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The Fine Structure of Giardia Muris

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The Fine Structure of Giardia Muris View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central THE FINE STRUCTURE OF GIARDIA MURIS DANIEL S. FRIEND From the Department of Anatomy, Harvard Medical School, Boston, Massachusetts. The author's present address is Department of Pathology, University of California School of Medicine, San Francisco Medical Center, San Francisco, California ABSTRACT Giardia is a noninvasive intestinal zooflagellate. This electron microscope study demon- strates the fine structure of the trophozoite of Giardia muris in the lumen of the duodenum of the mouse as it appears after combined glutaraldehyde and acrolein fixation and osmium tetroxide postfixation. Giardia muris is of teardrop shape, rounded anteriorly, with a convex dorsal surface and a concave ventral one. The anterior two-thirds of the ventral surface is modified to form an adhesive disc. The adhesive disc is divided into 2 lobes whose medial surfaces form the median groove. The marginal grooves are the spaces between the lateral crests of the adhesive disc and a protruding portion of the peripheral cytoplasm. The organ- ism has 2 nuclei, 1 dorsal to each lobe of the adhesive disc. Between the anterior poles of the nuclei, basal bodies give rise to 8 paired flagella. The median body, unique to Giardia, is situated between the posterior poles of the nuclei. The cytoplasm contains 300-A granules that resemble particulate glycogen, 150- to 200-A granules that resemble ribosomes, and fusiform clefts. The dorsal portion of the cell periphery is occupied by a linear array of flattened vacuoles, some of which contain clusters of dense particles. The ventrolateral cytoplasm is composed of regularly packed coarse and fine filaments which extend as a striated flange around the adhesive disc. The adhesive disc is composed of a layer of micro- tubules which are joined to the cytoplasm by regularly spaced fibrous ribbons. The plasma membrane covers the ventral and lateral surfaces of the disc. The median body consists of an oval aggregate of curved microtubules. Microtubules extend ventrally from the median body to lie alongside the caudal flagella. The intracytoplasmic portions of the caudal, lateral, and anterior flagella course considerable distances, accompanied by hollow filaments adjacent to their outer doublets. The intracytoplasmic portions of the anterior flagella are accompanied also by finely granular rodlike bodies. No structures identifiable as mito- chondria, smooth endoplasmic reticulum, the Golgi complex, lysosomes, or axostyles are recognized. INTRODUCTION Giardia is a zooflagellate which inhabits the intes- mian physician, Wilhelm Lambl.) Based upon tines of many vertebrates. Its trophozoite form was different host specificity and minor structural vari- first described by Antoni van Leeuwenhoek in 1681 ations, nearly 50 different species of Giardia re- (19). From his lucid description of the parasite, covered from the intestines of numerous verte- zoologists of later generations were able to recog- brates have been reported. As methods for the in- nize the organism described, as Giardia lamblia. vestigation of unicellular organisms improved, (The genus was later named for the 19th century however, the multiplicity of species listed could be French biologist, and the species after the Bohe- reduced to 2 morphologic groups. This simplifica- 317 tion was possible because the major cytologic vari- bedding medium was Epon 812 ('20). Sections were ations among the species of Giardia were in their cut with glass or diamond knives on a Porter-Blum dimensions, and the size, incidence, and shape of microtome. Sections displaying silver to gold inter- the median body, a transient organelle peculiar to ference colors were picked up on uncoated, or Form- vat- and carbon-coated copper grids. Various electron Giardia. The following general description of the microscopic stains, urany1 acetate, lead citrate, lead fine structure of the trophozoite of is Giardia muris hydroxide, and lead tartrate, were used singly and in thus applicable to the genus as a whole, with only combination to increase contrast of the material. those parts devoted to the median body perhaps Sections were examined with an RCA EMU 3-F or a being peculiar to Giardia muris. Siemens Elmiskop I. Sections for light microscopy With the recognition of its widespread distribu- were cut at 1 # and stained with toluidine blue in tion, its association with certain intestinal diseases borate or by the periodic acid Schiff (PAS) reaction. in man (30, 32), and the recent development of an in vitro culture method for Giardia (17), interest in OBSERVATIONS this noninvasive, intestinal flagellate has greatly General Configuration and Structural Re- increased. There are several detailed light micro- scope studies of Giardia (9), but no comparable lationships electron microscope description of the parasite Giardia muds is a binucleate zooflagellate, 10 to has yet appeared. In 1954, Rossi-Espagnet and 12 ~ in length and 5 to 7 # in width. It is rounded Piccardo (27) studied whole mounts of the organ- anteriorly and tapered posteriorly in a discoid form, ism with the electron microscope but were unable with a convex dorsal surface and a concave ventral to extend descriptions beyond those previously surface (Fig. 1). A bilobed adhesive disc occupies based upon light microscopy. Cheissin (5) in 1964 the anterior 2/~ of the ventral surface. One nucleus described the fine structure of the sucking disc and is located above each lobe of the disc (Fig. 3). The the median bodies of Lamblia duodenalis from the medial edges of the lobes of the adhesive disc form rabbit, and Takano and Yardley (30) recently the ventral (median) groove and the outer edge described Giardia lamblia found in human ileum forms the medial limit of the lateral (marginal) biopsies, but inadequacy of preservation of the groove (Figs. 2, 15). The lateral limit of the mar- organism with osmium tetroxide prevented de- ginal groove is formed by a striated portion of the tailed interpretation of several aspects of its fine cytoplasm above and lateral to the adhesive disc structure, particularly the microtubular compon- (Figs. 2, 15). ent of the adhesive disc, the relationships between Giardia has 8 flagella, 2 of which emerge ven- the microtubules of the median body and other trally, 2 anterolaterally, 2 posterolaterally, and 2 organelles, and the striations of the peripheral ven- caudally. Their basal bodies are near the midline, tral cytoplasm. The purpose of this study is to des- cribe the fine structure of the trophozoite of Giardia in the lumen of the duodenum of the mouse as it appears after combined glutaraldehyde and acro- lein fixation and osmium postfixation. MATERIALS AND METHODS The trophozoites of Giardia muris were located in the duodenum of mice of the AKD-2 strain. The pro- tozoa were fixed in situ by removing the duodenum and inunersing and mincing the tissue in cold fixa- tive. The fixative employed was 6.5% glutaraldehyde and 2% acrolein (28) buffered to pH 7.45 with 0.1 M phosphate buffer. After 2-hr fixation, the tissues were washed for 2 hr in the buffer and then postfixed for 2 hr in cold 1.3% osmium tetroxide buffered to pH 7.4 FIGURE 1 An idealized representation of the ventro- with the 0.1 ~ phosphate. The tissues were then de- lateral aspect of Giardla muris as seen by light micros- hydrated in a graded series of cold alcohols, brought eopy. AD, adhesive disc. C, ventrolateral flange. to room temperature in 100~ ethanol, and dehydra- MB, median body. AF, CF, PF, VF, anterior, caudal, tion was completed in propylene oxide. The am- posterior, and ventral flagella. N, nucleus. 318 THE JOURNAL OF CELL BIOLOGY • VOLLrI~E~9, 1966 FIGURE ~ A transverse section through Giardia muds, showing its discoid shape, general topography, and cytoplasmic structures. The marginal groove (MG) is the space between the striated rim of cyto- plasm (C) and the lateral ridge of the adhesive disc (AD). The ventral groove (VG) is the space be- tween the medial lips of the ~ lobes of the adhesive disc. One nucleus (N) is over each lobe of the disc. The central area of cytoplasm contains granules and clefts, whereas the dorsal portion of the cytoplasm is agranular and is occupied by vacuoles (V). The flagella are cut in cross-section. )< 15,500. anteroventral to the nuclei (Fig. 4), so that the clefts which vary in length and width (Fig. 14). intracytoplasmic portions of the anterior, caudal, The peripheral cytoplasm is agranular. Ellipsoid and lateral flagella subsequently course consider- vacuoles occupy most of the cell periphery that is able distances (Fig. 1). not occupied by the adhesive disc. The median body is located dorsal to the poste- No structures identifiable as mitochondria, rior poles of the nuclei. It consists of an oval ag- smooth endoplasmic reticulum, the Golgi complex, gregate of curved microtubules, some of which lysosomes, pigment bodies, or axostyles are recog- extend ventrally along side the intracytoplasmic nized. portions of the caudal flagella (Figs. 12, 13). Peripheral to the areas occupied by the median Nudei body, basal bodies, and flagella, the central area The 2 nuclei together occupy approximately of cytoplasm contains 2 types of granules embedded the length and ~ the width of the organism. Each in a matrix of moderate density. The larger of the nuclear envelope enclosing a 300- to 600-A peri- granules conform in structure and staining char- nuclear cistern, the outer membrane of which is acteristics to particulate glycogen, and the smaller, partially studded with ribosomes. The nuclear en- to ribosomes. Scattered in varying numbers velope is interrupted at irregular intervals with cir- throughout the granular cytoplasm are fusiform cular nuclear pores, traversed by thin diaphragms. DANIEL S. I~IEND Fine Structure of Giardia muris 319 FIGURE 3 A transverse section through Giardia muris farther anterior than in Fig.
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