Identification of a secreted casein kinase 1 in Leishmania donovani: Effect of protein over expression on parasite growth and virulence

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Dan Goor, Mary ^a   Nasereddin, Abedelmajeed ^a   Jaber, Hanan ^a   Jaffe, Charles L ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE I;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME RELEASE; FLOW CYTOMETRY; LEISHMANIA DONOVANI; LEISHMANIASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PARASITE VIRULENCE; PROMASTIGOTE; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALS; CASEIN KINASE I; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; VIRULENCE FACTORS;

EID: 84896732966     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079287     Document Type: Article

References (45)

1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.
2. Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27: 305-318.
3. Rosenzweig D, Smith D, Opperdoes F, Stern S, Olafson RW, et al. (2008) Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB J 22: 590-602. (Pubitemid 351225595)
4. Mougneau E, Bihl F, Glaichenhaus N (2011) Cell biology and immunology of Leishmania. Immunological Reviews 240: 286-296.
5. Johnson LN (2009) The regulation of protein phosphorylation. Biochemical Society Transactions 37: 627-641.
6. Bhardwaj S, Srivastava N, Sudan R, Saha B (2010) Leishmania interferes with host cell signaling to devise a survival strategy. Journal of Biomedicine and Biotechnology 2010: 109189.
7. Ma HT, Poon RYC (2011) How protein kinases co-ordinate mitosis in animal cells. Biochemical Journal 435: 17-31.
8. Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, et al. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biology 9: R35.31-R35.21.
9. Hermoso T, Fishelson Z, Becker SI, Hirschberg K, Jaffe CL (1991) Leishmanial protein kinases phosphorylate components of the complement system. Embo J 10: 4061-4067. (Pubitemid 21905436)
10. Sacerdoti-Sierra N, Jaffe CL (1997) Release of ecto-protein kinases by the protozoan parasite Leishmania major. J Biol Chem 272: 30760-30765. (Pubitemid 27527512)
11. Vieira LL, Sacerdoti-Sierra N, Jaffe CL (2002) Effect of pH and temperature on protein kinase release by Leishmania donovani. Int J Parasitol 32: 1085-1093. (Pubitemid 34761902)
12. Silverman JM, Clos J, de'Oliveira CC, Shirvani O, Fang Y, et al. (2010) An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. Journal of Cell Science 123: 842-852.
13. Silverman JM, Clos J, Horakova E, Wang AY, Wiesgigl M, et al. (2010) Leishmania Exosomes Modulate Innate and Adaptive Immune Responses through Effects on Monocytes and Dendritic Cells. The Journal of Immunology 185: 5011-5022.
14. Zilberstein D, Shapira M (1994) The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48: 449-470. (Pubitemid 24334105)
15. Debrabant A, Joshi MB, Pimenta PF, Dwyer DM (2004) Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int J Parasitol 34: 205-217. (Pubitemid 38229824)
16. Knippschild U, Gocht A, Wolff S, Huber N, L̂hler Jr, et al. (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cellular Signalling 17: 675-689. (Pubitemid 40250168)
17. Gross SD, Anderson RA (1998) Casein Kinase I: Spatial Organization and Positioning of a Multifunctional Protein Kinase Family. Cellular Signalling 10: 699-711. (Pubitemid 28520022)
18. Parsons M, Worthey EA, Ward PN, Mottram JC (2005) Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6: 127.
19. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
20. Urbaniak MD (2009) Casein kinase 1 isoform 2 is essential for bloodstream form Trypanosoma brucei. Molecular and Biochemical Parasitology 166: 183-185.
21. Allocco JJ, Donald R, Zhong T, Lee A, Tang YS, et al. (2006) Inhibitors of casein kinase 1 block the growth of Leishmania major promastigotes in vitro. International Journal for Parasitology 36: 1249-1259. (Pubitemid 44353484)
22. Knockaert M, Gray N, Damiens E, Chang YT, Grellier P, et al. (2000) Intracellular targets of cyclin-dependent kinase inhibitors: identification by affinity chromatography using immobilised inhibitors. Chem Biol 7: 411-422. (Pubitemid 30400044)
23. Liu J, Carvalho LP, Bhattacharya S, Carbone CJ, Kumar KGS, et al. (2009) Mammalian Casein Kinase 1{alpha} and Its Leishmanial Ortholog Regulate Stability of IFNAR1 and Type I Interferon Signaling. Mol Cell Biol 29: 6401-6412.
24. Shimony O, Jaffe CL (2008) Rapid fluorescent assay for screening drugs on Leishmania amastigotes. J Microbiol Methods 75: 196-200.
25. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution.
26. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, et al. (2009) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38: D457-D462.
27. Dyrl̄v Bendtsen J, Nielsen H, von Heijne G, Brunak Sr (2004) Improved Prediction of Signal Peptides: SignalP 3.0. Journal of Molecular Biology 340: 783-795.
28. Beverley SM, Clayton C (1993) Transfection of Leishmania and Trypanosoma brucei by electroporation. In: Hyde JE, editor. Protocols in Molecular Parasitology (Methods in Molecular Biology). Totowa, N.J.: Humana Press. 338-348.
29. Talmi-Frank D, Jaffe CL, Nasereddin A, Baneth G (2012) Leishmania tropica experimental infection in the rat using luciferase-transfected parasites. Vet Parasitol 187: 57-62.
30. Mifllitz A, Mottram JC, Overath P, Aebischer T (2000) Targeted integration into a rRNA locus results in uniform and high level expression of transgenes in Leishmania amastigotes. Molecular and Biochemical Parasitology 107: 251-261. (Pubitemid 30211639)
31. Saraiva EM, Pinto-da-Silva LH, Wanderley JoLM, Bonomo AC, Barcinski MA, et al. (2005) Flow cytometric assessment of Leishmania spp metacyclic differentiation: Validation by morphological features and specific markers. Experimental Parasitology 110: 39-47. (Pubitemid 40404075)
32. Yao C, Chen Y, Sudan B, Donelson JE, Wilson ME (2008) Leishmania chagasi: homogenous metacyclic promastigotes isolated by buoyant density are highly virulent in a mouse model. Exp Parasitol 118: 129-133. (Pubitemid 350299341)
33. Spath GF, Beverley SM (2001) A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Experimental Parasitology 99: 97-103. (Pubitemid 34038221)
34. Ehrenfreund-Kleinman T, Domb AJ, Jaffe CL, Nasereddin A, Leshem B, et al. (2005) The effect of Amphotericin B derivatives on Leishmania and immune functions. Journal of Parasitology 91: 158-163. (Pubitemid 40804315)
35. Diez H, Sarmiento L, Caldas ML, Montilla M, Thomas Mdel C, et al. (2008) Cellular location of KMP-11 protein in Trypanosoma rangeli. Vector Borne Zoonotic Dis 8: 93-96. (Pubitemid 351271588)
36. Stebeck CE, Beecroft RP, Singh BN, Jardim A, Olafson RW, et al. (1995) Kinetoplastid membrane protein-11 (KMP-11) is differentially expressed during the life cycle of African trypanosomes and is found in a wide variety of kinetoplastid parasites. Mol Biochem Parasitol 71: 1-13.
37. Vancura A, Sessler A, Leichus B, Kuret J (1994) A prenylation motif is required for plasma membrane localization and biochemical function of casein kinase I in budding yeast. Journal of Biological Chemistry 269: 19271-19278. (Pubitemid 24233444)
38. Knockaert M, Wieking K, Schmitt S, Leost M, Grant KM, et al. (2002) Intracellular Targets of Paullones. Identification following affinity purification on immobilized inhibitor. J Biol Chem 277: 25493-25501. (Pubitemid 34951864)
39. Florez A, Park D, Bhak J, Kim B-C, Kuchinsky A, et al. (2010) Protein network prediction and topological analysis in Leishmania major as a tool for drug target selection. BMC Bioinformatics 11: 484.
40. Foucher AL, Rachidi N, Gharbi S, Blisnick T, Bastin P, et al. (2013) Apoptotic marker expression in the absence of cell death in staurosporine- treated Leishmania donovani. Antimicrob Agents Chemother 57: 1252-1261.
41. Corrales RM, Sereno D, Mathieu-Daudé F (2010) Deciphering the Leishmania exoproteome: what we know and what we can learn. FEMS Immunology & Medical Microbiology 58: 27-38.
42. Silverman JM, Reiner NE (2011) Exosomes and other microvesicles in infection biology: organelles with unanticipated phenotypes. Cellular Microbiology 13: 1-9.
43. Hassani K, Antoniak E, Jardim A, Olivier M (2011) Temperature-induced protein secretion by Leishmania mexicana modulates macrophage signalling and function. PLoS ONE 6: e18724.
44. Lahav T, Sivam D, Volpin H, Ronen M, Tsigankov P, et al. (2011) Multiple levels of gene regulation mediate differentiation of the intracellular pathogen Leishmania. The FASEB Journal 25: 515-525.
45. Rochette A, Raymond F, Corbeil J, Ouellette M, Papadopoulou B (2009) Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum. Molecular and Biochemical Parasitology 165: 32-47.