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Location of the 18/28S Ribosomal RNA Genes in Two

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Location of the 18/28S Ribosomal RNA Genes in Two Proc. NatL Acad. Sci. USA Vol. 78, No. 6, pp. 3751-3754, June 1981 Genetics Location of the 18/28S ribosomal RNA genes in two Hawaiian Drosophila species by monoclonal immunological identification of RNADNA hybrids in situ (hybridoma/chromosomes/immunofluorescence/nucleolus) W. DORSEY STUART, JOHN G. BISHOP, HAMPTON L. CARSON, AND M. B. FRANK* Department of Genetics, John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, Hawaii 96822 Contributed by Hampton L. Carson, March 2, 1981 ABSTRACT Using both heterologous rabbit antisera and MATERIALS AND METHODS mouse monoclonal antibody to RNA-DNA hybrids, we have mapped the in situ hybridization locus of the 18/28S ribosomal Chromosomal Preparations. Salivary glands from larvae RNA fraction to a single large band on polytene autosome 3 in were excised in Grace's insect medium (GIBCO), fixed for 8-10 -Drosophila heteroneura and Drosophila silvestris. This portion of min in methanol/acetic acid, 3:1 (vol/vol), placed on acid- the chromosome is not physically connected with the nucleolus at washed slides with one drop of 45% acetic acid, and squashed the end of larval salivary gland development. In mature larvae, under siliconized coverslips. The preparations were held at little or no hybridization with the material in the nucleolus can be -20°C for at least 30 min and then immersed in liquid nitrogen. detected. In younger larvae, hybridization of the ribosomal RNA After 1 min, the slides were withdrawn and the coverslips were probe to the nucleolus itself can be observed. The chromosome removed by inserting a no. 10 surgical blade between the slide 3 locus is the only band in the polytene genome that shows variation and the coverslip. The slides were immediately immersed in in size and intensity of staining between populations and species. 95% ethanol. The slides remained in ethanol for at least 4 hr The interband chromosome regions that are immediately distal or prior to the in situ hybridization. Preparations may be stored proximal to the 18/28S tRNA locus have been involved in a dis- in ethanol for to 2 weeks proportionately large number of natural inversion breaks ob- up without deterioration of structure served in the euchromatic portion of the polytene chromosome. or hybridization results. In 104 species of Hawaiian Drosophila in which chromosome 3 RNA Probe. RNA was isolated from larvae quick-frozen in polytene sequences have been determined, 15 breaks occur in liquid nitrogen and stored at -70°C for up to 2 weeks. The these two regions. On a random basis, only one such break is ex- isolation method of Kirby (5) was used with the following mod- pected. We propose that this locus may be flanked by substantial ifications: sodium triisopropylnaphthalenesulfonate was substi- heterochromatic blocks which are not represented in the salivary tuted for sodium p-toluenesulfonate; the phenol/cresol extrac- gland chromosome. tion was repeated twice; and 3 M NaCl was substituted for 3 M sodium acetate to remove glycogen and tRNA. The high In the course of producing an antibody to RNA-DNA hybrid- molecular weight RNA salt precipitate was resuspended and duplexes, we have used in situ hybrids formed on polytene reprecipitated with 3 M NaCl a total of three times. The final chromosomes as an antigenic test system (1). The reports that precipitate was resuspended and made 0.12 M in NaCl, 0.01 fused immunoglobulin-producing cells would subsequently M in Tris-HC1 at pH 7.6, 1 mM in EDTA, and 0.02% in sodium produce both types ofparental immunoglobulins. have led to the dodecyl sulfate at an RNA concentration of2 mg/ml and applied development ofmonoclonal cell lines that produce large quan- to an oligo(dT)-cellulose column to remove polyadenylylated tities of specific antibody in culture (2, 3). Recently, we devel- RNA species (6). RNA not adsorbed to the column was collected oped a monoclonal cell line that produces antibody to RNA-DNA and precipitated with 2.5 vol of ethanol at -20°C overnight. hybrids (4) as part ofan experimental attempt to. identify in situ The precipitate was collected by centrifugation and resus- RNA-DNA hybrid-duplexes in human chromosomal prepara- pended at a concentration of 800 ,ug/ml in 0.01 M Tris-HCl, tions. As one assay for the presence of antibody, we used the pH 7.4/1 mM EDTA/0. 1 M NaCl. At this point the RNA sam- salivary gland chromosomes of larvae of Drosophila silvestris ple was further purified by either (a) sucrose gradient fraction- and D. heteroneura, two members of the Hawaiian picture- ation or (b) preparative electrophoresis as follows. winged species group, hybridized in situ with homologous ri- (a) A 500-,ul sample ofRNA was heated to 38°C for 5 min and bosomal RNA. Antibodies reactive with RNA-DNA hybrids applied directly to a 17-ml linear sucrose gradient (5-20%) made were obtained from immunized rabbits and from clonal.cultures in the same buffer. Heating to 65°C was avoided because this ofimmunized mouse spleen cells fused with a mouse myeloma treatment results in the denaturation of the 28S rRNA species cell line. found in insects and the denatured RNA comigrates with the Using these immunological reagents in a secondary immu- 18S species during centrifugation (7). The gradient was centri- nofluorescent assay, we have identified the in situ hybridization fuged in a Beckman instrument using an SW 27.1 rotor at 25,000 site for 18/28S rRNA. The genes are located in a chromosome rpm for 21.5 hr at 4°C. Fractions were collected and those con- region that is involved in an unusually large proportion of in- taining 28S RNA were pooled, precipitated, and resuspended version breaks which have occurred in the polytene sequence in hybridization solution (1:1 mixture offormamide and 0;6 M during phylogeny of the Hawaiian picture-winged species. NaCV0.06 M Na citrate, pH 7) (1). (b) RNA (230 ,ug) was applied in 2.5 ml of sample buffer (8) The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertise- * Present address: Department of Microbiology, College of Medicine, ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. University of California at Irvine, Irvine, CA 92717. 3751 3752 Genetics: Stuart et al. Proc. Natl. Acad. Sci. USA 78 (1981) to a 6 M urea/1% agarose gel (53 X 120 mm) formulated by the observed. (b) When the RNA normally present in the polytene method of Long and Dawid (8). The gel was run for 8 hr at 95 preparation was not predigested with RNase A, multiple flu- V (100 mA) and then stained for 15 min with ethidium bromide orescent bands were observed after hybridization. This indi- (8). The portion ofgel containing the large fragment ofthe dena- cated that the antibodies were not reactive with chromosomal tured 28S rRNA, 28S b (8), was placed in a dialysis bag with 3 DNA but did have the capacity to react with RNADNA du- ml ofgel buffer and electroeluted from the agarose for 3 hr. The plexes formed with more than one specific gene sequence. (c) eluted 28S fragment was precipitated with ethanol and resus- Absorption of antibody reagents with single-stranded pended in hybridization solution. poly(rA)-methylated albumin complexes or with RNA purified by either method gave similar hybridization poly(dT)-methylated albumin complexes did not reduce im- results. munofluorescent visualization ofin situ RNADNA hybrids. (d) In Situ Hybridization. Hybrids were prepared as reported Absorption of antibody reagents with poly(rA).poly(dT) du- (1). Estimates ofhybridization rates were obtained by incubat- plexes complexed to methylated albumin removed all activity ing preparations (sealed with rubber cement) at 70'C for 1 hr responsible for the secondary immunofluorescent bands. and then immediately shifting the preparations to 40'C by im- Therefore, the antibodies recognized RNA-DNA hybrids but mersion in a thermostatted water bath. Crt values were calcu- not other forms of RNA or DNA. lated as initial concentration of the RNA probe in mol per liter Localization ofthe 18/28S rRNA Locus. The in situ hybrid- multiplied by time (sec) ofincubation at40'C. The hybridization ization locus of the 18/28S rRNA is on chromosome 3 in both was terminated by immersion in an ice-water bath. D. silvestris (stock U28T2; Kilauea Forest Reserve, Hawaii) and Antibody Production. Rabbit antibody to poly(rA)-poly(dT) D. heteroneura (stock Q71G12; Olaa Tract, Hawaii). This chro- hybrids complexed to methylated bovine serum albumin was mosome is anautosomal element, designated B by Muller (11). prepared by the method ofStollar (9). Mouse monoclonal hybrid It is homologous to arm 2L ofD. melanogaster. The locus maps cell cultures to the same antigen were prepared by the method to a single band interstitially located in the basal third of the ofOi and Herzenberg (10). Immunized spleen cells were fused euchromatic arm. The relevant band isjustproximal to the distal with P3-NS-1 BALB/c myeloma cells (originally derived from break ofinversion 3b (figure 2 in ref. 12). The band is just distal the BALB/c MOPC-21 cell line) provided by Douglas Vann. to the three coincident breaks mapped for inversions 3i, 3c, and Positive fusion cultures were cloned by the limiting dilution 3a. We have examined several hundred preparations from both method (10). One positive clone (FS/B12-G10) was chosen for D. silvestris and D. heteroneura. After the fluorescent regions use in this study. were visualized, a phase condenser was inserted into the system Identification of Hybrids. Regions of in situ hybridization and phase-contrast photomicrographs were taken.
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