Proteomic analysis of acidocalcisomes of Trypanosoma brucei uncovers their role in phosphate metabolism, cation homeostasis, and calcium signaling

References

• Vercesi AE, Moreno SN, Docampo R. Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei. Biochem J 1994; 304:227-33; PMID:7998937
   PubMed Web of Science ®Google Scholar
• Docampo R, Scott DA, Vercesi AE, Moreno SN. Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem J 1995; 310:1005-12; PMID:7575396
   PubMed Web of Science ®Google Scholar
• Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN. Acidocalcisomes – conserved from bacteria to man. Nat Rev Microbiol 2005; 3:251-261; PMID:15738951; http://dx.doi.org/10.1038/nrmicro1097
   PubMed Web of Science ®Google Scholar
• Babes V. Beobachtungen über die metachromatischen körperchen, sporenbildung, verzwiegung, kolben- und kapsel-bildung pathogener bakterien. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 1895; 20:412-20
   Google Scholar
• Meyer A. Orientierende untersuchungen über verbreitung, morphologie und chemie des volutins. Bot Zeit 1904; 62:113-52
   Google Scholar
• Seufferheld M, Lea CR, Vieira M, Oldfield E, Docampo R. The H+-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J Biol Chem 2004; 279:51193-202; PMID:15371423; http://dx.doi.org/10.1074/jbc.M406099200
   PubMed Web of Science ®Google Scholar
• Seufferheld M, Vieira MC, Ruiz FA, Rodrigues CO, Moreno SN, Docampo R. Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J Biol Chem 2003; 278:29971-78; PMID:12783865; http://dx.doi.org/10.1074/jbc.M304548200
   PubMed Web of Science ®Google Scholar
• Yang L, Ding Y, Chen Y, Zhang S, Huo C, Wang Y, Yu J, Zhang P, Na H, Zhang H, et al. The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans. J Lipid Res 2012; 53:1245-53; PMID:22534641; http://dx.doi.org/10.1194/jlr.R024117
   PubMed Web of Science ®Google Scholar
• Docampo R, Moreno SN. Acidocalcisomes. Cell Calcium 2011; 50:113-9; PMID:21752464; http://dx.doi.org/10.1016/j.ceca.2011.05.012
   PubMed Web of Science ®Google Scholar
• Moreno SN, Docampo R. The role of acidocalcisomes in parasitic protists. J Eukaryot Microbiol 2009; 56:208-13; PMID:19527347; http://dx.doi.org/10.1111/j.1550-7408.2009.00404.x
   PubMed Web of Science ®Google Scholar
• Huang G, Ulrich PN, Storey M, Johnson D, Tischer J, Tovar JA, Moreno SN, Orlando R, Docampo R. Proteomic analysis of the acidocalcisome, an organelle conserved from bacteria to human cells. PLoS Pathog 2014; 10:e1004555; PMID:25503798; http://dx.doi.org/10.1371/journal.ppat.1004555
   PubMedGoogle Scholar
• Maeshima M. Vacuolar H+-pyrophosphatase. Biochim Biophys Acta 2000; 1465:37-51; PMID:10748246; http://dx.doi.org/10.1016/S0005-2736(00)00130-9
   PubMed Web of Science ®Google Scholar
• Miranda K, Pace DA, Cintron R, Rodrigues JC, Fang J, Smith A, Rohloff P, Coelho E, de Haas F, de Souza W, et al. Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 2010; 76:1358-75; PMID:20398214; http://dx.doi.org/10.1111/j.1365-2958.2010.07165.x
   PubMed Web of Science ®Google Scholar
• Saliba KJ, Allen RJ, Zissis S, Bray PG, Ward SA, Kirk K. Acidification of the malaria parasite's digestive vacuole by a H+-ATPase and a H+-pyrophosphatase. J Biol Chem 2003; 278:5605-12; PMID:12427765; http://dx.doi.org/10.1074/jbc.M208648200
   PubMed Web of Science ®Google Scholar
• Ruiz FA, Rodrigues CO, Docampo R. Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J Biol Chem 2001; 276:26114-21; PMID:11371561; http://dx.doi.org/10.1074/jbc.M102402200
   PubMed Web of Science ®Google Scholar
• Rodrigues CO, Scott DA, Docampo R. Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes. Mol Cell Biol 1999; 19:7712-23; PMID:10523660
   PubMed Web of Science ®Google Scholar
• Salto ML, Kuhlenschmidt T, Kuhlenschmidt M, de Lederkremer RM, Docampo R. Phospholipid and glycolipid composition of acidocalcisomes of Trypanosoma cruzi. Mol Biochem Parasitol 2008; 158:120-30; PMID:18207579; http://dx.doi.org/10.1016/j.molbiopara.2007.12.001
   PubMed Web of Science ®Google Scholar
• Yagisawa F, Nishida K, Yoshida M, Ohnuma M, Shimada T, Fujiwara T, Yoshida Y, Misumi O, Kuroiwa H, Kuroiwa T. Identification of novel proteins in isolated polyphosphate vacuoles in the primitive red alga Cyanidioschyzon merolae. Plant J 2009; 60:882-93; PMID:19709388; http://dx.doi.org/10.1111/j.1365-313X.2009.04008.x
   PubMed Web of Science ®Google Scholar
• Lemercier G, Dutoya S, Luo S, Ruiz FA, Rodrigues CO, Baltz T, Docampo R, Bakalara N. A vacuolar-type H+-pyrophosphatase governs maintenance of functional acidocalcisomes and growth of the insect and mammalian forms of Trypanosoma brucei. J Biol Chem 2002; 277:37369-76; PMID:12121996; http://dx.doi.org/10.1074/jbc.M204744200
   PubMed Web of Science ®Google Scholar
• Luo S, Rohloff P, Cox J, Uyemura SA, Docampo R. Trypanosoma brucei plasma membrane-type Ca2+-ATPase 1 (TbPMC1) and 2 (TbPMC2) genes encode functional Ca2+-ATPases localized to the acidocalcisomes and plasma membrane, and essential for Ca2+ homeostasis and growth. J Biol Chem 2004; 279:14427-39; PMID:14724285; http://dx.doi.org/10.1074/jbc.M309978200
   PubMed Web of Science ®Google Scholar
• 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; 110:1887-92; PMID:23319604; http://dx.doi.org/10.1073/pnas.1216955110
   PubMed Web of Science ®Google Scholar
• Lander N, Ulrich PN, Docampo R. Trypanosoma brucei vacuolar transporter chaperone 4 (TbVtc4) Is an acidocalcisome polyphosphate kinase required for in vivo infection. J Biol Chem 2013; 288:34205-16
   PubMed Web of Science ®Google Scholar
• Lemercier G, Espiau B, Ruiz FA, Vieira M, Luo S, Baltz T, Docampo R, Bakalara N. A pyrophosphatase regulating polyphosphate metabolism in acidocalcisomes is essential for Trypanosoma brucei virulence in mice. J Biol Chem 2004; 279:3420-5; PMID:14615483; http://dx.doi.org/10.1074/jbc.M309974200
   PubMed Web of Science ®Google Scholar
• Ferella M, Nilsson D, Darban H, Rodrigues C, Bontempi EJ, Docampo R, Andersson B. Proteomics in Trypanosoma cruzi–localization of novel proteins to various organelles. Proteomics 2008; 8:2735-49; PMID:18546153; http://dx.doi.org/10.1002/pmic.200700940
   PubMed Web of Science ®Google Scholar
• Li L, Chen OS, McVey Ward D, Kaplan J. CCC1 is a transporter that mediates vacuolar iron storage in yeast. J Biol Chem 2001; 276:29515-9; PMID:11390404; http://dx.doi.org/10.1074/jbc.M103944200
   PubMed Web of Science ®Google Scholar
• Hasne MP, Coppens I, Soysa R, Ullman B. A high-affinity putrescine-cadaverine transporter from Trypanosoma cruzi. Mol Microbiol 2010; 76:78-91; PMID:20149109; http://dx.doi.org/10.1111/j.1365-2958.2010.07081.x
   PubMed Web of Science ®Google Scholar
• Aksoy M, Pootakham W, Grossman AR. Critical function of a Chlamydomonas reinhardtii putative polyphosphate polymerase subunit during nutrient deprivation. Plant Cell 2014; 26:4214-29; PMID:25281687; http://dx.doi.org/10.1105/tpc.114.129270
   PubMed Web of Science ®Google Scholar
• Fang J, Rohloff P, Miranda K, Docampo R. Ablation of a small transmembrane protein of Trypanosoma brucei (TbVTC1) involved in the synthesis of polyphosphate alters acidocalcisome biogenesis and function, and leads to a cytokinesis defect. Biochem J 2007; 407:161-70; PMID:17635107; http://dx.doi.org/10.1042/BJ20070612
   PubMed Web of Science ®Google Scholar
• Miranda K, Benchimol M, Docampo R, de Souza W. The fine structure of acidocalcisomes in Trypanosoma cruzi. Parasitol Res 2000; 86:373-384; PMID:10836511; http://dx.doi.org/10.1007/s004360050682
   PubMed Web of Science ®Google Scholar
• Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. Organization and function of membrane contact sites. Biochim Biophys Acta 2013; 1833:2526-41; PMID:23380708; http://dx.doi.org/10.1016/j.bbamcr.2013.01.028
   PubMed Web of Science ®Google Scholar
• Scott DA, Docampo R. Characterization of isolated acidocalcisomes of Trypanosoma cruzi. J Biol Chem 2000; 275:24215-21; PMID:10816577; http://dx.doi.org/10.1074/jbc.M002454200
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Enomoto M, Morales J, Kurebayashi N, Sakurai T, Hashimoto T, Nara T, Mikoshiba K. Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi. Mol Microbiol 2013; 87:1133-1150; PMID:23320762; http://dx.doi.org/10.1111/mmi.12155
   PubMed Web of Science ®Google Scholar
• Docampo R, Moreno SN, Plattner H. Intracellular calcium channels in protozoa. Eur J Pharmacol 2014; 739:4-18; PMID:24291099; http://dx.doi.org/10.1016/j.ejphar.2013.11.015
   PubMed Web of Science ®Google Scholar
• Ulrich PN, Lander N, Kurup S, Reiss L, Brewer J, Soares Medeiros LC, Miranda K, Docampo R. The aciodcalcisome vacuolar transporter chaperone 4 catalyzes the synthesis of polyphosphate in insect-stages of Trypanosoma brucei and T. cruzi. J Eukaryot Microbiol 2014; 61:155-65; PMID:24386955; http://dx.doi.org/10.1111/jeu.12093
   PubMed Web of Science ®Google Scholar
• Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, Uttenweiler A, Reinhardt M, Schmidt A, Seiler J, et al. Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 2009 324:513-6; PMID:19390046; http://dx.doi.org/10.1126/science.1168120
   PubMed Web of Science ®Google Scholar
• Gerasimaite R, Sharma S, Desfougeres Y, Schmidt A, Mayer A. Coupled synthesis and translocation restrains polyphosphate to acidocalcisome-like vacuoles and prevents its toxicity. J Cell Sci 2014; 127:5093-104; PMID:25315834; http://dx.doi.org/10.1242/jcs.159772
   PubMed Web of Science ®Google Scholar
• Hurlimann HC, Stadler-Waibel M, Werner TP, Freimoser FM. Pho91 Is a vacuolar phosphate transporter that regulates phosphate and polyphosphate metabolism in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18:4438-45; PMID:17804816; http://dx.doi.org/10.1091/mbc.E07-05-0457
   PubMed Web of Science ®Google Scholar
• Vercesi AE, Docampo R. Sodium-proton exchange stimulates Ca2+ release from acidocalcisomes of Trypanosoma brucei. Biochem J 1996; 315:265-70; PMID:8670117
   PubMed Web of Science ®Google Scholar
• Vercesi AE, Grijalba MT, Docampo R. Inhibition of Ca2+ release from Trypanosoma brucei acidocalcisomes by 3,5-dibutyl-4-hydroxytoluene: role of the Na+/H+ exchanger. Biochem J 1997; 328:479-82; PMID:9371704
   PubMed Web of Science ®Google Scholar
• MacDiarmid CW, Gaither LA, Eide D. Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 2000; 19:2845-55; PMID:10856230; http://dx.doi.org/10.1093/emboj/19.12.2845
   PubMed Web of Science ®Google Scholar
• Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 2006; 314:1295-8; PMID:17082420; http://dx.doi.org/10.1126/science.1132563
   PubMed Web of Science ®Google Scholar
• Tomitori H, Kashiwagi K, Asakawa T, Kakinuma Y, Michael AJ, Igarashi K. Multiple polyamine transport systems on the vacuolar membrane in yeast. Biochem J 2001; 353:681-8; PMID:11171066; http://dx.doi.org/10.1042/0264-6021:3530681
   PubMed Web of Science ®Google Scholar
• Ruiz FA, Marchesini N, Seufferheld M, Govindjee, Docampo R. The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 2001; 276:46196-203; PMID:11579086; http://dx.doi.org/10.1074/jbc.M105268200
   PubMed Web of Science ®Google Scholar
• Hong-Hermesdorf A, Miethke M, Gallaher SD, Kropat J, Dodani SC, Chan J, Barupala D, Domaille DW, Shirasaki DI, Loo JA, et al. Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. Nat Chem Biol 2014; 10:1034-42; PMID:25344811; http://dx.doi.org/10.1038/nchembio.1662
   PubMed Web of Science ®Google Scholar
• Huang G, Fang J, Sant'Anna C, Li ZH, Wellems DL, Rohloff P, Docampo R. Adaptor protein-3 (AP-3) complex mediates the biogenesis of acidocalcisomes and is essential for growth and virulence of Trypanosoma brucei. J Biol Chem 2011; 286:36619-30; PMID:21880705; http://dx.doi.org/10.1074/jbc.M111.284661
   PubMed Web of Science ®Google Scholar
• Li FJ, He CY. Acidocalcisome is required for autophagy in Trypanosoma brucei. Autophagy 2014; 10:1978-88; PMID:25484093; http://dx.doi.org/10.4161/auto.36183
   PubMed Web of Science ®Google Scholar
• Galizzi M, Bustamante JM, Fang J, Miranda K, Soares Medeiros LC, Tarleton RL, Docampo R. Evidence for the role of vacuolar soluble pyrophosphatase and inorganic polyphosphate in Trypanosoma cruzi persistence. Mol Microbiol 2013; 90:699-715; PMID:24033456; http://dx.doi.org/10.1111/mmi.12392
   PubMed Web of Science ®Google Scholar