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Molecular cloning, characterization, and expression analysis of a QM homologue in the ant Polyrhachis vicina (Hymenoptera: Formicidae)

Published online by Cambridge University Press:  02 April 2012

Shumin Lü ,
Gengsi Xi  and
Xiaohui Wang
Shumin Lü
Affiliation:
College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, People's Republic of China
Gengsi Xi*
Affiliation:
College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, People's Republic of China
Xiaohui Wang
Affiliation:
College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, People's Republic of China
*
1Corresponding author (e-mail: [email protected]).
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Abstract

QM, a tumor-suppressor gene, plays an important role in cell growth, differentiation, and apoptosis. In this report, a homologue of human QM was isolated from the ant Polyrhachis vicina Roger. The full-length cDNA of P. vicina QM (PvQM) is 827 base pairs (bp) and contains a 5′-untranslated region of 91 bp and a 3′-untranslated region of 77 bp. The open reading frame of PvQM encodes a deduced 219-amino acid peptide with a predicted molecular mass of 25.1 kilodaltons. The results of sequence alignments indicate that the PvQM protein shares an overall identity of 76.7%–98.2% with other known QM homologues, and is most closely related to that of Apis mellifera L. (Hymenoptera: Apidae). Real-time quantitative reverse transcription - polymerase chain reaction was performed to compare PvQM mRNA expression during P. vicina development and within different castes. The data revealed that PvQM mRNA is differentially expressed during P. vicina development, with the highest expression level in embryos and the lowest in late-instar larvae and pupae. The levels of PvQM transcripts also vary among castes, with higher levels in workers and lower levels in both males and females. These results suggest that PvQM is developmentally and caste-specifically regulated at the level of transcription.

Résumé

Le gène suppresseur de tumeurs QM joue un rôle important dans la croissance cellulaire, la différenciation et l’apoptose. Dans notre travail, nous avons isolé un homologue du QM humain chez la fourmi Polyrhachis vicina Roger. La longueur totale de l’ADN complémentaire du QM de P. vicina (PvQM) est de 827 paires de bases (bp) avec une région non transcrite en 5′ de 91 bp et une région non transcrite en 3′ de 77 bp. Le cadre ouvert de lecture (ORF) de PvQM code un peptide déduit de 219 acides aminés de masse moléculaire prédite de 25,1 kilodaltons. L’alignement des séquences indique que la protéine PvQM possède une identité globale commune de 76,7 % – 98,2 % avec les autres homologues connus de QM et qu’elle est le plus apparentée à celle d’Apismellifera L. (Hymenoptera: Apidae). Une analyse quantitative en temps réel d’amplification en chaîne par polymérase a permis de comparer l’expression de l’ARNm de PvQM durant le développement de P. vicina et au sein des diverses castes. Nos données montrent que l’ARNm de PvQM est exprimé de façon différente au cours du développement de P. vicina, l’expression maximale se retrouvant chez les embryons et la plus faible chez les larves de derniers stades et les nymphes. Les valeurs des produits de transcription de PvQM varient aussi en fonction des castes et sont plus élevées chez les ouvrières et moins élevées chez les fourmis, tant mâles que femelles. Nos résultats indiquent une régulation spécifique de PvQM au niveau de la transcription en fonction du stade de développement et de la caste.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 140 , Issue 3 , June 2008 , pp. 312 - 323
Copyright
Copyright © Entomological Society of Canada 2008

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References

Angelini, D.R., and Kaufman, T.C. 2005. Insect appendages and comparative ontogenetics. Developmental Biology, 286: 57–77.CrossRefGoogle ScholarPubMed
Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3.0. Journal of Biochemistry and Molecular Biology, 340: 783–795.Google Scholar
Bodenstein, D. 1965. The postembryonic development of Drosophila. In Biology of Drosophila. Edited by Demerec, M.. Hafner Publishing Company, New York. pp. 257–267.Google Scholar
Chan, Y.L., Diaz, J.J., Denoroy, L., Madjar, J.J., and Wool, I.G. 1996. The primary structure of rat ribosomal protein L10: relationship to a Jun-binding protein and to a putative Wilm tumor suppressor. Biochemical and Biophysical Research Communications, 225: 952–956.Google Scholar
Chen, C., Wanduragala, S., Becker, D.F., and Dickman, M.B. 2006. Tomato QM-like protein protects Saccharomyces cerevisiae cells against oxidative stress by regulating intracellular proline levels. Applied and Environmental Microbiology, 72: 4001–4006.Google Scholar
Claeys, I., Simonet, G., Van Loy, T., De Loof, A., and Vanden Broeck, J. 2003. cDNA cloning and transcript distribution of two novel members of the neuroparsin family in the desert locust, Schistocerca gregaria. Insect Molecular Biology, 12: 473–481.CrossRefGoogle ScholarPubMed
Dearden, P.K., Wilson, M.J., Sablan, L., Osborne, P.W., Havler, M., McNaughton, E., Kimura, K., Milshina, N.V., Hasselmann, M., Gempe, T., Schioett, M., Brown, S.J., Elsik, C.G., Holland, P.W., Kadowaki, T., and Beye, M. 2006. Patterns of conservation and change in honey bee developmental genes. Genome Research, 16: 1376–1384.Google Scholar
Dick, F.A., and Trumpower, B.L. 1998. Heterologous complementation reveals that mutant alleles of QSR1 render 60S ribosomal subunits unstable and translationally inactive. Nucleic Acids Research, 26: 2442–2448.Google Scholar
Dowdy, S.F., Lai, K.M., Weissman, B.E., Matsui, Y., Hogan, B.L.M., and Stanbridge, E.J. 1991. The isolation and characterization of a novel cDNA demonstrating an altered mRNA level in nontumorigenic Wilms microcell hybrid cells. Nucleic Acids Research, 19: 5763–5769.Google Scholar
Eisinger, D.P., Jiang, H.P., and Serrero, G. 1993. A novel mouse gene highly conserved throughout evolution: regulation in adipocyte differentiation and in tumorigenic cell lines. Biochemical and Biophysical Research Communications, 196: 1227–1232.Google Scholar
Eisinger, D.P., Dick, F.A., and Trumpower, B.L. 1997. Qsr1p, a 60S ribosomal subunit protein, is required for joining of 40S and 60S subunits. Molecular and Cellular Biology, 17: 5136–5145.Google Scholar
Farmer, A.A., Loftus, T.M., Mills, A.A., Sato, K.Y., Neill, J.D., Tron, T., Yang, M., Trumpower, B.L., and Stanbridge, E.J. 1994. Extreme evolutionary conservation of QM, a novel c-Jun associated transcription factor. Human Molecular Genetics, 3: 723–728.Google Scholar
Fitzgerald, M., and Shenk, T. 1981. The sequence 5′-AAUAAA-3′ forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell, 24: 251–260.Google Scholar
Green, H., Canfield, A.E., Hillarby, M.C., Grant, M.E., Boot-Handford, R.P., Freemont, A.J., and Wallis, G.A. 2000. The ribosomal protein QM is expressed differentially during vertebrate endochondral bone development. Journal of Bone and Mineral Research, 15: 1066–1075.Google Scholar
Hu, X.B., Wang, W.J., Zhang, D.H., Jiao, J.H., Tan, W.B., Sun, Y., Ma, L., and Zhu, C.L. 2007. Cloning and characterization of 40S ribosomal protein S4 gene from Culex pipiens pallens. Comparative Biochemistry and Physiology, Part B, 146: 265–270.Google Scholar
Hwang, J.S., Goo, T.W., Yun, E.Y., Lee, J.H., Kang, S.W., Kim, K.Y., and Kwon, O.Y. 2000. Tissue-/stage-dependent expression of a cloned Bombyx mandarina QM homologue. Biomolecular Engineering, 16: 211–215.Google Scholar
Imafuku, I., Masaki, T., Waragai, M., Takeuchi, S., Kawabata, M., Hirai, S., Ohno, S., Nee, L.E., Lippa, C.F., Kanazawa, I., Imagawa, M., and Okazawa, H. 1999. Presenilin 1 suppresses the function of c-Jun homodimers via interaction with QM/Jif–1. Journal of Cell Biology, 147: 121–133.Google Scholar
Inada, H., Mukai, J., Matsushima, S., and Tanaka, T. 1997. QM is a novel zinc-binding transcription regulatory protein: its binding to c-Jun is regulated by zinc ions and phosphorylation by protein kinase C. Biochemical and Biophysical Research Communications, 230: 331–334.CrossRefGoogle ScholarPubMed
Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. 1998. Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences, 23: 403–405.Google Scholar
Karin, M., Liu, Z., and Zandi, E. 1997. AP-1 function and regulation. Current Opinion in Cell Biology, 9: 240–246.Google Scholar
Klauck, S.M., Felder, B., Kolb-Kokocinski, A., Schuster, C., Chiocchetti, A., Schupp, I., Wellenreuther, R., Schmötzer, G., Poustka, F., Breitenbach-Koller, L., and Poustka, A. 2006. Mutations in the ribosomal protein gene RPL10 suggest a novel modulating disease mechanism for autism. Molecular Psychiatry, 11: 1073–1084.Google Scholar
Levine, M., and Davidson, E.H. 2005. Gene regulatory networks for development. Proceedings of the National Academy of Sciences of the United States of America, 102: 4936–4942.CrossRefGoogle ScholarPubMed
Loftus, T.M., Nguyen, Y.H., and Stanbridge, E.J. 1997. The QM protein associates with ribosomes in the rough endoplasmic reticulum. Biochemistry, 36: 8224–8230.Google Scholar
Mills, A.A., Mills, M.J., Gardiner, D.M., Bryant, S.V., and Stanbridge, E.J. 1999. Analysis of the pattern of QM expression during mouse development. Differentiation, 64: 161–171.Google Scholar
Monteclaro, F.S., and Vogt, P.K. 1993. A Jun-binding protein related to a putative tumor suppressor. Proceedings of the National Academy of Sciences of the United States of America, 90: 6726–6730.Google Scholar
Oh, H.S., Kwon, H., Sun, S.K., and Yang, C.H. 2002. QM, a putative tumor suppressor, regulates proto-oncogene c-Yes. Journal of Biological Chemistry, 277: 36 489– 36 498.Google Scholar
Panfilio, K.A. 2008. Extraembryonic development in insects and the acrobatics of blastokinesis. Developmental Biology, 313: 471–491.Google Scholar
Park, S., and Jeong, D.G. 2006. Ribosomal protein L10 interacts with the SH3 domain and regulates GDNF-induced neurite growth in SH-SY-5y cells. Journal of Cellular Biochemistry, 99: 624–634.Google Scholar
Simonet, G., Claeys, I., Breugelmans, B., Van Soest, S., De Loof, A., and Vanden Broeck, J. 2004. Transcript profiling of pacifastin-like peptide precursors in crowd-and isolated-reared desert locusts. Biochemical and Biophysical Research Communications, 317: 565–569.CrossRefGoogle Scholar
SPSS Inc. 2004. SPSS version 13.0. SPSS Inc., Chicago.Google Scholar
Stanbridge, E., Farmer, A., Mills, A., Loftus, T., Kongkasuriyachai, D., and Dowdy, S. 1994. Molecular characterization of QM, a novel gene with properties consistent with tumor suppressor function. Cold Spring Harbor Symposia on Quantitative Biology, 59: 573–576.Google Scholar
Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24: 1596–1599.Google Scholar
Tron, T., Yang, M., Dick, F.A., Schmitt, M.E., and Trumpower, B.L. 1995. QSR1, an essential yeast gene with a genetic relationship to a subunit of the mitochondrial cytochrome bc1 complex, is homologous to a gene implicated in eucaryotic cell differentiation. Journal of Biological Chemistry, 270: 9961–9970.Google Scholar
Verras, M., Theodoraki, M.A., and Mintzas, A.C. 2004. Cloning, characterization, and developmental expression of the ribosomal protein S21 gene of the Mediterranean fruit fly Ceratitis capitata. Archives of Insect Biochemistry and Physiology, 56: 133–142.Google Scholar
Wang, L.Y., Wang, J.X., Zhao, X.F., and Wang, L.C. 2001. Modified method for isolation of house fly total RNA. Sichuan Journal of Zoology, 21: 67–69.Google Scholar
Zhang, C.Y., Xu, S.G., and Huang, X.X. 2005. A novel and convenient relative quantitative method of fluorescence real time RT-PCR assay based on slope of standard curve. Progress in Biochemistry and Biophysiology, 32: 883–888.Google Scholar