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A Widely Distributed Antigen Developmentally Regulated in the Nervous System

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A Widely Distributed Antigen Developmentally Regulated in the Nervous System Development 109, 743-752 (1990) 743 Printed in Great Britain ©The Company of Biologists Limited 1990 A widely distributed antigen developmentally regulated in the nervous system OLIVIER POURQUIE, MONIQUE COLTEY, JEAN-LEON THOMAS and NICOLE M. LE DOUARIN Institut d'embryologie cellulaire el moliculaire du CNRS et du College de France, 49 bis avenue de la Belle Gabnelle, 94 736 Nogent sur Marne, Cedex, France Summary We have identified a glycoprotein (BEN) of ively from the fibres. The loss of expression is concomi- 95-100 xK^Mr using a monoclonal antibody. This pro- tant with the onset of intense proliferation of satellite and tein is transiently expressed at the cell surface of the Schwann cells. This modulated expression within the peripherally projecting neurons, i.e. motoneurons of the nervous sytem is unlike that of any surface glycoprotein spinal cord and cranial nuclei, sensory neurons of the so far described in vertebrates. Preliminary biochemical dorsal root and cranial sensory ganglia and sympathetic, analysis indicates that, although it bears the adhesion- parasympathetic and enteric neurons. In vitro cultures associated epitope HNK-1, BEN does not share charac- of dorsal root and sympathetic ganglia have shown that teristics with any previously described axonal glyco- BEN is expressed on neurons but not on glial cells. On protein. Consequently, we speculate that this glyco- motor and sensory neurons, BEN first appears at the protein might be a novel molecule implicated in selective level of the cell body just after withdrawal from the cell adhesion phenomena, such as axonal fasciculation. cycle. Soon afterwards, expression of the antigen ex- tends to the elongating axon. After a few days, BEN is no longer expressed by the motor and sensory neurons, Key words: monoclonal antibody, BEN, glycoprotein, disappearing first from the cell body and then progress- neurogenesis, HNK-1. Introduction nants of the epithelial component of the bursa of Fabricius, an organ unique to birds, in which B lympho- Morphogenesis and cell differentiation are processes cytes differentiate. The antigen recognized by this that occur in a highly integrated manner during embry- MAb, which we have named BEN, turned out to be onic development. They are the result of the interplay expressed by several other cell types, including neurons between inherited information and the environmental of both the central (CNS) and peripheral (PNS) ner- influences to which differentiating cells are subjected. vous systems. The pattern of BEN expression in the Cellular interactions are mediated by molecular entities developing nervous system appears to be strictly devel- expressed on the cell surface and interacting either with opmentally regulated, in a way that is suggestive of a defined components of the extracellular matrix (ECM) role for this surface molecule in the establishment of the or with their counterpart on other cells. Deciphering neural network during axonal extension and growth the 'grammar' that underlies cellular interactions during cone navigation. development first necessitates the identification of the molecular structures involved. The search for mono- clonal antibodies (MAb) (Kdhler and Milstein, 1975) specific for certain cell types or defining antigens Materials and methods expressed on certain cell lineages at precise develop- mental stages has been a successful way to approach this Embryos problem. Fertilized eggs from chick {Callus gallus) and quail (Coturnix coturnix japonica) were obtained from commercial sources, In this laboratory, we have long been interested in and were incubated in a rotary incubator at 37 °C. Stages of the development of the nervous and immune systems in development of the embryos were expressed according to which monoclonal antibody technology has revealed Hamburger and Hamilton (1951), in pair of somites for early the existence of several common antigens (Dalchau et stages, or in days of incubation for later stages. al. 1980; Clark et al. 1985; P6ault et al. 1987). We describe here the cellular specificity of a MAb Generation of monoclonal antibodies (MAb) that was prepared in mouse against surface determi- BEN MAb was obtained by the following immunization 744 O. Pourquii and others procedure. The epithelium of the bursa of Fabricius of E15 single bursa homogenized in PBS and mixed with an equal chick embryos was mechanically depleted of hemopoietic volume of incomplete Freund's adjuvant. Four days later, cells, and was then grafted into the spleen of 3-month Balb/C splenocytes were fused with SP2O myeloma cells (Kdhler and mice. One month later, the mice were boosted by direct Milstein, 1975). Hybridoma supernatants were used for im- injection in the spleen (without surgery) of the epithelium of a munocytochemical screening of frozen sections of E15 bursa Fig. 1. BEN MAb staining of a transverse section of a E14 quail bursa of Fabricius. The follicular (FE) and the luminal (LE) epithelia are strongly immunoreactive. L, lumen; M, mesenchyme. (x90). Fig. 2. In vitro cultures of sympathetic (A) and dorsal root (B) ganglia from E12 chick, grown for 5 days and stained with BEN MAb showing clusters of immunoreactive neurons. (x280). BEN expression in embryonic nervous system 745 of Fabricius, thymus and gut. Various clones presenting a (IBF) column (Corthier et al. 1984). This purified antibody reactivity against the bursal epithelium were obtained. Some was coupled to CNBr-Sepharose (Pharmacia) in order to of them also displayed a reactivity against the ganglionic make the affinity matrix. BEN affinity purification was carried plexuses of the gut. These clones were subcloned twice and out using the batch procedure, with columns made of 10 ml one of them, BEN, was subjected to further immunochemical matrix in 50 ml Falcon tubes. Either frozen E16 bursas or and biochemical examination. The BEN MAb is an IgGl that spinal cords, or whole E5 chicks were used. Tissues were recognizes the bursal epithelium and the enteric plexuses of homogeneized in the extraction buffer (PBS, 0.5% NP40, both chick and quail species. No reactivity was detected on 50 mM phenylmethyl-sulfonide-fluoride (PMSF)) and left on sections of E13 mouse embryos. ice for lh. The homogenate was then centrifuged at 13 000 revs min"1 for at least 3h and the supernatant was Histological and immunocytochemical procedures added to a non-specific column to which affinity-purified Whole embryos (until 8 days), or isolated organs (after 8 mouse IgG (Nordic) had been coupled. The column was left days) were fixed in a solution of 1% acetic acid in 100% to rotate overnight at 4°C, centrifuged and the supernatant ethanol at —20°C, then embedded in paraffin, and sectioned. Immunocytochemical staining was carried out on 5jun serial sections as follows. Paraffin was removed from slides by toluene-ethanol treatment. For immunoperoxidase staining, slides were left 30min in 0.3% H2O2 in phosphate-buffered saline (PBS), and washed 3 times lOmin in PBS containing 5% newborn calf serum (NCS; GIBCO), before application of the BEN MAb. For immunofluorescence, slides were left 30 min in PBS/5 % NCS, before treating with the BEN MAb. The BEN MAb was used either as a culture supernatant, or as 1/500 dilution of ascitic fluid and was applied on slides overnight at 4°C. The slides were then washed 3 times in PBS and the second antibody was applied for 1 h at room tempera- ture. Immunofluorescence staining was performed using either an anti-IgG or an anti-IgGl antibody coupled to fluorescein isothiocyanate (Southern Biotechnologies Associ- ates) and diluted 1/50 in PBS. Immunoperoxidase staining was carried out using an anti-IgGl antibody coupled to horseradish peroxidase (Southern Biotechnologies Associ- ates) and diluted 1/50 in PBS. Slides were then washed three times in PBS and mounted in 90% glycerol and paraphenyle- nediamine (lOOmgr1) in PBS for immunofluorescence; the peroxidase reaction was carried as described by Bucy et al. (1988). We have also used the MAb 13F4 (Rong et al. 1987) as a marker of myogenic lineage; double staining were carried out with the BEN MAb revealed with the peroxidase reac- tion, and 13F4 revealed with the alkaline phosphatase reac- tion as described by Malik and Daymon (1982). Cultures of sympathetic and dorsal root ganglia Cultures of sympathetic ganglia (SG) and dorsal root ganglia (DRG) of E12 chick embryos were obtained by excising the ganglia and dissociating the cells in 0.1% trypsin (Difco), 0.1% EDTA solution in PBS for 15min at 37°C. The cell suspension was then washed with PBS containing 5 % NCS, the cells were plated on 35 mm dishes (Nunc), and grown for 5 days in Dulbecco's Modified Eagle's Medium supplemented with 5% foetal calf serum. Cultures were then fixed in 4% paraformaldehyde, or in 100% ethanol for 1 h, rinsed in PBS and processed for immunostaining. Fig. 3. Immunofluorescence staining with BEN MAb of a Biochemistry transverse section in the cervical region of a stage 16 chick Western blotting was carried out as described elsewhere embryo. A few cells are immunoreactive in the floor plate (Dulac et al. 1988) using E7, E10, E12, E16 and adult DRG, (FPC) and in the ventral zone (VZ) of the neural tube (NT) SG, spinal cord and bursa of Fabricius as well as whole E5 where the postmitotic motoneurons first appear. The arrow embryos. The samples, subjected to SDS-PAGE (Laemmli, points to immunoreactive fibres growing dorsally in the 1970) on 7.5 or 10% acrylamide gels prior to blotting, were neural tube. The double arrow shows the growing ventral homogenized in PBS containing 0.5% Nonidet P40 (NP 40), root exiting into the sclerotome (Scl). (X400). left on ice for 1 h and then centrifuged at 15 000 revs min~l for Fig. 4. Immunoperoxidase staining with BEN MAb of a 15 min in a Sigma microfuge. For the blotting assay, BEN transverse section of a stage 19 chick embryo at the brachial ascitic fluid was used at a dilution of 1/250 in washing solution level.
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