Identification of proteins interacting with HSP70 mRNAs in Leishmania Braziliensis

Journal of Proteomics

Volumn 94, Issue , 2013, Pages 124-137

  Ramirez C A ^a,b   Dea Ayuela, M A ^c,d   Gutierrez Blazquez M D ^e   Bolas Fernandez F ^d   Requena, J M ^b   Puerta, C J ^a  

^a PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

HSP70 protein; HSP70 UTRs; Leishmania braziliensis; Mass spectrometry; MRNA expression regulation; Pull down

Indexed keywords

HEAT SHOCK PROTEIN 70; MESSENGER RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; LEISHMANIA BRAZILIENSIS; MASS SPECTROMETRY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEOMICS; RNA METABOLISM; RNA TRANSLATION; RNA TRANSPORT; TWO DIMENSIONAL ELECTROPHORESIS;

HSP70 PROTEIN; HSP70 UTRS; LEISHMANIA BRAZILIENSIS; MASS SPECTROMETRY; MRNA EXPRESSION REGULATION; PULL-DOWN;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; LEISHMANIA BRAZILIENSIS; PROTOZOAN PROTEINS; RNA, PROTOZOAN;

EID: 84885221255     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.09.008     Document Type: Article

References (76)

1. Murray H.W., Berman J.D., Davies C.R., Saravia N.G. Advances in Leishmaniasis. Lancet 2005, 366:1561-1577.
2. Alvar J., Velez I.D., Bern C., Herrero M., Desjeux P., Cano J., et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 2012, 7:e35671.
3. Oddone R., Schweynoch C., Schonian G., de Sousa Cdos S., Cupolillo E., Espinosa D., et al. Development of a multilocus microsatellite typing approach for discriminating strains of Leishmania (Viannia) species. J Clin Microbiol 2009, 47:2818-2825.
4. Shapira M., McEwen J.G., Jaffe C.L. Temperature effects on molecular processes which lead to stage differentiation in Leishmania. EMBO J 1988, 7:2895-2901.
5. Maresca B., Kobayashi G.S. Hsp70 in parasites: as an inducible protective protein and as an antigen. Experientia 1994, 50:1067-1074.
6. Quijada L., Soto M., Alonso C., Requena J.M. Analysis of post-transcriptional regulation operating on transcription products of the tandemly linked Leishmania infantum hsp70 genes. J Biol Chem 1997, 272:4493-4499.
7. Krobitsch S., Clos J. A novel role for 100 kD heat shock proteins in the parasite Leishmania donovani. Cell Stress Chaperones 1999, 4:191-198.
8. Zilka A., Garlapati S., Dahan E., Yaolsky V., Shapira M. Developmental regulation of heat shock protein 83 in Leishmania. 3' processing and mRNA stability control transcript abundance, and translation id directed by a determinant in the 3'-untranslated region. J Biol Chem 2001, 276:47922-47929.
9. Bente M., Harder S., Wiesgigl M., Heukeshoven J., Gelhaus C., Krause E., et al. Developmentally induced changes of the proteome in the protozoan parasite Leishmania donovani. Proteomics 2003, 3:1811-1829.
10. Asea A. Initiation of the immune response by extracellular Hsp72: chaperokine activity of Hsp72. Curr Immunol Rev 2006, 2:209-215.
11. Requena J.M. The stressful life of pathogenic Leishmania species. Stress response in microbiology 2012, 323-346. Caister Academic Press, Norfolk, UK. J.M. Requena (Ed.).
12. Raina P., Kaur S. Knockdown of LdMC1 and Hsp70 by antisense oligonucleotides causes cell-cycle defects and programmed cell death in Leishmania donovani. Mol Cell Biochem 2012, 359:135-149.
13. Folgueira C., Carrion J., Moreno J., Saugar J.M., Canavate C., Requena J.M. Effects of the disruption of the HSP70-II gene on the growth, morphology, and virulence of Leishmania infantum promastigotes. Int Microbiol 2008, 11:81-89.
14. Biyani N., Singh A.K., Mandal S., Chawla B., Madhubala R. Differential expression of proteins in antimony-susceptible and -resistant isolates of Leishmania donovani. Mol Biochem Parasitol 2011, 179:91-99.
15. Brochu C., Haimeur A., Ouellette M. The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite Leishmania. Cell Stress Chaperones 2004, 9:294-303.
16. Drummelsmith J., Girard I., Trudel N., Ouellette M. Differential protein expression analysis of Leishmania major reveals novel roles for methionine adenosyltransferase and S-adenosylmethionine in methotrexate resistance. J Biol Chem 2004, 279:33273-33280.
17. Folgueira C., Quijada L., Soto M., Abanades D.R., Alonso C., Requena J.M. The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3'-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. J Biol Chem 2005, 280:35172-35183.
18. Folgueira C., Canavate C., Chicharro C., Requena J.M. Genomic organization and expression of the HSP70 locus in new and old world Leishmania species. Parasitology 2007, 134:369-377.
19. Ramirez C.A., Requena J.M., Puerta C.J. Identification of the HSP70-II gene in Leishmania braziliensis HSP70 locus: genomic organization and UTRs characterization. Parasite Vectors 2011, 4:166.
20. Requena J.M. Lights and shadows on gene organization and regulation of gene expression in Leishmania. Front Biosci 2011, 16:2069-2085.
21. Clayton C., Shapira M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 2007, 156:93-101.
22. Charest H., Zhang W.W., 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 1996, 271:17081-17090.
23. Mishra K.K., Holzer T.R., Moore L.L., LeBowitz J.H. A negative regulatory element controls mRNA abundance of the Leishmania mexicana Paraflagellar rod gene PFR2. Eukaryot Cell 2003, 2:1009-1017.
24. Larreta R., Soto M., Quijada L., Folgueira C., Abanades D.R., Alonso C., et al. The expression of HSP83 genes in Leishmania infantum is affected by temperature and by stage-differentiation and is regulated at the levels of mRNA stability and translation. BMC Mol Biol 2004, 5:3.
25. Purdy J.E., Donelson J.E., Wilson M.E. Leishmania chagasi: the alpha-tubulin intercoding region results in constant levels of mRNA abundance despite protein synthesis inhibition and growth state. Exp Parasitol 2005, 110:102-107.
26. Zick A., Onn I., Bezalel R., Margalit H., Shlomai J. Assigning functions to genes: identification of S-phase expressed genes in Leishmania major based on post-transcriptional control elements. Nucleic Acids Res 2005, 33:4235-4242.
27. Holzer T.R., Mishra K.K., LeBowitz J.H., Forney J.D. Coordinate regulation of a family of promastigote-enriched mRNAs by the 3'UTR PRE element in Leishmania mexicana. Mol Biochem Parasitol 2008, 157:54-64.
28. Ramírez C.A., Requena J.M., Puerta C.J. Alpha tubulin genes from Leishmania braziliensis: genomic organization, gene structure and insights on their expression. BMC Genomics 2013, 14:454.
29. Pacheco A., Reigadas S., Martinez-Salas E. Riboproteomic analysis of polypeptides interacting with the internal ribosome-entry site element of foot-and-mouth disease viral RNA. Proteomics 2008, 8:4782-4790.
30. Dea-Ayuela M.A., Ordonez-Gutierrez L., Bolas-Fernandez F. Changes in the proteome and infectivity of Leishmania infantum induced by in vitro exposure to a nitric oxide donor. Int J Med Microbiol 2009, 299:221-232.
31. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K.F., Itoh M., Kawashima S., et al. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 2006, 34:D354-D357.
32. Mi H., Dong Q., Muruganujan A., Gaudet P., Lewis S., Thomas P.D. PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 2010, 38:D204-D210.
33. Tsvetanova N.G., Klass D.M., Salzman J., Brown P.O. Proteome-wide search reveals unexpected RNA-binding proteins in Saccharomyces cerevisiae. PLoS One 2010, 5(9):e12671.
34. Clayton C.E. Life without transcriptional control? From fly to man and back again. EMBO J 2002, 21:1881-1888.
35. Wilkie G.S., Dickson K.S., Gray N.K. Regulation of mRNA translation by 5'- and 3'-UTR-binding factors. Trends Biochem Sci 2003, 28:182-188.
36. David M., Gabdank I., Ben-David M., Zilka A., Orr I., Barash D., et al. Preferential translation of Hsp83 in Leishmania requires a thermosensitive polypyrimidine-rich element in the 3' UTR and involves scanning of the 5' UTR. RNA 2010, 16:364-374.
37. Kramer S., Carrington M. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol 2011, 27:23-30.
38. Jackson R.J., Hellen C.U., Pestova T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010, 11:113-127.
39. Ahmed R., Duncan R.F. Translational regulation of Hsp90 mRNA. AUG-proximal 5'-untranslated region elements essential for preferential heat shock translation. J Biol Chem 2004, 279:49919-49930.
40. Rubtsova M.P., Sizova D.V., Dmitriev S.E., Ivanov D.S., Prassolov V.S., Shatsky I.N. Distinctive properties of the 5'-untranslated region of human hsp70 mRNA. J Biol Chem 2003, 278:22350-22356.
41. Mateyak M.K., Kinzy T.G. eEF1A: Thinking outside the ribosome. J Biol Chem 2010, 285:21209-21213.
42. Mittal N., Subramanian G., Butikofer P., Madhubala R. Unique posttranslational modifications in eukaryotic translation factors and their roles in protozoan parasite viability and pathogenesis. Mol Biochem Parasitol 2013, 187:21-31.
43. Justice M.C., Hsu M.J., Tse B., Ku T., Balkovec J., Schmatz D., et al. Elongation factor 2 as a novel target for selective inhibition of fungal protein synthesis. J Biol Chem 1998, 273:3148-3151.
44. Noble C.G., Song H. Structural studies of elongation and release factors. Cell Mol Life Sci 2008, 65:1335-1346.
45. Gingras A.C., Raught B., Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 1999, 68:913-963.
46. Dhalia R., Reis C.R., Freire E.R., Rocha P.O., Katz R., Muniz J.R., et al. Translation initiation in Leishmania major: characterisation of multiple eIF4F subunit homologues. Mol Biochem Parasitol 2005, 140:23-41.
47. Barhoumi M., Tanner N.K., Banroques J., Linder P., Guizani I. Leishmania infantum LeIF protein is an ATP-dependent RNA helicase and an eIF4A-like factor that inhibits translation in yeast. FEBS J 2006, 273:5086-5100.
48. Singh C.R., Watanabe R., Zhou D., Jennings M.D., Fukao A., Lee B., et al. Mechanisms of translational regulation by a human eIF5-mimic protein. Nucleic Acids Res 2011, 39:8314-8328.
49. Hinnebusch A.G. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem Sci 2006, 31:553-562.
50. Mayeur G.L., Fraser C.S., Peiretti F., Block K.L., Hershey J.W. Characterization of eIF3k: a newly discovered subunit of mammalian translation initiation factor elF3. Eur J Biochem 2003, 270:4133-4139.
51. Wei Z., Zhang P., Zhou Z., Cheng Z., Wan M., Gong W. Crystal structure of human eIF3k, the first structure of eIF3 subunits. J Biol Chem 2004, 279:34983-34990.
52. da Costa Lima T.D., Moura D.M., Reis C.R., Vasconcelos J.R., Ellis L., Carrington M., et al. Functional characterization of three Leishmania poly(a) binding protein homologues with distinct binding properties to RNA and protein partners. Eukaryot Cell 2010, 9:1484-1494.
53. Mittra B., Ray D.S. Presence of a poly(A) binding protein and two proteins with cell cycle-dependent phosphorylation in Crithidia fasciculata mRNA cycling sequence binding protein II. Eukaryot Cell 2004, 3:1185-1197.
54. Yang Q., Jankowsky E. ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 2005, 44:13591-13601.
55. Beckham C., Hilliker A., Cziko A.M., Noueiry A., Ramaswami M., Parker R. The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol Biol Cell 2008, 19:984-993.
56. Hilliker A., Gao Z., Jankowsky E., Parker R. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol Cell 2011, 43:962-972.
57. Sbicego S., Alfonzo J.D., Estevez A.M., Rubio M.A., Kang X., Turck C.W., et al. RBP38, a novel RNA-binding protein from trypanosomatid mitochondria, modulates RNA stability. Eukaryot Cell 2003, 2:560-568.
58. Neto J.L., Lira C.B., Giardini M.A., Khater L., Perez A.M., Peroni L.A., et al. Leishmania replication protein A-1 binds in vivo single-stranded telomeric DNA. Biochem Biophys Res Commun 2007, 358:417-423.
59. Kim S., Coulombe P.A. Emerging role for the cytoskeleton as an organizer and regulator of translation. Nat Rev Mol Cell Biol 2010, 11:75-81.
60. Scherrer T., Mittal N., Janga S.C., Gerber A.P. A screen for RNA-binding proteins in yeast indicates dual functions for many enzymes. PLoS One 2010, 5:e15499.
61. Cieśla J. Metabolic enzymes that bind RNA: yet another level of cellular regulatory network?. Acta Biochim Pol 2006, 53:11-32.
62. Hentze M.W., Preiss T. The REM phase of gene regulation. Trends Biochem Sci 2010, 35:423-426.
63. Collingridge P.W., Brown R.W., Ginger M.L. Moonlighting enzymes in parasitic protozoa. Parasitology 2010, 137:1467-1475.
64. Janssens V., Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 2001, 353:417-439.
65. Ding X.Z., Tsokos G.C., Kiang J.G. Overexpression of HSP-70 inhibits the phosphorylation of HSF1 by activating protein phosphatase and inhibiting protein kinase C activity. FASEB J 1998, 12:451-459.
66. Pais S.M., Tellez-Inon M.T., Capiati D.A. Serine/threonine protein phosphatases type 2A and their roles in stress signaling. Plant Signal Behav 2009, 4:1013-1015.
67. Gonzalez J., Cornejo A., Santos M.R., Cordero E.M., Gutierrez B., Porcile P., et al. A novel protein phosphatase 2A (PP2A) is involved in the transformation of human protozoan parasite Trypanosoma cruzi. Biochem J 2003, 374:647-656.
68. Cloutier S., Laverdière M., Chou M.N., Boilard N., Chow C., Papadopoulou B. Translational control through eIF2alpha phosphorylation during the Leishmania differentiation process. PLoS One 2012, 7:e35085.
69. da Silva R.A., Bartholomeu D.C., Teixeira S.M. Control mechanisms of tubulin gene expression in Trypanosoma cruzi. Int J Parasitol 2006, 36:87-96.
70. Wilson G.M., Sutphen K., Bolikal S., Chuang K.Y., Brewer G. Thermodynamics and kinetics of Hsp70 association with A+U-rich mRNA-destabilizing sequences. J Biol Chem 2001, 276:44450-44456.
71. Kishor A., Tandukar B., Ly Y.V., Toth E.A., Suarez Y., Brewer G., et al. Hsp70 is a novel posttranscriptional regulator of gene expression that binds and stabilizes selected mRNAs containing AU-rich elements. Mol Cell Biol 2013, 33:71-84.
72. Kramer S., Queiroz R., Ellis L., Webb H., Hoheisel J.D., Clayton C., 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, 121:3002-3014.
73. Cushman I., Bowman B.R., Sowa M.E., Lichtarge O., Quiocho F.A., Moore M.S. Computational and biochemical identification of a nuclear pore complex binding site on the nuclear transport carrier NTF2. J Mol Biol 2004, 344:303-310.
74. Kobe B., Kajava A.V. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 2001, 11:725-732.
75. Kilchert C., Weidner J., Prescianotto-Baschong C., Spang A. Defects in the secretory pathway and high Ca2+ induce multiple P-bodies. Mol Biol Cell 2010, 21:2624-2638.
76. Wardleworth B.N., Russell R.J., Bell S.D., Taylor G.L., White M.F. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J 2002, 21:4654-4662.