Assembling the components of the quorum sensing pathway in African trypanosomes

Molecular Microbiology

Volumn 96, Issue 2, 2015, Pages 220-232

  Mony, Binny M ^a   Matthews, Keith R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AFRICAN TRYPANOSOME; AFRICAN TRYPANOSOMIASIS; BLOOD FLOW; CELL CYCLE G1 PHASE; CELL TRANSFORMATION; EUKARYOTIC CELL; EVOLUTION; GLOSSINIDAE; HOST; HUMAN; INTRACELLULAR SIGNALING; MAMMAL; NONHUMAN; NUTRITION; PARASITE DEVELOPMENT; PARASITE VECTOR; PRIORITY JOURNAL; QUORUM SENSING; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STRESS; TRYPANOSOMA; ANIMAL; GENETICS; METABOLISM; PARASITOLOGY; TRYPANOSOMA BRUCEI BRUCEI;

DICTYOSTELIUM; EUKARYOTA; GLOSSINA (GENUS); MAMMALIA; PROTOZOA;

PROTOZOAL PROTEIN;

ANIMALS; HUMANS; PROTOZOAN PROTEINS; QUORUM SENSING; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 84926420072     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12949     Document Type: Review

References (73)

1. Alsford, S., Turner, D.J., Obado, S.O., Sanchez-Flores, A., Glover, L., Berriman, M., etal. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21: 915-924.
2. Amiguet-Vercher, A., Perez-Morga, D., Pays, A., Poelvoorde, P., Van Xong, H., Tebabi, P., Vanhamme, L., and Pays, E. (2004) Loss of the mono-allelic control of the VSG expression sites during the development of Trypanosoma brucei in the bloodstream. Mol Microbiol 51: 1577-1588.
3. Aranda, S., Laguna, A., and de la Luna, S. (2011) DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J 25: 449-462.
4. Atkinson, S., and Williams, P. (2009) Quorum sensing and social networking in the microbial world. J R Soc Interface 6: 959-978.
5. Bahler, J., and Pringle, J.R. (1998) Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes Dev 12: 1356-1370.
6. Barquilla, A., Saldivia, M., Diaz, R., Bart, J.M., Vidal, I., Calvo, E., etal. (2012) Third target of rapamycin complex negatively regulates development of quiescence in Trypanosoma brucei. Proc Natl Acad Sci USA 109: 14399-14404.
7. Batram, C., Jones, N.G., Janzen, C.J., Markert, S.M., and Engstler, M. (2014) Expression site attenuation mechanistically links antigenic variation and development in Trypanosoma brucei. Elife 3: e02324.
8. Beeser, A.E., and Cooper, T.G. (2000) The dual-specificity protein phosphatase Yvh1p regulates sporulation, growth, and glycogen accumulation independently of catalytic activity in Saccharomyces cerevisiae via the cyclic AMP-dependent protein kinase cascade. J Bacteriol 182: 3517-3528.
9. Broach, J.R. (2012) Nutritional control of growth and development in yeast. Genetics 192: 73-105.
10. Carling, D., Mayer, F.V., Sanders, M.J., and Gamblin, S.J. (2011) AMP-activated protein kinase: nature's energy sensor. Nat Chem Biol 7: 512-518.
11. Clarke, M., and Gomer, R.H. (1995) PSF and CMF, autocrine factors that regulate gene expression during growth and early development of Dictyostelium. Experientia 51: 1124-1134.
12. Clayton, C.E. (2014) Networks of gene expression regulation in Trypanosoma brucei. Mol Biochem Parasitol 195: 96-106.
13. Cox, A.P., Tosas, O., Tilley, A., Picozzi, K., Coleman, P., Hide, G., and Welburn, S.C. (2010) Constraints to estimating the prevalence of trypanosome infections in East African zebu cattle. Parasit Vectors 3: 82.
14. Cully, D.F., Gibbs, C.P., and Cross, G.A. (1986) Identification of proteins encoded by variant surface glycoprotein expression site-associated genes in Trypanosoma brucei. Mol Biochem Parasitol 21: 189-197.
15. De Virgilio, C. (2012) The essence of yeast quiescence. FEMS Microbiol Rev 36: 306-339.
16. Dean, S., Marchetti, R., Kirk, K., and Matthews, K.R. (2009) A surface transporter family conveys the trypanosome differentiation signal. Nature 459: 213-217.
17. Deep, A., Chaudhary, U., and Gupta, V. (2011) Quorum sensing and bacterial pathogenicity: from molecules to disease. J Lab Physicians 3: 4-11.
18. Deng, Y., Lim, A., Lee, J., Chen, S., An, S., Dong, Y.H., and Zhang, L.H. (2014) Diffusible signal factor (DSF) quorum sensing signal and structurally related molecules enhance the antimicrobial efficacy of antibiotics against some bacterial pathogens. BMC Microbiol 14: 51.
19. Domenicali Pfister, D., Burkard, G., Morand, S., Renggli, C.K., Roditi, I., and Vassella, E. (2006) A Mitogen-activated protein kinase controls differentiation of bloodstream forms of Trypanosoma brucei. Eukaryot Cell 5: 1126-1135.
20. Dukanovic, J., Dimmer, K.S., Bonnefoy, N., Krumpe, K., and Rapaport, D. (2009) Genetic and functional interactions between the mitochondrial outer membrane proteins Tom6 and Sam37. Mol Cell Biol 29: 5975-5988.
21. Erben, E.D., Fadda, A., Lueong, S., Hoheisel, J.D., and Clayton, C. (2014) A genome-wide tethering screen reveals novel potential post-transcriptional regulators in Trypanosoma brucei. PLoS Pathog 10: e1004178.
22. Frazier, A.E., Dudek, J., Guiard, B., Voos, W., Li, Y.F., Lind, M., etal. (2004) Pam16 has an essential role in the mitochondrial protein import motor. Nat Struct Mol Biol 11: 226-233.
23. Fry, A.M., O'Regan, L., Sabir, S.R., and Bayliss, R. (2012) Cell cycle regulation by the NEK family of protein kinases. J Cell Sci 125: 4423-4433.
24. Garrett, S., Menold, M.M., and Broach, J.R. (1991) The Saccharomyces cerevisiae YAK1 gene encodes a protein kinase that is induced by arrest early in the cell cycle. Mol Cell Biol 11: 4045-4052.
25. Goldstone, D.C., Flower, T.G., Ball, N.J., Sanz-Ramos, M., Yap, M.W., Ogrodowicz, R.W., etal. (2013) A unique spumavirus Gag N-terminal domain with functional properties of orthoretroviral matrix and capsid. PLoS Pathog 9: e1003376.
26. Gomer, R.H., Jang, W., and Brazill, D. (2011) Cell density sensing and size determination. Dev Growth Differ 53: 482-494.
27. Gonzalez, J.E., and Keshavan, N.D. (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70: 859-875.
28. Gorner, W., Durchschlag, E., Martinez-Pastor, M.T., Estruch, F., Ammerer, G., Hamilton, B., etal. (1998) Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12: 586-597.
29. Gorner, W., Durchschlag, E., Wolf, J., Brown, E.L., Ammerer, G., Ruis, H., and Schuller, C. (2002) Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J 21: 135-144.
30. Granek, J.A., Kayikci, O., and Magwene, P.M. (2011) Pleiotropic signaling pathways orchestrate yeast development. Curr Opin Microbiol 14: 676-681.
31. Griffioen, G., Anghileri, P., Imre, E., Baroni, M.D., and Ruis, H. (2000) Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae. J Biol Chem 275: 1449-1456.
32. Griffioen, G., Branduardi, P., Ballarini, A., Anghileri, P., Norbeck, J., Baroni, M.D., and Ruis, H. (2001) Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol Cell Biol 21: 511-523.
33. Gustin, M.C., Albertyn, J., Alexander, M., and Davenport, K. (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264-1300.
34. Heikaus, C.C., Pandit, J., and Klevit, R.E. (2009) Cyclic nucleotide binding GAF domains from phosphodiesterases: structural and mechanistic insights. Structure 17: 1551-1557.
35. Hoek, M., Zanders, T., and Cross, G.A. (2002) Trypanosoma brucei expression-site-associated-gene-8 protein interacts with a Pumilio family protein. Mol Biochem Parasitol 120: 269-283.
36. Hogan, D.A. (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5: 613-619.
37. Hughes, K., Wand, M., Foulston, L., Young, R., Harley, K., Terry, S., etal. (2007) A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J 26: 2400-2410.
38. Ikadai, H., Saliba, K.S., Kanzok, S.M., McLean, K.J., Tanaka, T.Q., Cao, J., etal. (2013) Transposon mutagenesis identifies genes essential for Plasmodium falciparum gametocytogenesis. Proc Natl Acad Sci USA 110: E1676-E1684.
39. Jones, N.G., Thomas, E.B., Brown, E., Dickens, N.J., Hammarton, T.C., and Mottram, J.C. (2014) Regulators of Trypanosoma brucei cell cycle progression and differentiation identified using a kinome-wide RNAi screen. PLoS Pathog 10: e1003886.
40. Kolev, N.G., Ramey-Butler, K., Cross, G.A., Ullu, E., and Tschudi, C. (2012) Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science 338: 1352-1353.
41. Kolev, N.G., Ullu, E., and Tschudi, C. (2014) The emerging role of RNA-binding proteins in the life cycle of Trypanosoma brucei. Cell Microbiol 16: 482-489.
42. Laxman, S., Riechers, A., Sadilek, M., Schwede, F., and Beavo, J.A. (2006) Hydrolysis products of cAMP analogs cause transformation of Trypanosoma brucei from slender to stumpy-like forms. Proc Natl Acad Sci USA 103: 19194-19199.
43. Li, Z., Tu, X., and Wang, C.C. (2006) Okadaic acid overcomes the blocked cell cycle caused by depleting Cdc2-related kinases in Trypanosoma brucei. Exp Cell Res 312: 3504-3516.
44. MacGregor, P., Savill, N.J., Hall, D., and Matthews, K.R. (2011) Transmission stages dominate trypanosome within-host dynamics during chronic infections. Cell Host Microbe 9: 310-318.
45. MacGregor, P., Szoor, B., Savill, N.J., and Matthews, K.R. (2012) Trypanosomal immune evasion, chronicity and transmission: an elegant balancing act. Nat Rev Microbiol 10: 431-438.
46. MacGregor, P., Ivens, A., Shave, S., Collie, I., Gray, D., Auer, M., and Matthews, K.R. (2014) High-throughput chemical screening for antivirulence developmental phenotypes in Trypanosoma brucei. Eukaryot Cell 13: 412-426.
47. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., etal. (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89: 737-745.
48. Mancini, P.E., and Patton, C.L. (1981) Cyclic 3′, 5′-adenosine monophosphate levels during the developmental cycle of Trypanosoma brucei brucei in the rat. Mol Biochem Parasitol 3: 19-31.
49. Moniz, L., Dutt, P., Haider, N., and Stambolic, V. (2011) Nek family of kinases in cell cycle, checkpoint control and cancer. Cell Div 6: 18.
50. Mony, B., Macgregor, P., Ivens, A., Cowton, A., Wilson, J., Horn, D., and Matthews, K. (2013) Genome wide dissection of the quorum sensing signaling pathiway in Trypanosoma brucei. Nature 505: 681-685. doi: 10.1038/nature12864
51. Nett, I.R., Martin, D.M., Miranda-Saavedra, D., Lamont, D., Barber, J.D., Mehlert, A., and Ferguson, M.A. (2009) The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol Cell Proteomics 8: 1527-1538.
52. 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.
53. Pays, E., Lips, S., Nolan, D., Vanhamme, L., and Perez-Morga, D. (2001) The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. Mol Biochem Parasitol 114: 1-16.
54. Reuner, B., Vassella, E., Yutzy, B., and Boshart, M. (1997) Cell density triggers slender to stumpy differentiation of Trypanosoma brucei bloodstream forms in culture. Mol Biochem Parasitol 90: 269-280.
55. Sanz, P., Alms, G.R., Haystead, T.A., and Carlson, M. (2000) Regulatory interactions between the Reg1-Glc7 protein phosphatase and the Snf1 protein kinase. Mol Cell Biol 20: 1321-1328.
56. Seed, J.R., and Sechelski, J.B. (1989) Mechanism of long slender (LS) to short stumpy (SS) transformation in the African trypanosomes. J Protozool 36: 572-577.
57. Sharma, R., Peacock, L., Gluenz, E., Gull, K., Gibson, W., and Carrington, M. (2008) Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist 159: 137-151.
58. Sheader, K., Vaughan, S., Minchin, J., Hughes, K., Gull, K., and Rudenko, G. (2005) Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes. Proceedings of the National Academy of Sciences of the United States of America 102: 8716-8721.
59. Simon, M.N., Pelegrini, O., Veron, M., and Kay, R.R. (1992) Mutation of protein kinase-a causes heterochronic development of dictyostelium. Nature 356: 171-172.
60. Smith, T.K., Vasileva, N., Gluenz, E., Terry, S., Portman, N., Kramer, S., Carrington, M., Michaeli, S., Gull, K., and Rudenko, G. (2009) Blocking variant surface glycoprotein synthesis in Trypanosoma brucei triggers a general arrest in translation initiation. PLoS One 4: e7532.
61. Souza, G.M., Lu, S.J., and Kuspa, A. (1998) YakA, a protein kinase required for the transition from growth to development in Dictyostelium. Development 125: 2291-2302.
62. Stanne, T.M., Kushwaha, M., Wand, M., Taylor, J.E., and Rudenko, G. (2011) TbISWI regulates multiple polymerase I (Pol I)-transcribed loci and is present at Pol II transcription boundaries in Trypanosoma brucei. Eukaryot Cell 10: 964-976.
63. Szoor, B., Wilson, J., McElhinney, H., Tabernero, L., and Matthews, K.R. (2006) Protein tyrosine phosphatase TbPTP1: a molecular switch controlling life cycle differentiation in trypanosomes. J Cell Biol 175: 293-303.
64. Szoor, B., Ruberto, I., Burchmore, R., and Matthews, K. (2010) A novel phosphatase cascade reglates differentiation in trypanosomes via a glycosomal signaling pathway. Genes Dev 24: 1306-1316.
65. Tuo, S., Nakashima, K., and Pringle, J.R. (2012) Apparent defect in yeast bud-site selection due to a specific failure to splice the pre-mRNA of a regulator of cell-type-specific transcription. PLoS ONE 7: e47621.
66. Turner, C.M. (1990) The use of experimental artefacts in African trypanosome research. Parasitol Today 6: 14-17.
67. Tyler, K.M., Matthews, K.R., and Gull, K. (2001) Anisomorphic cell division by African trypanosomes Protist, 152: 367-378.
68. Urbaniak, M.D., Martin, D.M., and Ferguson, M.A. (2013) Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 12: 2233-2244.
69. Vanhollebeke, B., Uzureau, P., Monteyne, D., Perez-Morga, D., and Pays, E. (2010) Cellular and molecular remodeling of the endocytic pathway during differentiation of Trypanosoma brucei bloodstream forms. Eukaryot Cell 9: 1272-1282.
70. Vassella, E., Reuner, B., Yutzy, B., and Boshart, M. (1997) Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J Cell Sci 110 (Part 21): 2661-2671.
71. Vassella, E., Kramer, R., Turner, C.M., Wankell, M., Modes, C., Van Den Bogaard, M., and Boshart, M. (2001) Deletion of a novel protein kinase with PX and FYVE-related domains increases the rate of differentiation of Trypanosoma brucei. Mol Microbiol 41: 33-46.
72. Winter, V., and Hauser, M.T. (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11: 115-123.
73. Zaman, S., Lippman, S.I., Zhao, X., and Broach, J.R. (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42: 27-81.