Diacylglycerol-stimulated endocytosis of transferrin in trypanosomatids is dependent on tyrosine kinase activity

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Subramanya, Sandesh ^a,b   Mensa Wilmot, Kojo ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; GLYCOSYLPHOSPHATIDYLINOSITOL DIACYLGLYCEROL LYASE; MICROBIAL ENZYME; PHORBOL ESTER; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; TRANSFERRIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PROTOZOAL PROTEIN;

ARTICLE; CELL ACTIVATION; CELL STIMULATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; HOST CELL; LEISHMANIA MAJOR; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE HOMOLOGY;

LEISHMANIA MAJOR; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; DIGLYCERIDES; ENDOCYTOSIS; GLYCOSYLPHOSPHATIDYLINOSITOL DIACYLGLYCEROL-LYASE; MOLECULAR SEQUENCE DATA; PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE; TRANSFERRIN; TRYPANOSOMA;

EID: 77649157803     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008538     Document Type: Article

References (56)

1. Sorkin A, Von Zastrow M (2002) Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3: 600-614.
2. Colon-Gonzalez F, Kazanietz MG (2006) C1 domains exposed: from diacylglycerol binding to protein-protein interactions. Biochim Biophys Acta 1761: 827-837.
3. Hereld D, Krakow JL, Bangs JD, Hart GW, Englund PT (1986) A phospholipase C from Trypanosoma brucei which selectively cleaves the glycolipid on the variant surface glycoprotein. J Biol Chem 261: 13813-13819.
4. Fox JA, Duszenko M, Ferguson MA, Low MG, Cross GAM (1986) Purification and characterization of a novel glycan-phosphatidylinositol-specific phospholipase C from Trypanosoma brucei. J Biol Chem 261: 15767-15771.
5. Morris JC, Ping-Sheng L, Shen TY, Mensa-Wilmot K (1995) Glycan requirements of glycosylphosphatidylinositol phospholipase C from Trypanosoma brucei. Glucosaminylinositol derivatives inhibit phosphatidylinositol phospholipase C. J Biol Chem 270: 2517-2524.
6. Subramanya S, Mensa-Wilmot K (2006) Regulated cleavage of intracellular glycosylphosphatidylinositol in a trypanosome. Peroxisome-to-endoplasmic reticulum translocation of a phospholipase C. FEBS J 273: 2110-2126.
7. Subramanya S, Hardin CF, Steverding D, Mensa-Wilmot K (2009) Glycosyl-phosphatidylinositol-specific phospholipase C regulates transferrin endocytosis in the African trypanosome. Biochem J 417: 685-694.
8. Webb H, Carnall N, Vanhamme L, Rolin S, Van Den Abbeele J, et al. (1997) The GPI-phospholipase C of Trypanosoma brucei is nonessential but influences parasitemia in mice. J Cell Biol 139: 103-114.
9. Gruszynski AE, van Deursen FJ, Albareda MC, Best A, Chaudhary K, et al. (2006) Regulation of surface coat exchange by differentiating African trypanosomes. Mol Biochem Parasitol 147: 211-223.
10. Sengupta S, Tripathi J, Tandon R, Raje M, Roy RP, et al. (1999) Hemoglobin endocytosis in Leishmania is mediated through a 46-kDa protein located in the flagellar pocket. J Biol Chem 274: 2758-2765.
11. Singh SB, Tandon R, Krishnamurthy G, Vikram R, Sharma N, et al. (2003) Rab5-mediated endosome-endosome fusion regulates hemoglobin endocytosis in Leishmania donovani. EMBO J 22: 5712-5722.
12. Krishnamurthy G, Vikram R, Singh SB, Patel N, Agarwal S, et al. (2005) Hemoglobin receptor in Leishmania is a hexokinase located in the flagellar pocket. J Biol Chem 280: 5884-5891.
13. Wilson ME, Lewis TS, Miller MA, McCormick ML, Britigan BE (2002) Leishmania chagasi: uptake of iron bound to lactoferrin or transferrin requires an iron reductase. Exp Parasitol 100: 196-207.
14. Voyiatzaki CS, Soteriadou KP (1992) Identification and isolation of the Leishmania transferrin receptor. J Biol Chem 267: 9112-9117.
15. Voyiatzaki CS, Soteriadou KP (1992) Identification and isolation of the Leishmania transferrin receptor. J Biol Chem 267: 9112-9117.
16. Britigan BE, Lewis TS, McCormick ML, Wilson ME (1998) Evidence for the existence of a surface receptor for ferriclactoferrin and ferrictransferrin associated with the plasma membrane of the protozoan parasite Leishmania donovani. Adv Exp Med Biol 443: 135-140.
17. Zheng Z, Butler KD, Tweten RK, Mensa-Wilmot K (2004) Endosomes, glycosomes, and GPI catabolism in Leishmania major. J Biol Chem.
18. Rashid MB, Russell M, Mensa-Wilmot K (1999) Roles of Gln81 and Cys80 in catalysis by glycosylphosphatidylinositol-phospholipase C from Trypanosoma brucei. Eur J Biochem 264: 914-920.
19. Brose N, Rosenmund C (2002) Move over protein kinase C, you've got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 115: 4399-4411.
20. Kotsonis P, Majewski H (1996) The structural requirements for phorbol esters to enhance noradrenaline and dopamine release from rat brain cortex. Br J Pharmacol 119: 115-125.
21. Yang C, Kazanietz MG (2003) Divergence and complexities in DAG signaling: looking beyond PKC. Trends Pharmacol Sci 24: 602-608.
22. Wilkinson SE, Parker PJ, Nixon JS (1993) Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem J 294 (Pt 2): 335-337.
23. Birchall AM, Bishop J, Bradshaw D, Cline A, Coffey J, et al. (1994) Ro 32-0432, a selective and orally active inhibitor of protein kinase C prevents T-cell activation. J Pharmacol Exp Ther 268: 922-929.
24. Kazanietz MG (2000) Eyes wide shut: protein kinase C isozymes are not the only receptors for the phorbol ester tumor promoters. Mol Carcinog 28: 5-11.
25. Hurley JH, Newton AC, Parker PJ, Blumberg PM, Nishizuka Y (1997) Taxonomy and function of C1 protein kinase C homology domains. Protein Sci 6: 477-480.
26. Moraru II, Laky M, Stanescu T, Buzila L, Popescu LM (1990) Protein kinase C controls Fc gamma receptor-mediated endocytosis in human neutrophils. FEBS Lett 274: 93-95.
27. Rambaratsingh RA, Stone JC, Blumberg PM, Lorenzo PS (2003) RasGRP1 represents a novel non-protein kinase C phorbol ester signaling pathway in mouse epidermal keratinocytes. J Biol Chem 278: 52792-52801.
28. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The Genome of the African Trypanosome Trypanosoma brucei. Science 309: 416-422.
29. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, et al. (2004) The Pfam protein families database. Nucleic Acids Res 32 Database issue: D138-141.
30. Pearson WR (1996) Effective protein sequence comparison. Methods Enzymol 266: 227-258.
31. Jonassen I (1997) Efficient discovery of conserved patterns using a pattern graph. Comput Appl Biosci 13: 509-522.
32. Bairoch A (1991) PROSITE: a dictionary of sites and patterns in proteins. Nucleic Acids Res 19 Suppl: 2241-2245.
33. Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, et al. (2002) PROSITE: a documented database using patterns and profiles as motif descriptors. Brief Bioinform 3: 265-274.
34. Chopra LC, Hucks D, Twort CH, Ward JP (1997) Effects of protein tyrosine kinase inhibitors on contractility of isolated bronchioles of the rat. Am J Respir Cell Mol Biol 16: 372-378.
35. Mustafa E, Bakhiet M, Jaster R, Bittorf T, Mix E, et al. (1997) Tyrosine kinases are required for interferon-gamma-stimulated proliferation of Trypanosoma brucei brucei. J Infect Dis 175: 669-673.
36. Eltayeb R, Sharafeldin A, Jaster R, Bittorf T, Mix E, et al. (2000) Trypanosoma brucei brucei induces interferon-gamma expression in rat dorsal root ganglia cells via a tyrosine kinase-dependent pathway. J Infect Dis 181: 400-404.
37. Wilson ME, Vorhies RW, Andersen KA, Britigan BE (1994) Acquisition of iron from transferrin and lactoferrin by the protozoan Leishmania chagasi. Infect Immun 62: 3262-3269.
38. Merschjohann K, Steverding D (2006) In vitro growth inhibition of bloodstream forms of Trypanosoma brucei and Trypanosoma congolense by iron chelators. Kinetoplastid Biol Dis 5: 3.
39. Steverding D (1998) Bloodstream forms of Trypanosoma brucei require only small amounts of iron for growth. Parasitol Res 84: 59-62.
40. Schell D, Borowy NK, Overath P (1991) Transferrin is a growth factor for the bloodstream form of Trypanosoma brucei. Parasitol Res 77: 558-560.
41. Maier A, Steverding D (1996) Low affinity of Trypanosoma brucei transferrin receptor to apotransferrin at pH 5 explains the fate of the ligand during endocytosis. FEBS Lett 396: 87-89.
42. Steverding D, Stierhof YD, Fuchs H, Tauber R, Overath P (1995) Transferrin-binding protein complex is the receptor for transferrin uptake in Trypanosoma brucei. JCell Biol 131: 1173-1182.
43. Zheng Z, Butler KD, Tweten RK, Mensa-Wilmot K (2004) Endosomes, Glycosomes, and Glycosylphosphatidylinositol Catabolism in Leishmania major. J Biol Chem 279: 42106-42113.
44. Liberali P, Ramo P, Pelkmans L (2008) Protein Kinases: Starting a Molecular-Systems View of Endocytosis. Annu Rev Cell Dev Biol.
45. Alvi F, Idkowiak-Baldys J, Baldys A, Raymond JR, Hannun YA (2007) Regulation of membrane trafficking and endocytosis by protein kinase C: emerging role of the pericentrion, a novel protein kinase C-dependent subset of recycling endosomes. Cell Mol Life Sci 64: 263-270.
46. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, et al. (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33: 411-424.
47. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, et al. (2002) Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108: 121-133.
48. Parsons M, Ruben L (2000) Pathways involved in environmental sensing in trypanosomatids. Parasitol Today 16: 56-62.
49. Seebeck T, Schaub R, Johner A (2004) cAMP signalling in the kinetoplastid protozoa. Curr Mol Med 4: 585-599.
50. Hurley JH, Misra S (2000) Signaling and subcellular targeting by membrane-binding domains. Annu Rev Biophys Biomol Struct 29: 49-79.
51. Le TL, Joseph SR, Yap AS, Stow JL (2002) Protein kinase C regulates endocytosis and recycling of E-cadherin. Am J Physiol Cell Physiol 283: C489-499.
52. Reinhardt J, Kosch M, Lerner M, Bertram H, Lemke D, et al. (2002) Stimulation of protein kinase C pathway mediates endocytosis of human nongastric H+-K+-ATPase, ATP1AL1. Am J Physiol Renal Physiol 283: F335-343.
53. Eichholtz T, Vossebeld P, van Overveld M, Ploegh H (1992) Activation of protein kinase C accelerates internalization of transferrin receptor but not of major histocompatibility complex class I, independent of their phosphorylation status. J Biol Chem 267: 22490-22495.
54. Kohno H, Taketani S, Tokunaga R (1986) Phorbol ester-induced regulation of transferrin receptors in human leukemia K562 cells. Cell Struct Funct 11: 181-190.
55. Mensa-Wilmot K, LeBowitz JH, Chang KP, al-Qahtani A, McGwire BS, et al. (1994) A glycosylphosphatidylinositol (GPI)-negative phenotype produced in Leishmania major by GPI phospholipase C from Trypanosoma brucei: topography of two GPI pathways. J Cell Biol 124: 935-947.
56. Wallis AE, McMaster WR (1987) Identification of Leishmania genes encoding proteins containing tandemly repeating peptides. J Exp Med 166: 1814-1824.