Toxoplasma Gondii

The Model Apicomplexan - Perspectives and Methods

Louis M. Weiss,Kami Kim

• Editore: Academic Press
• Anno: 2020
• ISBN:
  9780128150429
• Edizione: 3
• Argomento: Biological Sciences
• Categoria: Microbiology

Toxoplasma gondii: The Model Apicomplexan - Perspectives and Methods, Third Edition, reflects significant advances in the field in the last five years, including new information on the genomics, epigenomics and proteomics of T. gondii, along with a new understanding of the population biology and genetic diversity of this organism. This edition expands information on the effects of T. gondii on human psychiatric disease and new molecular techniques, such as CAS9/CSPR. T gondii remains the best model system for studying the entire Apicomplexa group of protozoans, which includes Malaria, making this new edition essential for a broad group of researchers and scientists.

• Presents a complete review of molecular and cellar biology and immunology of Toxoplasma gondii combined with methods and resources for working with this pathogen
• Provides a single source reference for a wide range of scientists and physicians working with this pathogen, including parasitologists, cell and molecular biologists, veterinarians, neuroscientists, physicians and food scientists
• Covers recent advances in the genomics, related bioinformatics analysis, epigenomics, gene regulation, genetic manipulation and proteomics of T. gondii
• Details advances in the molecular and cellular biology and immunology of Toxoplasma, and in the epidemiology, diagnosis, treatment and prevention of toxoplasmosis

Chapter 1

The history and life cycle of Toxoplasma gondii

J.P. Dubey, Animal Parasitic Diseases Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD, United States

Abstract

Infections by the protozoan parasite Toxoplasma gondii are widely prevalent in humans and other animals on all continents. There are many thousands of references to this parasite in the literature, and it is not possible to give equal treatment to all authors and discoveries. The objective of this chapter is, rather, to provide a history of the milestones in our acquisition of knowledge of the biology of this parasite.

Keywords

Toxoplasma gondii; history; cats; oocyst

1.1 Introduction

Infections by the protozoan parasite Toxoplasma gondii are widely prevalent in humans and other animals on all continents. There are many thousands of references to this parasite in the literature, and it is not possible to give equal treatment to all authors and discoveries (Dubey, 2008). The objective of this chapter is, rather, to provide a history of the milestones in our acquisition of knowledge of the biology of this parasite.

1.2 The etiological agent

Nicolle and Manceaux (1908) found a protozoan in tissues of a hamster-like rodent, the gundi, Ctenodactylus gundi, which was being used for leishmaniasis research in the laboratory of Charles Nicolle at the Pasteur Institute in Tunis. They initially believed the parasite to be Leishmania but soon realized that they had discovered a new organism and named it T. gondii based on the morphology (mod. L. toxo=arc or bow, plasma=life) and the host (Nicolle and Manceaux, 1909). Thus its complete designation is T. gondii (Nicolle and Manceaux, 1908, 1909). In retrospect the correct name for the parasite should have been T. gundii, as Nicolle and Manceaux (1908) had incorrectly identified the host as Ctenodactylus gondi. Splendore (1908, see also English translation Splendore, 2009) discovered the same parasite in a rabbit in Brazil, also erroneously identifying it as Leishmania, but he did not name it. It is a remarkable coincidence that this disease was first recognized in laboratory animals and was first thought to be Leishmania by both groups of investigators.

1.3 Parasite morphology and life cycle

1.3.1 Tachyzoites

The tachyzoite (Frenkel, 1973) is lunate (Figs. 1.1 and 1.2A) and is the stage that Nicolle and Manceaux (1909) found in the gundi. This stage has also been called trophozoite, the proliferative form, the feeding form, and endozoite. It can infect virtually any cell in the body. It divides by a specialized process called endodyogeny, first described by Goldman et al. (1958). Gustafson et al. (1954) first studied the ultrastructure of the tachyzoite. Sheffield and Melton (1968) provided a complete description of endodyogeny when they fully described its ultrastructure.

Figure 1.1 Life cycle of Toxoplasma gondii.

Figure 1.2 Life cycle stages of Toxoplasma gondii.
(A) Tachyzoites (arrowhead) in smear. Giemsa stain. Note nucleus dividing into two nuclei (arrow). (B) A small tissue cyst in smear stained with Giemsa and a silver stain. Note the silver-positive tissue cyst wall (arrowhead) enclosing bradyzoites that have a terminal nucleus (arrow). (C) Tissue cyst in section, PAS. Note PAS-positive bradyzoites (arrow) enclosed in a thin PAS-negative cyst wall. (D) Unsporulated oocysts in cat feces. Unstained. PAS, Periodic acid–Schiff.

1.3.2 Bradyzoite and tissue cysts

The term “bradyzoite” (Gr. brady=slow) was proposed by Frenkel (1973) to describe the stage encysted in tissues. Bradyzoites are also called cystozoites. Dubey and Beattie (1988) proposed that cysts should be called tissue cysts (Figs. 1.1, 1.2B, and 1.2C) to avoid confusion with oocysts. It is difficult to determine from the early literature who first identified the encysted stage of the parasite (Lainson, 1958). Levaditi et al. (1928) apparently were the first to report that T. gondii may persist in tissues for many months as “cysts”; however, considerable confusion between the term “pseudocysts” (group of tachyzoites) and tissue cysts existed for many years. Frenkel and Friedlander (1951) and Frenkel (1956) characterized cysts cytologically as containing organisms with a subterminal nucleus and periodic acid–Schiff-positive granules (Fig. 1.2C) surrounded by an argyrophilic cyst wall (Fig. 1.2B). Wanko et al. (1962) first described the ultrastructure of the T. gondii cyst and its contents. Jacobs et al. (1960a) first provided a biological characterization of cysts when they found that the cyst wall was destroyed by pepsin or trypsin, but the cystic organisms were resistant to digestion by gastric juices (pepsin-HCl), whereas tachyzoites were destroyed immediately. Thus tissue cysts were shown to be important in the life cycle of T. gondii because carnivorous hosts can become infected by ingesting infected meat. Jacobs et al. (1960b) used the pepsin digestion procedure to isolate viable T. gondii from tissues of chronically infected animals. When T. gondii oocysts were discovered in cat feces in 1970, oocyst excretion was added to the biological description of the cyst (Dubey and Frenkel, 1976).

Dubey and Frenkel (1976) performed the first in depth study of the development of tissue cysts and bradyzoites and described their ontogeny and morphology. They found that tissue cysts formed in mice as early as 3 days after their inoculation with tachyzoites. Cats excrete oocysts (Fig. 1.2D) with a short prepatent period (3–10 days) after ingesting tissue cysts or bradyzoites, whereas after they ingested tachyzoites or oocysts, the prepatent period was longer (≥18 days), irrespective of the number of organisms in the inocula (Dubey and Frenkel, 1976; Dubey, 1996, 2001, 2006). Prepatent periods of 11–17 days are thought to result from the ingestion of transitional stages between tachyzoite and bradyzoite (Dubey, 2002, 2005).

Wanko et al. (1962) and Ferguson and Hutchison (1987) reported on the ultrastructural of the development of T. gondii tissue cysts. The biology of bradyzoites including morphology, development in cell culture in vivo, conversion of tachyzoites to bradyzoites, and vice versa, tissue cyst rupture, and distribution of tissue cysts in various hosts and tissues was reviewed critically by Dubey et al. (1998).

1.3.3 Enteroepithelial asexual and sexual stages

Asexual and sexual stages (Figs. 1.3 and 1.4) were reported in the intestine of cats in 1970 (Frenkel, 1970). Dubey and Frenkel (1972) described the asexual and sexual development of T. gondii in enterocytes of the cat and designated the asexual enteroepithelial stages as Types A through E (Figs. 1.3 and 1.4) rather than as generations conventionally known as schizonts in other coccidian parasites. These stages were distinguished morphologically from tachyzoites (Fig. 1.3D) and bradyzoites, which also occur in cat intestine. The challenge was to distinguish different stages in the cat intestine because there was profuse multiplication of T. gondii 3 days postinfection (Fig. 1.4A). The entire cycle was completed in 66 hours after feeding tissue cysts to cats (Dubey and Frenkel, 1972). There are reports on the ultrastructure of schizonts (Sheffield, 1970; Piekarski et al., 1971; Ferguson et al., 1974), gamonts (Ferguson et al., 1974, 1975; Speer and Dubey, 2005), oocysts, and sporozoites (Christie et al., 1978; Ferguson et al., 1979a,b; Speer et al., 1998; Freppel et al., 2019). In 2005 Speer and Dubey described the ultrastructure of asexual enteroepitheli...