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The Journal of Heredity 2001:92(3)
© 2001 The American Genetic Association 92:282-287

Brief Communication

Chromosomal Mapping of 18S-28S rRNA Genes and 10 cDNA Clones of Human Chromosome 1 in the Musk Shrew (Suncus murinus)

A. Kuroiwa, K. Matsubara, T. Nagase, N. Nomura, J. K. Seong, A. Ishikawa, R. V. P. Anunciado, K. Tanaka, T. Yamagata, J. S. Masangkay, V.-B. Dang, T. Namikawa, and Y. Matsuda

From the Laboratory of Animal Genetics, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan (Kuroiwa, Ishikawa, Anunciado, Tanaka, Yamagata, and Namikawa), Laboratory of Cytogenetics, Division of Bioscience, Graduate School of Environmental Earth Science, Hokkaido University, Sapporo, Japan (Kuroiwa and Matsubara), Laboratory of Gene Structure I, Kazusa DNA Research Institute, Chiba, Japan (Nagase and Nomura), Division of Laboratory Animal Science, Medical Research Center, College of Medicine, Yonsei University, Seoul, Korea (Seong), College of Veterinary Medicine, University of the Philippines at Los Baños, Laguna, the Philippines (Anunciado and Masangkay), Faculty of Animal Science, Hanoi Agricultural University, Gialam, Hanoi, Vietnam (Dang), and Chromosome Research Unit, Faculty of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060-0810, Japan (Matsuda).

Address correspondence to Yoichi Matsuda at the address above or e-mail: yoimatsu{at}ees.hokudai.ac.jp.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
The direct R-banding fluorescence in situ hybridization (FISH) method was used to map 18S-28S ribosomal RNA genes and 10 human cDNA clones on the chromosomes of the musk shrew (Suncus murinus). The chromosomal locations of 18S-28S ribosomal RNA genes were examined in the five laboratory lines and wild animals captured in the Philippines and Vietnam, and the genes were found on chromosomes 5, 6, 9, and 13 with geographic variation. The comparative mapping of 10 cDNA clones of human chromosome 1 demonstrated that human chromosome 1 consisted of at least three segments homologous to Suncus chromosomes (chromosomes 7, 10, and 14). This approach with the direct R-banding FISH method is useful for constructing comparative maps between human and insectivore species and for explicating the process of chromosomal rearrangements during the evolution of mammals.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
The musk shrew [Suncus murinus (Soricidae, Insectivora)] is distributed widely from eastern Africa to East and Southeast Asia, and the basic chromosome number of this species is 2n = 40. The chromosome number ranges from 30 to 40 in wild populations of several localities (Aswathanarayana and Prakash 1976; Ishikawa et al. 1989; Sam et al. 1979; Yosida 1982), and variation has been reported in the size and morphology of both autosomes and sex chromosomes (Manna and Talukdar 1967; Obara and Miyai 1981; Sharma et al. 1970; Yosida 1982). Laboratory lines of this species have been established and several spontaneous mutations in coat hair, behavior, diabetes, morphology, and others have been reported (Ishikawa et al. 1998; Matsuura et al. 1999; Ohno et al. 1994, 1998). Effects of various emetic and antiemetic drugs have been well studied using Suncus for its potential use as an experimental animal model of mammals in emetic research (Ueno et al. 1987), because Suncus is one of the few mammalian species (e.g., dog, cat, monkey) that vomit in response to emetic drugs. Therefore Suncus is very useful as a small experimental mammal for screening drugs that prevent motion sickness (Matsuki et al. 1997; Okada et al. 1995). The importance of Suncus is increasing in the field of biomedical sciences as an experimental animal, however, genetic analysis is almost impossible in this species because no chromosome maps have been established.

Direct R-banding fluorescence in situ hybridization (FISH) is a powerful technique for constructing high-resolution cytogenetic maps rapidly and efficiently by localizing cloned DNA sequences precisely onto banded metaphase chromosomes (Matsuda et al. 1992; Takahashi et al. 1990). Furthermore, this technique makes it possible to detect chromosomal homology between different species by localizing cDNA clones isolated from map-rich species to chromosomes of map-poor species (Kuroiwa et al. 1998).

In this study, to apply the direct R-banding FISH method for genome mapping in Suncus, first we demonstrated replication R-banding patterns of Suncus chromosomes and compared the karyotypes of the five laboratory lines derived from different localities. Using this method we mapped 18S-28S ribosomal RNA (rRNA) genes in the five laboratory lines and wild animals captured in Southeast Asia. Furthermore, 10 cDNA clones of human chromosome 1 were localized directly to Suncus chromosomes to detect conserved homology between human chromosome 1 and Suncus chromosomes.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
Animals
Five laboratory lines and wild animals listed in Table 1 were used in this study. The laboratory lines are maintained at the Laboratory of Animal Genetics, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan.


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  		Table 1.. Chromosomal locations of 18S-28S ribosomal RNA genes in five laboratory lines and wild animals

 
DNA Probes
A 6.6 kb mouse genomic DNA fragment was used for chromosomal localization of 18S-28S rRNA genes (Kominami et al. 1982). Human cDNA clones of HSA1 (Homo sapiens chromosome 1) listed in Table 2 were used for comparative mapping between human chromosome 1 and Suncus chromosomes. The cDNA clones were isolated from the size-fractionated cDNA libraries of the human brain (Seki et al. 1997) and these clones have been mapped by GeneBridge 4 radiation hybrid panel (Ishikawa et al. 1997). Their cytogenetic locations were estimated by the DNA markers close to the cDNA clones, of which precise locations on chromosomal bands have been determined [see the genome directory in Nature 1995;377(suppl)]. The information on these clones is available to the public in the KDRI database (http://www.kazusa.or.jp). KIAA444 and 463 clones showed 89.2% and 99.3% identities to human 218kD Mi-2 and OCT (plexin A2) genes, respectively (Ishikawa et al., 1997). Other clones showed less than 65% identities.


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  		Table 2.. List of human cDNA clones used for FISH mapping and their chromosomal locations

 
Chromosome Preparation and in situ Hybridization
Cell culture for R-banded chromosome preparations and FISH were performed as described by Matsuda and Chapman (1995) with slight modifications. Lymphocytes were isolated from the spleen of adult animals, washed twice with serum-free TC199 medium, and transferred to 25 cm2 culture flasks containing 10 ml TC199 supplemented with 20% fetal calf serum, 3 µg/ml concanavarin A, 10 µg/ml lipopolysaccharide, 50 µg/ml HA15 (Murex), and 5 x 10–5 M mercaptoethanol. The splenocytes were cultured for 46 h, and thymidine (300 µg/ml) was added in culture medium. After 14 h the cells were washed twice with serum-free TC199 medium, transferred to the culture medium, and then cultured with BrdU (30 µg/ml) for an additional 3.5 h. Colcemid (0.02 µg/ml) was added 30 min before harvesting the cells (total culture time with BrdU is 4 h). The chromosome slides were exposed to ultraviolet (UV) light after staining with Hoechst 33258 and stained with Giemsa for analyzing R-banded patterns. For G-band analysis, the cells were cultured without thymidine and BrdU treatments. The G-banded chromosomes were obtained by trypsin-treatment as described by Seabright (1971).

The DNA probes were labeled by nick translation with biotinylated 16-dUTP (Roche Diagnostics). The hybridized 18S-28S rRNA gene probes were stained with fluoresceinated avidin (Vector Laboratories). The hybridized cDNA probes were reacted with goat antibiotin antibodies (Vector Laboratories) and then stained with fluoresceinated donkey anti-goat IgG (Nordic Immunology). The slides were stained with 0.75 µg/ml propidium iodide (PI) for observation. FISH images were observed under a Nikon fluorescence microscope using Nikon filter sets B-2A and UV-2A. Kodak Ektachrome ASA100 films were used for microphotography.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
Variations of Chromosomal Morphology
The G- and R-banded karyotypes of the NAG line are shown in Figure 1. The G- and R-banded patterns were analyzed in detail using 13 and 10 metaphase spreads of the NAG line, respectively. Ambiguous or unusual banded patterns were observed for only a small number of chromosomes, 1.9% (10/520 chromosomes) and 1.5% (6/400 chromosomes) in G- and R-banded metaphases, respectively. These included unclear bands, dark-stained minor bands, and light-stained major bands. The replication R-banded pattern was the complete reverse of the G-banded pattern obtained by trypsin treatment as shown in Figure 1. Next we examined 4, 5, 5, 5, and 23 metaphase spreads of the OKI, TKU, BAN, KAT, and NAG lines, respectively, and found morphologic variations in chromosomes 16 and Y (Figure 2). We measured the length of the long arm (q) and short arm (p) of chromosomes 16 and Y in these five lines, and calculated the ratio of the long arm to the short arm (r = q/p). The r values of chromosomes 16 were 3.4, 4.1, 16.8, 23.3, and 39.6 in the OKI, TKU, NAG, BAN, and KAT lines, respectively. The r values of Y chromosomes were 1.2, 1.3, 1.3, 1.4, and 2.2 in the OKI, TKU, NAG, BAN, and KAT lines, respectively. Following the nomenclature for the centromeric position of chromosomes (Levan et al. 1964), chromosome 16 was subacrocentric in the OKI and TKU lines and acrocentric in other three lines. Y chromosomes were submetacentric in the KAT line and metacentric in the other four lines (Figure 2). The morphology of chromosomes 16 and Y was consistent with that reported by Rogatcheva et al. (1996). Geographical variation in the size and morphology of the sex chromosomes has been reported for both the X chromosome (Obara and Miyai 1981) and the Y chromosome (Sharma et al. 1970; Yosida 1982). Y chromosomes were not different in the size among the laboratory lines used in this study, hence the variation found in this study appears to be caused by pericentric inversion. Robertsonian fusion of acrocentric chromosomes has been reported by many researchers (Aswathanarayana and Prakash 1976; Ishikawa et al. 1989; Rogatcheva et al. 1997; Sam et al. 1979; Yosida 1982). The variation in the morphology of chromosome 16 was first found by chromosome banding analysis in this study.



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  		Figure 1.. The G- (left) and replication R-banded (right) patterns in NAG line of Suncus murinus.

 


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  		Figure 2.. The morphological variation of chromosomes 16 and Y in the five laboratory lines. M, SM, A, and SA are metacentric, submetacentric, acrocentric, and subacrocentric chromosomes, respectively. Arrowheads on the left side of the chromosomes indicate the centromeric regions.

 
Chromosomal Locations of 18S-28S rRNA Genes
The chromosomal locations of 18S-28S rRNA genes in the five laboratory lines and wild animals are shown in Table 1, and the hybridization patterns in the TKU, OKI, and KAT lines are shown in Figure 3. The hybridization signals were observed in the telomeric regions of chromosomes 9 and 13 in all the lines and wild animals, while variations in signal distributions were found in the short arms of chromosomes 5 and 6. The signals were detected in chromosome 5 in the TKU line, chromosome 6 in the OKI and BAN lines, and both chromosomes 5 and 6 in the NAG and KAT lines and the wild animals. No variation was observed between individuals in the wild populations of the Philippines and Vietnam. We observed 130, 123, 115, 135, 112, 144, and 108 metaphase spreads in the OKI, KAT, TKU, BAN, and NAG lines, and the Vietnam and Philippines wild animals, respectively. The frequencies of metaphases, in which the probes completely hybridized to the chromosomes with low copy number of the genes, were 43.8, 70.3, 87.0, 61.4, 84.3, 87.5, and 70.4% in the OKI, KAT, TKU, BAN, and NAG lines, and the Vietnam and Philippines wild animals, respectively.



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  		Figure 3.. Chromosomal localization of 18S-28S ribosomal RNA genes to chromosomes in (a,b) TKU, (c) OKI, and (d) KAT lines. A 6.6 kb genomic fragment of the 18S-28S ribosomal RNA gene was used as a biotinylated probe. Numbers indicate the chromosomes to which ribosomal RNA genes are localized. PI-stained R-banded patterns and Hoechst 33258 stained G-banded pattern are demonstrated in (a,c,d) and (b), respectively.

 
The mtDNA haplotype analysis by Yamagata et al. (1995) indicated that the wild populations of Suncus were classified into three groups: the continental group (Bangladesh and Nepal), the island's group (insular countries and Vietnam), and the Malay group. Following this classification the BAN and KAT lines should be classified into the continental group, and the OKI, NAG, and TKU lines and the wild animals of the Philippines and Vietnam into the island's group. However, the five laboratory lines and the wild populations were not classified into the two groups by the distribution patterns of the 18S-28S rRNA genes. The present results suggest that the chromosomal locations of the 18S-28S rRNA genes were conserved in chromosomes 9 and 13, and that either of chromosomes 5 and 6 with signals in the wild population was fixed in the TKU, OKI, and BAN lines in the process of domestication. Rogatcheva et al. (1997) reported that the 18S-28S rRNA genes were localized to the telomeric region of chromosomes 9 and 13 and the short arms of chromosome 5 in the four males of the KAT line by FISH methods. In this study, the hybridization signals of the rRNA genes in the short arms of chromosome 6 were observed in addition to chromosomes 5, 9, and 13 in three males of the KAT line maintained in our laboratory (Table 1). These results suggest a possibility that this variation arose in the process of domestication from the wild population with polymorphism in the chromosomal distribution of the rRNA genes.

Mapping of Human cDNA Clones
We localized 10 cDNA clones of HSA1, which were isolated as long-sized full-length cDNA clones, to Suncus murinus (SMU) chromosomes. The hybridization patterns of two clones, KIAA444 and 445, on Suncus chromosomes are demonstrated in Figure 4. The chromosomal locations of the 10 cDNA clones and the hybridization efficiency for each clone to Suncus chromosomes are shown in Table 2. No consistent fluorescence signals were observed on other chromosomes. The comparative mapping in this study revealed the presence of homology between HSA1 and Suncus chromosomes 7, 10, and 14 (SMU7, 10, and 14) (Figure 5). The homologous regions of SMU10 identified by six genes were divided into four segments in HSA1. The order of KIAA456, 449, and 463 clones in HSA1 was conserved in Suncus chromosomes, and the other three genes, KIAA450, 445, and 448, were mapped in the small q5.1-q5.2 region of SMU10. Three genes, KIAA444, 458, and 452, were mapped in the distal region of SMU14, however, the homologous block was interrupted by KIAA445 in HSA1. These results suggest the presence of multiple inversion events in HSA1 that occurred after the divergence of primates and insectivores.



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  		Figure 4.. Chromosomal localization of the (a,b) KIAA444 and (c,d) 445 clones to Suncus chromosomes. Arrows indicate the hybridization signals. KIAA444 and 445 were localized subregionally to SMU14q4.4-q4.5 and SMU10q5.1, respectively. R- and G-banded patterns are demonstrated in (a,c) and (b,d), respectively.

 


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  		Figure 5.. A comparative map between HSA1 and Suncus chromosomes. The chromosomal segments of HSA1 homologous to Suncus chromosomes are represented on the right side of the ideogram of HSA1. The clone numbers are represented by accession numbers in the KDRI database. The ideograms of HSA1 and SMU7, 10, and 14 were demonstrated on referring to ISCN (1995) and Rogatcheva et al. (1996), respectively.

 
In view of the fact that the insectivore appeared in the Cretaceous period around 150 million years ago (Ohno 1993), comparing insectivore chromosomes with human chromosomes is one of important approaches for explaining the process of chromosomal evolution in mammals. Dixkens et al. (1998) suggested by the ZOO-FISH analysis that only 10 breakages were necessary to transform the human karyotype into the karyotype of the common shrew (Sorex araneus, Insectivora). Although the small segments and intrachromosomal inversions were not detectable in their study, they revealed that the present-day human karyotype was very similar to the ancestral mammalian founder karyotype. On the contrary, our present study indicates a possibility that more chromosomal rearrangements occurred between human and S. murinus, although the information of comparative mapping is limited to HSA1-linked genes. The search of chromosomal homology by comparative mapping of functional genes provides a clue for clarifying the phylogenetic relationship between human and insectivore chromosomes and the ancestral genome structure prior to the separation of the primate and insectivore lineage.

A considerable amount of information on comparative mapping to human chromosomes is being accumulated for several other species than mouse. The comparative maps of human chromosome 1 and chromosomes of several species, including rat, zebrafish, and goat, were reported recently (White et al. 1999). Our research is the first report of comparative mapping between Suncus and human, and the direct R-banding FISH used in this study will contribute to construction of the comparative maps between Suncus and other mammalian species. It is necessary to increase mapping data, and making a substantial map between human and S. murinus is our essential subject in the future.


   Acknowledgments
 
This work was supported by a research grant (no. 09680829) from the Ministry of Education, Science, Sports, and Culture of Japan (to Y.M.).


   Footnotes
 
Corresponding Editor: Williams S. Modi

Received April 21, 2000
Accepted November 11, 2001


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 Materials and Methods
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