Probing the Biology of Giardia intestinalis Mitosomes Using In Vivo Enzymatic Tagging

REFERENCES

• Adam RD. 2001. Biology of Giardia lamblia. Clin Microbiol Rev 14:447–475. http://dx.doi.org/10.1128/CMR.14.3.447-475.2001.
   PubMed Web of Science ®Google Scholar
• Ankarklev J, Jerlström-Hultqvist J, Ringqvist E, Troell K, Svärd SG. 2010. Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 8:413–422. http://dx.doi.org/10.1038/nrmicro2317.
   PubMed Web of Science ®Google Scholar
• Hehl AB, Marti M. 2004. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol 53:19–28. http://dx.doi.org/10.1111/j.1365-2958.2004.04115.x.
   PubMed Web of Science ®Google Scholar
• Lanfredi-Rangel A, Attias M, de Carvalho TM, Kattenbach WM, De Souza W. 1998. The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysosomes. J Struct Biol 123:225–235. http://dx.doi.org/10.1006/jsbi.1998.4035.
   PubMedGoogle Scholar
• Konrad C, Spycher C, Hehl AB. 2010. Selective condensation drives partitioning and sequential secretion of cyst wall proteins in differentiating Giardia lamblia. PLoS Pathog 6:e1000835. http://dx.doi.org/10.1371/journal.ppat.1000835.
   PubMedGoogle Scholar
• Dolezal P, Smíd O, Rada P, Zubácová Z, Bursać D, Suták R, Nebesárová J, Lithgow T, Tachezy J. 2005. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci U S A 102:10924–10929. http://dx.doi.org/10.1073/pnas.0500349102.
   PubMedGoogle Scholar
• Jedelský PL, Doležal P, Rada P, Pyrih J, Smíd O, Hrdý I, Sedinová M, Marcinčiková M, Voleman L, Perry AJ, Beltrán NC, Lithgow T, Tachezy J. 2011. The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One 6:e17285. http://dx.doi.org/10.1371/journal.pone.0017285.
   PubMedGoogle Scholar
• Regoes A, Zourmpanou D, León-Avila G, van der Giezen M, Tovar J, Hehl AB. 2005. Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem 280:30557–30563. http://dx.doi.org/10.1074/jbc.M500787200.
   PubMedGoogle Scholar
• Roger AJ, Svärd SG, Tovar J, Clark CG, Smith MW, Gillin FD, Sogin ML. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A 95:229–234. http://dx.doi.org/10.1073/pnas.95.1.229.
   PubMed Web of Science ®Google Scholar
• Tachezy J, Sánchez LB, Müller M. 2001. Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18:1919–1928. http://dx.doi.org/10.1093/oxfordjournals.molbev.a003732.
   PubMedGoogle Scholar
• Likic VA, Dolezal P, Celik N, Dagley M, Lithgow T. 2010. Using hidden markov models to discover new protein transport machines. Methods Mol Biol 619:271–284. http://dx.doi.org/10.1007/978-1-60327-412-8_16.
   PubMedGoogle Scholar
• Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schönfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci U S A 100:13207–13212. http://dx.doi.org/10.1073/pnas.2135385100.
   PubMed Web of Science ®Google Scholar
• Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, Xie Y, Loo JA, Johnson PJ. 2011. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol 41:1421–1434. http://dx.doi.org/10.1016/j.ijpara.2011.10.001.
   PubMed Web of Science ®Google Scholar
• Panigrahi AK, Ogata Y, Zíková A, Anupama A, Dalley RA, Acestor N, Myler PJ, Stuart KD. 2009. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9:434–450. http://dx.doi.org/10.1002/pmic.200800477.
   PubMed Web of Science ®Google Scholar
• Wampfler PB, Tosevski V, Nanni P, Spycher C, Hehl AB. 2014. Proteomics of secretory and endocytic organelles in Giardia lamblia. PLoS One 9:e94089. http://dx.doi.org/10.1371/journal.pone.0094089.
   PubMedGoogle Scholar
• Keister DB. 1983. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487–488. http://dx.doi.org/10.1016/0035-9203(83)90120-7.
   PubMed Web of Science ®Google Scholar
• Martincová E, Voleman L, Najdrová V, De Napoli M, Eshar S, Gualdron M, Hopp CS, Sanin DE, Tembo DL, Van Tyne D, Walker D, Marcinčiková M, Tachezy J, Doležal P. 2012. Live imaging of mitosomes and hydrogenosomes by HaloTag technology. PLoS One 7:e36314. http://dx.doi.org/10.1371/journal.pone.0036314.
   PubMedGoogle Scholar
• Dagley MJ, Dolezal P, Likic VA, Smid O, Purcell AW, Buchanan SK, Tachezy J, Lithgow T. 2009. The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol Biol Evol 26:1941–1947. http://dx.doi.org/10.1093/molbev/msp117.
   PubMedGoogle Scholar
• Howarth M, Takao K, Hayashi Y, Ting AY. 2005. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc Natl Acad Sci U S A 102:7583–7588. http://dx.doi.org/10.1073/pnas.0503125102.
   PubMed Web of Science ®Google Scholar
• Gehde N, Hinrichs C, Montilla I, Charpian S, Lingelbach K, Przyborski JM. 2009. Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol Microbiol 71:613–628. http://dx.doi.org/10.1111/j.1365-2958.2008.06552.x.
   PubMedGoogle Scholar
• Rada P, Doležal P, Jedelský PL, Bursac D, Perry AJ, Šedinová M, Smíšková K, Novotný M, Beltrán NC, Hrdý I, Lithgow T, Tachezy J. 2011. The core components of organelle biogenesis and membrane transport in the hydrogenosomes of Trichomonas vaginalis. PLoS One 6:e24428. http://dx.doi.org/10.1371/journal.pone.0024428.
   PubMedGoogle Scholar
• Söding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248. http://dx.doi.org/10.1093/nar/gki408.
   PubMed Web of Science ®Google Scholar
• Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. http://dx.doi.org/10.1371/journal.pcbi.1002195.
   PubMed Web of Science ®Google Scholar
• Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. http://dx.doi.org/10.1186/1471-2105-9-40.
   PubMed Web of Science ®Google Scholar
• Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. http://dx.doi.org/10.1006/jmbi.2000.4315.
   PubMed Web of Science ®Google Scholar
• Käll L, Krogh A, Sonnhammer ELL. 2007. Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 35:W429–W432. http://dx.doi.org/10.1093/nar/gkm256.
   PubMed Web of Science ®Google Scholar
• Howarth M, Ting AY. 2008. Imaging proteins in live mammalian cells with biotin ligase and monovalent streptavidin. Nat Protoc 3:534–545. http://dx.doi.org/10.1038/nprot.2008.20.
   PubMed Web of Science ®Google Scholar
• Chacinska A, van der Laan M, Mehnert CS, Guiard B, Mick DU, Hutu DP, Truscott KN, Wiedemann N, Meisinger C, Pfanner N, Rehling P. 2010. Distinct forms of mitochondrial TOM-TIM supercomplexes define signal-dependent states of preprotein sorting. Mol Cell Biol 30:307–318. http://dx.doi.org/10.1128/MCB.00749-09.
   PubMed Web of Science ®Google Scholar
• Tieu Q, Okreglak V, Naylor K, Nunnari J. 2002. The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J Cell Biol 158:445–452. http://dx.doi.org/10.1083/jcb.200205031.
   PubMedGoogle Scholar
• Yoon Y, Krueger EW, Oswald BJ, McNiven MA. 2003. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23:5409–5420. http://dx.doi.org/10.1128/MCB.23.15.5409-5420.2003.
   PubMed Web of Science ®Google Scholar
• Merlin A, Voos W, Maarse AC, Meijer M, Pfanner N, Rassow J. 1999. The J-related segment of tim44 is essential for cell viability: a mutant Tim44 remains in the mitochondrial import site, but inefficiently recruits mtHsp70 and impairs protein translocation. J Cell Biol 145:961–972. http://dx.doi.org/10.1083/jcb.145.5.961.
   PubMedGoogle Scholar
• Ting S-Y, Schilke BA, Hayashi M, Craig EA. 2014. Architecture of the TIM23 inner mitochondrial translocon and interactions with the matrix import motor. J Biol Chem 289:28689–28696. http://dx.doi.org/10.1074/jbc.M114.588152.
   PubMedGoogle Scholar
• Brown A, Amunts A, Bai X-C, Sugimoto Y, Edwards PC, Murshudov G, Scheres SHW, Ramakrishnan V. 2014. Structure of the large ribosomal subunit from human mitochondria. Science 346:718–722. http://dx.doi.org/10.1126/science.1258026.
   PubMed Web of Science ®Google Scholar
• Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM. 2006. Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J 25:1603–1610. http://dx.doi.org/10.1038/sj.emboj.7601070.
   PubMedGoogle Scholar
• Lauwaet T, Davids BJ, Torres-Escobar A, Birkeland SR, Cipriano MJ, Preheim SP, Palm D, Svärd SG, McArthur AG, Gillin FD. 2007. Protein phosphatase 2A plays a crucial role in Giardia lamblia differentiation. Mol Biochem Parasitol 152:80–89. http://dx.doi.org/10.1016/j.molbiopara.2006.12.001.
   PubMedGoogle Scholar
• Cipollone R, Ascenzi P, Visca P. 2007. Common themes and variations in the rhodanese superfamily. IUBMB Life 59:51–59. http://dx.doi.org/10.1080/15216540701206859.
   PubMed Web of Science ®Google Scholar
• Bonomi F, Pagani S, Cerletti P, Cannella C. 1977. Rhodanese-mediated sulfur transfer to succinate dehydrogenase. Eur J Biochem 72:17–24. http://dx.doi.org/10.1111/j.1432-1033.1977.tb11219.x.
   PubMedGoogle Scholar
• Ohno K, Takahashi Y, Hirose F, Inoue YH, Taguchi O, Nishida Y, Matsukage A, Yamaguchi M. 2000. Characterization of a Drosophila homologue of the human myelodysplasia/myeloid leukemia factor (MLF). Gene 260:133–143. http://dx.doi.org/10.1016/S0378-1119(00)00447-9.
   PubMedGoogle Scholar
• Elias EV, Quiroga R, Gottig N, Nakanishi H, Nash TE, Neiman A, Lujan HD. 2008. Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J Biol Chem 283:35996–36010. http://dx.doi.org/10.1074/jbc.M806545200.
   PubMedGoogle Scholar
• Eilers M, Schatz G. 1986. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322:228–232.
   PubMedGoogle Scholar
• Wang CC, Aldritt S. 1983. Purine salvage networks in Giardia lamblia. J Exp Med 158:1703–1712. http://dx.doi.org/10.1084/jem.158.5.1703.
   PubMedGoogle Scholar
• van der Giezen M, Tovar J. 2005. Degenerate mitochondria. EMBO Rep 6:525–530. http://dx.doi.org/10.1038/sj.embor.7400440.
   PubMed Web of Science ®Google Scholar
• Clements A, Bursac D, Gatsos X, Perry AJ, Civciristov S, Celik N, Likic VA, Poggio S, Jacobs-Wagner C, Strugnell RA, Lithgow T. 2009. The reducible complexity of a mitochondrial molecular machine. Proc Natl Acad Sci U S A 106:15791–15795. http://dx.doi.org/10.1073/pnas.0908264106.
   PubMedGoogle Scholar
• Schey KL, Grey AC, Nicklay JJ. 2013. Mass spectrometry of membrane proteins: a focus on aquaporins. Biochemistry 52:3807–3817. http://dx.doi.org/10.1021/bi301604j.
   PubMed Web of Science ®Google Scholar
• Xu F, Jerlström-Hultqvist J, Einarsson E, Astvaldsson A, Svärd SG, Andersson JO. 2014. The genome of Spironucleus salmonicida highlights a fish pathogen adapted to fluctuating environments. PLoS Genet 10:e1004053. http://dx.doi.org/10.1371/journal.pgen.1004053.
   PubMedGoogle Scholar
• Dolezal P, Dagley MJ, Kono M, Wolynec P, Likić VA, Foo JH, Sedinová M, Tachezy J, Bachmann A, Bruchhaus I, Lithgow T. 2010. The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6:e1000812. http://dx.doi.org/10.1371/journal.ppat.1000812.
   PubMedGoogle Scholar
• Waller RF, Jabbour C, Chan NC, Celik N, Likic VA, Mulhern TD, Lithgow T. 2009. Evidence of a reduced and modified mitochondrial protein import apparatus in microsporidian mitosomes. Eukaryot Cell 8:19–26. http://dx.doi.org/10.1128/EC.00313-08.
   PubMedGoogle Scholar
• Handa N, Kishishita S, Morita S, Akasaka R, Jin Z, Chrzas J, Chen L, Liu Z-J, Wang B-C, Sugano S, Tanaka A, Terada T, Shirouzu M, Yokoyama S. 2007. Structure of the human Tim44 C-terminal domain in complex with pentaethylene glycol: ligand-bound form. Acta Crystallogr D Biol Crystallogr 63:1225–1234. http://dx.doi.org/10.1107/S0907444907051463.
   PubMedGoogle Scholar
• Zarsky V, Tachezy J, Dolezal P. 2012. Tom40 is likely common to all mitochondria. Curr Biol 22:R479–R481; author reply, R481–R482. http://dx.doi.org/10.1016/j.cub.2012.03.057.
   PubMedGoogle Scholar
• Baker KP, Schaniel A, Vestweber D, Schatz G. 1990. A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature 348:605–609. http://dx.doi.org/10.1038/348605a0.
   PubMed Web of Science ®Google Scholar
• Yamano K, Tanaka-Yamano S, Endo T. 2010. Mdm10 as a dynamic constituent of the TOB/SAM complex directs coordinated assembly of Tom40. EMBO Rep 11:187–193. http://dx.doi.org/10.1038/embor.2009.283.
   PubMedGoogle Scholar
• Yano M, Kanazawa M, Terada K, Namchai C, Yamaizumi M, Hanson B, Hoogenraad N, Mori M. 1997. Visualization of mitochondrial protein import in cultured mammalian cells with green fluorescent protein and effects of overexpression of the human import receptor Tom20. J Biol Chem 272:8459–8465. http://dx.doi.org/10.1074/jbc.272.13.8459.
   PubMedGoogle Scholar
• Rojo M, Legros F, Chateau D, Lombès A. 2002. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J Cell Sci 115:1663–1674.
   PubMed Web of Science ®Google Scholar
• Dolezal P, Likic V, Tachezy J, Lithgow T. 2006. Evolution of the molecular machines for protein import into mitochondria. Science 313:314–318. http://dx.doi.org/10.1126/science.1127895.
   PubMed Web of Science ®Google Scholar
• Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278:48520–48523. http://dx.doi.org/10.1074/jbc.C300442200.
   PubMed Web of Science ®Google Scholar
• Gentle I, Gabriel K, Beech P, Waller R, Lithgow T. 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164:19–24. http://dx.doi.org/10.1083/jcb.200310092.
   PubMed Web of Science ®Google Scholar
• Josyula R, Jin Z, Fu Z, Sha B. 2006. Crystal structure of yeast mitochondrial peripheral membrane protein Tim44p C-terminal domain. J Mol Biol 359:798–804. http://dx.doi.org/10.1016/j.jmb.2006.04.020.
   PubMedGoogle Scholar
• Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. http://dx.doi.org/10.1093/nar/gku340.
   PubMed Web of Science ®Google Scholar