Receptor-mediated endocytosis for drug delivery in African trypanosomes: Fulfilling Paul Ehrlich's vision of chemotherapy

Trends in Parasitology

Volumn 29, Issue 5, 2013, Pages 207-212

  Alsford, Sam ^a   Field, Mark C ^b   Horn, David ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Drug delivery; Endocytosis; Suramin; Trypanolytic factor; Trypanosoma brucei

Indexed keywords

APOLIPOPROTEIN A1; CARRIER PROTEIN; EFLORNITHINE; GLYCOPROTEIN; HIGH DENSITY LIPOPROTEIN; MELARSOPROL; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; NIFURTIMOX; PENTAMIDINE; PROTEIN VARIANT; SURAMIN; TRYPANOLYTIC FACTOR 1; TRYPANOLYTIC FACTOR 2; UNCLASSIFIED DRUG;

AFRICAN TRYPANOSOMIASIS; CHEMOTHERAPY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG RECEPTOR BINDING; DRUG TRANSPORT; ENDOCYTOSIS; ENDOSOME; PATIENT COMPLIANCE; PROTIST LIFE CYCLE STAGE; REVIEW; RNA INTERFERENCE; SCREENING; SUBSPECIES; TRYPANOSOMA BRUCEI;

ANIMALS; ENDOCYTOSIS; ENDOSOMES; HUMANS; MEMBRANE GLYCOPROTEINS; PROTOZOAN PROTEINS; SURAMIN; TRANSPORT VESICLES; TRYPANOCIDAL AGENTS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

HEXAPODA; TRYPANOSOMA BRUCEI;

EID: 84876864817     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2013.03.004     Document Type: Review

References (60)

1. Steverding D. The history of African trypanosomiasis. Parasit. Vectors 2008, 1:3.
2. Barrett M.P., Croft S.L. Management of trypanosomiasis and leishmaniasis. Br. Med. Bull. 2012, 104:175-196.
3. Priotto G., et al. Nifurtimox-eflornithine combination therapy for second-stage African Trypanosoma brucei gambiense trypanosomiasis: a multicentre, randomised, Phase III, non-inferiority trial. Lancet 2009, 374:56-64.
4. Ehrlich P. Address in pathology, on chemiotherapy. Delivered before the Seventeenth International Congress of Medicine. Br. Med. J. 1913, 2:353-359.
5. Alsford S., et al. High-throughput decoding of antitrypanosomal drug efficacy and resistance. Nature 2012, 482:232-236.
6. Overath P., et al. Invariant surface proteins in bloodstream forms of Trypanosoma brucei. Parasitol. Today 1994, 10:53-58.
7. Vanhollebeke B., et al. A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 2008, 320:677-681.
8. Prull C.R. Part of a scientific master plan? Paul Ehrlich and the origins of his receptor concept. Med. Hist. 2003, 47:332-356.
9. Vanhollebeke B., Pays E. The trypanolytic factor of human serum: many ways to enter the parasite, a single way to kill. Mol. Microbiol. 2010, 76:806-814.
10. Hajduk S.L., et al. Lysis of Trypanosoma brucei by a toxic subspecies of human high density lipoprotein. J. Biol. Chem. 1989, 264:5210-5217.
11. Rifkin M.R. Identification of the trypanocidal factor in normal human serum: high density lipoprotein. Proc. Natl. Acad. Sci. U.S.A. 1978, 75:3450-3454.
12. Raper J., et al. Characterization of a novel trypanosome lytic factor from human serum. Infect. Immun. 1999, 67:1910-1916.
13. Tomlinson S., et al. High-density-lipoprotein-independent killing of Trypanosoma brucei by human serum. Mol. Biochem. Parasitol. 1995, 70:131-138.
14. Molina-Portela M.P., et al. Trypanosome lytic factor, a subclass of high-density lipoprotein, forms cation-selective pores in membranes. Mol. Biochem. Parasitol. 2005, 144:218-226.
15. Perez-Morga D., et al. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 2005, 309:469-472.
16. Vanhollebeke B., et al. Distinct roles of haptoglobin-related protein and apolipoprotein L-I in trypanolysis by human serum. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:4118-4123.
17. Bullard W., et al. Haptoglobin-hemoglobin receptor independent killing of African trypanosomes by human serum and trypanosome lytic factors. Virulence 2012, 3:72-76.
18. Xong H.V., et al. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 1998, 95:839-846.
19. Stephens N.A., Hajduk S.L. Endosomal localization of the serum resistance-associated protein in African trypanosomes confers human infectivity. Eukaryot. Cell 2011, 10:1023-1033.
20. Vanhamme L., et al. Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 2003, 422:83-87.
21. Higgins M.K., et al. Structure of the trypanosome haptoglobin-hemoglobin receptor and implications for nutrient uptake and innate immunity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1905-1910.
22. Symula R.E., et al. Trypanosoma brucei gambiense group 1 is distinguished by a unique amino acid substitution in the HpHb receptor implicated in human serum resistance. PLoS Negl. Trop. Dis. 2012, 6:e1728.
23. Kieft R., et al. Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16137-16141.
24. Capewell P., et al. Differences between Trypanosoma brucei gambiense groups 1 and 2 in their resistance to killing by trypanolytic factor 1. PLoS Negl. Trop. Dis. 2011, 5:e1287.
25. Genovese G., et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 2010, 329:841-845.
26. Baral T.N., et al. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nat. Med. 2006, 12:580-584.
27. Lecordier L., et al. C-terminal mutants of apolipoprotein L-I efficiently kill both Trypanosoma brucei brucei and Trypanosoma brucei rhodesiense. PLoS Pathog. 2009, 5:e1000685.
28. Stephens N.A., et al. Trypanosome resistance to human innate immunity: targeting Achilles' heel. Trends Parasitol. 2012, 28:539-545.
29. Burri C. Chemotherapy against human African trypanosomiasis: is there a road to success?. Parasitology 2010, 137:1987-1994.
30. Vansterkenburg E.L., et al. The uptake of the trypanocidal drug suramin in combination with low-density lipoproteins by Trypanosoma brucei and its possible mode of action. Acta Trop. 1993, 54:237-250.
31. Pal A., et al. Evidence for a non-LDL-mediated entry route for the trypanocidal drug suramin in Trypanosoma brucei. Mol. Biochem. Parasitol. 2002, 122:217-221.
32. Lumb J.H., et al. Rab28 function in trypanosomes: interactions with retromer and ESCRT pathways. J. Cell Sci. 2011, 124:3771-3783.
33. Peck R.F., et al. The LAMP-like protein p67 plays an essential role in the lysosome of African trypanosomes. Mol. Microbiol. 2008, 68:933-946.
34. Koumandou V.L., et al. Evidence for recycling of invariant surface transmembrane domain proteins in African trypanosomes. Eukaryot. Cell 2013, 12:330-342.
35. Leung K.F., et al. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 2008, 9:1698-1716.
36. Leung K.F., et al. Ubiquitylation and developmental regulation of invariant surface protein expression in trypanosomes. Eukaryot. Cell 2011, 10:916-931.
37. Engstler M., et al. Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 2007, 131:505-515.
38. Alsford S., et al. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 2011, 21:915-924.
39. Koumandou V.L., et al. Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 2011, 124:1496-1509.
40. Di Cosimo S., Baselga J. Targeted therapies in breast cancer: where are we now?. Eur. J. Cancer 2008, 44:2781-2790.
41. Morgan H.P., et al. The trypanocidal drug suramin and other trypan blue mimetics are inhibitors of pyruvate kinases and bind to the adenosine site. J. Biol. Chem. 2011, 286:31232-31240.
42. Madhumathi J., Verma R.S. Therapeutic targets and recent advances in protein immunotoxins. Curr. Opin. Microbiol. 2012, 15:300-309.
43. Stijlemans B., et al. High affinity nanobodies against the Trypanosoma brucei VSG are potent trypanolytic agents that block endocytosis. PLoS Pathog. 2011, 7:e1002072.
44. Schwede A., et al. The VSG C-terminal domain is inaccessible to antibodies on live trypanosomes. Mol. Biochem. Parasitol. 2011, 175:201-204.
45. Chung W.L., et al. Cytoplasmic targeting signals in transmembrane invariant surface glycoproteins of trypanosomes. J. Biol. Chem. 2004, 279:54887-54895.
46. Field M.C., Carrington M. The trypanosome flagellar pocket. Nat. Rev. Microbiol. 2009, 7:775-786.
47. Matovu E., et al. Genetic variants of the TbAT1 adenosine transporter from African trypanosomes in relapse infections following melarsoprol therapy. Mol. Biochem. Parasitol. 2001, 117:73-81.
48. Morris J.C., et al. Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO J. 2002, 21:4429-4438.
49. Baker N., et al. Genome-wide RNAi screens in African trypanosomes identify the nifurtimox activator NTR and the eflornithine transporter AAT6. Mol. Biochem. Parasitol. 2011, 176:55-57.
50. Allen C.L., et al. Dileucine signal-dependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol. Biochem. Parasitol. 2007, 156:175-190.
51. Aguilar P.S., et al. A plasma-membrane E-MAP reveals links of the eisosome with sphingolipid metabolism and endosomal trafficking. Nat. Struct. Mol. Biol. 2010, 17:901-908.
52. Jean S., et al. Sbf/MTMR13 coordinates PI(3)P and Rab21 regulation in endocytic control of cellular remodeling. Mol. Biol. Cell 2012, 23:2723-2740.
53. Tazeh N.N., et al. Role of AP-1 in developmentally regulated lysosomal trafficking in Trypanosoma brucei. Eukaryot. Cell 2009, 8:1352-1361.
54. Lingnau A., et al. Characterization of tGLP-1, a Golgi and lysosome-associated, transmembrane glycoprotein of African trypanosomes. J. Cell Sci. 1999, 112:3061-3070.
55. Dutoya S., et al. A novel C-terminal kinesin is essential for maintaining functional acidocalcisomes in Trypanosoma brucei. J. Biol. Chem. 2001, 276:49117-49124.
56. Allen C.L., et al. Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J. 2003, 22:4991-5002.
57. Field M.C., et al. Macromolecular trafficking and immune evasion in African trypanosomes. Int. Rev. Cell Mol. Biol. 2009, 278:1-67.
58. Pal A., et al. Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem. J. 2003, 374:443-451.
59. Chung W.L., et al. Ubiquitylation is required for degradation of transmembrane surface proteins in trypanosomes. Traffic 2008, 9:1681-1697.
60. Frearson J.A., et al. N-Myristoyltransferase inhibitors as new leads to treat sleeping sickness. Nature 2010, 464:728-732.