KHARON1 mediates flagellar targeting of a glucose transporter in Leishmania mexicana and is critical for viability of infectious intracellular amastigotes

Journal of Biological Chemistry

Volumn 288, Issue 31, 2013, Pages 22721-22733

  Tran, Khoa D ^a   Rodriguez Contreras, Dayana ^a   Vieira, Danielle P ^a   Yates, Phillip A ^a   David, Larry ^a   Beatty, Wandy ^b   Elferich, Johannes ^a   Landfear, Scott M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTERS; KINETOPLASTID PARASITE; LEISHMANIA; MEMBRANE PROTEINS; NOVEL PROTEINS;

BIOLOGICAL MEMBRANES; CELLS; PROTEINS;

MUTAGENESIS;

GLUCOSE TRANSPORTER; KHARON1; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

AMASTIGOTE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXONEME; BINDING AFFINITY; CELL VIABILITY; CONTROLLED STUDY; FLAGELLUM; IN VIVO STUDY; LEISHMANIA MEXICANA; LIFE CYCLE STAGE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN TARGETING;

AMASTIGOTE VIABILITY; FLAGELLAR MEMBRANE PROTEIN TARGETING; GLUCOSE TRANSPORT; GLUCOSE TRANSPORTER; LEISHMANIA; MASS SPECTROMETRY (MS); PATHOGENESIS; PROTEIN TARGETING; TAP TAGGING;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CHROMATOGRAPHY, AFFINITY; DNA PRIMERS; FLAGELLA; GLUCOSE; LEISHMANIA MEXICANA; MOLECULAR SEQUENCE DATA; MONOSACCHARIDE TRANSPORT PROTEINS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84881221113     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.483461     Document Type: Article

References (58)

1. Berbari, N. F., O'Connor, A. K., Haycraft, C. J., and Yoder, B. K. (2009) The primary cilium as a complex signaling center. Curr. Biol. 19, R526-535
2. Bloodgood, R. A. (2010) Sensory reception is an attribute of both primary cilia and motile cilia. J. Cell Sci. 123, 505-509
3. Ginger, M. L., Portman, N., and McKean, P. G. (2008) Swimming with protists. Perception, motility and flagellum assembly. Nat. Rev. Microbiol. 6, 838-850
4. Pazour, G. J., and Witman, G. B. (2003) The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15, 105-110
5. Clapham, D. E. (2003) TRP channels as cellular sensors. Nature 426, 517-524
6. Maric, D., Epting, C. L., and Engman, D. M. (2010) Composition and sensory function of the trypanosome flagellar membrane. Curr. Opin. Microbiol. 13, 466-472
7. Marshall, W. F., and Nonaka, S. (2006) Cilia. Tuning in to the cell's antenna. Curr. Biol. 16, R604-614
8. Singla, V., and Reiter, J. F. (2006) The primary cilium as the cell's antenna. Signaling at a sensory organelle. Science 313, 629-633
9. WHO, W. H. O. (2013) Neglected tropical diseases. www.who.int/neglected- diseases/diseases/en
10. Oberholzer, M., Langousis, G., Nguyen, H. T., Saada, E. A., Shimogawa, M. M., Jonsson, Z. O., Nguyen, S. M., Wohlschlegel, J. A., and Hill, K. L. (2011) Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei. Mol. Cell. Proteomics 10, M111.010538-1-M111.010538-14
11. Buchanan, K. T., Ames, J. B., Asfaw, S. H., Wingard, J. N., Olson, C. L., Campana, P. T., Araújo, A. P., and Engman, D. M. (2005) A flagellumspecific calcium sensor. J. Biol. Chem. 280, 40104-40111
12. Emmer, B. T., Maric, D., and Engman, D. M. (2010) Molecular mechanisms of protein and lipid targeting to ciliary membranes. J. Cell Sci. 123, 529-536
13. Engman, D. M., Krause, K. H., Blumin, J. H., Kim, K. S., Kirchhoff, L. V., and Donelson, J. E. (1989) A novel flagellar Ca2+-binding protein in trypanosomes. J. Biol. Chem. 264, 18627-18631
14. Paindavoine, P., Rolin, S., Van Assel, S., Geuskens, M., Jauniaux, J. C., Dinsart, C., Huet, G., and Pays, E. (1992) A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei. Mol. Cell. Biol. 12, 1218-1225
15. Figarella, K., Uzcategui, N. L., Zhou, Y., LeFurgey, A., Ouellette, M., Bhattacharjee, H., and Mukhopadhyay, R. (2007) Biochemical characterization of Leishmania major aquaglyceroporin LmAQP1. Possible role in volume regulation and osmotaxis. Mol. Microbiol. 65, 1006-1017
16. Burchmore, R. J., Rodriguez-Contreras, D., McBride, K., Merkel, P., Barrett, M. P., Modi, G., Sacks, D., and Landfear, S. M. (2003) Genetic characterization of glucose transporter function in Leishmania mexicana. Proc. Natl. Acad. Sci. U.S.A. 100, 3901-3906
17. Tran, K. D., Rodriguez-Contreras, D., Shinde, U., and Landfear, S. M. (2012) Both sequence and context are important for flagellar targeting of a glucose transporter. J. Cell Sci. 125, 3293-3298
18. Pazour, G. J., and Bloodgood, R. A. (2008) Targeting proteins to the ciliary membrane. Curr. Top. Dev. Biol. 85, 115-149
19. Nachury, M. V., Seeley, E. S., and Jin, H. (2010) Trafficking to the ciliary membrane. How to get across the periciliary diffusion barrier? Annu. Rev. Cell Dev. Biol. 26, 59-87
20. Robinson, K. A., and Beverley, S. M. (2003) Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol. Biochem. Parasitol. 128, 217-228
21. Tagwerker, C., Flick, K., Cui, M., Guerrero, C., Dou, Y., Auer, B., Baldi, P., Huang, L., and Kaiser, P. (2006) A tandem affinity tag for two-step purification under fully denaturing conditions. Application in ubiquitin profiling and protein complex identification combined with in vivo cross-linking. Mol. Cell Proteomics 5, 737-748
22. Valdés, R., Vasudevan, G., Conklin, D., and Landfear, S. M. (2004) Transmembrane domain 5 of the LdNT1.1 nucleoside transporter is an amphipathic helix that forms part of the nucleoside translocation pathway. Biochemistry 43, 6793-6802
23. Fulwiler, A. L., Soysa, D. R., Ullman, B., and Yates, P. A. (2011) A rapid, efficient and economical method for generating leishmanial gene targeting constructs. Mol. Biochem. Parasitol. 175, 209-212
24. Nasser, M. I., and Landfear, S. M. (2004) Sequences required for the flagellar targeting of an integral membrane protein. Mol. Biochem. Parasitol. 135, 89-100
25. Tran, K. D., Miller, M. R., and Doe, C. Q. (2010) Recombineering Hunchback identifies two conserved domains required to maintain neuroblast competence and specify early-born neuronal identity. Development 137, 1421-1430
26. Ha, D. S., Schwarz, J. K., Turco, S. J., and Beverley, S. M. (1996) Use of the green fluorescent protein as a marker in transfected Leishmania. Mol. Biochem. Parasitol. 77, 57-64
27. Gourbal, B., Sonuc, N., Bhattacharjee, H., Legare, D., Sundar, S., Ouellette, M., Rosen, B. P., and Mukhopadhyay, R. (2004) Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J. Biol. Chem. 279, 31010-31017
28. Heras, S. R., Thomas, M. C., García-Canadas, M., de Felipe, P., García-Pérez, J. L., Ryan, M. D., and López, M. C. (2006) L1Tc non-LTR retrotransposons from Trypanosoma cruzi contain a functional viral-like selfcleaving 2A sequence in-frame with the active proteins they encode. Cell Mol. Life Sci. 63, 1449-1460
29. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B. P., Carrington, M., Depledge, D. P., Fischer, S., Gajria, B., Gao, X., Gardner, M. J., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hertz-Fowler, C., Houston, R., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Logan, F. J., Miller, J. A., Mitra, S., Myler, P. J., Nayak, V., Pennington, C., Phan, I., Pinney, D. F., Ramasamy, G., Rogers, M. B., Roos, D. S., Ross, C., Sivam, D., Smith, D. F., Srinivasamoorthy, G., Stoeckert, C. J., Jr., Subramanian, S., Thibodeau, R., Tivey, A., Treatman, C., Velarde, G., and Wang, H. (2010) TriTrypDB. A functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38, D457-462
30. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
31. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
32. Eddy, S. R. (1998) Profile hidden Markov models. Bioinformatics 14, 755-763
33. Cruz, A., and Beverley, S. M. (1990) Gene replacement in parasitic protozoa. Nature 348, 171-173
34. McConville, M. J., Mullin, K. A., Ilgoutz, S. C., and Teasdale, R. D. (2002) Secretory pathway of trypanosomatid parasites. Microbiol Mol. Biol. Rev. 66, 122-154
35. Zheng, Z., Butler, K. D., Tweten, R. K., and Mensa-Wilmot, K. (2004) Endosomes, glycosomes, and glycosylphosphatidylinositol catabolism in Leishmania major. J. Biol. Chem. 279, 42106-42113
36. Mandal, G., Sharma, M., Kruse, M., Sander-Juelch, C., Munro, L. A., Wang, Y., Vilg, J. V., Tamás, M. J., Bhattacharjee, H., Wiese, M., and Mukhopadhyay, R. (2012) Modulation of Leishmania major aquaglyceroporin activity by a mitogen-activated protein kinase. Mol. Microbiol. 85, 1204-1218
37. Fridberg, A., Buchanan, K. T., and Engman, D. M. (2007) Flagellar membrane trafficking in kinetoplastids. Parasitol. Res. 100, 205-212
38. Godsel, L. M., and Engman, D. M. (1999) Flagellar protein localization mediated by a calcium-myristoyl/palmitoyl switch mechanism. EMBO J. 18, 2057-2065
39. Maric, D., McGwire, B. S., Buchanan, K. T., Olson, C. L., Emmer, B. T., Epting, C. L., and Engman, D. M. (2011) Molecular determinants of ciliary membrane localization of Trypanosoma cruzi flagellar calcium-binding protein. J. Biol. Chem. 286, 33109-33117
40. Tull, D., Vince, J. E., Callaghan, J. M., Naderer, T., Spurck, T., McFadden, G. I., Currie, G., Ferguson, K., Bacic, A., and McConville, M. J. (2004) SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol. Biol. Cell 15, 4775-4786
41. Denny, P. W., Gokool, S., Russell, D. G., Field, M. C., and Smith, D. F. (2000) Acylation-dependent protein export in Leishmania. J. Biol. Chem. 275, 11017-11025
42. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., and Tada, K. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26, 171-176
43. Gluenz, E., Ginger, M. L., and McKean, P. G. (2010) Flagellum assembly and function during the Leishmania life cycle. Curr. Opin. Microbiol. 13, 473-479
44. Gluenz, E., Höög, J. L., Smith, A. E., Dawe, H. R., Shaw, M. K., and Gull, K. (2010) Beyond 9-0. Noncanonical axoneme structures characterize sensory cilia from protists to humans. FASEB J. 24, 3117-3121
45. Sacks, D. L., and Melby, P. C. (2001) Animal models for the analysis of immune responses to leishmaniasis. Curr. Protoc. Immunol. 28, 19.2.1-19.2.20
46. Lacomble, S., Vaughan, S., Gadelha, C., Morphew, M. K., Shaw, M. K., McIntosh, J. R., and Gull, K. (2009) Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J. Cell Sci. 122, 1081-1090
47. Garcia-Gonzalo, F. R., Corbit, K. C., Sirerol-Piquer, M. S., Ramaswami, G., Otto, E. A., Noriega, T. R., Seol, A. D., Robinson, J. F., Bennett, C. L., Josifova, D. J., García-Verdugo, J. M., Katsanis, N., Hildebrandt, F., and Reiter, J. F. (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat. Genet. 43, 776-784
48. Chih, B., Liu, P., Chinn, Y., Chalouni, C., Komuves, L. G., Hass, P. E., Sandoval, W., and Peterson, A. S. (2012) A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat. Cell Biol. 14, 61-72
49. Williams, C. L., Li, C., Kida, K., Inglis, P. N., Mohan, S., Semenec, L., Bialas, N. J., Stupay, R. M., Chen, N., Blacque, O. E., Yoder, B. K., and Leroux, M. R. (2011) MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J. Cell Biol. 192, 1023-1041
50. Hu, Q., Milenkovic, L., Jin, H., Scott, M. P., Nachury, M. V., Spiliotis, E. T., and Nelson, W. J. (2010) A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436-439
51. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Doré, G., Julkowska, D., Tavenet, A., and Bastin, P. (2008) Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol. Biol. Cell 19, 929-944
52. Denny, P. W., Field, M. C., and Smith, D. F. (2001) GPI-anchored proteins and glycoconjugates segregate into lipid rafts in Kinetoplastida. FEBS Lett. 491, 148-153
53. Denny, P. W., and Smith, D. F. (2004) Rafts and sphingolipid biosynthesis in the kinetoplastid parasitic protozoa. Mol. Microbiol. 53, 725-733
54. Söding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951-960
55. Liu, J., and Rost, B. (2003) NORSp. Predictions of long regions without regular secondary structure. Nucleic Acids Res. 31, 3833-3835
56. Gruber, M., Söding, J., and Lupas, A. N. (2005) REPPER. Repeats and their periodicities in fibrous proteins. Nucleic Acids Res. 33, W239-243
57. Wittig, I., and Schägger, H. (2008) Features and applications of blue-native and clear-native electrophoresis. Proteomics 8, 3974-3990
58. Alsford, S., Turner, D. J., Obado, S. O., Sanchez-Flores, A., Glover, L., Berriman, M., Hertz-Fowler, C., and Horn, D. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 21, 915-924