Previous Article | Next Article 
Molecular and Cellular Biology, March 1999, p. 2198-2205, Vol. 19, No. 3
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Hsp60 Is Targeted to a Cryptic
Mitochondrion-Derived Organelle ("Crypton") in the Microaerophilic
Protozoan Parasite Entamoeba histolytica
Zhiming
Mai,1
Sudip
Ghosh,1
Marta
Frisardi,1
Ben
Rosenthal,1
Rick
Rogers,2 and
John
Samuelson1,*
Department of Immunology and Infectious
Diseases1 and BioMedical Imaging
Institute,2 Harvard School of Public Health,
Boston, Massachusetts 02115
Received 2 October 1998/Returned for modification 22 November
1998/Accepted 1 December 1998
Entamoeba histolytica is a microaerophilic protozoan
parasite in which neither mitochondria nor mitochondrion-derived
organelles have been previously observed. Recently, a segment of an
E. histolytica gene was identified that encoded a protein
similar to the mitochondrial 60-kDa heat shock protein (Hsp60 or
chaperonin 60), which refolds nuclear-encoded proteins after passage
through organellar membranes. The possible function and localization of
the amebic Hsp60 were explored here. Like Hsp60 of mitochondria, amebic
Hsp60 RNA and protein were both strongly induced by incubating
parasites at 42°C. 5' and 3' rapid amplifications of cDNA ends were
used to obtain the entire E. histolytica hsp60 coding
region, which predicted a 536-amino-acid Hsp60. The E. histolytica hsp60 gene protected from heat shock
Escherichia coli groEL mutants, demonstrating the
chaperonin function of the amebic Hsp60. The E. histolytica Hsp60, which lacked characteristic carboxy-terminal Gly-Met repeats, had a 21-amino-acid amino-terminal, organelle-targeting presequence that was cleaved in vivo. This presequence was necessary to target Hsp60 to one (and occasionally two or three) short, cylindrical organelle(s). In contrast, amebic alcohol dehydrogenase 1 and ferredoxin, which are bacteria-like enzymes, were diffusely distributed throughout the cytosol. We suggest that the Hsp60-associated, mitochondrion-derived organelle identified here be named "crypton," as its structure was previously hidden and its function is still cryptic.
*
Corresponding author. Mailing address: Department of
Immunology and Infectious Diseases, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115. Phone: (617) 432-4670. Fax:
(617) 738-4914. E-mail: jsamuels{at}hsph.harvard.edu.
Molecular and Cellular Biology, March 1999, p. 2198-2205, Vol. 19, No. 3
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Hjort, K., Goldberg, A. V., Tsaousis, A. D., Hirt, R. P., Embley, T. M.
(2010). Diversity and reductive evolution of mitochondria among microbial eukaryotes. Phil Trans R Soc B
365: 713-727
[Abstract]
[Full Text]
-
Lithgow, T., Schneider, A.
(2010). Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Phil Trans R Soc B
365: 799-817
[Abstract]
[Full Text]
-
Mi-ichi, F., Yousuf, M. A., Nakada-Tsukui, K., Nozaki, T.
(2009). Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc. Natl. Acad. Sci. USA
106: 21731-21736
[Abstract]
[Full Text]
-
Perez-Brocal, V., Clark, C. G.
(2008). Analysis of Two Genomes from the Mitochondrion-Like Organelle of the Intestinal Parasite Blastocystis: Complete Sequences, Gene Content, and Genome Organization. Mol Biol Evol
25: 2475-2482
[Abstract]
[Full Text]
-
Mentel, M., Martin, W.
(2008). Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Phil Trans R Soc B
363: 2717-2729
[Abstract]
[Full Text]
-
Ali, V., Nozaki, T.
(2007). Current Therapeutics, Their Problems, and Sulfur-Containing-Amino-Acid Metabolism as a Novel Target against Infections by "Amitochondriate" Protozoan Parasites. Clin. Microbiol. Rev.
20: 164-187
[Abstract]
[Full Text]
-
Satrustegui, J., Pardo, B., del Arco, A.
(2007). Mitochondrial Transporters as Novel Targets for Intracellular Calcium Signaling. Physiol. Rev.
87: 29-67
[Abstract]
[Full Text]
-
Burri, L., Williams, B. A. P., Bursac, D., Lithgow, T., Keeling, P. J.
(2006). Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc. Natl. Acad. Sci. USA
103: 15916-15920
[Abstract]
[Full Text]
-
Weber, C., Guigon, G., Bouchier, C., Frangeul, L., Moreira, S., Sismeiro, O., Gouyette, C., Mirelman, D., Coppee, J. Y., Guillen, N.
(2006). Stress by Heat Shock Induces Massive Down Regulation of Genes and Allows Differential Allelic Expression of the Gal/GalNAc Lectin in Entamoeba histolytica. Eukaryot Cell
5: 871-875
[Abstract]
[Full Text]
-
Ginger, M. L
(2006). Niche metabolism in parasitic protozoa. Phil Trans R Soc B
361: 101-118
[Abstract]
[Full Text]
-
Hampl, V., Horner, D. S., Dyal, P., Kulda, J., Flegr, J., Foster, P. G., Embley, T. M.
(2005). Inference of the Phylogenetic Position of Oxymonads Based on Nine Genes: Support for Metamonada and Excavata. Mol Biol Evol
22: 2508-2518
[Abstract]
[Full Text]
-
van der Giezen, M., Leon-Avila, G., Tovar, J.
(2005). Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiology
151: 3107-3115
[Abstract]
[Full Text]
-
Dolezal, P., Smid, O., Rada, P., Zubacova, Z., Bursac, D., Sutak, R., Nebesarova, J., Lithgow, T., Tachezy, J.
(2005). Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl. Acad. Sci. USA
102: 10924-10929
[Abstract]
[Full Text]
-
Samuelson, J., Banerjee, S., Magnelli, P., Cui, J., Kelleher, D. J., Gilmore, R., Robbins, P. W.
(2005). The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc. Natl. Acad. Sci. USA
102: 1548-1553
[Abstract]
[Full Text]
-
Yarlett, N.
(2004). Anaerobic protists and hidden mitochondria. Microbiology
150: 1127-1129
[Full Text]
-
Leon-Avila, G., Tovar, J.
(2004). Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology
150: 1245-1250
[Abstract]
[Full Text]
-
LaGier, M. J., Tachezy, J., Stejskal, F., Kutisova, K., Keithly, J. S.
(2003). Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology
149: 3519-3530
[Abstract]
[Full Text]
-
Tokoro, M., Asai, T., Kobayashi, S., Takeuchi, T., Nozaki, T.
(2003). Identification and Characterization of Two Isoenzymes of Methionine {gamma}-Lyase from Entamoeba histolytica: A KEY ENZYME OF SULFUR-AMINO ACID DEGRADATION IN AN ANAEROBIC PARASITIC PROTIST THAT LACKS FORWARD AND REVERSE TRANS-SULFURATION PATHWAYS. J. Biol. Chem.
278: 42717-42727
[Abstract]
[Full Text]
-
Satish, S., Bakre, A. A., Bhattacharya, S., Bhattacharya, A.
(2003). Stress-Dependent Expression of a Polymorphic, Charged Antigen in the Protozoan Parasite Entamoeba histolytica. Infect. Immun.
71: 4472-4486
[Abstract]
[Full Text]
-
Haque, R., Huston, C. D., Hughes, M., Houpt, E., Petri, W. A. Jr.
(2003). Amebiasis. NEJM
348: 1565-1573
[Full Text]
-
Martin, W., Borst, P.
(2003). Secondary loss of chloroplasts in trypanosomes. Proc. Natl. Acad. Sci. USA
100: 765-767
[Full Text]
-
Nixon, J. E. J., Field, J., McArthur, A. G., Sogin, M. L., Yarlett, N., Loftus, B. J., Samuelson, J.
(2003). Iron-Dependent Hydrogenases of Entamoeba histolytica and Giardia lamblia: Activity of the Recombinant Entamoebic Enzyme and Evidence for Lateral Gene Transfer. Biol. Bull.
204: 1-9
[Abstract]
[Full Text]
-
Edgcomb, V. P., Simpson, A. G. B., Zettler, L. A., Nerad, Thomas. A., Patterson, D. J., Holder, M. E., Sogin, M. L.
(2002). Pelobionts are Degenerate Protists: Insights from Molecules and Morphology. Mol Biol Evol
19: 978-982
[Abstract]
[Full Text]
-
Lloyd, D., Harris, J. C., Maroulis, S., Wadley, R., Ralphs, J. R., Hann, A. C., Turner, M. P., Edwards, M. R.
(2002). The 'primitive' microaerophile Giardia intestinalis (syn. lamblia, duodenalis) has specialized membranes with electron transport and membrane-potential-generating functions. Microbiology
148: 1349-1354
[Abstract]
[Full Text]
-
Silberman, J. D., Simpson, A. G. B., Kulda, J., Cepicka, I., Hampl, V., Johnson, P. J., Roger, A. J.
(2002). Retortamonad Flagellates are Closely Related to Diplomonads--Implications for the History of Mitochondrial Function in Eukaryote Evolution. Mol Biol Evol
19: 777-786
[Abstract]
[Full Text]
-
Nixon, J. E. J., Wang, A., Field, J., Morrison, H. G., McArthur, A. G., Sogin, M. L., Loftus, B. J., Samuelson, J.
(2002). Evidence for Lateral Transfer of Genes Encoding Ferredoxins, Nitroreductases, NADH Oxidase, and Alcohol Dehydrogenase 3 from Anaerobic Prokaryotes to Giardialamblia and Entamoebahistolytica. Eukaryot Cell
1: 181-190
[Abstract]
[Full Text]
-
Bapteste, E., Brinkmann, H., Lee, J. A., Moore, D. V., Sensen, C. W., Gordon, P., Durufle, L., Gaasterland, T., Lopez, P., Muller, M., Philippe, H.
(2002). The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc. Natl. Acad. Sci. USA
99: 1414-1419
[Abstract]
[Full Text]
-
Tachezy, J., Sanchez, L. B., Muller, 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
[Abstract]
[Full Text]
-
Horner, D. S., Embley, T. M.
(2001). Chaperonin 60 Phylogeny Provides Further Evidence for Secondary Loss of Mitochondria Among Putative Early-Branching Eukaryotes. Mol Biol Evol
18: 1970-1975
[Full Text]
-
Dacks, J. B., Silberman, J. D., Simpson, A. G. B., Moriya, S., Kudo, T., Ohkuma, M., Redfield, R. J.
(2001). Oxymonads Are Closely Related to the Excavate Taxon Trimastix. Mol Biol Evol
18: 1034-1044
[Abstract]
[Full Text]
-
Upcroft, P., Upcroft, J. A.
(2001). Drug Targets and Mechanisms of Resistance in the Anaerobic Protozoa. Clin. Microbiol. Rev.
14: 150-164
[Abstract]
[Full Text]
-
Ghosh, S., Field, J., Rogers, R., Hickman, M., Samuelson, J.
(2000). The Entamoeba histolytica Mitochondrion-Derived Organelle (Crypton) Contains Double-Stranded DNA and Appears To Be Bound by a Double Membrane. Infect. Immun.
68: 4319-4322
[Abstract]
[Full Text]
-
Samuelson, J.
(1999). Why Metronidazole Is Active against both Bacteria and Parasites. Antimicrob. Agents Chemother.
43: 1533-1541
[Full Text]
-
Ghosh, S. K., Field, J., Frisardi, M., Rosenthal, B., Mai, Z., Rogers, R., Samuelson, J.
(1999). Chitinase Secretion by Encysting Entamoeba invadens and Transfected Entamoeba histolytica Trophozoites: Localization of Secretory Vesicles, Endoplasmic Reticulum, and Golgi Apparatus. Infect. Immun.
67: 3073-3081
[Abstract]
[Full Text]