Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum

Molecular and Biochemical Parasitology

Volumn 165, Issue 1, 2009, Pages 32-47

  Rochette, Annie ^a,b   Raymond, Frédéric ^a,b   Corbeil, Jacques ^a,b   Ouellette, Marc ^a,b   Papadopoulou, Barbara ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Axenic amastigotes; DNA microarrays; Intracellular amastigotes; Leishmania infantum; MRNA abundance

Indexed keywords

MESSENGER RNA; PROTEIN KINASE; RNA BINDING PROTEIN;

AMASTIGOTE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA MICROARRAY; FATTY ACID METABOLISM; GENE; GENOME ANALYSIS; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LEISHMANIA INFANTUM; MACROPHAGE; MEMBRANE VESICLE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; UPREGULATION;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, PROTOZOAN; LEISHMANIA INFANTUM; LIFE CYCLE STAGES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; UP-REGULATION;

LEISHMANIA INFANTUM; VERTEBRATA;

EID: 60649102005     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2008.12.012     Document Type: Article

References (85)

1. Chappuis F., Sundar S., Hailu A., et al. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control?. Nat Rev Microbiol 5 (2007) 873-882
2. Murray H.W., Berman J.D., Davies C.R., and Saravia N.G. Advances in leishmaniasis. Lancet 366 (2005) 1561-1577
3. Bates P.A., and Rogers M.E. New insights into the developmental biology and transmission mechanisms of Leishmania. Curr Mol Med 4 (2004) 601-609
4. MacFarlane J., Blaxter M.L., Bishop R.P., Miles M.A., and Kelly J.M. Identification and characterisation of a Leishmania donovani antigen belonging to the 70-kDa heat-shock protein family. Eur J Biochem 190 (1990) 377-384
5. Glaser T.A., Moody S.F., Handman E., Bacic A., and Spithill T.W. An antigenically distinct lipophosphoglycan on amastigotes of Leishmania major. Mol Biochem Parasitol 45 (1991) 337-344
6. Turco S.J., and Descoteaux A. The lipophosphoglycan of Leishmania parasites. Annu Rev Microbiol 46 (1992) 65-94
7. McConville M.J., and Blackwell J.M. Developmental changes in the glycosylated phosphatidylinositols of Leishmania donovani. Characterization of the promastigote and amastigote glycolipids. J Biol Chem 266 (1991) 15170-15179
8. McConville M.J., and Handman E. The molecular basis of Leishmania pathogenesis. Int J Parasitol 37 (2007) 1047-1051
9. Charest H., and Matlashewski G. Developmental gene expression in Leishmania donovani: differential cloning and analysis of an amastigote-stage-specific gene. Mol Cell Biol 14 (1994) 2975-2984
10. Argaman M., Aly R., and Shapira M. Expression of heat shock protein 83 in Leishmania is regulated post-transcriptionally. Mol Biochem Parasitol 64 (1994) 95-110
11. Hubel A., Krobitsch S., Horauf A., and Clos J. Leishmania major Hsp100 is required chiefly in the mammalian stage of the parasite. Mol Cell Biol 17 (1997) 5987-5995
12. Burchmore R.J., and Landfear S.M. Differential regulation of multiple glucose transporter genes in Leishmania mexicana. J Biol Chem 273 (1998) 29118-29126
13. Rochette A., McNicoll F., Girard J., et al. Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. Mol Biochem Parasitol 140 (2005) 205-220
14. Handman E., Osborn A.H., Symons F., van Driel R., and Cappai R. The Leishmania promastigote surface antigen 2 complex is differentially expressed during the parasite life cycle. Mol Biochem Parasitol 74 (1995) 189-200
15. Barr S.D., and Gedamu L. Cloning and characterization of three differentially expressed peroxidoxin genes from Leishmania chagasi. Evidence for an enzymatic detoxification of hydroxyl radicals. J Biol Chem 276 (2001) 34279-34287
16. Moore L.L., Santrich C., and LeBowitz J.H. Stage-specific expression of the Leishmania mexicana paraflagellar rod protein PFR-2. Mol Biochem Parasitol 80 (1996) 125-135
17. Holzer T.R., McMaster W.R., and Forney J.D. Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol Biochem Parasitol 146 (2006) 198-218
18. Leifso K., Cohen-Freue G., Dogra N., Murray A., and McMaster W.R. Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: the Leishmania genome is constitutively expressed. Mol Biochem Parasitol 152 (2007) 35-46
19. Rochette A., Raymond F., Ubeda J.M., et al. Genome-wide gene expression profiling analysis of Leishmania major and Leishmania infantum developmental stages reveals substantial differences between the two species. BMC Genomics 9 (2008) 255
20. Bates P.A. Complete developmental cycle of Leishmania mexicana in axenic culture. Parasitology 108 Pt 1 (1994) 1-9
21. Saar Y., Ransford A., Waldman E., et al. Characterization of developmentally regulated activities in axenic amastigotes of Leishmania donovani. Mol Biochem Parasitol 95 (1998) 9-20
22. Gupta N., Goyal N., and Rastogi A.K. In vitro cultivation and characterization of axenic amastigotes of Leishmania. Trends Parasitol 17 (2001) 150-153
23. Somanna A., Mundodi V., and Gedamu L. In vitro cultivation and characterization of Leishmania chagasi amastigote-like forms. Acta Trop 83 (2002) 37-42
24. Debrabant A., Joshi M.B., Pimenta P.F., and Dwyer D.M. Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int J Parasitol 34 (2004) 205-217
25. Barak E., Amin-Spector S., Gerliak E., Goyard S., Holland N., and Zilberstein D. Differentiation of Leishmania donovani in host-free system: analysis of signal perception and response. Mol Biochem Parasitol 141 (2005) 99-108
26. Wu Y., El Fakhry Y., Sereno D., Tamar S., and Papadopoulou B. A new developmentally regulated gene family in Leishmania amastigotes encoding a homolog of amastin surface proteins. Mol Biochem Parasitol 110 (2000) 345-357
27. Alves C.R., Corte-Real S., Bourguignon S.C., Chaves C.S., and Saraiva E.M. Leishmania amazonensis: early proteinase activities during promastigote-amastigote differentiation in vitro. Exp Parasitol 109 (2005) 38-48
28. Saxena A., Lahav T., Holland N., et al. Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Mol Biochem Parasitol 152 (2007) 53-65
29. Srividya G., Duncan R., Sharma P., Raju B.V., Nakhasi H.L., and Salotra P. Transcriptome analysis during the process of in vitro differentiation of Leishmania donovani using genomic microarrays. Parasitology 134 (2007) 1527-1539
30. Goyard S., Segawa H., Gordon J., et al. An in vitro system for developmental and genetic studies of Leishmania donovani phosphoglycans. Mol Biochem Parasitol 130 (2003) 31-42
31. Bates P.A., Robertson C.D., Tetley L., and Coombs G.H. Axenic cultivation and characterization of Leishmania mexicana amastigote-like forms. Parasitology 105 Pt 2 (1992) 193-202
32. Sereno D., and Lemesre J.L. Axenically cultured amastigote forms as an in vitro model for investigation of antileishmanial agents. Antimicrob Agents Chemother 41 (1997) 972-976
33. Teixeira M.C., de Jesus Santos R., Sampaio R.B., Pontes-de-Carvalho L., and dos-Santos W.L. A simple and reproducible method to obtain large numbers of axenic amastigotes of different Leishmania species. Parasitol Res 88 (2002) 963-968
34. Hodgkinson V.H., Soong L., Duboise S.M., and McMahon-Pratt D. Leishmania amazonensis: cultivation and characterization of axenic amastigote-like organisms. Exp Parasitol 83 (1996) 94-105
35. Walker J., Vasquez J.J., Gomez M.A., et al. Identification of developmentally regulated proteins in Leishmania panamensis by proteome profiling of promastigotes and axenic amastigotes. Mol Biochem Parasitol 147 (2006) 64-73
36. McNicoll F., Drummelsmith J., Muller M., et al. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 6 (2006) 3567-3581
37. Rosenzweig D., Smith D., Opperdoes F., Stern S., Olafson R.W., and Zilberstein D. Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB J 22 (2008) 590-602
38. Saxena A., Worthey E.A., Yan S., Leland A., Stuart K.D., and Myler P.J. Evaluation of differential gene expression in Leishmania major Friedlin procyclics and metacyclics using DNA microarray analysis. Mol Biochem Parasitol 129 (2003) 103-114
39. Akopyants N.S., Matlib R.S., Bukanova E.N., et al. Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Mol Biochem Parasitol 136 (2004) 71-86
40. Sereno D., Cavaleyra M., Zemzoumi K., Maquaire S., Ouaissi A., and Lemesre J.L. Axenically grown amastigotes of Leishmania infantum used as an in vitro model to investigate the pentavalent antimony mode of action. Antimicrob Agents Chemother 42 (1998) 3097-3102
41. Sereno D., Holzmuller P., Mangot I., Cuny G., Ouaissi A., and Lemesre J.L. Antimonial-mediated DNA fragmentation in Leishmania infantum amastigotes. Antimicrob Agents Chemother 45 (2001) 2064-2069
42. Ubeda J.M., Legare D., Raymond F., et al. Modulation of gene expression in drug resistant Leishmania is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol 9 (2008) R115
43. Smyth G.K., and Speed T. Normalization of cDNA microarray data. Methods 31 (2003) 265-273
44. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3 (2004) Article3
45. Smyth G.K., Michaud J., and Scott H.S. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21 (2005) 2067-2075
46. Ritchie M.E., Silver J., Oshlack A., et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 23 (2007) 2700-2707
47. Yang Y., Hoh J., Broger C., et al. Statistical methods for analyzing microarray feature data with replications. J Comput Biol 10 (2003) 157-169
48. Harris M.A., Clark J., Ireland A., et al. The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32 (2004) D258-D261
49. Voth B.R., Kelly B.L., Joshi P.B., Ivens A.C., and McMaster W.R. Differentially expressed Leishmania major gp63 genes encode cell surface leishmanolysin with distinct signals for glycosylphosphatidylinositol attachment. Mol Biochem Parasitol 93 (1998) 31-41
50. Knuepfer E., Stierhof Y.D., McKean P.G., and Smith D.F. Characterization of a differentially expressed protein that shows an unusual localization to intracellular membranes in Leishmania major. Biochem J 356 (2001) 335-344
51. McKean P.G., Denny P.W., Knuepfer E., Keen J.K., and Smith D.F. Phenotypic changes associated with deletion and overexpression of a stage-regulated gene family in Leishmania. Cell Microbiol 3 (2001) 511-523
52. Dobson D.E., Scholtes L.D., Myler P.J., Turco S.J., and Beverley S.M. Genomic organization and expression of the expanded SCG/L/R gene family of Leishmania major: internal clusters and telomeric localization of SCGs mediating species-specific LPG modifications. Mol Biochem Parasitol 146 (2006) 231-241
53. Castro H., Budde H., Flohe L., et al. Specificity and kinetics of a mitochondrial peroxiredoxin of Leishmania infantum. Free Radic Biol Med 33 (2002) 1563-1574
54. Oza S.L., Shaw M.P., Wyllie S., and Fairlamb A.H. Trypanothione biosynthesis in Leishmania major. Mol Biochem Parasitol 139 (2005) 107-116
55. Blanc V., Alfonzo J.D., Aphasizhev R., and Simpson L. The mitochondrial RNA ligase from Leishmania tarentolae can join RNA molecules bridged by a complementary RNA. J Biol Chem 274 (1999) 24289-24296
56. Gao G., and Simpson L. Is the Trypanosoma brucei REL1 RNA ligase specific for U-deletion RNA editing, and is the REL2 RNA ligase specific for U-insertion editing?. J Biol Chem 278 (2003) 27570-27574
57. Zilberstein D., and Shapira M. The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48 (1994) 449-470
58. Sarkar D., and Bhaduri A. Temperature-induced rapid increase in cytoplasmic free Ca2+ in pathogenic Leishmania donovani promastigotes. FEBS Lett 375 (1995) 83-86
59. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 74 (2005) 739-789
60. Kramer S., Queiroz R., Ellis L., et al. Heat shock causes a decrease in polysomes and the appearance of stress granules in trypanosomes independently of eIF2{alpha} phosphorylation at Thr169. J Cell Sci (2008)
61. Cotter P.D., and Hill C. Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67 (2003) 429-453 (table of contents)
62. Konno N., Ishii M., Nagai A., et al. Mechanism of Candida albicans transformation in response to changes of pH. Biol Pharm Bull 29 (2006) 923-926
63. Charest H., Zhang W.W., and Matlashewski G. The developmental expression of Leishmania donovani A2 amastigote-specific genes is post-transcriptionally mediated and involves elements located in the 3′-untranslated region. J Biol Chem 271 (1996) 17081-17090
64. McNicoll F., Muller M., Cloutier S., et al. Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J Biol Chem 280 (2005) 35238-35246
65. Joshi M., Dwyer D.M., and Nakhasi H.L. Cloning and characterization of differentially expressed genes from in vitro-grown 'amastigotes' of Leishmania donovani. Mol Biochem Parasitol 58 (1993) 345-354
66. Rainey P.M., Spithill T.W., McMahon-Pratt D., and Pan A.A. Biochemical and molecular characterization of Leishmania pifanoi amastigotes in continuous axenic culture. Mol Biochem Parasitol 49 (1991) 111-118
67. Olivier M., Gregory D.J., and Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 18 (2005) 293-305
68. Spath G.F., Garraway L.A., Turco S.J., and Beverley S.M. The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci USA 100 (2003) 9536-9541
69. Naderer T., and McConville M.J. The Leishmania-macrophage interaction: a metabolic perspective. Cell Microbiol 10 (2008) 301-308
70. Haile S., and Papadopoulou B. Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr Opin Microbiol 10 (2007) 569-577
71. Ilg T. Generation of myo-inositol-auxotrophic Leishmania mexicana mutants by targeted replacement of the myo-inositol-1-phosphate synthase gene. Mol Biochem Parasitol 120 (2002) 151-156
72. Lee S.H., Stephens J.L., Paul K.S., and Englund P.T. Fatty acid synthesis by elongases in trypanosomes. Cell 126 (2006) 691-699
73. Lee S.H., Stephens J.L., and Englund P.T. A fatty-acid synthesis mechanism specialized for parasitism. Nat Rev Microbiol 5 (2007) 287-297
74. Florin-Christensen M., Florin-Christensen J., de Isola E.D., et al. Temperature acclimation of Trypanosoma cruzi epimastigote and metacyclic trypomastigote lipids. Mol Biochem Parasitol 88 (1997) 25-33
75. Naderer T., Ellis M.A., Sernee M.F., et al. Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 103 (2006) 5502-5507
76. Opperdoes F.R., and Coombs G.H. Metabolism of Leishmania: proven and predicted. Trends Parasitol 23 (2007) 149-158
77. Ivens A.C., Peacock C.S., Worthey E.A., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442
78. Fukuda R., McNew J.A., Weber T., et al. Functional architecture of an intracellular membrane t-SNARE. Nature 407 (2000) 198-202
79. Coppolino M.G., Kong C., Mohtashami M., et al. Requirement for N-ethylmaleimide-sensitive factor activity at different stages of bacterial invasion and phagocytosis. J Biol Chem 276 (2001) 4772-4780
80. Duclos S., Diez R., Garin J., et al. Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J Cell Sci 113 Pt 19 (2000) 3531-3541
81. Besteiro S., Coombs G.H., and Mottram J.C. The SNARE protein family of Leishmania major. BMC Genomics 7 (2006) 250
82. Besteiro S., Tonn D., Tetley L., Coombs G.H., and Mottram J.C. The AP3 adaptor is involved in the transport of membrane proteins to acidocalcisomes of Leishmania. J Cell Sci 121 (2008) 561-570
83. Huynh C., and Andrews N.W. Iron acquisition within host cells and the pathogenicity of Leishmania. Cell Microbiol 10 (2008) 293-300
84. Marin-Villa M., Vargas-Inchaustegui D.A., Chaves S.P., et al. The C-terminal extension of Leishmania pifanoi amastigote-specific cysteine proteinase Lpcys2: A putative function in macrophage infection. Mol Biochem Parasitol 162 (2008) 52-59
85. Paape D., Lippuner C., Schmid M., et al. Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Mol Cell Proteomics 7 (2008) 1688-1701