Phosphoinositide signaling and regulation in Trypanosoma brucei: Specialized functions in a protozoan pathogen

1. Stuart K, Brun R, Croft S, Fairlamb A, Gurtler RE, McKerrow J, et al. Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest. 2008;118(4):1301–10. doi: 10.1172/JCI33945 18382742; PubMed Central PMCID: PMC2276762.

2. Saldivia M, Ceballos-Perez G, Bart JM, Navarro M. The AMPKalpha1 Pathway Positively Regulates the Developmental Transition from Proliferation to Quiescence in Trypanosoma brucei. Cell Rep. 2016;17(3):660–70. doi: 10.1016/j.celrep.2016.09.041 27732844; PubMed Central PMCID: PMC5074416.

3. Barquilla A, Saldivia M, Diaz R, Bart JM, Vidal I, Calvo E, et al. Third target of rapamycin complex negatively regulates development of quiescence in Trypanosoma brucei. Proc Natl Acad Sci U S A. 2012;109(36):14399–404. doi: 10.1073/pnas.1210465109 22908264; PubMed Central PMCID: PMC3437835.

4. Cestari I, Stuart K. Transcriptional Regulation of Telomeric Expression Sites and Antigenic Variation in Trypanosomes. Curr Genomics. 2018;19(2):119–32. Epub 2018/03/02. doi: 10.2174/1389202918666170911161831 29491740; PubMed Central PMCID: PMC5814960.

5. Cestari I, McLeland-Wieser H, Stuart K. Nuclear Phosphatidylinositol 5-Phosphatase Is Essential for Allelic Exclusion of Variant Surface Glycoprotein Genes in Trypanosomes. Mol Cell Biol. 2019;39(3). Epub 2018/11/14. doi: 10.1128/MCB.00395-18 30420356; PubMed Central PMCID: PMC6336139.

6. Cestari I, Anupama A, Stuart K. Inositol polyphosphate multikinase regulation of Trypanosoma brucei life stage development. Mol Biol Cell. 2018;29(9):1137–52. Epub 2018/03/09. doi: 10.1091/mbc.E17-08-0515 29514930; PubMed Central PMCID: PMC5921579.

7. Cestari I, Stuart K. Inositol phosphate pathway controls transcription of telomeric expression sites in trypanosomes. Proc Natl Acad Sci U S A. 2015;112(21):E2803–12. doi: 10.1073/pnas.1501206112 25964327; PubMed Central PMCID: PMC4450425.

8. Szoor B, Ruberto I, Burchmore R, Matthews KR. A novel phosphatase cascade regulates differentiation in Trypanosoma brucei via a glycosomal signaling pathway. Genes Dev. 2010;24(12):1306–16. Epub 2010/06/17. doi: 10.1101/gad.570310 20551176; PubMed Central PMCID: PMC2885665.

9. Gilden JK, Umaer K, Kruzel EK, Hecht O, Correa RO, Mansfield JM, et al. The role of the PI(3,5)P2 kinase TbFab1 in endo/lysosomal trafficking in Trypanosoma brucei. Mol Biochem Parasitol. 2017;214:52–61. Epub 2017/03/31. doi: 10.1016/j.molbiopara.2017.03.005 28356223; PubMed Central PMCID: PMC5474170.

10. Hall BS, Gabernet-Castello C, Voak A, Goulding D, Natesan SK, Field MC. TbVps34, the trypanosome orthologue of Vps34, is required for Golgi complex segregation. J Biol Chem. 2006;281(37):27600–12. doi: 10.1074/jbc.M602183200 16835237.

11. Rodgers MJ, Albanesi JP, Phillips MA. Phosphatidylinositol 4-kinase III-beta is required for Golgi maintenance and cytokinesis in Trypanosoma brucei. Eukaryot Cell. 2007;6(7):1108–18. doi: 10.1128/EC.00107-07 17483288; PubMed Central PMCID: PMC1951100.

12. Huang G, Bartlett PJ, Thomas AP, Moreno SN, Docampo R. Acidocalcisomes of Trypanosoma brucei have an inositol 1,4,5-trisphosphate receptor that is required for growth and infectivity. Proc Natl Acad Sci U S A. 2013;110(5):1887–92. doi: 10.1073/pnas.1216955110 23319604; PubMed Central PMCID: PMC3562765.

13. Cestari I, Haas P, Moretti NS, Schenkman S, Stuart K. Chemogenetic Characterization of Inositol Phosphate Metabolic Pathway Reveals Druggable Enzymes for Targeting Kinetoplastid Parasites. Cell Chem Biol. 2016;23(5):608–17. doi: 10.1016/j.chembiol.2016.03.015 27133314; PubMed Central PMCID: PMC4876820.

14. Martin KL, Smith TK. The myo-inositol-1-phosphate synthase gene is essential in Trypanosoma brucei. Biochem Soc Trans. 2005;33(Pt 5):983–5. doi: 10.1042/BST20050983 16246027.

15. Martin KL, Smith TK. Phosphatidylinositol synthesis is essential in bloodstream form Trypanosoma brucei. Biochem J. 2006;396(2):287–95. doi: 10.1042/BJ20051825 16475982; PubMed Central PMCID: PMC1462709.

16. Steger DJ, Haswell ES, Miller AL, Wente SR, O'Shea EK. Regulation of chromatin remodeling by inositol polyphosphates. Science. 2003;299(5603):114–6. doi: 10.1126/science.1078062 12434012; PubMed Central PMCID: PMC1458531.

17. Szijgyarto Z, Garedew A, Azevedo C, Saiardi A. Influence of inositol pyrophosphates on cellular energy dynamics. Science. 2011;334(6057):802–5. doi: 10.1126/science.1211908 22076377.

18. Cordeiro CD, Saiardi A, Docampo R. The inositol pyrophosphate synthesis pathway in Trypanosoma brucei is linked to polyphosphate synthesis in acidocalcisomes. Mol Microbiol. 2017;106(2):319–33. Epub 2017/08/10. doi: 10.1111/mmi.13766 28792096; PubMed Central PMCID: PMC5630508.

19. Hashimoto M, Enomoto M, Morales J, Kurebayashi N, Sakurai T, Hashimoto T, et al. Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi. Mol Microbiol. 2013;87(6):1133–50. doi: 10.1111/mmi.12155 23320762.

20. Morii H, Ogawa M, Fukuda K, Taniguchi H. Ubiquitous distribution of phosphatidylinositol phosphate synthase and archaetidylinositol phosphate synthase in Bacteria and Archaea, which contain inositol phospholipid. Biochem Biophys Res Commun. 2014;443(1):86–90. Epub 2013/11/26. doi: 10.1016/j.bbrc.2013.11.054 24269814.

21. Pires-daSilva A, Sommer RJ. The evolution of signalling pathways in animal development. Nat Rev Genet. 2003;4(1):39–49. Epub 2003/01/02. doi: 10.1038/nrg977 12509752.

22. Patterson RL, Boehning D, Snyder SH. Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu Rev Biochem. 2004;73:437–65. Epub 2004/06/11. doi: 10.1146/annurev.biochem.73.071403.161303 15189149.

23. Ladenburger EM, Korn I, Kasielke N, Wassmer T, Plattner H. An Ins(1,4,5)P3 receptor in Paramecium is associated with the osmoregulatory system. J Cell Sci. 2006;119(Pt 17):3705–17. Epub 2006/08/17. doi: 10.1242/jcs.03075 16912081.

24. Denis V, Cyert MS. Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol. 2002;156(1):29–34. Epub 2002/01/10. doi: 10.1083/jcb.200111004 11781332; PubMed Central PMCID: PMC2173594.

25. Odom AR, Stahlberg A, Wente SR, York JD. A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science. 2000;287(5460):2026–9. Epub 2000/03/17. doi: 10.1126/science.287.5460.2026 10720331.

26. Millard CJ, Watson PJ, Celardo I, Gordiyenko Y, Cowley SM, Robinson CV, et al. Class I HDACs share a common mechanism of regulation by inositol phosphates. Mol Cell. 2013;51(1):57–67. doi: 10.1016/j.molcel.2013.05.020 23791785; PubMed Central PMCID: PMC3710971.

27. Wu M, Chong LS, Perlman DH, Resnick AC, Fiedler D. Inositol polyphosphates intersect with signaling and metabolic networks via two distinct mechanisms. Proc Natl Acad Sci U S A. 2016;113(44):E6757–E65. Epub 2016/11/03. doi: 10.1073/pnas.1606853113 27791083; PubMed Central PMCID: PMC5098652.

28. Ginger ML. Niche metabolism in parasitic protozoa. Philos Trans R Soc Lond B Biol Sci. 2006;361(1465):101–18. doi: 10.1098/rstb.2005.1756 16553311; PubMed Central PMCID: PMC1626543.

29. Kolev NG, Ramey-Butler K, Cross GA, Ullu E, Tschudi C. Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein. Science. 2012;338(6112):1352–3. doi: 10.1126/science.1229641 23224556; PubMed Central PMCID: PMC3664091.

30. Mugo E, Egler F, Clayton C. Conversion of procyclic-form Trypanosoma brucei to the bloodstream form by transient expression of RBP10. Mol Biochem Parasitol. 2017;216:49–51. Epub 2017/06/28. doi: 10.1016/j.molbiopara.2017.06.009 28651963.

31. Bang S, Kim S, Dailey MJ, Chen Y, Moran TH, Snyder SH, et al. AMP-activated protein kinase is physiologically regulated by inositol polyphosphate multikinase. Proc Natl Acad Sci U S A. 2012;109(2):616–20. doi: 10.1073/pnas.1119751109 22203993; PubMed Central PMCID: PMC3258619.

32. Kim S, Kim SF, Maag D, Maxwell MJ, Resnick AC, Juluri KR, et al. Amino acid signaling to mTOR mediated by inositol polyphosphate multikinase. Cell Metab. 2011;13(2):215–21. Epub 2011/02/03. doi: 10.1016/j.cmet.2011.01.007 21284988; PubMed Central PMCID: PMC3042716.

33. Devlin R, Marques CA, McCulloch R. Does DNA replication direct locus-specific recombination during host immune evasion by antigenic variation in the African trypanosome? Curr Genet. 2017;63(3):441–9. Epub 2016/11/09. doi: 10.1007/s00294-016-0662-7 27822899; PubMed Central PMCID: PMC5422504.

34. Irvine RF. Nuclear lipid signalling. Nat Rev Mol Cell Biol. 2003;4(5):349–60. doi: 10.1038/nrm1100 12728269.

35. Mellman DL, Gonzales ML, Song C, Barlow CA, Wang P, Kendziorski C, et al. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature. 2008;451(7181):1013–7. Epub 2008/02/22. doi: 10.1038/nature06666 18288197.

36. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol. 2008;9(2):99–111. doi: 10.1038/nrm2328 18216767.

37. Lin A, Hu Q, Li C, Xing Z, Ma G, Wang C, et al. The LINK-A lncRNA interacts with PtdIns(3,4,5)P3 to hyperactivate AKT and confer resistance to AKT inhibitors. Nat Cell Biol. 2017;19(3):238–51. Epub 2017/02/22. doi: 10.1038/ncb3473 28218907; PubMed Central PMCID: PMC5332298.