Genome-wide analysis reveals increased levels of transcripts related with infectivity in peanut lectin non-agglutinated promastigotes of Leishmania infantum

Genomics

Volumn 93, Issue 6, 2009, Pages 551-564

  Alcolea, Pedro J ^a   Alonso, Ana ^a   Sánchez Gorostiaga, Alicia ^a   Moreno Paz, Mercedes ^b   Gómez, Manuel J ^b   Ramos, Irene ^a   Parro, Víctor ^b   Larraga, Vicente ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

Author keywords

Infectivity; Leishmania infantum; Metacyclic promastigotes; Peanut lectin agglutination; Shotgun DNA microarrays

Indexed keywords

AMINOPEPTIDASE; LECTIN; LIPOPHOSPHOGLYCAN;

ANTIGEN ANTIBODY REACTION; ARTICLE; CELL LINE; CELL STRAIN U937; DNA MICROARRAY; GENE CONTROL; GENE EXPRESSION PROFILING; GENOME ANALYSIS; GLYCATION; GLYCOPROTEIN SYNTHESIS; HUMAN; HUMAN CELL; INFECTION RATE; LEISHMANIA INFANTUM; LEISHMANIASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEANUT; PHENOTYPE; PRIORITY JOURNAL; PROMASTIGOTE; UNINDEXED SEQUENCE; UPREGULATION;

AGGLUTINATION; AMINO ACIDS; ANIMALS; CELL LINE; CYSTEINE ENDOPEPTIDASES; FATTY ACIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, PROTOZOAN; HUMANS; LEISHMANIA INFANTUM; LIFE CYCLE STAGES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEANUT AGGLUTININ; VIRULENCE;

ARACHIS HYPOGAEA; LEISHMANIA INFANTUM;

EID: 67349224641     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2009.01.007     Document Type: Article

References (82)

1. Alvar J., Canavate C., Molina R., Moreno J., and Nieto J. Canine leishmaniasis. Adv. Parasitol. 57 (2004) 1-88
2. Pasquau F., Ena J., Sanchez R., Cuadrado J.M., Amador C., Flores J., Benito C., Redondo C., Lacruz J., Abril V., and Onofre J. Leishmaniasis as an opportunistic infection in HIV-infected patients: determinants of relapse and mortality in a collaborative study of 228 episodes in a Mediterreanean region. Eur. J. Clin. Microbiol. Infect. Dis. 24 (2005) 411-418
3. Cruz I., Nieto J., Moreno J., Canavate C., Desjeux P., and Alvar J. Leishmania/HIV co-infections in the second decade. Indian J. Med. Res. 123 (2006) 357-388
4. da Silva R., and Sacks D.L. Metacyclogenesis is a major determinant of Leishmania promastigote virulence and attenuation. Infect. Immun. 55 (1987) 2802-2806
5. McConville M.J., Turco S.J., Ferguson M.A., and Sacks D.L. Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 11 (1992) 3593-3600
6. Sacks D.L., Hieny S., and Sher A. Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J. Immunol. 135 (1985) 564-569
7. Spath G.F., and Beverley S.M. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp. Parasitol. 99 (2001) 97-103
8. Almeida R., Gilmartin B.J., McCann S.H., Norrish A., Ivens A.C., Lawson D., Levick M.P., Smith D.F., Dyall S.D., Vetrie D., Freeman T.C., Coulson R.M., Sampaio I., Schneider H., and Blackwell J.M. Expression profiling of the Leishmania life cycle: cDNA arrays identify developmentally regulated genes present but not annotated in the genome. Mol. Biochem. Parasitol. 136 (2004) 87-100
9. Louassini M., Adroher F.J., Foulquie M.R., and Benitez R. Investigations on the in vitro metacyclogenesis of a visceral and a cutaneous human strain of Leishmania infantum. Acta Trop. 70 (1998) 355-368
10. Rodriguez-Gonzalez I., Marin C., Vargas F., Cordova O., Barrera M., Gutierrez-Sanchez R., Alunda J.M., and Sanchez-Moreno M. Identification and biochemical characterization of Leishmania strains isolated in Peru, Mexico, and Spain. Exp. Parasitol. 112 (2006) 44-51
11. Turco S.J., and Descoteaux A. The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46 (1992) 65-94
12. McConville M.J., Collidge T.A., Ferguson M.A., and Schneider P. The glycoinositol phospholipids of Leishmania mexicana promastigotes. Evidence for the presence of three distinct pathways of glycolipid biosynthesis. J. Biol. Chem. 268 (1993) 15595-15604
13. Beverley S.M., and Turco S.J. Lipophosphoglycan (LPG) and the identification of virulence genes in the protozoan parasite Leishmania. Trends Microbiol. 6 (1998) 35-40
14. McConville M.J., Mullin K.A., Ilgoutz S.C., and Teasdale R.D. Secretory pathway of trypanosomatid parasites. Microbiol. Mol. Biol. Rev. 66 (2002) 122-154 table of contents
15. Joshi P.B., Sacks D.L., Modi G., and McMaster W.R. Targeted gene deletion of Leishmania major genes encoding developmental stage-specific leishmanolysin (GP63). Mol. Microbiol. 27 (1998) 519-530
16. Clayton C., and Shapira M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol. 156 (2007) 93-101
17. Beverley S.M., Akopyants N.S., Goyard S., Matlib R.S., Gordon J.L., Brownstein B.H., Stormo G.D., Bukanova E.N., Hott C.T., Li F., MacMillan S., Muo J.N., Schwertman L.A., Smeds M.R., and Wang Y. Putting the Leishmania genome to work: functional genomics by transposon trapping and expression profiling. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357 (2002) 47-53
18. 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
19. Akopyants N.S., Matlib R.S., Bukanova E.N., Smeds M.R., Brownstein B.H., Stormo G.D., and Beverley S.M. 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
20. Peacock C.S., Seeger K., Harris D., Murphy L., Ruiz J.C., Quail M.A., Peters N., Adlem E., Tivey A., Aslett M., Kerhornou A., Ivens A., Fraser A., Rajandream M.A., Carver T., Norbertczak H., Chillingworth T., Hance Z., Jagels K., Moule S., Ormond D., Rutter S., Squares R., Whitehead S., Rabbinowitsch E., Arrowsmith C., White B., Thurston S., Bringaud F., Baldauf S.L., Faulconbridge A., Jeffares D., Depledge D.P., Oyola S.O., Hilley J.D., Brito L.O., Tosi L.R., Barrell B., Cruz A.K., Mottram J.C., Smith D.F., and Berriman M. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet. 39 (2007) 839-847
21. Clarke L., and Carbon J. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome. 1976. Biotechnology 24 (1992) 179-187
22. Cleveland W.S. Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 74 (1979) 829-836
23. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., and Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30 (2002) e15
24. FTP data download from GeneDB.
25. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., and Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21 (2005) 3674-3676
26. Ono Y., Sorimachi H., and Suzuki K. Structure and physiology of calpain, an enigmatic protease. Biochem. Biophys. Res. Commun. 245 (1998) 289-294
27. Sato K., and Kawashima S. Calpain function in the modulation of signal transduction molecules. Biol. Chem. 382 (2001) 743-751
28. Burgers P.M., Koonin E.V., Bruford E., Blanco L., Burtis K.C., Christman M.F., sCopeland W.C., Friedberg E.C., Hanaoka F., Hinkle D.C., Lawrence C.W., Nakanishi M., Ohmori H., Prakash L., Prakash S., Reynaud C.A., Sugino A., Todo T., Wang Z., Weill J.C., and Woodgate R. Eukaryotic DNA polymerases: proposal for a revised nomenclature. J. Biol. Chem. 276 (2001) 43487-43490
29. Sen B., Venugopal V., Chakraborty A., Datta R., Dolai S., Banerjee R., and Datta A.K. Amino acid residues of Leishmania donovani cyclophilin key to interaction with its adenosine kinase: biological implications. Biochemistry 46 (2007) 7832-7843
30. Chakraborty A., Sen B., Datta R., and Datta A.K. Isomerase-independent chaperone function of cyclophilin ensures aggregation prevention of adenosine kinase both in vitro and under in vivo conditions. Biochemistry 43 (2004) 11862-11872
31. Detke S. TOR-induced resistance to toxic adenosine analogs in Leishmania brought about by the internalization and degradation of the adenosine permease. Exp. Cell Res. 313 (2007) 1963-1978
32. Richard D., Kundig C., and Ouellette M. A new type of high affinity folic acid transporter in the protozoan parasite Leishmania and deletion of its gene in methotrexate-resistant cells. J. Biol. Chem. 277 (2002) 29460-29467
33. Vetter I.R., Arndt A., Kutay U., Gorlich D., and Wittinghofer A. Structural view of the Ran-Importin beta interaction at 2.3 A resolution. Cell 97 (1999) 635-646
34. Cavener D.R. GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J. Mol. Biol. 223 (1992) 811-814
35. Gerald N.J., Coppens I., and Dwyer D.M. Molecular characterization and expression of a novel kinesin which localizes with the kinetoplast in the human pathogen, Leishmania donovani. Cell. Motil. Cytoskeleton. 65 (2008) 269-280
36. Brennicke A., Marchfelder A., and Binder S. RNA editing. FEMS Microbiol. Rev. 23 (1999) 297-316
37. Ivens A.C., Peacock C.S., Worthey E.A., Murphy L., Aggarwal G., Berriman M., Sisk E., Rajandream M.A., Adlem E., Aert R., Anupama A., Apostolou Z., Attipoe P., Bason N., Bauser C., Beck A., Beverley S.M., Bianchettin G., Borzym K., Bothe G., Bruschi C.V., Collins M., Cadag E., Ciarloni L., Clayton C., Coulson R.M., Cronin A., Cruz A.K., Davies R.M., De Gaudenzi J., Dobson D.E., Duesterhoeft A., Fazelina G., Fosker N., Frasch A.C., Fraser A., Fuchs M., Gabel C., Goble A., Goffeau A., Harris D., Hertz-Fowler C., Hilbert H., Horn D., Huang Y., Klages S., Knights A., Kube M., Larke N., Litvin L., Lord A., Louie T., Marra M., Masuy D., Matthews K., Michaeli S., Mottram J.C., Muller-Auer S., Munden H., Nelson S., Norbertczak H., Oliver K., O'Neil S., Pentony M., Pohl T.M., Price C., Purnelle B., Quail M.A., Rabbinowitsch E., Reinhardt R., Rieger M., Rinta J., Robben J., Robertson L., Ruiz J.C., Rutter S., Saunders D., Schafer M., Schein J., Schwartz D.C., Seeger K., Seyler A., Sharp S., Shin H., Sivam D., Squares R., Squares S., Tosato V., Vogt C., Volckaert G., Wambutt R., Warren T., Wedler H., Woodward J., Zhou S., Zimmermann W., Smith D.F., Blackwell J.M., Stuart K.D., Barrell B., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442
38. Saxena A., Lahav T., Holland N., Aggarwal G., Anupama A., Huang Y., Volpin H., Myler P.J., and Zilberstein D. 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
39. 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
40. 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
41. McNicoll F., Drummelsmith J., Muller M., Madore E., Boilard N., Ouellette M., and Papadopoulou B. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 6 (2006) 3567-3581
42. Rochette A., Raymond F., Ubeda J.M., Smith M., Messier N., Boisvert S., Rigault P., Corbeil J., Ouellette M., and Papadopoulou B. 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
43. Bhattacharya S., Bakre A., and Bhattacharya A. Mobile genetic elements in protozoan parasites. J. Genet. 81 (2002) 73-86
44. Wickstead B., Ersfeld K., and Gull K. Repetitive elements in genomes of parasitic protozoa. Microbiol. Mol. Biol. Rev. 67 (2003) 360-375 table of contents
45. Smith D.F., Peacock C.S., and Cruz A.K. Comparative genomics: from genotype to disease phenotype in the leishmaniases. Int. J. Parasitol. 37 (2007) 1173-1186
46. Hermoso T., and Jaffe C.L. Phosphorylation of proteins in virulent promastigotes from Leishmania major. Biol. Res. 26 (1993) 267-271
47. Schlein Y., and Jacobson R.L. Haemoglobin inhibits the development of infective promastigotes and chitinase secretion in Leishmania major cultures. Parasitology 109 Pt 1 (1994) 23-28
48. Howard M.K., Sayers G., and Miles M.A. Leishmania donovani metacyclic promastigotes: transformation in vitro, lectin agglutination, complement resistance, and infectivity. Exp. Parasitol. 64 (1987) 147-156
49. Almeida M.C., Cuba C.A., de Sa C.M., Pharoah M.M., Howard K.M., and Miles M.A. Metacyclogenesis of Leishmania (Viannia) braziliensis in vitro: evidence that lentil lectin is a marker of complement resistance and enhanced infectivity. Trans. R. Soc. Trop. Med. Hyg. 87 (1993) 325-329
50. 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
51. Garami A., Mehlert A., and Ilg T. Glycosylation defects and virulence phenotypes of Leishmania mexicana phosphomannomutase and dolicholphosphate-mannose synthase gene deletion mutants. Mol. Cell. Biol. 21 (2001) 8168-8183
52. Sacks D.L., and Perkins P.V. Identification of an infective stage of Leishmania promastigotes. Science 223 (1984) 1417-1419
53. Kuru T., Jirata D., Genetu A., Barr S., Mengistu Y., Assefa A., and Gedamu L. Leishmania aethiopica: identification and characterization of cathepsin-L-like cysteine protease genes. Exp. Parasitol. 115 (2007) 283-290
54. Mottram J.C., Coombs G.H., and Alexander J. Cysteine peptidases as virulence factors of Leishmania. Curr. Opin. Microbiol. 7 (2004) 375-381
55. Cazzulo Franke M.C., Vernal J., Cazzulo J.J., and Nowicki C. The NAD-linked aromatic alpha-hydroxy acid dehydrogenase from Trypanosoma cruzi. A new member of the cytosolic malate dehydrogenases group without malate dehydrogenase activity. Eur. J. Biochem. 266 (1999) 903-910
56. Nowicki C., and Cazzulo J.J. Aromatic amino acid catabolism in trypanosomatids. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 151 (2007) 381-390
57. Montemartini M., Santome J.A., Cazzulo J.J., and Nowicki C. Purification and partial structural and kinetic characterization of tyrosine aminotransferase from epimastigotes of Trypanosoma cruzi. Biochem. J. 292 Pt 3 (1993) 901-906
58. Leelayoova S., Marbury D., Rainey P.M., Mackenzie N.E., and Hall J.E. In vitro tryptophan catabolism by Leishmania donovani donovani promastigotes. J. Protozool. 39 (1992) 350-358
59. Berger B.J., Dai W.W., Wang H., Stark R.E., and Cerami A. Aromatic amino acid transamination and methionine recycling in trypanosomatids. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 4126-4130
60. Sacks D., and Kamhawi S. Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu. Rev. Microbiol. 55 (2001) 453-483
61. Hubscher U., Maga G., and Spadari S. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 71 (2002) 133-163
62. Mukhopadhyay N.K., Saha A.K., Lovelace J.K., Da Silva R., Sacks D.L., and Glew R.H. Comparison of the protein kinase and acid phosphatase activities of five species of Leishmania. J. Protozool. 35 (1988) 601-607
63. Genestra M., Cysne-Finkelstein L., and Leon L. Protein kinase A activity is associated with metacyclogenesis in Leishmania amazonensis. Cell Biochem. Funct. 22 (2004) 315-320
64. Dreyfus M., and Regnier P. The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell 111 (2002) 611-613
65. Koslowsky D.J., Riley G.R., Feagin J.E., and Stuart K. Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life cycle stages of Trypanosoma brucei. Mol. Cell. Biol. 12 (1992) 2043-2049
66. Dumas C., Chow C., Muller M., and Papadopoulou B. A novel class of developmentally regulated noncoding RNAs in Leishmania. Eukaryot. Cell 5 (2006) 2033-2046
67. Sambrook J., Fritsch E.F., and Maniatis T. Purification of nucleic acids. Molecular Cloning (1989) E.3
68. Weis J.H., and Quertermous T. Preparation of insert DNA from genomic DNA. Curr. Protocols Mol. Biol. 5.3 (1987) 1-8
69. Parro V., and Moreno-Paz M. Gene function analysis in environmental isolates: the nif regulon of the strict iron oxidizing bacterium Leptospirillum ferrooxidans. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7883-7888
70. Hedge P., Qi R., Abernathy K., Dharap G.C.S., Gaspard R., Hughes J.E., Snesrud E., Lee N., and Quackenbush J. A concise guide to cDNA microarray analysis. BioTechniques 29 (2000) 548-562
71. Hanke T., Ramiro M.J., Trigueros S., Roca J., and Larraga V. Cloning, functional analysis and post-transcriptional regulation of a type II DNA topoisomerase from Leishmania infantum. A new potential target for anti-parasite drugs. Nucleic Acids Res. 31 (2003) 4917-4928
72. Taladriz S., Hanke T., Ramiro M.J., Garcia-Diaz M., Garcia De Lacoba M., Blanco L., and Larraga V. Nuclear DNA polymerase beta from Leishmania infantum. Cloning, molecular analysis and developmental regulation. Nucleic Acids Res. 29 (2001) 3822-3834
73. Gonzalez-Aseguinolaza G., Taladriz S., Marquet A., and Larraga V. Molecular cloning, cell localization and binding affinity to DNA replication proteins of the p36/LACK protective antigen from Leishmania infantum. Eur. J. Biochem. 259 (1999) 909-916
74. Stein L.D., Mungall C., Shu S., Caudy M., Mangone M., Day A., Nickerson E., Stajich J.E., Harris T.W., Arva A., and Lewis S. The generic genome browser: a building block for a model organism system database. Genome Res. 12 (2002) 1599-1610
75. Sanger F., Nicklen S., and Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74 (1977) 5463-5467
76. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
77. Delcher A.L., Bratke K.A., Powers E.C., and Salzberg S.L. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23 (2007) 673-679
78. Ewing B., Hillier L., Wendl M.C., and Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8 (1998) 175-185
79. Ewing B., and Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8 (1998) 186-194
80. Gordon D., Abajian C., and Green P. Consed: a graphical tool for sequence finishing. Genome Res. 8 (1998) 195-202
81. P. Green, Laboratory of Phil Green, 1994.
82. Bookout A.L., Cummins C.L., Kramer M.F., Pesola J.M., and Mangelsdorf D.J. High-throughput real-time quantitative reverse transcription PCR. Curr. Protocols Mol. Biol. 15.8 (2006) 1-28