Host cell transcriptional profiling during malaria liver stage infection reveals a coordinated and sequential set of biological events

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Albuquerque, Sónia S ^a   Carret, Céline ^a   Grosso, Ana Rita ^a   Tarun, Alice S ^b   Peng, Xinxia ^b   Kappe, Stefan H I ^b   Prudêncio, Miguel ^a   Mota, Maria M ^a,c  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEPATITIS; HOST PARASITE INTERACTION; IMMUNE RESPONSE; LIVER CELL; MALARIA; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM YOELII; ANIMAL; BAGG ALBINO MOUSE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; LIVER; METABOLISM; PARASITOLOGY; SPOROZOITE; TIME; TUMOR CELL LINE;

MUS; PLASMODIUM BERGHEI; PLASMODIUM PARASITES; PLASMODIUM YOELII; RODENTIA;

ANIMALS; CELL LINE, TUMOR; GENE EXPRESSION PROFILING; HEPATOCYTES; HOST-PARASITE INTERACTIONS; LIVER; MALARIA; MICE; MICE, INBRED BALB C; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM BERGHEI; SPOROZOITES; TIME FACTORS;

EID: 67650520138     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-270     Document Type: Article

References (44)

1. Guerra CA Gikandi PW Tatem AJ Noor AM Smith DL Hay SI Snow RW The limits and intensity of Plasmodium falciparum transmission: Implications for malaria control and elimination worldwide PLoS Med 2008, 5(2):e38. 2253602 18303939 10.1371/journal.pmed.0050038
2. Sinnis P Zavala F The skin stage of malaria infection: Biology and relevance to the malaria vaccine effort Future Microbiol 2008, 3:275-278. 10.2217/17460913.3.3.275 18505393
3. Frevert U Engelmann S Zougbede S Stange J Ng B Matuschewski K Liebes L Yee H Intravital observation of Plasmodium berghei sporozoite infection of the liver PLoS Biol 2005, 3(6):e192. 1135295 15901208 10.1371/ journal.pbio.0030192
4. Mota MM Pradel G Vanderberg JP Hafalla JC Frevert U Nussenzweig RS Nussenzweig V Rodriguez A Migration of Plasmodium sporozoites through cells before infection Science 2001, 291(5501):141-144. 10.1126/ science.291.5501.141 11141568
5. Prudencio M Rodriguez A Mota MM The silent path to thousands of merozoites: The Plasmodium liver stage Nat Rev Microbiol 2006, 4(11):849-856. 10.1038/nrmicro1529 17041632
6. Heussler V Doerig C In vivo imaging enters parasitology Trends Parasitol 2006, 22(5):192-195. 10.1016/j.pt.2006.03.001 16545613
7. Janse CJ Ramesar J Waters AP High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei Nat Protoc 2006, 1(1):346-356. 10.1038/ nprot.2006.53 17406255
8. Prudencio M Rodrigues CD Hannus M Martin C Real E Goncalves LA Carret C Dorkin R Rohl I Jahn-Hoffmann K et al Kinome-wide RNAi screen implicates at least 5 host hepatocyte kinases in Plasmodium sporozoite infection PLoS Pathog 2008, 4(11):e1000201. 2574010 18989463 10.1371/ journal.ppat.1000201
9. Rodrigues CD Hannus M Prudencio M Martin C Goncalves LA Portugal S Epiphanio S Akinc A Hadwiger P Jahn-Hofmann K et al Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection Cell Host Microbe 2008, 4(3):271-282. 10.1016/ j.chom.2008.07.012 18779053
10. Cunha-Rodrigues M Prudencio M Mota MM Haas W Antimalarial drugs - host targets (re)visited Biotechnol J 2006, 1(3):321-332. 10.1002/ biot.200500038 16897712
11. Prudencio M Rodrigues CD Ataide R Mota MM Dissecting in vitro host cell infection by Plasmodium sporozoites using flow cytometry Cell Microbiol 2007, 10(1):218-224. 17697130
12. Mota MM Rodriguez A Plasmodium yoelii: Efficient in vitro invasion and complete development of sporozoites in mouse hepatic cell lines Exp Parasitol 2000, 96(4):257-259. 10.1006/expr.2000.4570 11162379
13. Franke-Fayard B Trueman H Ramesar J Mendoza J Keur van der M Linden van der R Sinden RE Waters AP Janse CJ A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle Mol Biochem Parasitol 2004, 137(1):23-33. 10.1016/ j.molbiopara.2004.04.007 15279948
14. Kaiser K Camargo N Kappe SH Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells J Exp Med 2003, 197(8):1045-1050. 2193875 12707302 10.1084/jem.20022100
15. Gentleman RC Carey VJ Bates DM Bolstad B Dettling M Dudoit S Ellis B Gautier L Ge Y Gentry J et al Bioconductor: Open software development for computational biology and bioinformatics Genome Biol 2004, 5(10):R80. 545600 15461798 10.1186/gb-2004-5-10-r80
16. Carracedo A Lorente M Egia A Blazquez C Garcia S Giroux V Malicet C Villuendas R Gironella M Gonzalez-Feria L et al The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells Cancer Cell 2006, 9(4):301-312. 10.1016/j.ccr.2006.03.005 16616335
17. Benali-Furet NL Chami M Houel L De Giorgi F Vernejoul F Lagorce D Buscail L Bartenschlager R Ichas F Rizzuto R et al Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion Oncogene 2005, 24(31):4921-4933. 10.1038/ sj.onc.1208673 15897896
18. He CH Gong P Hu B Stewart D Choi ME Choi AM Alam J Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation J Biol Chem 2001, 276(24):20858-20865. 10.1074/jbc.M101198200 11274184
19. Epiphanio S Mikolajczak SA Goncalves LA Pamplona A Portugal S Albuquerque S Goldberg M Rebelo S Anderson DG Akinc A et al Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection Cell Host Microbe 2008, 3(5):331-338. 10.1016/ j.chom.2008.04.003 18474360
20. Du K Herzig S Kulkarni RN Montminy M TRB3: A tribbles homolog that inhibits Akt/PKB activation by insulin in liver Science 2003, 300(5625):1574-1577. 10.1126/science.1079817 12791994
21. Sirvent P Mercier J Vassort G Lacampagne A Simvastatin triggers mitochondria-induced Ca2+ signaling alteration in skeletal muscle Biochem Biophys Res Commun 2005, 329(3):1067-1075. 10.1016/ j.bbrc.2005.02.070 15752763
22. Besecker B Bao S Bohacova B Papp A Sadee W Knoell DL The human zinc transporter SLC39A8 (Zip8) is critical in zinc-mediated cytoprotection in lung epithelia Am J Physiol Lung Cell Mol Physiol 2008, 294(6):L1127-1136. 10.1152/ajplung.00057.2008 18390834
23. Fouts AE Boothroyd JC Infection with Toxoplasma gondii bradyzoites has a diminished impact on host transcript levels relative to tachyzoite infection Infect Immun 2007, 75(2):634-642. 1828502 17088349 10.1128/ IAI.01228-06
24. Kim SK Fouts AE Boothroyd JC Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: Insights from a genome-wide transcriptional profiling J Immunol 2007, 178(8):5154-5165. 17404298
25. Molestina RE Sinai AP Host and parasite-derived IKK activities direct distinct temporal phases of NF-kappaB activation and target gene expression following Toxoplasma gondii infection J Cell Sci 2005, 118(Pt 24):5785-5796. 10.1242/jcs.02709 16339966
26. Shapira S Harb OS Margarit J Matrajt M Han J Hoffmann A Freedman B May MJ Roos DS Hunter CA Initiation and termination of NF-kappaB signaling by the intracellular protozoan parasite Toxoplasma gondii J Cell Sci 2005, 118(Pt 15):3501-3508. 10.1242/jcs.02428 16079291
27. Torgler R Bongfen SE Romero JC Tardivel A Thome M Corradin G Sporozoite-mediated hepatocyte wounding limits Plasmodium parasite development via MyD88-mediated NF-kappa B activation and inducible NO synthase expression J Immunol 2008, 180(6):3990-3999. 18322208
28. Lee CW Bennouna S Denkers EY Screening for Toxoplasma gondii-regulated transcriptional responses in lipopolysaccharide-activated macrophages Infect Immun 2006, 74(3):1916-1923. 1418623 16495567 10.1128/ IAI.74.3.1916-1923.2006
29. Iizuka N Oka M Yamada-Okabe H Mori N Tamesa T Okada T Takemoto N Tangoku A Hamada K Nakayama H et al Comparison of gene expression profiles between hepatitis B virus- and hepatitis C virus-infected hepatocellular carcinoma by oligonucleotide microarray data on the basis of a supervised learning method Cancer Res 2002, 62(14):3939-3944. 12124323
30. Xu XR Huang J Xu ZG Qian BZ Zhu ZD Yan Q Cai T Zhang X Xiao HS Qu J et al Insight into hepatocellular carcinogenesis at transcriptome level by comparing gene expression profiles of hepatocellular carcinoma with those of corresponding noncancerous liver Proc Natl Acad Sci USA 2001, 98(26):15089-15094. 64988 11752456 10.1073/pnas.241522398
31. Protzer U Seyfried S Quasdorff M Sass G Svorcova M Webb D Bohne F Hosel M Schirmacher P Tiegs G Antiviral activity and hepatoprotection by heme oxygenase-1 in hepatitis B virus infection Gastroenterology 2007, 133(4):1156-1165. 10.1053/j.gastro.2007.07.021 17919491
32. Shiloh MU Manzanillo P Cox JS Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection Cell Host Microbe 2008, 3(5):323-330. 10.1016/j.chom.2008.03.007 18474359
33. Mikolajczak SA Jacobs-Lorena V MacKellar DC Camargo N Kappe SH L-FABP is a critical host factor for successful malaria liver stage development Int J Parasitol 2007, 37(5):483-489. 10.1016/j.ijpara.2007.01.002 17303141
34. Franco R Schoneveld OJ Pappa A Panayiotidis MI The central role of glutathione in the pathophysiology of human diseases Arch Physiol Biochem 2007, 113(4-5):234-258. 10.1080/13813450701661198 18158646
35. Carrolo M Giordano S Cabrita-Santos L Corso S Vigario AM Silva S Leiriao P Carapau D Armas-Portela R Comoglio PM et al Hepatocyte growth factor and its receptor are required for malaria infection Nat Med 2003, 9(11):1363-1369. 10.1038/nm947 14556002
36. Leiriao P Albuquerque SS Corso S van Gemert GJ Sauerwein RW Rodriguez A Giordano S Mota MM HGF/MET signalling protects Plasmodium-infected host cells from apoptosis Cell Microbiol 2005, 7(4):603-609. 10.1111/ j.1462-5822.2004.00490.x 15760460
37. Sand van de C Horstmann S Schmidt A Sturm A Bolte S Krueger A Lutgehetmann M Pollok JM Libert C Heussler VT The liver stage of Plasmodium berghei inhibits host cell apoptosis Mol Microbiol 2005, 58(3):731-742. 10.1111/j.1365-2958.2005.04888.x 16238623
38. Leiriao P Mota MM Rodriguez A Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells J Infect Dis 2005, 191(10):1576-1581. 10.1086/429635 15838783
39. Tarun AS Peng X Dumpit RF Ogata Y Silva-Rivera H Camargo N Daly TM Bergman LW Kappe SH A combined transcriptome and proteome survey of malaria parasite liver stages Proc Natl Acad Sci USA 2008, 105(1):305-310. 2224207 18172196 10.1073/pnas.0710780104
40. Preiser PR Khan S Costa FT Jarra W Belnoue E Ogun S Holder AA Voza T Landau I Snounou G et al Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle Science 2002, 295(5553):342-345. 10.1126/science.1064938 11786645
41. Irizarry RA Hobbs B Collin F Beazer-Barclay YD Antonellis KJ Scherf U Speed TP Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4(2):249-264. 10.1093/biostatistics/4.2.249 12925520
42. Wettenhall JM Smyth GK limmaGUI: A graphical user interface for linear modeling of microarray data Bioinformatics 2004, 20(18):3705-3706. 10.1093/bioinformatics/bth449 15297296
43. Falcon S Gentleman R Using GOstats to test gene lists for GO term association Bioinformatics 2007, 23(2):257-258. 10.1093/bioinformatics/ btl567 17098774
44. Preiser PR Khan S Costa FT Jarra W Belnoue E Ogun S Holder AA Voza T Landau I Snounou G et al Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle Science 2002, 295(5553):342-345. 10.1126/science.1064938 11786645