Localization of putative Onchocerca volvulus antigens by in situ hybridization and immunochemistry

by Rocky S. Tuan

Our efforts during this past year have been devoted to two main areas:

1) application of the existing histological techniques of in situ hybridization (ISH) and immunohistochemistry (IMH) to localize gene expression of antigen of O. volvulus 3in various developmental stages of the parasite, using cloned DNA's and antibodies directed against recombinant antigens provided by investigators in the field; and

2) further development of ultrastructural protocols using the scanning electron microscope (SEM) for ISH and IMH mapping of antigen expression.

Localization of Gene Expression by ISH and IMH

These studies have been carried out in collaboration with the following investigators: Francine Perler (New England Biolabs), Thomas Unnasch (University of Alabama), Sara Lustigman (New York Blood Center), Alan Scott (Johns Hopkins University), A. E. Bianco (Liverpool School of Tropical Medicine), and R. Chandrashekar (Washington University). Parasite specimens of various developmental stages, including larval (L2 and L3, both free and embedded within the blackfly host) and adult/microfilarial (contained within human skin nodules), have been processed for ISH and IMH. For ISH, the DNA probe is biotin-labelled and hybridization is detected via biotin-labelled secondary antibodies and streptavidin-peroxidase histochemistry. The antigens (and the available probes) include:

Perler: O13/O15 (DNA and antibodies)
Unnasch: RAL-2 (DNA and antibodies)
Lustigman: OV7 (DNA and antibodies) and OV103 (DNA)
Scott: M3/M4 (DNA)
Bianco: B20 (DNA)
Chandrashekar: OV1C (DNA), OV-1 and OV-5 (antibodies)

All of these studies have been completed, with each ISH and IMH repeated two to three times to ensure consistent signals. All specimens are examined by Nomarski differential interference optics and recorded using Kodak Ektar film. The results have revealed significant differences among these antigens in terms of tissue/cell distribution as well developmental stage specificity. This information should be useful for the evaluation of these antigens as potential vaccine candidates.

Ultrastructural SEM Procedure for IMH and ISH

The histolocalization procedures we have used for the gene expression studies described above utilize sections of paraffin-embedded parasite specimens. The fixation and embedding conditions are such that both mRNA and proteinaceous antigens appear to retain their reactivity with the respective DNA probe and antibodies. The calorimetric signals generated via enzyme-catalyzed chromogenic reactions permit observations at the light microscopy level, and with the use of Nomarski differential interference optics yield excellent resolution of the distribution and location of the mRNA- and antigen-derived signals. To gain further insight into the ultrastructural aspects of gene expression, it is preferable to carry out such analysis at the electron microscopy level. In this funding period, we have developed the following protocol for SEM analysis of antigen expression.

The protocol utilizes specimens which have already been processed into 8 µm tissue sections placed onto a glass slide, thereby allowing access of the DNA/antibody probes. Briefly, the procedure involves: 1) for IMH, incubation of the immuno-reacted sections with latex-polystyrene beads conjugated with Protein A (Polysciences, Inc.); and 2) for ISH, sequential incubation of the sections, which have been hybridized with biotin-labelled probe, with antibodies against biotin and Protein A-conjugated beads. Since the Protein A-conjugated beads are also tagged with a fluorescent dye, the efficacy of the labelling procedure is conveniently established prior to processing for SEM (i.e. dehydration and critical point drying).

Figure 1

Results we have obtained at this point are very promising and representative micrographs are shown in the accompanying figure (Figure 1). To summarize, the SEM IMH analysis provides high resolution, discrete localization of the antigen, yielding information consistent with that seen previously by light microscopy; O13/O15 and RAL2 have been examined so far. The results on the SEM ISH are more preliminary and will require additional troubleshooting. The main technical difficulty here is that the extensive digestion required to render the mRNA accessible to the probe also increases the "stickness" of the specimen, resulting in a higher level of background binding by the polystyrene-latex beads.

Figure 2

We are currently testing various incubation conditions to overcome this difficulty, which we believe is surmountable. [A presentation of our recent findings using SEM was made in the 50th Meeting of the Electron Microscopy Society of America held in Boston, MA, in August, 1992 (Immunohistochemical localization of gene expression in Onchocerca volvulus using latex spheres as SEM marker by Kreitzer, Tuan and Shepley)].


SEM Morphology of Insect Stage O. volvulus L3 Larvae

An additional accompanying project which we have undertaken while processing the various parasite specimens, is to carry out a detailed SEM study of the L3 larvae located within the mouthpart of the Simulium fly, to gain some insight as to how the larvae invade and inhabit the fly head. Specimens fixed in Carnoy's solution are dehydrated and dried for SEM. The labial structures of the fly proboscis are then sequentially and carefully removed to uncover the internally localized L3 larvae. The observations are shown in the accompanying figure (Figure 2). A large number of L3 larvae, up to 15-20, are usually found located within the opening of the labia, and are aligned along the axis from the labial pharynx to the labia, i.e. along the axis of the fly head. One end of the larva therefore lies deep within the mouth cavity, whereas the other end is situated close to the mandibular opening. This type of arrangement most likely contributes to the easy delivery of the parasite to the human host as a result of the insect bite. How the larvae migrate from the thoracic muscle, concomitant with an L2 to L3 molting stage, to their location in the mouthpart is presently poorly understood. We intend to carry out additional SEM observation of the fly at various stages after ingestion of the microfilariae to gain further insight into this interesting developmental event in the life cycle of the parasite.

Figure Legends

Figure 1. Localization of O13/O15 antigen in O. volvulus within human skin nodule by SEM IMH. (A) Intrauterine, mature microfilariae (MF) are seen decorated with 1 µm beads (arrows) in sample incubated with antibodies to O13/O15. (B) Control treated similarly except that the primary antibodies are omitted from the incubation mixture, showing absence of beads. C, cuticle; H, hypodermis; M, muscle layer; U, uterine wall. Magnification bar = 10 µm.

Figure 2. SEM view of Simulium stage O.volvulus L3 larvae. (A) Frontal low magnification view of the fly head structure, clearly displaying the labia of the proboscis. (B) Exposure of abundant L3 larvae (arrow) after removal of the labia. (C) High magnification of L3 larvae, showing cuticular ridges on the surface of the parasites. Magnification bar = 100 µm (A) or 10 µm (B and C).