Plasmodium and Toxoplasma belong to a group of unicellular parasites which actively penetrate their respective mammalian host cells. During the process of invasion, they initiate the formation of a membrane, the so-called parasitophorous vacuolar membrane, which surrounds the intracellular parasite and which differs substantially from endosomal membranes or the membrane of phagolysosomes. The biogenesis and the maintenance of the vacuolar membrane are closely related to the peculiar cellular organization of these parasites and are unique phenomena in cell biology. Here we compare biological similarities and differences between the two parasites, with respect to: (i) the formation, (ii) the maintenance, and (iii) the biological role of the vacuolar membrane. We conclude that most differences between the organisms primarily reflect the different biosynthetic capacities of the host cells they invade.

REFERENCES

Adams
J.
,
Hudson
D.
,
Torii
M.
,
Ward
G.
,
Wellems
T.
,
Aikawa
M.
,
Miller
L.
(
1990
).
The duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites.
Cell
63
,
141
153
Aikawa
M.
,
Miller
L. H.
,
Rabbege
J. R.
,
Epstein
N.
(
1981
).
Freeze fracture study on erythrocyte membrane during malarial parasite invasion.
J. Cell Biol
91
,
55
62
Ajioka
J. W.
,
Boothrody
J. C.
,
Brunk
B. P.
,
Hehl
A.
,
Hillier
L.
,
Manger
I. D.
,
Marra
M.
,
Overton
G. C.
,
Roos
D. S.
,
Wan
K. L.
,
Waterston
R.
,
Sibley
L. D.
(
1998
).
Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to apicomplexa.
Genome Res
8
,
18
28
Ansorge
I.
,
Benting
J.
,
Bhakdi
S.
,
Lingelbach
K.
(
1996
).
Protein sorting in Plasmodium falciparum -infected red blood cells permeabilized with the pore-forming protein streptolysin O.
Biochem. J
315
,
307
314
Ansorge
I.
,
Paprotka
K.
,
Bhakdi
S.
,
Lingelbach
K.
(
1997
).
Permeabilization of the erythrocyte membrane with streptolysin O allows access to the vacuolar membrane of Plasmodium falciparum and a molecular analysis of membrane topology.
Mol. Biochem. Parasitol
84
,
259
261
Atkinson
C. T.
,
Aikawa
M.
,
Perry
G.
,
Fujino
T.
,
Bennett
V.
,
Davidson
E. A.
,
Howard
R. J.
(
1987
).
Ultrastructural localization of erythrocyte cytoskeleton and integral membrane proteins in Plasmodium falciparum infected erythrocytes.
Eur. J. Cell Biol
45
,
192
199
Baruch
D. I.
,
Pasloske
B. L.
,
Singh
H. B.
,
Bi
X.
,
Ma
X. C.
,
Feldman
M.
,
Taraschi
T. F.
,
Howard
R. J.
(
1995
).
Cloning of the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes.
Cell
82
,
77
87
Beckers
C. J. M.
,
Dubremetz
J. F.
,
Mercereau-Puijalon
O.
,
Joiner
K. A.
(
1994
).
The Toxoplasma gondii rhoptry protein ROP2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm.
J. Cell Biol
127
,
947
961
Bejon
P. A.
,
Bannister
L. H.
,
Fowler
R. E.
,
Fookes
R. E.
,
Webb
S. E.
,
Wright
A.
,
Mitchell
G. H.
(
1997
).
A role for microtubules in Plasmodium falciparum merozoite invasion.
Parasitology
114
,
1
6
Bushell
G. R.
,
Ingram
L. T.
,
Fardoulys
C. A.
,
Cooper
J. A.
(
1988
).
An antigenic complex in the rhoptries of Plasmodium falciparum.
Mol. Biochem. Parasitol
28
,
105
112
Cabantchik
Z. I.
(
1990
).
Properties of permeation pathways induced in the human red cell membrane by malaria parasites.
Blood Cells
16
,
421
432
Carruthers
V. B.
,
Sibley
L. D.
(
1997
).
Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts.
Eur. J. Cell Biol
73
,
114
123
de Castro
F. A.
,
Ward
G. E.
,
Jambou
R.
,
Attal
G.
,
Mayau
V.
,
Jaureguiberry
G.
,
Braun-Breton
C.
,
Chakrabarti
D.
,
Langsley
G.
(
1996
).
Identification of a family of Rab G-proteins in Plasmodium falciparum and a detailed characterisation of pfrab6.
Mol. Biochem. Parasitol
80
,
77
88
Desai
S. A.
,
Rosenberg
R. L.
(
1997
).
Pore size of the malaria parasite's nutrient channel.
Proc. Nat. Acad. Sci. USA
94
,
2045
2049
Dieckmann-Schuppert
A.
,
Bender
S.
,
Odenthal-Schnittler
M.
,
Bause
E.
,
Schwarz
R. T.
(
1992
).
Apparent lack of N-glycosylation in the asexual intraerythrocytic stage of Plasmodium falciparum.
Eur. J. Biochem
205
,
815
825
Dluzewski
A. R.
,
Fryer
P. R.
,
Griffiths
S.
,
Wilson
R. J. M.
,
Gratzer
W. B.
(
1989
).
Red cell protein distribution during malarial invasion.
J. Cell Sci
92
,
691
699
Dluzewski
A. R.
,
Zicha
D.
,
Dunn
G. A.
,
Gratzer
W. B.
(
1995
).
Origins of the parasitophorous vacuole membrane of the malaria parasite: surface area of the parasitized red cell.
Eur. J. Cell Biol
68
,
446
449
Dobrowolski
J. M.
,
Sibley
L. D.
(
1996
).
Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite.
Cell
84
,
933
939
Dubremetz
J. F.
,
Achbarou
A.
,
Bermudes
D.
,
Joiner
K. A.
(
1993
).
Kinetics of apical organelle exocytosis during Toxoplasma gondii host cell interaction.
Parasitol. Res
79
,
402
408
Elmendorf
H. G.
,
Haldar
K.
(
1994
).
Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes.
J. Cell Biol
124
,
449
462
Formaux
M. N.
,
Achbarou
A.
,
Mercereau-Puijalon
O.
,
Biderre
C.
,
Briche
I.
,
Loyens
A.
,
Odberg-Ferragut
C.
,
Camus
D.
,
Dubremetz
J. F.
(
1996
).
The MIC1 microneme protein of Toxoplasma gondii contains a duplicated receptor-like domain and binds to host cell surface.
Mol. Biochem. Parasitol
83
,
201
210
Foussard
F.
,
Leriche
M. A.
,
Dubremetz
J. F.
(
1991
).
Characterization of the lipid content of Toxoplasma gondii rhoptries.
Parasitology
102
,
367
370
Galinski
M. R.
,
Corredor Medina
C.
,
Ingravallo
P.
,
Barnwell
J. W.
(
1992
).
A reticulocyte-binding protein complex of Plasmodium vivax merozoites.
Cell
69
,
1213
1226
Ginsburg
H.
(
1994
).
Transport pathways in the malaria-infected erythrocyte. Their characterization and their use as potential targets for chemotherapy.
Biochem. Pharmacol
48
,
1847
1856
Gunther
K.
,
Tummler
M.
,
Arnold
H.-H.
,
Ridley
R.
,
Goman
M.
,
Scaife
J.
,
Lingelbach
K.
(
1991
).
An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein.
Mol. Biochem. Parasitol
46
,
149
158
Haldar
K.
,
Uyetake
L.
,
Ghori
N.
,
Elmendorf
H. G.
,
Li
W. L.
(
1991
).
The accumulation and metabolism of a fluorescent ceramide derivative in Plasmodium falciparum -infected erythrocytes.
Mol. Biochem. Parasitol
49
,
143
56
Haldar
K.
,
Uyetake
L.
(
1992
).
The movement of fluorescent endocytic tracers in Plasmodium falciparum infected erythrocytes.
Mol. Biochem. Parasitol
50
,
161
177
Hibbs
A. R.
,
Stenzel
D. J.
,
Saul
A.
(
1997
).
Macromolecular transport in malaria- does the duct exist?.
Eur. J. Cell Biol
72
,
182
188
Hinterberg
K.
,
Scherf
A.
,
Gysin
J.
,
Toyoshima
T.
,
Aikawa
M.
,
Mazie
J.-C.
,
Pereira da Silva
L.
,
Mattei
D.
(
1994
).
Plasmodium falciparum: The Pf332 antigen is secreted from the parasite by a brefeldin A-dependent pathway and is translocated to the erythrocyte membrane via the Maurer's clefts.
Exp. Parasitol
79
,
279
291
Kim
K. D.
,
Soldati
D.
,
Boothroyd
J. C.
(
1993
).
Gene replacement in Toxoplasma gondii with chloramphenicol acetyl transferase as a selectable marker.
Science
262
,
911
914
Kimura
E. A.
,
Couto
A. S.
,
Peres
V. J.
,
Casal
O. L.
,
Katzin
A. M.
(
1996
).
N-linked glycoproteins are related to schizogony of the intraerythrocytic stage in Plasmodium falciparum.
J. Biol. Chem
271
,
14452
14461
Kumar
N.
,
Syin
C.
,
Carter
R.
,
Quakyi
I.
,
Miller
L. H.
(
1988
).
Plasmodium falciparum gene encoding a protein similar to the 78-kDa ratglucose-regulated stress protein.
Proc. Nat. Acad. Sci. USA
85
,
6277
6281
Lauer
S. A.
,
Ghori
N.
,
Haldar
K.
(
1995
).
Sphingolipid synthesis as a target for chemotherapy against malaria parasites.
Proc. Nat. Acad. Sci. USA
92
,
9181
9185
Lauer
S. A.
,
Rathod
P. K.
,
Ghori
N.
,
Haldar
K.
(
1997
).
A membrane network for nutrient import in red cells infected with the malaria parasite.
Science
276
,
1122
1125
Lecordier
L.
,
Mercier
C.
,
Torpier
G.
,
Tourvieille
B.
,
Darcy
F.
,
Liu
J. L.
,
Maes
P.
,
Tartar
A.
,
Capron
A.
,
Cesbron-Delauw
M.-F.
(
1993
).
Molecular structure of a Toxoplasma gondii dense granule antigen (GRA 5) associated with the parasitophorous vacuole membrane.
Mol. Biochem. Parasitol
59
,
143
154
Lingelbach
K.
(
1993
).
Plasmodium falciparum: a molecular view of protein transport from the parasite into the host erythrocyte.
Exp. Parasitol
76
,
318
327
Lingelbach
K.
(
1997
).
Protein trafficking in the Plasmodium falciparum -infected erythrocyte- from models to mechanisms.
Annal. Trop. Med. Parasitol
91
,
543
549
Lycke
N.
,
Norrby
R.
(
1966
).
Demonstration of a factor of Toxoplasma gondii enhancing the penetration of Toxoplasma parasites into culture host cells.
Br. J. Exp. Pathol
47
,
248
256
Ndengele
M. M.
,
Messineo
D. G.
,
Sam-Yellowe
T.
,
Harwalkar
J. A.
(
1995
).
Plasmodium falciparum: effects of membrane modulating agents on direct binding of rhoptry proteins to human erythrocytes.
Exp. Parasitol
81
,
191
201
Ogun
S. A.
,
Holder
A. A.
(
1994
).
Plasmodium yoelii: brefeldin A-sensitive processing of proteins targeted to the rhoptries.
Exp. Parasitol
79
,
270
278
Ogun
S. A.
,
Holder
A. A.
(
1996
).
A high molecular mass Plasmodium yoelii rhoptry protein binds to erythrocytes.
Mol. Biochem. Parasitol
76
,
321
324
Orlandi
P. A.
,
Sim
B. K. L.
,
Chulay
D.
,
Haynes
J. D.
(
1990
).
Characterization of the 175 kilodalton erythrocyte binding antigen of Plasmodium falciparum.
Mol. Biochem. Parasitol
40
,
285
294
Ossorio
P. N.
,
Schwartzman
J. D.
,
Boothroyd
J. C.
(
1992
).
A Toxoplasma gondii rhoptry protein associated with host cell penetration has unusual charge assymetry.
Mol. Biochem. Parasitol
50
,
1
16
Ossorio
P. N.
,
Dubremetz
J. F.
,
Joiner
K. A.
(
1994
).
A soluble secretory protein of the intracellular parasite Toxoplasma gondii associates with the parasitophorous vacuole membrane through hydrophobic interactions.
J. Biol. Chem
269
,
15350
15357
Pouvelle
B.
,
Gormley
J.
,
Taraschi
T.
(
1994
).
Characterization of trafficking pathways and membrane genesis in malaria-infected erythrocytes.
Mol. Biochem. Parasitol
66
,
83
96
Pouvelle
B.
,
Spiegel
R.
,
Hsiao
L.
,
Howard
R.
,
Morris
R.
,
Thomas
A.
,
Taraschi
T.
(
1991
).
Direct access to serum macromolecules by intraerythrocytic malaria parasites.
Nature
353
,
73
75
Roggwiller
E.
,
Betoulle
M. E.
,
Blisnick
T.
,
Braun Breton
C.
(
1996
).
A role for erythrocyte band 3 degradation by the parasite gp76 serine protease in the formation of the parasitophorous vacuole during invasion of erythrocytes by Plasmodium falciparum.
Mol. Biochem. Parasitol
82
,
13
24
Sadak
A.
,
Taghy
Z.
,
Fortier
B.
,
Dubremetz
J. F.
(
1988
).
Characterization of a family of rhoptry proteins of Toxoplasma gondii.
Mol. Biochem. Parasitol
29
,
203
211
Saffer
L. D.
,
Mercereau-Puijalon
O.
,
Dubremetz
J. F.
,
Schwartzman
J.
(
1992
).
Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration.
J. Protozool
39
,
526
530
Sam-Yellowe
T. Y.
,
Shio
H.
,
Perkins
M.
(
1988
).
Secretion of Plasmodium falciparum rhoptry protein into the plasma membrane of host erythrocytes.
J. Cell Biol
106
,
1507
1513
Sam-Yellowe
T. Y.
(
1992
).
Molecular factors responsible for host cell recognition and invasion in Plasmodium falciparum.
J. Protozool
39
,
181
189
Scholtyseck
E.
,
Piekarski
G.
(
1965
).
Elektronenmikroskopische Untersuchungen uber die Merozoiten von Eimeria stiedae und E. perforans und Toxoplasma gondii. Zur systematischen Stellung von T. gondii. Z.
Parasitenk
26
,
91
115
Schwab
J. C.
,
Beckers
C. J. M.
,
Joiner
K. A.
(
1994
).
The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve.
Proc. Nat. Acad. Sci. USA
91
,
509
513
Schwartzman
J. D.
(
1986
).
Inhibition of a penetration enhancing factor of Toxoplasma gondii by monoclonal antibodies specific for rhoptries.
Infect. Immun
51
,
760
764
Schwartzman
J. D.
,
Saffer
L. D.
(
1992
).
How Toxoplasma gondii gets into and out of host cells.
Subcell. Biochem
18
,
333
364
Schwarz
R. T.
,
Tomavo
S.
(
1993
).
The current status of the glycobiology of Toxoplasma gondii: glycosylphosphatidylinositols, N-and O-linked glycans.
Res. Immunol
144
,
24
31
Shiao
Y. J.
,
Lupo
G.
,
Vance
J. E.
(
1995
).
Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine.
J. Biol. Chem
270
,
11190
11198
Sim
B.
,
Orlandi
P.
,
Haynes
D.
,
Klotz
F.
,
Carter
M.
,
Camus
D.
,
Zegans
M.
,
Chulay
J.
(
1990
).
Primary structure of the 175K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion.
J. Cell Biol
111
,
1877
1884
Sinai
A. P.
,
Joiner
K. A.
(
1997
).
Safe haven: The cell biology of non-fusigenic pathogen vacuoles.
Annu. Rev. Microbiol
51
,
415
462
Sinai
A. P.
,
Webster
P.
,
Joiner
K. A.
(
1997
).
Association of host cell mitochondria and endoplasmic reticulum with the Toxoplasma gondii parasitophorous vacuole membrane- a high affinity interaction.
J. Cell Sci
110
,
2117
2128
Suss-Toby
E.
,
Zimmerberg
J.
,
Ward
G. E.
(
1996
).
Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore.
Proc. Nat. Acad. Sci. USA
93
,
8413
8418
Truong
R. M.
,
Francis
S. E.
,
Chakrabarti
D.
,
Goldberg
D. E.
(
1997
).
Cloning and characterization of Plasmodium falciparum ADP-ribosylation factor and factor-like genes.
Mol. Biochem. Parasitol
84
,
247
253
van Wye
J.
,
Ghori
N.
,
Webster
P.
,
Mitschler
R. R.
,
Elmendorf
H. G.
,
Haldar
K.
(
1996
).
Identification and localization of rab6, separation of rab6 from ERD2 and implications for an ‘unstacked’ Golgi, in Plasmodium falciparum.
Mol. Biochem. Parasitol
83
,
107
120
Wan
K. L.
,
Carruthers
V. B.
,
Sibley
L. D.
,
Ajioka
J. W.
(
1997
).
Molecular characterization of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2.
Mol. Biochem. Parasitol
84
,
203
214
Ward
G. E.
,
Miller
L. H.
,
Dvorak
J. A.
(
1993
).
The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes.
J. Cell Sci
106
,
237
248
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