.M.; Furness, S.G.B.; Christopoulos, G.; Coudrat, T.; Danev, R.; Baumeister, W.; Miller, L.J.; Christopoulos, A.; Kobilka, B.K.; Wootten, D.; Skiniotis, G.; Sexton, P.M. Phase-plate cryo-EM structure of a class B GPCR-G-protein complex. Nature, 2017, 546(7656), 118-123.
[http://dx.doi.org/10.1038/nature22327] [PMID: 28437792]
[36]
Zhang, Y.; Sun, B.; Feng, D.; Hu, H.; Chu, M.; Qu, Q.; Tarrasch, J.T.; Li, S.; Sun Kobilka, T.; Kobilka, B.K.; Skiniotis, G. Cryo-EM structure of the activated GLP-1 receptor in complex with a G protein. Nature, 2017, 546(7657), 248-253.
[http://dx.doi.org/10.1038/nature22394] [PMID: 28538729]
[37]
Zhou, X.E.; He, Y.; de Waal, P.W.; Gao, X.; Kang, Y.; Van Eps, N.; Yin, Y.; Pal, K.; Goswami, D.; White, T.A.; Barty, A.; Latorraca, N.R.; Chapman, H.N.; Hubbell, W.L.; Dror, R.O.; Stevens, R.C.; Cherezov, V.; Gurevich, V.V.; Griffin, P.R.; Ernst, O.P.; Melcher, K.; Xu, H.E. Identification of phosphorylation codes for arrestin recruitment by g protein-coupled receptors. Cell, 2017, 170(3), 457-469.e13.
[http://dx.doi.org/10.1016/j.cell.2017.07.002] [PMID: 28753425]
[38]
Cahill, T.J.; Thomsen, A.R.B.; Tarrasch, J.T.; Plouffe, B.; Nguyen, A.H.; Yang, F.; Huang, L.Y.; Kahsai, A.W.; Bassoni, D.L.; Gavino, B.J.; Lamerdin, J.E.; Triest, S.; Shukla, A.K.; Berger, B.; Little, J.; Antar, A.; Blanc, A.; Qu, C.X.; Chen, X.; Kawakami, K.; Inoue, A.; Aoki, J.; Steyaert, J.; Sun, J.P.; Bouvier, M.; Skiniotis, G.; Lefkowitz, R.J. Distinct conformations of gpcr-β-arrestin complexes mediate desensitization, signaling, and endocytosis. Proc. Natl. Acad. Sci. USA, 2017, 114(10), 2562-2567.
[39]
Kumari, P.; Srivastava, A.; Ghosh, E.; Ranjan, R.; Dogra, S.; Yadav, P.N.; Shukla, A.K. Core engagement with β-arrestin is dispensable for agonist-induced vasopressin receptor endocytosis and ERK activation. Mol. Biol. Cell, 2017, 28(8), 1003-1010.
[http://dx.doi.org/10.1091/mbc.e16-12-0818] [PMID: 28228552]
[40]
Moaven, H.; Koike, Y.; Jao, C.C.; Gurevich, V.V.; Langen, R.; Chen, J. Visual arrestin interaction with clathrin adaptor ap-2 regulates photoreceptor survival in the vertebrate retina. Proc. Natl. Acad. Sci. USA, 2013, 110(23), 9463-9468.
[http://dx.doi.org/10.1073/pnas.1301126110]
[41]
Huber, S.M. Purinoceptor signaling in malaria-infected erythrocytes. Microbes Infect., 2012, 14(10), 779-786.
[http://dx.doi.org/10.1016/j.micinf.2012.04.009] [PMID: 22580091]
[42]
Budu, A.; Garcia, C.R.S. Generation of second messengers in Plasmodium. Microbes Infect., 2012, 14(10), 787-795.
[http://dx.doi.org/10.1016/j.micinf.2012.04.012] [PMID: 22584103]
[43]
Touré, A.; Langsley, G.; Egée, S. Spermatozoa and plasmodium zoites: the same way to invade oocyte and host cells? Microbes Infect., 2012, 14(10), 874-879.
[http://dx.doi.org/10.1016/j.micinf.2012.04.014] [PMID: 22561468]
[44]
Miranda-Saavedra, D.; Gabaldón, T.; Barton, G.J.; Langsley, G.; Doerig, C. The kinomes of apicomplexan parasites. Microbes Infect., 2012, 14(10), 796-810.
[http://dx.doi.org/10.1016/j.micinf.2012.04.007] [PMID: 22587893]
[45]
Lasonder, E.; Treeck, M.; Alam, M.; Tobin, A.B. Insights into the Plasmodium falciparum schizont phospho-proteome. Microbes Infect., 2012, 14(10), 811-819.
[http://dx.doi.org/10.1016/j.micinf.2012.04.008] [PMID: 22569589]
[46]
Singh, S.; Chitnis, C.E. Signalling mechanisms involved in apical organelle discharge during host cell invasion by apicomplexan parasites. Microbes Infect., 2012, 14(10), 820-824.
[http://dx.doi.org/10.1016/j.micinf.2012.05.007] [PMID: 22634343]
[47]
Holder, A.A.; Mohd Ridzuan, M.A.; Green, J.L. Calcium dependent protein kinase 1 and calcium fluxes in the malaria parasite. Microbes Infect., 2012, 14(10), 825-830.
[http://dx.doi.org/10.1016/j.micinf.2012.04.006] [PMID: 22584104]
[48]
Hopp, C.S.; Bowyer, P.W.; Baker, D.A. The role of cGMP signalling in regulating life cycle progression of Plasmodium. Microbes Infect., 2012, 14(10), 831-837.
[http://dx.doi.org/10.1016/j.micinf.2012.04.011] [PMID: 22613210]
[49]
Haste, N.M.; Talabani, H.; Doo, A.; Merckx, A.; Langsley, G.; Taylor, S.S. Exploring the Plasmodium falciparum cyclic-adenosine monophosphate (cAMP)-dependent protein kinase (PfPKA) as a therapeutic target. Microbes Infect., 2012, 14(10), 838-850.
[http://dx.doi.org/10.1016/j.micinf.2012.05.004] [PMID: 22626931]
[50]
Fairhurst, R.M.; Bess, C.D.; Krause, M.A. Abnormal pfemp1/knob display on plasmodium falciparum-infected erythrocytes containing hemoglobin variants: fresh insights into malaria pathogenesis and protection. Microbes Infect., 2012, 14(10), 851-862.
[51]
Zhang, Y.; Xia, Y. Adenosine signaling in normal and sickle erythrocytes and beyond. Microbes Infect., 2012, 14(10), 863-873.
[http://dx.doi.org/10.1016/j.micinf.2012.05.005] [PMID: 22634345]
[52]
Hotta, C.T.; Gazarini, M.L.; Beraldo, F.H.; Varotti, F.P.; Lopes, C.; Markus, R.P.; Pozzan, T.; Garcia, C.R.S. Calcium-dependent modulation by melatonin of the circadian rhythm in malarial parasites. Nat. Cell Biol., 2000, 2(7), 466-468.
[http://dx.doi.org/10.1038/35017112] [PMID: 10878815]
[53]
Beraldo, F.H.; Garcia, C.R.S. Products of tryptophan catabolism induce Ca2+ release and modulate the cell cycle of Plasmodium falciparum malaria parasites. J. Pineal Res., 2005, 39(3), 224-230.
[http://dx.doi.org/10.1111/j.1600-079X.2005.00249.x] [PMID: 16150101]
[54]
Budu, A.; Peres, R.; Bueno, V.B.; Catalani, L.H.; Garcia, C.R.D.S. N1-acetyl-N2-formyl-5-methoxykynuramine modulates the cell cycle of malaria parasites. J. Pineal Res., 2007, 42(3), 261-266.
[http://dx.doi.org/10.1111/j.1600-079X.2006.00414.x] [PMID: 17349024]
[55]
Alves, E.; Bartlett, P.J.; Garcia, C.R.S.; Thomas, A.P. Melatonin and IP3-induced Ca2+ release from intracellular stores in the malaria parasite Plasmodium falciparum within infected red blood cells. J. Biol. Chem., 2011, 286(7), 5905-5912.
[http://dx.doi.org/10.1074/jbc.M110.188474] [PMID: 21149448]
[56]
Garcia, C.R.S.; Alves, E.; Pereira, P.H.S.; Bartlett, P.J.; Thomas, A.P.; Mikoshiba, K.; Plattner, H.; Sibley, L.D. InsP3 Signaling in Apicomplexan Parasites. Curr. Top. Med. Chem., 2017, 17(19), 2158-2165.
[http://dx.doi.org/10.2174/1568026617666170130121042] [PMID: 28137231]
[57]
Dorin, D.; Semblat, J.P.; Poullet, P.; Alano, P.; Goldring, J.P.D.; Whittle, C.; Patterson, S.; Chakrabarti, D.; Doerig, C. PfPK7, an atypical MEK-related protein kinase, reflects the absence of classical three-component MAPK pathways in the human malaria parasite Plasmodium falciparum. Mol. Microbiol., 2005, 55(1), 184-196.
[http://dx.doi.org/10.1111/j.1365-2958.2004.04393.x] [PMID: 15612927]
[58]
Dorin-Semblat, D.; Sicard, A.; Doerig, C.; Ranford-Cartwright, L.; Doerig, C. Disruption of the PfPK7 gene impairs schizogony and sporogony in the human malaria parasite Plasmodium falciparum. Eukaryot. Cell, 2008, 7(2), 279-285.
[http://dx.doi.org/10.1128/EC.00245-07] [PMID: 18083830]
[59]
Koyama, F.C.; Ribeiro, R.Y.; Garcia, J.L.; Azevedo, M.F.; Chakrabarti, D.; Garcia, C.R. Ubiquitin proteasome system and the atypical kinase PfPK7 are involved in melatonin signaling in Plasmodium falciparum. J. Pineal Res., 2012, 53(2), 147-153.
[http://dx.doi.org/10.1111/j.1600-079X.2012.00981.x] [PMID: 22348509]
[60]
Pease, B.N.; Huttlin, E.L.; Jedrychowski, M.P.; Dorin-Semblat, D.; Sebastiani, D.; Segarra, D.T.; Roberts, B.F.; Chakrabarti, R.; Doerig, C.; Gygi, S.P.; Chakrabarti, D. Characterization of Plasmodium falciparum Atypical kinase PfPK7- dependent phosphoproteome. J. Proteome Res., 2018, 17(6), 2112-2123.
[http://dx.doi.org/10.1021/acs.jproteome.8b00062] [PMID: 29678115]
[61]
Lima, W.R.; Tessarin-Almeida, G.; Rozanski, A.; Parreira, K.S.; Moraes, M.S.; Martins, D.C.; Hashimoto, R.F.; Galante, P.A.F.; Garcia, C.R.S. Signaling transcript profile of the asexual intraerythrocytic development cycle of Plasmodium falciparum induced by melatonin and cAMP. Genes Cancer, 2016, 7(9-10), 323-339.
[PMID: 28050233]
[62]
Koyama, F.C.; Azevedo, M.F.; Budu, A.; Chakrabarti, D.; Garcia, C.R.S. Melatonin-induced temporal up-regulation of gene expression related to ubiquitin/proteasome system (UPS) in the human malaria parasite Plasmodium falciparum. Int. J. Mol. Sci., 2014, 15(12), 22320-22330.
[http://dx.doi.org/10.3390/ijms151222320] [PMID: 25479077]
[63]
Lima, W.R.; Moraes, M.; Alves, E.; Azevedo, M.F.; Passos, D.O.; Garcia, C.R.S. The PfNF-YB transcription factor is a downstream target of melatonin and cAMP signalling in the human malaria parasite Plasmodium falciparum. J. Pineal Res., 2013, 54(2), 145-153.
[http://dx.doi.org/10.1111/j.1600-079X.2012.01021.x] [PMID: 22804732]
[64]
Lima, W.R.; Martins, D.C.; Parreira, K.S.; Scarpelli, P.; Santos de Moraes, M.; Topalis, P.; Hashimoto, R.F.; Garcia, C.R.S. Genome-wide analysis of the human malaria parasite Plasmodium falciparum transcription factor PfNF-YB shows interaction with a CCAAT motif. Oncotarget, 2017, 8(69), 113987-114001.
[http://dx.doi.org/10.18632/oncotarget.23053] [PMID: 29371963]
[65]
Scarpelli, P.; Almeida, G.T.; Vicoso, K.L.; Lima, W.R.; Pereira, L.B.; Meissner, K.A.; Wrenger, C.; Rafaello, A.; Rizzuto, R.; Pozzan, T.; Garcia, C.R.S. Melatonin activate fis1, dyn1 and dyn2 plasmodium falciparum related-genes for mitochondria fission: mitoemerald-gfp as a tool to visualize mitochondria structure. J. Pineal Res., 2018, 66(2)e12484
[PMID: 29480948]
[66]
Brancucci, N.M.B.; Gerdt, J.P.; Wang, C.; De Niz, M.; Philip, N.; Adapa, S.R.; Zhang, M.; Hitz, E.; Niederwieser, I.; Boltryk, S.D.; Laffitte, M-C.; Clark, M.A.; Grüring, C.; Ravel, D.; Blancke Soares, A.; Demas, A.; Bopp, S.; Rubio-Ruiz, B.; Conejo-Garcia, A.; Wirth, D.F.; Gendaszewska-Darmach, E.; Duraisingh, M.T.; Adams, J.H.; Voss, T.S.; Waters, A.P.; Jiang, R.H.Y.; Clardy, J.; Marti, M. Lysophosphatidylcholine regulates sexual stage differentiation in the human malaria parasite Plasmodium falciparum. Cell, 2017, 171(7), 1532-1544.
[http://dx.doi.org/10.1016/j.cell.2017.10.020] [PMID: 29129376]
[67]
Alves, E.; Maluf, F.V.; Bueno, V.B.; Guido, R.V.C.; Oliva, G.; Singh, M.; Scarpelli, P.; Costa, F.; Sartorello, R.; Catalani, L.H.; Brady, D.; Tewari, R.; Garcia, C.R.S. Biliverdin targets enolase and eukaryotic initiation factor 2 (eif2α) to reduce the growth of intraerythrocytic development of the malaria parasite plasmodium falciparum. Sci. Rep., 2016, 6, 22093.
[http://dx.doi.org/10.1038/srep22093]
[68]
Kalckar, H. 50 years of biological research: from oxidative phosphorylation to energy requiring transport regulation. Annu. Rev. Biochem., 1991, 60, 1-37.
[69]
Burnstock, G. Purinergic nerves. Pharmacol. Rev., 1972, 24(3), 509-581.
[PMID: 4404211]
[70]
Burnstock, G. Purinergic signalling: therapeutic developments. Front. Pharmacol., 2017, 8, 661.
[http://dx.doi.org/10.3389/fphar.2017.00661] [PMID: 28993732]
[71]
Burnstock, G. Purine and pyrimidine receptors. Cell. Mol. Life Sci., 2007, 64(12), 1471-1483.
[http://dx.doi.org/10.1007/s00018-007-6497-0] [PMID: 17375261]
[72]
Porowińska, D.; Czarnecka, J.; Komoszyński, M. [The role of ectonucleotides metabolizing enzymes in purinergic signaling] Postepy Biochem., 2011, 57(3), 294-303.
[PMID: 22235655]
[73]
Levano-Garcia, J.; Dluzewski, A.R.; Markus, R.P.; Garcia, C.R.S. Purinergic signalling is involved in the malaria parasite Plasmodium falciparum invasion to red blood cells. Purinergic Signal., 2010, 6(4), 365-372.
[http://dx.doi.org/10.1007/s11302-010-9202-y] [PMID: 21437007]
[74]
Cruz, L.N.; Juliano, M.A.; Budu, A.; Juliano, L.; Holder, A.A.; Blackman, M.J.; Garcia, C.R.S. Extracellular ATP triggers proteolysis and cytosolic Ca2+ rise in Plasmodium berghei and Plasmodium yoelii malaria parasites. Malar. J., 2012, 11, 69.
[http://dx.doi.org/10.1186/1475-2875-11-69] [PMID: 22420332]
[75]
Robson, S.C.; Sévigny, J.; Zimmermann, H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal., 2006, 2(2), 409-430.
[76]
Sansom, F.M. The role of the NTPDase enzyme family in parasites: what do we know, and where to from here? Parasitology, 2012, 139(8), 963-980.
[http://dx.doi.org/10.1017/S003118201200025X] [PMID: 22423612]
[77]
Borges-Pereira, L.; Meissner, K.A.; Wrenger, C.; Garcia, C.R.S. Plasmodium falciparum GFP-E-NTPDase expression at the intraerythrocytic stages and its inhibition blocks the development of the human malaria parasite. Purinergic Signal., 2017, 13(3), 267-277.
[http://dx.doi.org/10.1007/s11302-017-9557-4] [PMID: 28285440]
[78]
Akkaya, C.; Shumilina, E.; Bobballa, D.; Brand, V.B.; Mahmud, H.; Lang, F.; Huber, S.M. The Plasmodium falciparum-induced anion channel of human erythrocytes is an ATP-release pathway. Pflugers Arch., 2009, 457(5), 1035-1047.
[http://dx.doi.org/10.1007/s00424-008-0572-8] [PMID: 18696103]
[79]
Tanneur, V.; Duranton, C.; Brand, V.B.; Sandu, C.D.; Akkaya, C.; Kasinathan, R.S.; Gachet, C.; Sluyter, R.; Barden, J.A.; Wiley, J.S.; Lang, F.; Huber, S.M. Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J., 2006, 20(1), 133-135.
[http://dx.doi.org/10.1096/fj.04-3371fje] [PMID: 16267125]
[80]
Alvarez, C.L.; Schachter, J.; de Sá Pinheiro, A.A. Silva, Lde.S.; Verstraeten, S.V.; Persechini, P.M.; Schwarzbaum, P.J. Regulation of extracellular ATP in human erythrocytes infected with Plasmodium falciparum. PLoS One, 2014, 9(5)e96216
[http://dx.doi.org/10.1371/journal.pone.0096216] [PMID: 24858837]
[81]
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.; Rodriguez, A. Adenylyl cyclase α and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLoS Pathog., 2008, 4(2)e1000008
[http://dx.doi.org/10.1371/journal.ppat.1000008] [PMID: 18389080]
[82]
Wajant, H.; Pfizenmaier, K.; Scheurich, P. Tumor necrosis factor signaling. Cell Death Differ., 2003, 10(1), 45-65.
[http://dx.doi.org/10.1038/sj.cdd.4401189] [PMID: 12655295]
[83]
Cruz, L.N.; Wu, Y.; Ulrich, H.; Craig, A.G.; Garcia, C.R.S. Tumor necrosis factor reduces Plasmodium falciparum growth and activates calcium signaling in human malaria parasites. Biochim. Biophys. Acta, 2016, 1860(7), 1489-1497.
[http://dx.doi.org/10.1016/j.bbagen.2016.04.003] [PMID: 27080559]
[84]
Madeira, L.; Galante, P.A.F.; Budu, A.; Azevedo, M.F.; Malnic, B.; Garcia, C.R.S. Genome-wide detection of serpentine receptor-like proteins in malaria parasites. PLoS One, 2008, 3(3)e1889
[http://dx.doi.org/10.1371/journal.pone.0001889] [PMID: 18365025]
[85]
Wallin, E.; von Heijne, G. Properties of N-terminal tails in G-protein coupled receptors: a statistical study. Protein Eng., 1995, 8(7), 693-698.
[http://dx.doi.org/10.1093/protein/8.7.693] [PMID: 8577697]
[86]
Boddey, J.A.; Moritz, R.L.; Simpson, R.J.; Cowman, A.F. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic, 2009, 10(3), 285-299.
[http://dx.doi.org/10.1111/j.1600-0854.2008.00864.x] [PMID: 19055692]
[87]
Elsworth, B.; Matthews, K.; Nie, C.Q.; Kalanon, M.; Charnaud, S.C.; Sanders, P.R.; Chisholm, S.A.; Counihan, N.A.; Shaw, P.J.; Pino, P.; Chan, J-A.; Azevedo, M.F.; Rogerson, S.J.; Beeson, J.G.; Crabb, B.S.; Gilson, P.R.; de Koning-Ward, T.F. PTEX is an essential nexus for protein export in malaria parasites. Nature, 2014, 511(7511), 587-591.
[http://dx.doi.org/10.1038/nature13555] [PMID: 25043043]
[88]
Heiber, A.; Kruse, F.; Pick, C.; Grüring, C.; Flemming, S.; Oberli, A.; Schoeler, H.; Retzlaff, S.; Mesén-Ramírez, P.; Hiss, J.A.; Kadekoppala, M.; Hecht, L.; Holder, A.A.; Gilberger, T.W.; Spielmann, T. Identification of new PNEPs indicates a substantial non-PEXEL exportome and underpins common features in Plasmodium falciparum protein export. PLoS Pathog., 2013, 9(8)e1003546
[http://dx.doi.org/10.1371/journal.ppat.1003546] [PMID: 23950716]
[89]
Boddey, J.A.; O’Neill, M.T.; Lopaticki, S.; Carvalho, T.G.; Hodder, A.N.; Nebl, T.; Wawra, S.; van West, P.; Ebrahimzadeh, Z.; Richard, D.; Flemming, S.; Spielmann, T.; Przyborski, J.; Babon, J.J.; Cowman, A.F. Export of malaria proteins requires co-translational processing of the PEXEL motif independent of phosphatidylinositol-3-phosphate binding. Nat. Commun., 2016, 7, 10470.
[http://dx.doi.org/10.1038/ncomms10470] [PMID: 26832821]
[90]
Moraes, M.S.; Budu, A.; Singh, M.K.; Borges-Pereira, L.; Levano-Garcia, J.; Currà, C.; Picci, L.; Pace, T.; Ponzi, M.; Pozzan, T.; Garcia, C.R.S. Plasmodium falciparum GPCR-like receptor SR25 mediates extracellular K+ sensing coupled to Ca2+ signaling and stress survival. Sci. Rep., 2017, 7(1), 9545.
[http://dx.doi.org/10.1038/s41598-017-09959-8] [PMID: 28842684]
[91]
Dawn, A.; Singh, S.; More, K.R.; Siddiqui, F.A.; Pachikara, N.; Ramdani, G.; Langsley, G.; Chitnis, C.E. The central role of cAMP in regulating Plasmodium falciparum merozoite invasion of human erythrocytes. PLoS Pathog., 2014, 10(12)e1004520
[http://dx.doi.org/10.1371/journal.ppat.1004520] [PMID: 25522250]
[92]
Pereira, P.H.S.; Brito, G.; Moraes, M.; Kiyan, C.L.; Avet, C.; Bouvier, M.; Garcia, C.R. BRET sensors unravel that plasmodium falciparum serpentine receptor 12 (pfsr12) increases surface expression of mammalian gpcrs in hek293 cells. bioRxiv, 2020. (In Press)
[93]
Dyer, M.; Day, K. Expression of plasmodium falciparum trimeric g proteins and their involvement in switching to sexual development. Mol. Biochem. Parasitol., 2000, 110(2), 437-448.
[http://dx.doi.org/10.1016/S0166-6851(00)00288-7]
[94]
Harrison, T.; Samuel, B.U.; Akompong, T.; Hamm, H.; Mohandas, N.; Lomasney, J.W.; Haldar, K. Erythrocyte G protein-coupled receptor signaling in malarial infection Science (80-. ), 2003, 301(5640), 1734-1736.
[95]
Gurevich, V.V.; Gurevich, E.V. GPCR signaling regulation: the role of grks and arrestins. Front. Pharmacol., 2019, 10, 125.
[http://dx.doi.org/10.3389/fphar.2019.00125] [PMID: 30837883]
[96]
Soderling, S.H.; Beavo, J.A. Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr. Opin. Cell Biol., 2000, 12(2), 174-179.
[http://dx.doi.org/10.1016/S0955-0674(99)00073-3] [PMID: 10712916]
[97]
Claessens, A.; Affara, M.; Assefa, S.A.; Kwiatkowski, D.P.; Conway, D.J. Culture adaptation of malaria parasites selects for convergent loss-of-function mutants. Sci. Rep., 2017, 7, 41303.
[http://dx.doi.org/10.1038/srep41303] [PMID: 28117431]
[98]
Baker, D.A.; Kelly, J.M. Purine nucleotide cyclases in the malaria parasite. Trends Parasitol., 2004, 20(5), 227-232.
[http://dx.doi.org/10.1016/j.pt.2004.02.007] [PMID: 15105023]
[99]
Weber, J.H.; Vishnyakov, A.; Hambach, K.; Schultz, A.; Schultz, J.E.; Linder, J.U. Adenylyl cyclases from Plasmodium, Paramecium and Tetrahymena are novel ion channel/enzyme fusion proteins. Cell. Signal., 2004, 16(1), 115-125.
[http://dx.doi.org/10.1016/S0898-6568(03)00129-3] [PMID: 14607282]
[100]
Salazar, E.; Bank, E.M.; Ramsey, N.; Hess, K.C.; Deitsch, K.W.; Levin, L.R.; Buck, J. Characterization of Plasmodium falciparum adenylyl cyclase-β and its role in erythrocytic stage parasites. PLoS One, 2012, 7(6)e39769
[http://dx.doi.org/10.1371/journal.pone.0039769] [PMID: 22761895]
[101]
Singh, S.; Alam, M.M.; Pal-Bhowmick, I.; Brzostowski, J.A.; Chitnis, C.E. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog., 2010, 6(2)e1000746
[http://dx.doi.org/10.1371/journal.ppat.1000746] [PMID: 20140184]
[102]
Plattner, H.; Sehring, I.M.; Mohamed, I.K.; Miranda, K.; De Souza, W.; Billington, R.; Genazzani, A.; Ladenburger, E.M. Calcium signaling in closely related protozoan groups (Alveolata): non-parasitic ciliates (Paramecium, Tetrahymena) vs. parasitic Apicomplexa (Plasmodium, Toxoplasma). Cell Calcium, 2012, 51(5), 351-382.
[http://dx.doi.org/10.1016/j.ceca.2012.01.006] [PMID: 22387010]
[103]
Moreno, S.N.J.; Ayong, L.; Pace, D.A. Calcium storage and function in apicomplexan parasites. Essays Biochem., 2011, 51, 97-110.
[http://dx.doi.org/10.1042/bse0510097] [PMID: 22023444]
[104]
Vaid, A.; Thomas, D.C.; Sharma, P. Role of Ca2+/calmodulin-PfPKB signaling pathway in erythrocyte invasion by Plasmodium falciparum. J. Biol. Chem., 2008, 283(9), 5589-5597.
[http://dx.doi.org/10.1074/jbc.M708465200] [PMID: 18165240]
[105]
Madeira, L.; DeMarco, R.; Gazarini, M.L.; Verjovski-Almeida, S.; Garcia, C.R. Human malaria parasites display a receptor for activated C kinase ortholog. Biochem. Biophys. Res. Commun., 2003, 306(4), 995-1001.
[http://dx.doi.org/10.1016/S0006-291X(03)01074-X] [PMID: 12821141]

Rights & Permissions Print Cite
Article Metrics
39
1
© 2024 Bentham Science Publishers | Privacy Policy