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Chapter 8 : 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes

Authors: Mary R. Galinski1, Anton R. Dluzewski2, John W. Barnwell3
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Affiliations: 1: Emory Vaccine Center at the Yerkes National Primate Research Center and Division of Infectious Diseases, Department of Medicine, Emory University, 954 Gatewood Rd., Atlanta, GA 30329; 2: Department of Immunobiology, Guy's, King's and St. Thomas's School of Medicine, 2nd Floor,New Guy's House, King's College London, Guy's Hospital, London Bridge, London SE1 9RT, United Kingdom; 3: Malaria Branch, Division of Parasitic Diseases, Centers for Disease Control and Prevention, Mailstop F-36, A
Content Type: Monograph
Publication Year: 2005

Category: Microbial Genetics and Molecular Biology

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Abstract:

This chapter provides an overview of the dynamic nature of malaria from the perspective of the development of merozoites within an infected erythrocyte and the release of infectious merozoites, through the initiation and completion of the reinvasion process. The chapter encompasses discoveries or observations obtained through studies of different species of , which together have greatly aided and refined our understanding of these events. These species include not only the human malarias and , but also the simian malaria , the chimpanzee malaria , bird malarias such as and , and the rodent malarias, principally and . Malaria merozoites have a plasma membrane and the basic cellular machinery of typical eukaryotic cells, including a nucleus, endoplasmic reticulum, Golgi network, ribosomes, and mitochondria. As a merozoite begins to invade an red blood cells (RBCs), an internal membrane-lined invasion pit develops. The whole process of merozoite invasion can be divided into three or four distinct phases with a number of ultrastructural alterations and molecular events attributed to each phase, with an untold number of others likely to be discovered in the future. Merozoites must first be released from the wornout, hemoglobin-depleted, and extensively altered erythrocyte that hosted their development. Although many proteins have been identified in the spheroidal dense bodies of , only a few proteins besides ring-infected erythrocyte surface antigen (RESA) have been located in the dense bodies of .

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes
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Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
/content/10.1128/9781555817558.chap8.fig8-1
FIGURE 1

Generalized diagrammatic representation of a merozoite showing the main structural features and organelles and also depicting the process by which newly formed micronemes are translocated along the microtubules to their placement at the apical pole (Bannister et al., 2003).

10.1128/9781555817558/fig8-1_thmb.gif
10.1128/9781555817558/fig8-1.gif
Image of FIGURE 1
FIGURE 1

Generalized diagrammatic representation of a merozoite showing the main structural features and organelles and also depicting the process by which newly formed micronemes are translocated along the microtubules to their placement at the apical pole (Bannister et al., 2003).

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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/content/10.1128/9781555817558.chap8.fig8-2
FIGURE 2

Electron micrographs of (a) and (b) merozoites, showing the main structural features and organelles, as also detailed in the schematic shown in Fig. 1 .The parasite was obtained from an infected rhesus macaque and prepared for EM morphology fixation at the Emory Vaccine Center at the Yerkes National Primate Research Center. (The photograph of was produced with assistance from Michael J. Stewart and is reprinted from Galinski and Barnwell [1996], with permission from the publisher.)

10.1128/9781555817558/fig8-2_thmb.gif
10.1128/9781555817558/fig8-2.gif
Image of FIGURE 2
FIGURE 2

Electron micrographs of (a) and (b) merozoites, showing the main structural features and organelles, as also detailed in the schematic shown in Fig. 1 .The parasite was obtained from an infected rhesus macaque and prepared for EM morphology fixation at the Emory Vaccine Center at the Yerkes National Primate Research Center. (The photograph of was produced with assistance from Michael J. Stewart and is reprinted from Galinski and Barnwell [1996], with permission from the publisher.)

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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/content/10.1128/9781555817558.chap8.fig8-3
FIGURE 3

(a) EM featuring the triple membranes and surface coat of the merozoite shown in Fig. 2 with a tufted or spiked appearance. (b) Schematic representation of the merozoite membrane pellicle, consisting of the inner membrane complex, plasma membrane with connecting filaments, and a fibril bundled surface coat, as observed in .

10.1128/9781555817558/fig8-3_thmb.gif
10.1128/9781555817558/fig8-3.gif
Image of FIGURE 3
FIGURE 3

(a) EM featuring the triple membranes and surface coat of the merozoite shown in Fig. 2 with a tufted or spiked appearance. (b) Schematic representation of the merozoite membrane pellicle, consisting of the inner membrane complex, plasma membrane with connecting filaments, and a fibril bundled surface coat, as observed in .

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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FIGURE 4

Electron micrograph of a mature schizont with merozoites surrounding the residual body and their apical ends facing outwards. Note that the PVM still appears intact at this late stage of development. Caveola vesicle complex structures (CVC; the basis of Schüffner's stippling) ( ) can also be observed at the surface of the infected red blood cell membrane.The parasite was obtained from an infected rhesus macaque and prepared for EM morphology fixation at the Emory Vaccine Center at Yerkes.

10.1128/9781555817558/fig8-4_thmb.gif
10.1128/9781555817558/fig8-4.gif
Image of FIGURE 4
FIGURE 4

Electron micrograph of a mature schizont with merozoites surrounding the residual body and their apical ends facing outwards. Note that the PVM still appears intact at this late stage of development. Caveola vesicle complex structures (CVC; the basis of Schüffner's stippling) ( ) can also be observed at the surface of the infected red blood cell membrane.The parasite was obtained from an infected rhesus macaque and prepared for EM morphology fixation at the Emory Vaccine Center at Yerkes.

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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FIGURE 5

EM invasion sequence of merozoites. (a) Apically attached merozoite (cytochalasin B treated). (b) Invading merozoite with moving junction indicated. (c) Newly invaded, fully enveloped merozoite.The parasite preparations for panels a and c were generated for EM morphology fixation at the Emory Vaccine Center at the Yerkes National Primate Research Center. Figure 5b was contributed by Lawrence H. Bannister.

10.1128/9781555817558/fig8-5_thmb.gif
10.1128/9781555817558/fig8-5.gif
Image of FIGURE 5
FIGURE 5

EM invasion sequence of merozoites. (a) Apically attached merozoite (cytochalasin B treated). (b) Invading merozoite with moving junction indicated. (c) Newly invaded, fully enveloped merozoite.The parasite preparations for panels a and c were generated for EM morphology fixation at the Emory Vaccine Center at the Yerkes National Primate Research Center. Figure 5b was contributed by Lawrence H. Bannister.

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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FIGURE 6

Schematic representing the DBL, RBL, and AMA-1 protein families. Several members of each family are depicted with their predominant features highlighted, as indicated by the key at the bottom of the figure.

10.1128/9781555817558/fig8-6_thmb.gif
10.1128/9781555817558/fig8-6.gif
Image of FIGURE 6
FIGURE 6

Schematic representing the DBL, RBL, and AMA-1 protein families. Several members of each family are depicted with their predominant features highlighted, as indicated by the key at the bottom of the figure.

Citation: Galinski M, Dluzewski A, Barnwell J. 2005. 8 A Mechanistic Approach to Merozoite Invasion of Red Blood Cells: Merozoite Biogenesis, Rupture, and Invasion of Erythrocytes, p 113-168. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch8
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