Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1994 Jun;137(2):513–520. doi: 10.1093/genetics/137.2.513

A Drosophila Third Chromosome Minute Locus Encodes a Ribosomal Protein

S Andersson 1, S Sæbøe-Larssen 1, A Lambertsson 1, J Merriam 1, M Jacobs-Lorena 1
PMCID: PMC1205974  PMID: 8070662

Abstract

Minutes (M) are a group of over 50 phenotypically similar Drosophila mutations widely believed to affect ribosomal protein genes. This report describes the characterization of the P element-induced M(3)95A(Plac92) mutation [allelic to M(3)95A]. This mutation can be reversed by the mobilization of the P element, demonstrating that the mutation is caused by insertion of this transposable element. The gene interrupted by insertion of the P element was cloned by use of inverse polymerase chain reaction. Nucleotide sequence analysis revealed a 70-75% identity to the human and rat ribosomal protein S3 genes, and to the Xenopus ribosomal protein S1a gene. At the amino acid level, the overall identity is &78% for all three species. This is only the second time that a Minute has been demonstrated to encode a ribosomal protein.

Full Text

The Full Text of this article is available as a PDF (5.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrio R., del Arco A., Cabrera H., Arribas C. Cloning and analysis of the S2 ribosomal protein cDNA from Drosophila. Nucleic Acids Res. 1993 Jan 25;21(2):351–351. doi: 10.1093/nar/21.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baumgartner S., Martin D., Chiquet-Ehrismann R. Drosophila ribosomal protein S19 cDNA sequence. Nucleic Acids Res. 1993 Aug 11;21(16):3897–3897. doi: 10.1093/nar/21.16.3897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Broderick D. J., Roberts P. A. Localization of minutes to specific polytene chromosome bands by means of overlapping duplications. Genetics. 1982 Sep;102(1):71–74. doi: 10.1093/genetics/102.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown S. J., Rhoads D. D., Stewart M. J., Van Slyke B., Chen I. T., Johnson T. K., Denell R. E., Roufa D. J. Ribosomal protein S14 is encoded by a pair of highly conserved, adjacent genes on the X chromosome of Drosophila melanogaster. Mol Cell Biol. 1988 Oct;8(10):4314–4321. doi: 10.1128/mcb.8.10.4314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burns D. K., Stark B. C., Macklin M. D., Chooi W. Y. Isolation and characterization of cloned DNA sequences containing ribosomal protein genes of Drosophila melanogaster. Mol Cell Biol. 1984 Dec;4(12):2643–2652. doi: 10.1128/mcb.4.12.2643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chan Y. L., Devi K. R., Olvera J., Wool I. G. The primary structure of rat ribosomal protein S3. Arch Biochem Biophys. 1990 Dec;283(2):546–550. doi: 10.1016/0003-9861(90)90682-o. [DOI] [PubMed] [Google Scholar]
  7. Chooi W. Y., Sabatini L. M., Macklin M., Fraser D. Group fractionation and determination of the number of ribosomal subunit proteins from Drosophila melanogaster embryos. Biochemistry. 1980 Apr 1;19(7):1425–1433. doi: 10.1021/bi00548a025. [DOI] [PubMed] [Google Scholar]
  8. Di Cristina M., Menard R., Pierandrei-Amaldi P. Xenopus laevis ribosomal protein S1a cDNA sequence. Nucleic Acids Res. 1991 Apr 25;19(8):1943–1943. doi: 10.1093/nar/19.8.1943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dorer D. R., Anane-Firempong A., Christensen A. C. Ribosomal protein S14 is not responsible for the Minute phenotype associated with the M(1)7C locus in Drosophila melanogaster. Mol Gen Genet. 1991 Nov;230(1-2):8–11. doi: 10.1007/BF00290642. [DOI] [PubMed] [Google Scholar]
  10. Espelund M., Stacy R. A., Jakobsen K. S. A simple method for generating single-stranded DNA probes labeled to high activities. Nucleic Acids Res. 1990 Oct 25;18(20):6157–6158. doi: 10.1093/nar/18.20.6157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fruscoloni P., Al-Atia G. R., Jacobs-Lorena M. Translational regulation of a specific gene during oogenesis and embryogenesis of Drosophila. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3359–3363. doi: 10.1073/pnas.80.11.3359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hariharan N., Perry R. P. Functional dissection of a mouse ribosomal protein promoter: significance of the polypyrimidine initiator and an element in the TATA-box region. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1526–1530. doi: 10.1073/pnas.87.4.1526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Henry J. L., Coggin D. L., King C. R. High-level expression of the ribosomal protein L19 in human breast tumors that overexpress erbB-2. Cancer Res. 1993 Mar 15;53(6):1403–1408. [PubMed] [Google Scholar]
  14. Hultman T., Ståhl S., Hornes E., Uhlén M. Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res. 1989 Jul 11;17(13):4937–4946. doi: 10.1093/nar/17.13.4937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Itoh N., Ohta K., Ohta M., Kawasaki T., Yamashina I. The nucleotide sequence of a gene for a putative ribosomal protein S31 of Drosophila. Nucleic Acids Res. 1989 Mar 11;17(5):2121–2121. doi: 10.1093/nar/17.5.2121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Itoh N., Ohta K., Ohta M., Kawasaki T., Yamashina I. The nucleotide sequence of cDNA for a Drosophila ribosomal protein with homology to rat ribosomal protein S26. Nucleic Acids Res. 1989 Jan 11;17(1):441–441. doi: 10.1093/nar/17.1.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jakobsen K. S., Breivold E., Hornes E. Purification of mRNA directly from crude plant tissues in 15 minutes using magnetic oligo dT microspheres. Nucleic Acids Res. 1990 Jun 25;18(12):3669–3669. doi: 10.1093/nar/18.12.3669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kay M. A., Jacobs-Lorena M. Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster. Mol Cell Biol. 1985 Dec;5(12):3583–3592. doi: 10.1128/mcb.5.12.3583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kay M. A., Zhang J. Y., Jacobs-Lorena M. Identification and germline transformation of the ribosomal protein rp21 gene of Drosophila: complementation analysis with the Minute QIII locus reveals nonidentity. Mol Gen Genet. 1988 Aug;213(2-3):354–358. doi: 10.1007/BF00339602. [DOI] [PubMed] [Google Scholar]
  20. Kongsuwan K., Yu Q., Vincent A., Frisardi M. C., Rosbash M., Lengyel J. A., Merriam J. A Drosophila Minute gene encodes a ribosomal protein. Nature. 1985 Oct 10;317(6037):555–558. doi: 10.1038/317555a0. [DOI] [PubMed] [Google Scholar]
  21. Lambertsson A., Andersson S., Johansson T. Cloning and characterization of variable-sized gypsy mobile elements in Drosophila melanogaster. Plasmid. 1989 Jul;22(1):22–31. doi: 10.1016/0147-619x(89)90032-2. [DOI] [PubMed] [Google Scholar]
  22. Levy S., Avni D., Hariharan N., Perry R. P., Meyuhas O. Oligopyrimidine tract at the 5' end of mammalian ribosomal protein mRNAs is required for their translational control. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3319–3323. doi: 10.1073/pnas.88.8.3319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maki C., Rhoads D. D., Stewart M. J., Van Slyke B., Roufa D. J. The Drosophila melanogaster RPS17 gene encoding ribosomal protein S17. Gene. 1989 Jul 15;79(2):289–298. doi: 10.1016/0378-1119(89)90211-4. [DOI] [PubMed] [Google Scholar]
  24. McNabb S. L., Ashburner M. Identification of a Drosophila protein similar to rat S13 and archaebacterial S11 ribosomal proteins. Nucleic Acids Res. 1993 May 25;21(10):2523–2523. doi: 10.1093/nar/21.10.2523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mount S. M., Burks C., Hertz G., Stormo G. D., White O., Fields C. Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res. 1992 Aug 25;20(16):4255–4262. doi: 10.1093/nar/20.16.4255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Noselli S., Vincent A. The Drosophila melanogaster ribosomal protein L17A-encoding gene. Gene. 1992 Sep 10;118(2):273–278. doi: 10.1016/0378-1119(92)90199-y. [DOI] [PubMed] [Google Scholar]
  27. O'Kane C. J., Gehring W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9123–9127. doi: 10.1073/pnas.84.24.9123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Olson P. F., Salo T., Garrison K., Fessler J. H. Drosophila acidic ribosomal protein rpA2: sequence and characterization. J Cell Biochem. 1993 Mar;51(3):353–359. doi: 10.1002/jcb.240510315. [DOI] [PubMed] [Google Scholar]
  29. Patel R., Jacobs-Lorena M. Generation of Minute phenotypes by a transformed antisense ribosomal protein gene. Dev Genet. 1992;13(4):256–263. doi: 10.1002/dvg.1020130403. [DOI] [PubMed] [Google Scholar]
  30. Qian S., Hongo S., Jacobs-Lorena M. Antisense ribosomal protein gene expression specifically disrupts oogenesis in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9601–9605. doi: 10.1073/pnas.85.24.9601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Qian S., Zhang J. Y., Kay M. A., Jacobs-Lorena M. Structural analysis of the Drosophila rpA1 gene, a member of the eucaryotic 'A' type ribosomal protein family. Nucleic Acids Res. 1987 Feb 11;15(3):987–1003. doi: 10.1093/nar/15.3.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rafti F., Gargiulo G., Manzi A., Malva C., Grossi G., Andone S., Graziani F. Isolation and structural analysis of a ribosomal protein gene in D.melanogaster. Nucleic Acids Res. 1988 Jun 10;16(11):4915–4926. doi: 10.1093/nar/16.11.4915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ritossa F. M., Atwood K. C., Spiegelman S. On the redundancy of DNA complementary to amino acid tranfer RNA and its absence from the nucleolar organizer region of Drosophila melanogaster. Genetics. 1966 Aug;54(2):663–676. doi: 10.1093/genetics/54.2.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schultz J. The Minute Reaction in the Development of DROSOPHILA MELANOGASTER. Genetics. 1929 Jul;14(4):366–419. doi: 10.1093/genetics/14.4.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sinclair D. A., Suzuki D. T., Grigliatti T. A. Genetic and developmental analysis of a temperature-sensitive minute mutation of Drosophila melanogaster. Genetics. 1981 Mar-Apr;97(3-4):581–606. doi: 10.1093/genetics/97.3-4.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Spencer T. A., Mackie G. A. The nucleotide sequence of a cloned cDNA encoding ribosomal protein S6 from Drosophila melanogaster. Biochim Biophys Acta. 1993 Mar 20;1172(3):332–334. doi: 10.1016/0167-4781(93)90225-3. [DOI] [PubMed] [Google Scholar]
  38. Stewart M. J., Denell R. Mutations in the Drosophila gene encoding ribosomal protein S6 cause tissue overgrowth. Mol Cell Biol. 1993 Apr;13(4):2524–2535. doi: 10.1128/mcb.13.4.2524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vaslet C. A., O'Connell P., Izquierdo M., Rosbash M. Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster. Nature. 1980 Jun 26;285(5767):674–676. doi: 10.1038/285674a0. [DOI] [PubMed] [Google Scholar]
  40. Voelker R. A., Huang S. M., Wisely G. B., Sterling J. F., Bainbridge S. P., Hiraizumi K. Molecular and genetic organization of the suppressor of sable and minute (1) 1B region in Drosophila melanogaster. Genetics. 1989 Jul;122(3):625–642. doi: 10.1093/genetics/122.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vässin H., Vielmetter J., Campos-Ortega J. A. Genetic interactions in early neurogenesis of Drosophila melanogaster. J Neurogenet. 1985 Nov;2(5):291–308. doi: 10.3109/01677068509102325. [DOI] [PubMed] [Google Scholar]
  42. Watson K. L., Konrad K. D., Woods D. F., Bryant P. J. Drosophila homolog of the human S6 ribosomal protein is required for tumor suppression in the hematopoietic system. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11302–11306. doi: 10.1073/pnas.89.23.11302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wigboldus J. D. cDNA and deduced amino acid sequence of Drosophila rp21C, another 'A'-type ribosomal protein. Nucleic Acids Res. 1987 Dec 10;15(23):10064–10064. doi: 10.1093/nar/15.23.10064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wilson D. M., 3rd, Deutsch W. A., Kelley M. R. Cloning of the Drosophila ribosomal protein S3: another multifunctional ribosomal protein with AP endonuclease DNA repair activity. Nucleic Acids Res. 1993 May 25;21(10):2516–2516. doi: 10.1093/nar/21.10.2516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zhang X. T., Tan Y. M., Tan Y. H. Isolation of a cDNA encoding human 40S ribosomal protein s3. Nucleic Acids Res. 1990 Nov 25;18(22):6689–6689. doi: 10.1093/nar/18.22.6689. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES