- Email: [email protected]
Mapping of the Human Ribosomal Large Subunit Protein GeneRPL29to Human Chromosome 3q29–qter
SHORT COMMUNICATION Mapping of the Human Ribosomal Large Subunit Protein Gene RPL29 to Human Chromosome 3q29–qter M. Garcia-Barcelo, P. T. W. Law, S. K. W. Tsui, K. P. Fung, C. Y. Lee, and M. M. Y. Waye1 Department of Biochemistry, The Chinese University of Hong Kong, Basic Medical Sciences Building, Shatin, NT, Hong Kong Received April 28, 1997; accepted August 26, 1997
The human ribosomal protein L29, which we reported previously, was subsequently shown to have the same nucleotide sequence as that of cell surface heparin/heparan sulfate-binding protein, designated HP/HS interacting protein. A polymerase chain reaction-based strategy was used to distinguish the functional intron-containing gene RPL29 (HGMW-approved symbol) from multiple pseudogenes. By somatic cell hybrid analysis, radiation hybrid mapping, and fluorescence in situ hybridization, we have located RPL29 on the telomeric region of the q arm of chromosome 3. RPL29 is the most distal marker of the long arm of chromosome 3. Of the human ribosomal protein genes mapped, RPL29 is the shortest distance from another ribosomal protein gene marker, RPL35a which has also been mapped to the 3q29–qter region. q 1997 Academic Press
Mammalian ribosome proteins (rp) are members of multigene families that are composed predominantly of multiple processed pseudogenes and one functional intron-containing gene (17), although some, such as rat ribosomal protein S5 (14) and human ribosomal protein L37a (22), are present as single-copy genes. As we previously reported (15), during the large-scale partial sequencing of human heart cDNA clones, a novel clone (Accession No. U10248) that was very similar to the rat ribosomal protein L29 in both DNA and amino acid sequences was found. The cDNA encoded a protein that showed 80.4% homology to protein L29 from the large ribosomal subunit of rat. The putative protein has a large excess of basic residues over acidic residues, with a unique lysine-rich tandem repeat structure that suggests a binding function. Liu et al. (16) cloned and expressed a cell surface heparin/heparan sulfate (HP/ HS)-binding protein named HP/HS-interacting protein (HIP), which shows the same nucleotide sequence as that of the human ribosomal protein L29. They report different expression levels in a variety of human cell lines and normal tissues but its absence in some cell lines and some cell types of normal tissues. Heparan sulfate proteoglycans and their corresponding binding 1 To whom correspondence should be addressed. Telephone: /85226096874. Fax: /852-26035123. E-mail: [email protected].
GENOMICS
46, 148–151 (1997) GE974990
sites may play an important role during the initial attachment of murine blastocysts to uterine epithelium and human trophoblastic cell lines to uterine epithelium cell lines. Expression of HIP has been described in normal human lumenal epithelium, a location where HIP may participate in embryo attachment (16). Members of the L29 family may then be displayed on cell surfaces where they may participate in HP/HS-binding events. Analysis of gene organization by Southern blotting showed that of the approximately 10 copies of RPL29, all but 1 are pseudogenes (15). To isolate and map the functional copy and to distinguish it from the intronless pseudogenes, an intron-specific probe was synthesized according to the strategy adopted by Davies et al. (4) and reported elsewhere (15). Here we applied fluorescence in situ hybridization (FISH), somatic cell hybrid analysis, and radiation hybrid mapping to locate RPL29. To perform FISH mapping, the clone pUC18– hRPL29 (15), which carries the full open reading frame of RPL29 cDNA (800 bp), was labeled with biotin and used as a probe. FISH was performed according to a published protocol (9). Although 40% of the metaphase screened indicated the presence of fluorescent spots on the q telomeric region of chromosome 3 (data not shown), the FISH results were inconclusive mainly due to the small size of the insert and the signals from pseudogenes. To corroborate FISH data and help distinguish the functional intron-containing gene from multiple pseudogenes, somatic cell hybrid analysis and radiation hybrid mapping were performed using intron-specific primers. For somatic cell hybrid analysis, polymerase chain reaction (PCR) was applied to a monochromosomal NIGMS Human/Rodent Somatic Cell Hybrid Mapping Panel 2 (Coriell Institute, Camden, NJ) consisting of 23 genomic DNAs from the same number of humanon-rodent somatic cell lines containing a single human chromosome each plus three control DNAs (human, Chinese hamster, and mouse) (5). Fifty nanograms of genomic DNA was used for amplification in 50 ml of PCR buffer (0.25 mM MgCl2 ; 75 mM Tris–HCl, pH 8.8; 20 mM NH4SO4 ; 0.01% Tween 20) containing 1 unit of Taq polymerase (Boehringer Mannheim), 25 mM con-
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FIG. 1. PCR analysis of somatic cell hybrid DNA. Lanes are labeled 1–22, X, and Y to indicate the human chromosome retained in each hybrid. Hu, human genomic DNA; Ha, Chinese hamster DNA; Mo, mouse DNA; Po, positive control (pUC18 containing the intron); M, size markers of a l DNA–HindIII/fX174 DNA–HaeIII digest.
centrations of each of the four dNTPs, and 250 mM concentrations of each of the forward and reverse intron-specific primers. Several pairs of intron-specific primers were designed to obtain a human-specific band that is different from rodent background amplification products. The specific pair of primers successfully used was 5*-CCCTGCCTACCATCCCAGACC-3* for the forward direction (closer to the 5* splicing signal) and 5*AAAAGGGAATTAAGCCAACAAAGAAC-3* for the reverse direction. The amplified intron is probably the
149
first one of the RPL29 gene since the intron is 37 nucleotides away from the initiation codon as we reported previously (15). Cycling conditions were as follows: 957C for 2 min; 40 cycles of 947C for 38 s, 577C for 36 s, 727C for 1 min 28 s, followed by a final extension of 727C for 10 min. The expected size of the PCR product was about 300 bp. Human genomic DNA (human line IMR91) and DNA from the somatic cell hybrid line NA10253, which retains only human chromosome 3, yielded a 300-bp band. No 300-bp PCR amplification product was detected from the rest of hybrids retaining other human chromosomes and rodent DNA (Fig. 1). The same pair of primers was used for radiation hybrid mapping (3). The radiation hybrid mapping was performed by the GeneBridge 4 whole-genome radiation hybrid panel (Research Genetics, Huntsville, AL), consisting of 93 genomic DNAs from the same number of human-on-hamster somatic cell lines, plus the two control DNAs (HFL human, A23 hamster). Twenty-five nanograms of genomic DNA was used for amplification in 10 ml of PCR buffer using conditions described above. Samples were run on 2% agarose gels and scored for the presence or absence of a 300-bp amplification product generating the data vector 000000001010000001111000002111000011000100101111001000100000001000001000010100200000000011002. These data were submitted to the Whitehead Institute/MIT Center for Genome Research STS mapping server (Cambridge, MA). Using a LOD threshold of ú17, we were able to
FIG. 2. Portion of chromosome 3q with RPL29 placed on the radiation hybrid framework map. The numbers on the chromosome indicate the distance from the nearest marker shown on the right. 1 cR Å 1% frequency of breakage between the markers. Data were obtained from Whitehead Institute Center for Genome Research and are available at: http//www-genome.wi.mit.edu/ftp/pub/software/rhmapper.
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establish linkage of RPL29 to chromosome 3. Furthermore, the data placed the RPL29 gene at 45.57 cR (LOD ú 3) below framework marker WI-9695 (D3S3954), which maps 909.71 cR from the top of the chromosome 3 linkage group, placing RPL29 at about 955 cR from the top telomere of the short arm. The precise order of the markers is shown in Fig. 2. WI-9695 is a marker that codes for the functional intron-containing gene of ribosomal protein L35a, and it has also been mapped by FISH to the 3q29–qter region (2). Since RPL29 is the most distal gene mapped on chromosome 3, it extends chromosome 3 by 33.5 cR. Our RH mapping strategy was not confounded by a processed RNA pseudogene because the PCR primers we used were located in an intron. Ribosomal protein genes previously mapped (2, 6, 7, 11, 12, 19–21, 23) are encoded by intron-containing genes that are each located at a single autosomal site showing a complete lack of clustering of rp genes in the human genome. Two of these genes, RPL22 (20) and RPL35a (2), are located on chromosome 3, on the same arm but at different bands (3q26 and 3q29, respectively). In contrast to previous findings, our data locate RPL29 45.57 cR from RPL35a (WI-9695), suggesting the possibility of a coordinated expression; 45.47 cR corresponds roughly to 14 Mb in physical distance if we assume 1 cR/300 kb (10). A distance of 14 Mb exceeds the size of any known human gene cluster, but the conversion of centirays to basepairs of DNA can be inaccurate. It depends on several parameters, one of them being the region of the chromosome under study (8). It is known that the telomere domains have a notably higher number of recombination map units (cM) localized to within a few percent of the physical map at the chromosome termini. If loci are randomly distributed on a physical map, the density of markers on a genetic map will be inversely proportional to the recombination rate (8, 18), and recombination rates are elevated in both human and mouse telomeres (1, 8, 18). As mentioned above, RPL29 plays a role as a HIP, and it would be interesting to determine whether RPL35a has functions other than as a housekeeping protein. Determination of rp chromosomal location may also be important because of their association with possible genetic diseases. It has been suggested that haploinsufficiency of rpS4 is the cause of Turner syndrome, and many of the phenotypes caused by autosomal monosomies may be due to haploinsufficiency of other ribosomal proteins (7). It may be possible that due to the wide distribution throughout the genome of the rp genes, chromosomal rearrangements resulting in positioning of the 5* region of a rp gene in front of another gene might result in a genetic disorder as a result of the strong rp housekeeping promoter (13, 20). The sublocalization and genetic characterization of RPL29 facilitate linkage analysis of several disease genes mapped to this chromosome band as well as the correlation of genetic and physical markers in the region.
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ACKNOWLEDGMENTS This study was supported by the Hong Kong RGC Earmarked Grant CUHK 205/96M and the Ho Sing-Hang Education Endowment Fund. M. Garcia-Barcelo was supported by a postdoctoral fellowship from CUHK and the Ho Sing-Hang Education Endowment Fund.
REFERENCES 1. Bray-Ward, P., Menninger, J., Lieman, J., Desai, T., Mokady, N., Banks, A., and Ward, D. C. (1996). Integration of the cytogenetic, genetic, and physical maps of the human genome by FISH mapping of the CEPH YAC clones. Genomics 32: 1–14. 2. Colombo, P., Read, M., and Fried, M. (1996). The human L35a ribosomal protein (RPL35a) gene is located at chromosome band 3q29–qter. Genomics 32: 148–150. 3. Cox, R. D., Burmeister, M., Price, E. R., Kim, S., and Myers, R. M. (1990). Radiation hybrid mapping: A somatic cell genetic method for constructing high-resolution maps of mammalian chromosomes. Science 250: 245–250. 4. Davies, B., Feo, S., Heard, E., and Fried, M. (1989). A strategy to detect and isolate an intron-containing gene in the presence of multiple processed pseudogenes. Proc. Natl. Sci. USA 86: 6691–6695. 5. Drwinga, H. L., Toji, L. H., Kim, C. H., Greene, A. E., and Mulivor, R. A. (1993). NIGMS human/rodent somatic cell hybrid mapping panels 1 and 2. Genomics 16: 311–314. 6. Feo, S., Davies, B., and Fried, M. (1992). The mapping of seven intron-containing ribosomal protein genes shows they are unlinked in the human genome. Genomics 13: 201–207. 7. Fisher, E. M., Beer, R. P., Brown, L. G., Ridley, A., McNeil, J. A., Lawrence, J. B., Willard, H. F., Bieber, F. R., and Page, D. C. (1990). Homologous ribosomal protein genes on the human X and Y chromosomes: Escape from X inactivation and possible implications for Turner syndrome. Cell 63: 1205–1218. 8. Giacalone, J., Li, X., Lehrach, H., and Francke, U. (1996). High density radiation hybrid map of human chromosome 18 and contig of 18p. Genomics 37: 9–18. 9. Heng, H. H. Q., and Tsui, L. C. (1993). Modes of DAPI banding and simultaneous in situ hybridization. Chromosoma 102: 325– 332. 10. Hudson T. J., Stein, L. D., and Gerety, S. S., et al. (1995). An STS based map of the human genome. Science 270: 1945–1954. 11. Imai, T., Sudo, K., and Miwa, T. (1994). Assignment of the human ribosomal protein S25 gene (RPS25) to chromosome 11q23.3 by sequence analysis of the marker D11S456. Genomics 20: 142–143. 12. Jones, A. M., Marzella, R., Rocchi, M., and Hewitt, J. E. (1997). Mapping of the human ribosomal small subunit protein gene RPS24 to the chromosome 10q22–23 boundary. Genomics 39: 121–122. 13. Kozma, S. C., Redmond, S. M., Fu, X. C., Saurer, S. M., Groner, B., and Hynes, N. E. (1988). Activation of the receptor kinase domain of the trk oncogene by recombination with two different cellular sequences. EMBO J. 7: 147–154. 14. Kuwano, Y., Olvera, J., and Wool, I. G. (1992). The primary structure of rat ribosomal protein S5. J. Biol. Chem. 267: 25304–25308. 15. Law, P. T. W., Tsui, S. K. W., Lam W. Y., Luk, S. C. W., Hwaang D. M., Liew, C. C., Lee, C. Y., Fung, K. P., and Waye, M. M. Y. (1996). A novel cDNA encoding a human homologue of ribosomal protein L29. Biochem. Biophys. Acta 1305: 105–108. 16. Liu, S., Smith, S. E., Julian, J. A., Rohde, L. H., Karin, N. J., and Carson, D. D. (1996). cDNA cloning and expression of HIP, a novel surface heparan sulfate/heparin-binding protein of human uterine epithelial cells and cell lines. J. Biol. Chem. 271: 11817–11823.
gnmxa
SHORT COMMUNICATION 17. Monk, R. J., Meyuhas, O., and Perry, R. P. (1981). Mammals have multiple genes for individual ribosomal proteins. Cell 24: 301–306. 18. Nachman N. W., and Churcill, G. A. (1996). Heterogeneity in rates of recombination across the mouse genome. Genetics 142: 537–548. 19. Nakamichi, N. N., Kao, F. T., Wasmuth, J., and Roufa, D. J. (1986). Ribosomal gene sequences map to human chromosomes 5, 8, and 17. Somat. Cell. Mol. Genet. 12: 225–236. 20. Nucifora, G. (1993). The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the
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gene for EAP, a highly conserved protein associated with the Epstein–Barr virus small RNA EBER 1. Proc. Natl. Acad. Sci. USA 90: 7784–7788. 21. Rhoads, D. D., Dixit, A., and Roufa, D. J. (1986). Primary structure of human ribosomal protein S14 and the gene that encodes it. Mol. Cell. Biol. 6: 2774–2783. 22. Saha, D. P., Tirumalai, P. S., Scala, L. A., and Howells, R. D. (1993). Human ribosomal protein L37. Gene 132: 285–289. 23. Yon, J., Palmer, R. W., Sheer, D., and Fried, M. (1989). Localization of the Surfeit gene cluster containing the ribosomal protein gene L7a to chromosome bands 9q33–34. Ann. Hum. Genet. 53: 149–155.
gnmxa
The human ribosomal protein L29, which we reported previously, was subsequently shown to have the same nucleotide sequence as that of cell surface heparin/heparan sulfate-binding protein, designated HP/HS interacting protein. A polymerase chain reaction-based strategy was used to distinguish the functional intron-containing gene RPL29 (HGMW-approved symbol) from multiple pseudogenes. By somatic cell hybrid analysis, radiation hybrid mapping, and fluorescence in situ hybridization, we have located RPL29 on the telomeric region of the q arm of chromosome 3. RPL29 is the most distal marker of the long arm of chromosome 3. Of the human ribosomal protein genes mapped, RPL29 is the shortest distance from another ribosomal protein gene marker, RPL35a which has also been mapped to the 3q29–qter region. q 1997 Academic Press
Mammalian ribosome proteins (rp) are members of multigene families that are composed predominantly of multiple processed pseudogenes and one functional intron-containing gene (17), although some, such as rat ribosomal protein S5 (14) and human ribosomal protein L37a (22), are present as single-copy genes. As we previously reported (15), during the large-scale partial sequencing of human heart cDNA clones, a novel clone (Accession No. U10248) that was very similar to the rat ribosomal protein L29 in both DNA and amino acid sequences was found. The cDNA encoded a protein that showed 80.4% homology to protein L29 from the large ribosomal subunit of rat. The putative protein has a large excess of basic residues over acidic residues, with a unique lysine-rich tandem repeat structure that suggests a binding function. Liu et al. (16) cloned and expressed a cell surface heparin/heparan sulfate (HP/ HS)-binding protein named HP/HS-interacting protein (HIP), which shows the same nucleotide sequence as that of the human ribosomal protein L29. They report different expression levels in a variety of human cell lines and normal tissues but its absence in some cell lines and some cell types of normal tissues. Heparan sulfate proteoglycans and their corresponding binding 1 To whom correspondence should be addressed. Telephone: /85226096874. Fax: /852-26035123. E-mail: [email protected].
GENOMICS
46, 148–151 (1997) GE974990
sites may play an important role during the initial attachment of murine blastocysts to uterine epithelium and human trophoblastic cell lines to uterine epithelium cell lines. Expression of HIP has been described in normal human lumenal epithelium, a location where HIP may participate in embryo attachment (16). Members of the L29 family may then be displayed on cell surfaces where they may participate in HP/HS-binding events. Analysis of gene organization by Southern blotting showed that of the approximately 10 copies of RPL29, all but 1 are pseudogenes (15). To isolate and map the functional copy and to distinguish it from the intronless pseudogenes, an intron-specific probe was synthesized according to the strategy adopted by Davies et al. (4) and reported elsewhere (15). Here we applied fluorescence in situ hybridization (FISH), somatic cell hybrid analysis, and radiation hybrid mapping to locate RPL29. To perform FISH mapping, the clone pUC18– hRPL29 (15), which carries the full open reading frame of RPL29 cDNA (800 bp), was labeled with biotin and used as a probe. FISH was performed according to a published protocol (9). Although 40% of the metaphase screened indicated the presence of fluorescent spots on the q telomeric region of chromosome 3 (data not shown), the FISH results were inconclusive mainly due to the small size of the insert and the signals from pseudogenes. To corroborate FISH data and help distinguish the functional intron-containing gene from multiple pseudogenes, somatic cell hybrid analysis and radiation hybrid mapping were performed using intron-specific primers. For somatic cell hybrid analysis, polymerase chain reaction (PCR) was applied to a monochromosomal NIGMS Human/Rodent Somatic Cell Hybrid Mapping Panel 2 (Coriell Institute, Camden, NJ) consisting of 23 genomic DNAs from the same number of humanon-rodent somatic cell lines containing a single human chromosome each plus three control DNAs (human, Chinese hamster, and mouse) (5). Fifty nanograms of genomic DNA was used for amplification in 50 ml of PCR buffer (0.25 mM MgCl2 ; 75 mM Tris–HCl, pH 8.8; 20 mM NH4SO4 ; 0.01% Tween 20) containing 1 unit of Taq polymerase (Boehringer Mannheim), 25 mM con-
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FIG. 1. PCR analysis of somatic cell hybrid DNA. Lanes are labeled 1–22, X, and Y to indicate the human chromosome retained in each hybrid. Hu, human genomic DNA; Ha, Chinese hamster DNA; Mo, mouse DNA; Po, positive control (pUC18 containing the intron); M, size markers of a l DNA–HindIII/fX174 DNA–HaeIII digest.
centrations of each of the four dNTPs, and 250 mM concentrations of each of the forward and reverse intron-specific primers. Several pairs of intron-specific primers were designed to obtain a human-specific band that is different from rodent background amplification products. The specific pair of primers successfully used was 5*-CCCTGCCTACCATCCCAGACC-3* for the forward direction (closer to the 5* splicing signal) and 5*AAAAGGGAATTAAGCCAACAAAGAAC-3* for the reverse direction. The amplified intron is probably the
149
first one of the RPL29 gene since the intron is 37 nucleotides away from the initiation codon as we reported previously (15). Cycling conditions were as follows: 957C for 2 min; 40 cycles of 947C for 38 s, 577C for 36 s, 727C for 1 min 28 s, followed by a final extension of 727C for 10 min. The expected size of the PCR product was about 300 bp. Human genomic DNA (human line IMR91) and DNA from the somatic cell hybrid line NA10253, which retains only human chromosome 3, yielded a 300-bp band. No 300-bp PCR amplification product was detected from the rest of hybrids retaining other human chromosomes and rodent DNA (Fig. 1). The same pair of primers was used for radiation hybrid mapping (3). The radiation hybrid mapping was performed by the GeneBridge 4 whole-genome radiation hybrid panel (Research Genetics, Huntsville, AL), consisting of 93 genomic DNAs from the same number of human-on-hamster somatic cell lines, plus the two control DNAs (HFL human, A23 hamster). Twenty-five nanograms of genomic DNA was used for amplification in 10 ml of PCR buffer using conditions described above. Samples were run on 2% agarose gels and scored for the presence or absence of a 300-bp amplification product generating the data vector 000000001010000001111000002111000011000100101111001000100000001000001000010100200000000011002. These data were submitted to the Whitehead Institute/MIT Center for Genome Research STS mapping server (Cambridge, MA). Using a LOD threshold of ú17, we were able to
FIG. 2. Portion of chromosome 3q with RPL29 placed on the radiation hybrid framework map. The numbers on the chromosome indicate the distance from the nearest marker shown on the right. 1 cR Å 1% frequency of breakage between the markers. Data were obtained from Whitehead Institute Center for Genome Research and are available at: http//www-genome.wi.mit.edu/ftp/pub/software/rhmapper.
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establish linkage of RPL29 to chromosome 3. Furthermore, the data placed the RPL29 gene at 45.57 cR (LOD ú 3) below framework marker WI-9695 (D3S3954), which maps 909.71 cR from the top of the chromosome 3 linkage group, placing RPL29 at about 955 cR from the top telomere of the short arm. The precise order of the markers is shown in Fig. 2. WI-9695 is a marker that codes for the functional intron-containing gene of ribosomal protein L35a, and it has also been mapped by FISH to the 3q29–qter region (2). Since RPL29 is the most distal gene mapped on chromosome 3, it extends chromosome 3 by 33.5 cR. Our RH mapping strategy was not confounded by a processed RNA pseudogene because the PCR primers we used were located in an intron. Ribosomal protein genes previously mapped (2, 6, 7, 11, 12, 19–21, 23) are encoded by intron-containing genes that are each located at a single autosomal site showing a complete lack of clustering of rp genes in the human genome. Two of these genes, RPL22 (20) and RPL35a (2), are located on chromosome 3, on the same arm but at different bands (3q26 and 3q29, respectively). In contrast to previous findings, our data locate RPL29 45.57 cR from RPL35a (WI-9695), suggesting the possibility of a coordinated expression; 45.47 cR corresponds roughly to 14 Mb in physical distance if we assume 1 cR/300 kb (10). A distance of 14 Mb exceeds the size of any known human gene cluster, but the conversion of centirays to basepairs of DNA can be inaccurate. It depends on several parameters, one of them being the region of the chromosome under study (8). It is known that the telomere domains have a notably higher number of recombination map units (cM) localized to within a few percent of the physical map at the chromosome termini. If loci are randomly distributed on a physical map, the density of markers on a genetic map will be inversely proportional to the recombination rate (8, 18), and recombination rates are elevated in both human and mouse telomeres (1, 8, 18). As mentioned above, RPL29 plays a role as a HIP, and it would be interesting to determine whether RPL35a has functions other than as a housekeeping protein. Determination of rp chromosomal location may also be important because of their association with possible genetic diseases. It has been suggested that haploinsufficiency of rpS4 is the cause of Turner syndrome, and many of the phenotypes caused by autosomal monosomies may be due to haploinsufficiency of other ribosomal proteins (7). It may be possible that due to the wide distribution throughout the genome of the rp genes, chromosomal rearrangements resulting in positioning of the 5* region of a rp gene in front of another gene might result in a genetic disorder as a result of the strong rp housekeeping promoter (13, 20). The sublocalization and genetic characterization of RPL29 facilitate linkage analysis of several disease genes mapped to this chromosome band as well as the correlation of genetic and physical markers in the region.
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ACKNOWLEDGMENTS This study was supported by the Hong Kong RGC Earmarked Grant CUHK 205/96M and the Ho Sing-Hang Education Endowment Fund. M. Garcia-Barcelo was supported by a postdoctoral fellowship from CUHK and the Ho Sing-Hang Education Endowment Fund.
REFERENCES 1. Bray-Ward, P., Menninger, J., Lieman, J., Desai, T., Mokady, N., Banks, A., and Ward, D. C. (1996). Integration of the cytogenetic, genetic, and physical maps of the human genome by FISH mapping of the CEPH YAC clones. Genomics 32: 1–14. 2. Colombo, P., Read, M., and Fried, M. (1996). The human L35a ribosomal protein (RPL35a) gene is located at chromosome band 3q29–qter. Genomics 32: 148–150. 3. Cox, R. D., Burmeister, M., Price, E. R., Kim, S., and Myers, R. M. (1990). Radiation hybrid mapping: A somatic cell genetic method for constructing high-resolution maps of mammalian chromosomes. Science 250: 245–250. 4. Davies, B., Feo, S., Heard, E., and Fried, M. (1989). A strategy to detect and isolate an intron-containing gene in the presence of multiple processed pseudogenes. Proc. Natl. Sci. USA 86: 6691–6695. 5. Drwinga, H. L., Toji, L. H., Kim, C. H., Greene, A. E., and Mulivor, R. A. (1993). NIGMS human/rodent somatic cell hybrid mapping panels 1 and 2. Genomics 16: 311–314. 6. Feo, S., Davies, B., and Fried, M. (1992). The mapping of seven intron-containing ribosomal protein genes shows they are unlinked in the human genome. Genomics 13: 201–207. 7. Fisher, E. M., Beer, R. P., Brown, L. G., Ridley, A., McNeil, J. A., Lawrence, J. B., Willard, H. F., Bieber, F. R., and Page, D. C. (1990). Homologous ribosomal protein genes on the human X and Y chromosomes: Escape from X inactivation and possible implications for Turner syndrome. Cell 63: 1205–1218. 8. Giacalone, J., Li, X., Lehrach, H., and Francke, U. (1996). High density radiation hybrid map of human chromosome 18 and contig of 18p. Genomics 37: 9–18. 9. Heng, H. H. Q., and Tsui, L. C. (1993). Modes of DAPI banding and simultaneous in situ hybridization. Chromosoma 102: 325– 332. 10. Hudson T. J., Stein, L. D., and Gerety, S. S., et al. (1995). An STS based map of the human genome. Science 270: 1945–1954. 11. Imai, T., Sudo, K., and Miwa, T. (1994). Assignment of the human ribosomal protein S25 gene (RPS25) to chromosome 11q23.3 by sequence analysis of the marker D11S456. Genomics 20: 142–143. 12. Jones, A. M., Marzella, R., Rocchi, M., and Hewitt, J. E. (1997). Mapping of the human ribosomal small subunit protein gene RPS24 to the chromosome 10q22–23 boundary. Genomics 39: 121–122. 13. Kozma, S. C., Redmond, S. M., Fu, X. C., Saurer, S. M., Groner, B., and Hynes, N. E. (1988). Activation of the receptor kinase domain of the trk oncogene by recombination with two different cellular sequences. EMBO J. 7: 147–154. 14. Kuwano, Y., Olvera, J., and Wool, I. G. (1992). The primary structure of rat ribosomal protein S5. J. Biol. Chem. 267: 25304–25308. 15. Law, P. T. W., Tsui, S. K. W., Lam W. Y., Luk, S. C. W., Hwaang D. M., Liew, C. C., Lee, C. Y., Fung, K. P., and Waye, M. M. Y. (1996). A novel cDNA encoding a human homologue of ribosomal protein L29. Biochem. Biophys. Acta 1305: 105–108. 16. Liu, S., Smith, S. E., Julian, J. A., Rohde, L. H., Karin, N. J., and Carson, D. D. (1996). cDNA cloning and expression of HIP, a novel surface heparan sulfate/heparin-binding protein of human uterine epithelial cells and cell lines. J. Biol. Chem. 271: 11817–11823.
gnmxa
SHORT COMMUNICATION 17. Monk, R. J., Meyuhas, O., and Perry, R. P. (1981). Mammals have multiple genes for individual ribosomal proteins. Cell 24: 301–306. 18. Nachman N. W., and Churcill, G. A. (1996). Heterogeneity in rates of recombination across the mouse genome. Genetics 142: 537–548. 19. Nakamichi, N. N., Kao, F. T., Wasmuth, J., and Roufa, D. J. (1986). Ribosomal gene sequences map to human chromosomes 5, 8, and 17. Somat. Cell. Mol. Genet. 12: 225–236. 20. Nucifora, G. (1993). The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the
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