The Large, Free-living Amoebae: Wonderful Cells for Biological Studies
KWANG W. JEON
Department of Zoology, University of Tennessee, Knoxville, TN 37996
Search for more papers by this authorKWANG W. JEON
Department of Zoology, University of Tennessee, Knoxville, TN 37996
Search for more papers by this authorABSTRACT
The large, free-living amoebae have been widely used as model cells for studying a variety of biological phenomena, including cell motility, nucleocytoplasmic interactions, membrane function, and symbiosis. Results of studies by our group on amoebae as moving cells, as material for micrurgical manipulations, and as hosts for intracellular symbionts are summarized here. In particular, our recent studies of the amoeba as a microcosm, in which spontaneously infecting foreign microbes have become integrated as necessary cell components, are described in some detail. These processes have involved an initial microbial infection, mutual adaptation by the host and symbionts, and development of obligatory symbiosis. Evidence is presented to show that symbiont-derived macromolecules are involved in the protection of symbionts from digestion, the symbionts have acquired regulatory elements on their chromosomal genes to enhance production of beneficial gene products, and symbionts apparently utilize host-derived macromolecules to their benefit. These studies involved morphological observations both at light and electron microscopic levels, physiological and genetic studies, production and use of poly- and monoclonal antibodies, and molecular-biological approaches including gene cloning and sequencing. It is shown that amoebae are uniquely suited as model cells with which to study these phenomena.
Reference
- 1 Abshire, K. Z. & Niedhardt, F. C. 1993. Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J. Bacteriol., 175: 3734–3743.
- 2 Ahmadjian, V. 1986. An Introduction to Biological Associations. Univ. Press of New England, Hanover .
- 3 Ahn, G. S., Choi, E. Y. & Jeon, K. W. 1990. A symbiosome-membrane-specific protein in symbiont-bearing Amoeba proteus as studied with a monoclonal antibody. Endocyt. Cell Res., 7: 45–50.
- 4 Ahn, T. I. & Jeon, K. W. 1979. Growth and electron microscopic studies on an experimentally established bacterial endosymbiosis in amoebae. J. Cell Physiol., 98: 49–58.
- 5 Ahn, T. I. & Jeon, K. W. 1982. Structural and biochemical characteristics of the plasmalemma and vacuole membranes in amoebae. Exp. Cell Res., 137: 253–268.
- 6 Ahn, T. I. & Jeon, K. W. 1983. Strain-specific proteins of symbiont-containing Amoeba proteus detected by two-dimensional gel electrophoresis. J. Protozool., 30: 713–715.
- 7 Ahn, T. I., Lim, S. T., Leeu, H. K. & Jeon, K. W. 1994. A novel strong promoter of the groEx operon of symbiotic bacteria in Amoeba proteus. Gene, in press.
- 8 Arruda, S., Bomfim, G., Knights, R., Huima-Byron, T. & Riley, L. W. 1993. Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science, 261: 1454–1457.
- 9 Barbaree, J. M., Breiman, R. F. & Dufour, A. P. 1993. Legionella: Current Status and Emerging Perspectives. American Society for Microbiology, Washington , D.C .
- 10 Bell, L. G. E. & Jeon, K. W. 1962. Stimulation of cell locomotion and pseudopod formation by heparin. Nature, 195: 400–401.
- 11 Bell, L. G. E. & Jeon, K. W. 1963. Locomotion of A. proteus. Nature, 198: 675–667.
- 12 Berger, K. H. & Isberg, R. R. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol., 7: 7–19.
- 13 Bovee, E. C. 1982. Life among the amoebas and other matters. J. Protozool., 29: 145–149.
- 14 Buchmeier, N. A. & Heffron, F. 1990. Induction of Salmonella stress proteins upon infection of macrophages. Nature, 248: 730–732.
- 15 Buchmeier, N. A. & Heffron, F. 1991. Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium. Infect. Immun., 59: 2232–2238.
- 16 Cavalier-Smith, T. 1987. The simultaneous symbiotic origin of mitochondria, chloroplasts and microbodies. Ann. N.Y. Acad. Sci., 503: 55–71.
- 17 Cerrone, M. C., Ma, J.J. & Stephens, R. S. 1991. Cloning and sequence of the gene for heat shock protein 60 from Chlamydia trachomatis and immunological reactivity of the protein. Infect. Immun., 59: 79–90.
- 18 Chapman-Andresen, C. 1971. Biology of the large amoebae. Annu. Rev. Microbiol., 25: 27–48.
- 19 Choi, E. Y., Ahn, G. S. & Jeon, K. W. 1991. Elevated levels of stress proteins associated with bacterial symbiosis in Amoeba proteus and soybean root nodule cells. BioSystems, 25: 205–212.
- 20 Choi, E. Y. & Jeon, K. W. 1989. The presence of a spectrin-like protein on symbiosome membrane of symbiont-bearing Amoeba proteus as studied with monoclonal antibodies. Endocyt. Cell Res., 6: 99–108.
- 21 Choi, E. Y. & Jeon, K. W. 1989. A spectrin-like protein present on membranes of Amoeba proteus as studied with monoclonal antibodies. Exp. Cell Res., 185: 154–165.
- 22 Choi, E. Y. & Jeon, K. W. 1992. Bacterial-endosymbiont-derived lipopolysaccharides on amoeba symbiosome membranes. J. Protozool., 39: 205–210.
- 23 Choi, E. Y., Kim, K. J. & Jeon, K. W. 1992. Lysosomal membrane proteins of Amoeba proteus, as studied with monoclonal antibodies. J. Protozool., 39: 671–677.
- 24 Cianciotto, N. P. & Fields, B. S. 1992. Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl Acad. Sci. (USA), 89: 5188–5191.
- 25 de Carvalho, L. & de Souza, W. 1990. Internalization of surface anionic sites and phagosome-lysosome fusion during interaction of Toxoplasma gondii with macrophages. Eur. J. Cell Biol., 51: 211–219.
- 26 de Fonbrune, P. 1949. Technique de Micromanipulation. Masson, Paris .
- 27 Eissenberg, L. G., Goldman, W. E. & Schlesinger, P. H. 1993. Histoplasma capsulatum modulates the acidification of phagolysosomes. J. Exp. Med., 177: 1605–1611.
- 28 Engleberg, N. C., Carter, C., Weber, D. R., Cianciotto, N. P. & Eisenstein, B. I. 1989. DNA Sequence of mip. a Legionella pneumophila gene associated with macrophage infectivity. Infect. Immun., 57: 1263–1270.
- 29 Fayet, O., Ziegelhoffer, T. & Georgopoulos, C. 1989. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol., 171: 1379–1385.
- 30 Frenchick, P. J., Markham, R. J. & Cochrane, A. H. 1985. Inhibition of phagosome-lysosome fusion in macrophages by soluble extracts of virulent Brucella aborus. Amer. J. Vet. Res., 46: 332–335.
- 31
Friedman, H.,
Klein, T. W.,
Nakano, M. &
Nowotny, A.
1990. Endotoxin. Plenum Press,
New York
.
10.1007/978-1-4757-5140-6 Google Scholar
- 32 Galley, K. A., Singh, B. & Gupta, R. S. 1992. Cloning of HSP70 (dnaK) gene from Clostridium perfringens using a general polymerase chain reaction based approach. Biochim. Biophys. Acta. 1130: 203–208.
- 33 Gellissen, F. & Michaelis, G. 1987. Gene transfer: mitochondria to nucleus. Ann. N.Y. Acad. Sci., 503: 391–401.
- 34 Gor, D. & Mayfield, J. E. 1992. Cloning and nucleotide sequence of the Brucella abortus groE operon. Biochim. Biophys. Acta. 1130: 120–122.
- 35 Goren, M. B. & Mor, N. 1990. Influence of phagosomal contents on the apparent inhibition of phagosome-lysosome fusion mediated by polyanionic substances in mouse peritoneal macrophages. Biochem. Cell Biol., 68: 24–32.
- 36 Gray, M. W. 1992. The endosymbiont hypothesis revisited. Int. Rev. Cytol., 141: 233–357.
- 37 Hacker, J., Otto, M., Wintermeyer, E., Ludwig, B. & Fischer, G. 1993. Analysis of virulence factors of Legionella pneumophila. Int. J. Med. Microbiol. Virol., 278: 348–358.
- 38 Hall, B. F. & Joiner, K. A. 1991. Strategies of obligate intracellular parasites for evading host defences. Immunol. Today, 12: A22–A27.
- 39 Han, J. H. & Jeon, K. W. 1980. Isolation and partial characterization of two plasmid DNAs from endosymbiotic bacteria in Amoeba proteus. J. Bacteriol., 141: 1466–1469.
- 40 Hara, E., Fukatsu, T., Takeda, K., Kengaku, M., Ohtaka, C. & Ishikawa, H. 1990. Characterization of symbionin, only one protein produced by an aphid endosymbiont in vivo. In: P. Nardon, V. Gianianazzi-Pearson, A. M. Grenier, L. Margulis & D. C. Smith (ed.), Endocytobiology IV. INRA, Paris .
- 41 Hart, P. D. & Young, M. R. 1979. The effect of inhibitors and enhancers of phagosome-lysosome fusion in cultured macrophages on the phagosome membranes of ingested yeasts. Exp. Cell Res., 118: 365–375.
- 42
Hawkins, S. E.
1973. Genetic information in the cytoplasm of amoebae. In: K. W. Jeon (ed.), The Biology of Amoeba. Academic Press,
New York
. Pp.
525–547.
10.1016/B978-0-12-384850-5.50026-9 Google Scholar
- 43 Haylett, T. & Thilo, L. 1991. Endosome-lysosome fusion at low temperature. J. Biol. Chem., 266: 8322–8327.
- 44 Healy, A. M., Mariethoz, E., Pizurki, L. & Polla, B. S. 1992. Heat shock proteins in cellular defense mechanisms and immunity. Aging and Cellular Defense Mechanisms, 663: 320–330.
- 45
Hendrix, L. R.,
Mallavia, L. P. &
Samuel, J. E.
1993. Cloning and sequencing of Coxiella burnetii outer membrane protein gene com 1.
Infect. Immun., 61: 470–477.
10.1093/nar/16.13.6127 Google Scholar
- 46 Hindersson, P., Hoiby, N. & Bangsborg, J. 1991. Sequence analysis of the Legionella micdadei groESL operon. FEMS Microbiol. Lett., 77: 31–38.
- 47 Hoffman, P. S., Butler, C. A. & Quinn, F. D. 1989. Cloning and temperature-dependent expression in Escherichia coli of a Legionella pneumophila gene coding for a genus-common 60-kilodalton antigen. Infect. Immun., 57: 1731–1739.
- 48 Hoffman, P. S., Houston, L. & Butler, C. A. 1990. Legionella pneumophila htpAB heat shock operon: nucleotide sequence and expression of the 60-kilodalton antigen in L. pneumophila-infected HeLa cells. J. Bacteriol., 158: 3380–3387.
- 49
Holtzman, E.
1989. Lysosomes. Springer-Verlag,
New York
.
10.1007/978-1-4899-2540-4 Google Scholar
- 50 Ishibashi, Y., Nobuta, K. & Arai, T. 1992. Mutant of Salmonella typhimurium lacking the inhibitory function for phagosome lysosome fusion in murine macrophages. Microb. Pathog., 13: 317–323.
- 51 Ishikawa, H. 1984. Characterization of the protein species synthesized in vivo and in vitro by an aphid endosymbiont. Insect Biochem., 14: 417–425.
- 52 Jaconi, M. E., Lew, D., Carpentier, J. L., Magnusson, K. E., Sjögren, M. & Stendahl, O. 1990. Cytosolic free calcium elevation mediates the phagosome-lysosome fusion during phagocytosis in human neutrophils. J. Cell Biol., 110: 1555–1564.
- 53 Jeon, K. W. 1968. Nuclear control of cell movement in amoebae: nuclear transplantation study. Exp. Cell Res., 50: 467–471.
- 54 Jeon, K. W. 1975. Selective effects of enucleation and transfer of heterologous nuclei on cytoplasmic organelles in Amoeba proteus. J. Protozool., 22, 402.
- 55 Jeon, K. W. 1983. Intracellular Symbiosis. Academic Press, New York .
- 56 Jeon, K. W. 1987. Change of cellular pathogens into required cell components. Ann. N. Y. Acad. Sci., 503: 359–371.
- 57 Jeon, K. W. 1991. Amoeba and X-bacteria: symbiont acquisition and possible species change. In: L. Margulis & R. Fester (ed.), Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge , MA . Pp. 118–131.
- 58 Jeon, K. W. 1992. Macromolecules involved in the amoeba-bacteria symbiosis. J. Protozool., 39: 199–204.
- 59 Jeon, K. W. 1993. Symbiosis: advantages and disadvantages. In: S. Sato, M. Ishida & H. Ishikawa (ed.), Endocytobiology V. Tübingen Univ. Press, Tübingen , FRG . Pp. 1–7.
- 60 Jeon, K. W. & Ahn, T. I. 1978. Temperature sensitivity: a cell character determined by obligate endosymbionts in amoebas. Science, 202: 635–637.
- 61 Jeon, K. W. & Bell, L. G. E. 1962. Pseudopod and foodcup formation in A. proteus. Q. Exp. Cell Res., 27: 350–352.
- 62 Jeon, K. W. & Bell, L. G. E. 1964. Behavior of cell membrane in relation to locomotion in A. proteus. Exp. Cell Res., 33: 531–539.
- 63 Jeon, K. W. & Bell, L. G. E. 1965. Chemotaxis in large free-living amoebae. Exp. Cell Res., 38: 536–555.
- 64 Jeon, K. W. & Danielli, J. F. 1971. Micrurgical studies with large free-living amebas. Int. Rev. Cytol., 30: 49–89.
- 65 Jeon, K. W. & Hah, J. C. 1977. Effect of chloramphenicol on bacterial endosymbiotes in a strain of Amoeba proteus. J. Protozool., 24: 289–293.
- 66 Jeon, K. W. & Jeon, M. S. 1976. Endosymbiosis in amoebae: Recently established endosymbionts have become required cytoplasmic components. J. Cell. Physiol., 89: 337–347.
- 67 Jeon, K. W. & Jeon, M. S. 1982. Experimental cross-infection of Chaos carolinensis with endosymbiotic bacteria from Amoeba proteus. J. Protozool., 29: 493A.
- 68 Jeon, K. W. & Lorch, I. J. 1967. Unusual intra-cellular bacterial infection in large, free-living amoebae. Exp. Cell Res., 48: 236–240.
- 69 Jeon, K. W. & Lorch, I. J. 1979. Compatibility among cell components in the large, freeliving amoebae. Int. Rev. Cytol. Suppl., 9: 45–62.
- 70 Jeon, K. W., Lorch, I. J., Moran, J. F., Muggleton, A. & Danielli, J. F. 1967. Cytoplasmic inheritance in amoebae. Exp. Cell Res., 46: 615–617.
- 71 Joiner, K. A., Fuhrman, S. A., Miettinen, H. M., Kasper, L. H. & Mellman, I. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science, 249: 641–646.
- 72 Kakeda, K. & Ishikawa, H. 1991. Molecular chaperone produced by an intracellular symbiont. J. Biochem., 110: 583–587.
- 73 Kim, H. B. & Jeon, K. W. 1986. Protein synthesis by bacterial endosymbionts in amoebae. Endocyt. Cell Res., 3: 299–309.
- 74 Kim, H. B. & Jeon, K. W. 1987. Actin-like host protein accumulated within symbiont-containing vesicles of amoebae as studied using a monoclonal antibody. Endocyt. Cell Res., 3: 151–166.
- 75 Kim, H. B. & Jeon, K. W. 1987. A monoclonal antibody against a symbiont-synthesized protein in the cytosol of symbiont-dependent amoebae. J. Protozool., 34: 393–397.
- 76 Kim, K. J., Na, Y. E. & Jeon, K. W. 1994. Bacterial endosymbiont-derived lipopolysaccharides and a protein on symbiosome membranes in newly infected amoebae and their roles in lysosome-symbiosome fusion. Infect. Immun., 62: 65–71.
- 77 Kippert, F. 1987. Endocytobiotic coordination, intracellular calcium signaling, and the origin of endogenous rhythms. Ann. N.Y. Acad. Sci., 503: 476–495.
- 78 Koll, H., Guiard, B., Rassow, J., Ostermann, J., Horich, A. L., Neupert, W. & Hartl, F.-U. 1992. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell, 68: 1163–1175.
- 79 Kusukawa, N. & Yura, T. 1988. Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress. Genes Dev., 2: 874–882.
- 80 Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y. & Ito, K. 1989. Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J., 8: 3517–3521.
- 81 Lee, J. J. & Fredrick, J. F. 1987. Endocytobiology III. New York Academy of Sciences, New York .
- 82 Lorch, I. J. & Danielli, J. F. 1953. Nuclear transplantation in amoebae. I. Some characters of Amoeba proteus and Amoeba discoides. Quart. J. Microsc. Sci., 94: 445–460.
- 83 Lorch, I. J. & Jeon, K. W. 1969. Character changes induced by heterologous nuclei in amoeba heterokaryons. Exp. Cell Res., 57: 233–239.
- 84 Lorch, I. J., Kim, H. B. & Jeon, K. W. 1985. Symbiont-induced strain-specific lethal effect in amoebae. J. Protozool., 32: 745–746.
- 85 Lundermose, A. G., Rouch, D. A., Penn, C. W. & Pearce, J. H. 1993. The Chlamydia trachmatis Mip-like protein is a lipoprotein. J. Bacteriol., 175: 3669–3671.
- 86 Margulis, L. 1993. Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons, 2nd ed. W.H. Freeman, New York .
- 87 Margulis, L. & Fester, R. 1991. Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge .
- 88 Marshall, J. S., DeRocher, A. E., Keegstra, K. & Vierling, E. 1990. Identification of heat shock protein hsp70 homologues in chloroplasts. Proc. Natl. Acad. Sci. (USA), 87: 374–378.
- 89 Martin, J., Geromanos, S., Tempst, P. & Hartl, F. U. 1993. Identification of nucleotide-binding regions in the chaperonin proteins GroEL and GroES. Nature, 366: 279–282.
- 90 McAuley, P. J. 1982. Control of cell division of the intracellular chlorella symbionts in green hydra. J. Cell Sci., 47: 197–206.
- 91 McMullin, T. W. & Hallberg, R. L. 1988. A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli groEL gene. Mol. Cell Biol., 8: 371–380.
- 92 Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor , NY .
- 93 Morioka, M., Muraoka, H. & Ishikawa, H. 1993. Chaperonin produced by an intracellular symbiont is an energy-coupling protein with phosphotransferase activity. J. Biochem. 114: 246–250.
- 94 Morrison, R. P., Su, H., Lying, K. & Yuan, Y. 1990. The Chlamydia trachomatis hyp operon is homologous to the groE stress response operon of Escherichia coli. Infect. Immun., 58: 2701–2705.
- 95 Moulder, J. W. 1985. Comparative biology of intracellular parasitism. Microbiol. Rev., 49: 298–337.
- 96 Moulder, J. W. 1991. Intracellular Parasitism. CRC Press, Boca Raton .
- 97 Narberhaus, F. & Bahl, H. 1992. Cloning, sequencing, and molecular analysis of the groESL operon of Clostridium acetobutylicum. J. Bacteriol., 174: 3282–3289.
- 98 Nardon, P., Gianinazzi-Pearson, V., Grenier, A. M., Margulis, L. & Smith, D. C. 1990. Endocytobiology IV. INRA, Paris .
- 99 Ohtaka, C. & Ishikawa, H. 1993. Accumulation of adenine and thymine in a groE-homologous operon of an intracellular symbiont. J. Mol. Evol., 36: 121–126.
- 100 Ohtaka, C., Nakamura, H. & Ishikawa, H. 1992. Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants. J. Bacteriol., 174: 1869–1874.
- 101
Parakash, R. K. &
Atherly, A. G.
1986. Plasmids of Rhyzobium and their role in symbiotic nitrogen fixation.
Int. Rev. Cytol., 104: 1–24.
10.1016/S0074-7696(08)61921-X Google Scholar
- 102 Parham, P. 1992. Chagas' disease: Defence cults begin to bite. Nature, 356: 291–292.
- 103 Park, M. S. & Jeon K. W. 1988. A symbiont gene coding for a protein required for the host amoeba: cloning and expression in phage-transformed E. coli. Endocyt. Cell Res., 5: 215–224.
- 104 Parsons, L. M., Waring, A. L. & Shayegani, M. 1992. Molecular analysis of the Haemophilus ducreyi groE heat shock operon. Infect. Immun., 60: 4111–4118.
- 105 Polla, B. S. 1991. Heat shock proteins in host-parasite interactions. Immunoparasitol. Today, A38–A41.
- 106 Rabinovitch, M. & Plaut, W. 1962. Cytoplasmic DNA synthesis in Amoeba proteus. II. On the behavior and possible nature of the DNA-containing elements. J. Cell Biol., 15: 535–540.
- 107 Rands, M. L., Douglas, A. E., Loughman, B. C. & Hawes, C. R. 1992. The pH of the perisymbiont space in the green hydra-Chlorella symbiosis — an immunocytochemical investigation. Protoplasma, 170: 90–93.
- 108 Rastogi, N. & Frëhel, C. 1989. Resistance of Mycobacterium avium to microbicidal activities in bone-marrow macrophages from naturally-susceptible (C57B1/6) and naturally resistant (DBA-2) mice. Acta Leprol. (Geneve), 7 Suppl 1: 177–178.
- 109 Rest, R. F., Coohey, M. H. & Spitznagel, J. K. 1977. Susceptibility of lipopolysaccharide mutants to the bactericidal action of human neutrophil lysosomal fractions. Infect. Immun., 16: 145–151.
- 110 Robertson, D. C., Riley, L. K., Kreutznem, D. L. & Dreyfus, C. A. 1979. Intracellular survival of smooth and rough strains of Brucells. In: D. Schlessinger (ed.), Microbiology. American Society for Microbiology, Washington , D.C . Pp. 150–153.
- 111 Rolfe, B. G. & Gresshoff, P. M. 1988. Genetic analysis of legume nodule initiation. Annu. Rev. Plant Physiol., 39: 297–319.
- 112 Roth, L. E. & Daniels, E. W. 1961. Infective organisms in the cytoplasm of Amoeba proteus. J. Biophys. Biochem. Cytol. 9: 317–323.
- 113 Sadosky, A. B., Wiater, L. A. & Shuman, H. A. 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect. Immun., 61: 5361–5373.
- 114 Sato, S., Ishida, M. & Ishikawa, H. (ed). 1994. Endocytobiology V. Tübingen Univ. Press, Tübingen , FRG .
- 115 Schenk, H. E. A. & Schwemmler, W. 1983. Endocytobiology II. Intracellular Space as Oligogenetic Ecosystems. de Gruyter, Berlin .
- 116 Schofield, P. R., Gibson, A. H., Dudman, W. F. & Watson, J. M. 1987. Appl. Env. Microbiol., 53: 2942–2947.
- 117 Schwemmler, W. & Schenk, H. E. A. 1980. Endocytobiology: Endosymbiosis and Cell Biology. de Gruyter, Berlin .
- 118 Shinnick, T. M., Plikaytis, B. B., Hyche, A. D., Van Landingham, R. M. & Walker, L. L. 1989. The Mycobacterium tuberculosis BCG-a protein has homology with the Escherichia coli GroES protein. Nucleic Acids Res., 17: 1254.
- 119 Smith, D.C. & Douglas, A. E. 1987. The Biology of Symbiosis. Edward Arnold, Baltimore .
- 120 Springer, Ludwig W., Drozanski, W., Amann, R. & Schleifer, K. H. 1992. The Phylogenetic Status of Sarcobium-Lyticum, an Obligate Intracellular Bacterial Parasite of Small Amoebae. FEMS Microbiol. Lett., 96: 199–202.
- 121 Steinhoff, U., Golecki, J. R., Kazda, J. & Kaufmann, S. H. 1989. Evidence for phagosome-lysosome fusion in Mycobacterium leprae-infected murine Schwann cells. Infect. Immun., 57: 1008–1010.
- 122 Stern, D.B. 1987. DNA transposition between plant organellar genomes. J. Cell Sci. Suppl., 7: 145–154.
- 123 Sturgin-Koszycki, S., Schlesinger, P. H., Charkraborty, P., Haddix, P. L., Gluck, S. L., Heuser, J. & Russell, D. G. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science, 263: 678–681.
- 124 Tarleton, R. L. 1991. Regulation of immunity in Trypanosoma cruzi infection. Exp. Parasitol., 73: 106–109.
- 125 Taura, T., Kusukawa, N., Yura, T. & Ito, K. 1989. Transient shut off of Escherichia coli heat shock protein synthesis upon temperature shift down. Biochem. Biophys. Res. Commun., 163: 438–443.
- 126 Taylor, F.J.R. 1987. An overview of the status of evolutionary cell symbiosis theories. Ann. N.Y. Acad. Sci., 503: 1–16.
- 127 Vaara, M. & Nikaido, H. 1984. Molecular organization of bacterial outer membrane. In: E. T. Trietschel (ed.), Handbook of Endotoxin, Vol. 1. Chemistry of Endotoxin. Elsevier Science Publishers, Amsterdam . Pp. 1–45.
- 128
Vodkin, M. H. &
Williams, J. C.
1988. A heat shock operon in Coxiella burnetii produces a major antigen homologous to a protein in both Mycobacteria and Escherichia coli.
J. Bacteriol., 170: 1227–1234.
10.1128/jb.170.3.1227-1234.1988 Google Scholar
- 129 von Rosenhof, R. 1755. Proteus diffluens. Monatl. herausgegebene Insektenbelustigungen, 3: 622.
- 130 Westphal, O., Jann, K. & Himmelspack, K. 1983. Chemistry and immunochemistry of bacterial lipopolysaccharides as cell wall antigens and endotoxins. Prog. Allerg., 33: 9–39.
- 131 Wolstenholme, D. R. 1966. Cytoplasmic DNA-containing bodies in amoebae. Nature, 211: 652–653.
- 132 Young, D. B. & Garbe, T. R. 1991. Heat shock proteins and antigens of Mycobacterium tuberculosis. Infect. Immun., 59: 3086–3093.
- 133 Yudin, A. L. 1979. Nuclear transplantation studies in Amoeba proteus. Int. Rev. Cytol. Suppl., 9: 63–100.