Identification of a tubulin-α gene specifically expressed in testis and adductor muscle during stable reference gene selection in the hermaphrodite gonad of the lion's paw scallop Nodipecten subnodosus

Marine Genomics

Volumn 6, Issue , 2012, Pages 33-44

  Llera Herrera, Raúl ^a   García Gasca, Alejandra ^b   Huvet, Arnaud ^c   Ibarra, Ana M ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

^b CENTRO DE INVESTIGACIÓN EN ALIMENTACIÓN Y DESARROLLO   (Mexico)

^c Universite de Bretagne Occidentale   (France)

Author keywords

Gametogenesis; Nodipecten; Real time qPCR; Reference gene; Testis specific; tub

Indexed keywords

TUBULIN;

ANIMAL; ARTICLE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GONAD; HERMAPHRODITIC SPECIES; MALE; METABOLISM; MUSCLE; PHYSIOLOGY; SCALLOP; TESTIS;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; GONADS; HERMAPHRODITIC ORGANISMS; MALE; MUSCLES; PECTINIDAE; TESTIS; TUBULIN;

HEXAPODA; NODIPECTEN; NODIPECTEN SUBNODOSUS;

EID: 84860622639     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2012.03.003     Document Type: Article

References (58)

1. Andersen C.L., Jensen J.L., Ørntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004, 64:5245-5250.
2. Barreau C., Benson E., Gudmannsdottir E., Newton F., White-Cooper H. Post-meiotic transcription in Drosophila testes. Development 2008, 135:1897-1902.
3. Bo J., Wensink P.C. The promoter region of the Drosophila α2-tubulin gene directs testicular and neural specific expression. Development 1989, 106:581-587.
4. Bustin S.A., Benes V., Nolan T., Pfaffl M.W. Quantitative real-time RT-PCR - a perspective. J. Mol. Endocrinol. 2005, 34:597-601.
5. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
6. Ciocan C.M., Cubero-Leon E., Minier C., Rotchell J.M. Identification of reproduction-specific genes associated with maturation and estrogen exposure in a marine bivalve Mytilus edulis. PloS one. 2011, 6:e22326. 10.1371/journal.pone.0022326.
7. De Santis C., Smith-Keune C., Jerry D.R. Normalizing RT-qPCR data: are we getting the right answers? An appraisal of normalization approaches and internal reference genes from a case study in the finfish Lates calcarifer. Mar. Biotechnol. 2010, 13:170-180.
8. Dheilly N.M., Lelong C., Huvet A., Favrel P. Development of a Pacific oyster (Crassostrea gigas) 31,918-gene microarray: identification of reference genes and tissue-specific expression patterns. BMC Genomics 2011, 12:468.
9. Fabioux C., Huvet A., Lelong C., Robert R., Pouvreau S., Daniel J.Y., Minguant C., Le Pennec M. Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem. Biophys. Res. Commun. 2004, 320:592-598.
10. Fackenthal J.D., Hutchens J.A., Turner F.R., Raff E.C. Structural analysis of mutations in the Drosophila b2-tubulin isoform reveals regions in the b-tubulin molecule required for general and for tissue-specific microtubule functions. Genetics 1995, 139:267-286.
11. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunasekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L.L., Eddy S.R., Bateman A. The Pfam protein database. Nucleic Acids Res. 2010, 38:D211-D222.
12. González I.L., Sylvester J.E. Incognito rRNA and rDNA in databases and libraries. Genome Res. 1997, 7:65-70.
13. Hammond J.W., Cai D., Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 2008, 20:71-76.
14. Hansen K.D., Brenner S.E., Dudoit S. Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res. 2010, 38:e131.
15. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007, 8:R19.
16. Hernández-Arteaga S., López-Revilla R. Quantitation of human papillomavirus type 16 E6 oncogene sequences by real-time or quantitative PCR with EvaGreen. Anal. Biochem. 2008, 380:131-133.
17. Hutchens J.A., Hoyle H.D., Turner F.R., Raff E.C. Structurally similar Drosophila alpha-tubulins are functionally distinct in vivo. Mol. Biol. Cell 1997, 8:481-500.
18. Ibarra A.M., Petersen J.L., Famula T.R., May B. Characterization of 35 microsatellite loci in the Pacific lion-paw scallop (Nodipecten subnodosus) and their cross-species amplification in four other scallops of the Pectinidae family. Mol. Ecol. Notes 2006, 6:153-156.
19. Jiang M., Ryu J., Kiraly M., Duke K., Reinke V., Kim S.K. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 2001, 98:218-233.
20. Kawasaki H., Sugaya K., Quan G.X., Nohata J., Mita K. Analysis of alpha- and beta-tubulin genes of Bombyx mori using an EST database. Insect Biochem. Mol. Biol. 2003, 33:131-137.
21. Kemphues K.J., Raff R.A., Kaufman T.C., Raff E.C. Mutation in a structural gene for a beta-tubulin specific to testis in Drosophila melanogaster. Proc. Natl. Acad. Sci. 1979, 76:3991-3995.
22. Kierszenbaum A.L. Sperm axoneme: a tale of tubulin posttranslation diversity. Mol. Reprod. Dev. 2002, 62:1-3.
23. Kortner T.M., Valen E.C., Kortner H., Marjara I.S., Krogdahl A., Bakke A.M. Candidate reference genes for quantitative real-time PCR (qPCR) assays during development of a diet-related enteropathy in Atlantic salmon (Salmo salar L.) and the potential pitfalls of uncritical use of normalization software tools. Aquaculture 2011, 318:355-363.
24. Kuai L., Fang F., Butler J.S., Sherman F. Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 2004, 101:8581-8586.
25. Lewis S.A., Cowan N.J. Complex regulation and functional versatility of mammalian α- and β-tubulin isotypes during the differentiation of testis and muscle cells. J. Cell Biol. 1988, 106:2011-2022.
26. Llera-Herrera R., García-Gasca A., Romero-Vivas E., Huvet A., Ibarra A.M. Identification and comparative expression of gametogenic-related genes in the ovary and testis of the hermaphrodite lion-paw scallop Nodipecten subnodosus. Physiomar '10 Workshop. Quebec City, Canada 2010.
27. Lu X., Wu X.-I. Sex, sex chromosomes and gene expression. BMC Biol. 2011, 9:30.
28. Lycett G.J., Amenya D., Lynd A. The Anopheles gambiae alpha-tubulin-1b promoter directs neuronal, testes and developing imaginal tissue specific expression and is a sensitive enhancer detector. Insect Mol. Biol. 2011, 10.1111/j.1365-2583.2011.01112.x.
29. Nielsen M.G., Gadagkar S.R., Gutzwiller L. Tubulin evolution in insects: gene duplication and subfunctionalization provide specialized isoforms in a functionally constrained gene family. BMC Evol. Biol. 2010, 10:113.
30. Nolan T., Bustin S. Procedures for quality control of RNA samples for use in quantitative reverse transcription PCR. Essentials of Nucleic Acid Analysis: a Robust Approach 2008, The Royal Society of Chemistry, Cambridge, UK.
31. O'Connell, J. The basics of RT-PCR: some practical considerations. RT-PCR Protocols 2002, Humana Press, Totowa, NJ.
32. Osada M., Harata M., Kishida M., Kijima A. Molecular cloning and expression analysis of vitellogenin in scallop, Patinopecten yessoensis (Bivalvia, Mollusca). Mol. Reprod. Dev. 2004, 67:273-281.
33. Petersen J.L., Ibarra A.M., Ramirez J.L., May B. An induced mass spawn of the hermaphroditic lion-paw scallop, Nodipecten subnodosus: genetic assignment of maternal and paternal parentage. J. Hered. 2008, 99:337-348.
34. Petersen J.L., Baerwald M.R., Ibarra A.M., May B. Discovering QTL's underlying growth traits in the Pacific lion-paw scallop using a first generation microsatellite and AFLP linkage map. Plant & Animal Genome XVII Conference. January 10-14, 2009, San Diego California 2009, Abstract.
35. Petersen J.L., Ibarra A.M., May B. Thirty-seven additional microsatellite loci in the Pacific lion-paw scallop (Nodipecten subnodosus) and cross-amplification in other pectinids. Cons. Gen. Res. 2009, 1:101-105.
36. Petersen J.L., Baerwald M.R., Ibarra A.M., May B. A genetic linkage map of the Pacific lion-paw scallop - steps toward marker assisted selection in aquaculture. Aquaculture 2010, San Diego CA USA, March 1-5, 2010 2010, Abstract.
37. Petersen J.L., Ibarra A.M., May B. Nuclear and mtDNA lineage diversity in wild and cultured Pacific lion-paw scallop, Nodipecten subnodosus (Baja California Peninsula, Mexico). Mar. Biol. 2010, 157:2751-2767.
38. Pfaffl M.W. Quantification strategies in real-time PCR. AZ of Quantitative PCR 2004, 87-120. IUL Biotechnology, La Jolla, CA. S.A. Bustin (Ed.).
39. Pfaffl M.W., Tichopad A., Prgomet C., Neuvians T.P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestkeeper - Excel-based tool using pair-wise correlations. Biotechnol. Lett. 2004, 26:509-515.
40. Racotta I.S., Ramirez J.L., Ibarra A.M., Rodriguez-Jaramillo M.C., Carreño D., Palacios E. Growth and gametogenesis in the lion-paw scallop Nodipecten (Lyropecten) subnodosus. Aquaculture 2003, 217:335-349.
41. Radonic A., Thulke S., Mackay I.M., Landt O., Siegert W., Nitsche A. Guideline to reference gene selection for quantitative real-time PCR. Biochem. Biophys. Res. Commun. 2004, 313:856-862.
42. Raska I., Koberna K., Malínský J., Fidlerová H., Masata M. The nucleolus and transcription of ribosomal genes. Biol. Cell 2004, 96:579-594.
43. Ruijter J.M., Ramakers C., Hoogaars W.M.H., Karlen Y., Bakker O., van den Hoff M.J.B., Moorman A.F.M. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009, 37:e45.
44. Sambrook J., Russel D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
45. Sellars M., Lyons R., Grewe P., Vuocolo T., Leeton L., Coman G. A PL10 vasa-like gene in the kuruma shrimp, Marsupenaeus japonicus, expressed during development and in adult gonad. Mar. Biotechnol. 2007, 9:377-387.
46. Siebert K.S., Lorenzen M.D., Brown S.J., Park Y., Beeman R.W. Tubulin superfamily genes in Tribolium castaneum and the use of a tubulin promoter to drive transgene expression. Insect Biochem. Mol. Biol. 2008, 38:749-755.
47. Silveira E.D., Alves-Ferreira M., Guimarães L.A., da Silva F.R., Carneiro V. Selection of reference genes for quantitative real-time PCR expression studies in the apomictic and sexual grass Brachiaria brizantha. BMC Plant Biol. 2009, 9:84.
48. Slomovic S., Laufer D., Geiger D., Schuster G. Polyadenylation of ribosomal RNA in human cells. Nucleic Acids Res. 2006, 34:2966-2975.
49. Slomovic S., Fremder E., Staals R.H.G., Pruijn G.J.M., Schuster G. Addition of poly(A) and poly(A)-rich tails during RNA degradation in the cytoplasm of human cells. Proc. Natl. Acad. Sci. 2010, 107:7407-7412.
50. Stanchi F., Corso V., Scannapieco P., Ievolella C., Negrisolo E., Tiso N., Lanfranchi G., Valle G. TUBA8: a new tissue-specific isoform of alpha-tubulin that is highly conserved in human and mouse. Biochem. Biophys. Res. 2000, 270:1111-1118.
51. Theurkauf W.E., Baum H., Bo J., Wensink P.C. Tissue-specific and constitutive α-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl. Acad. Sci. 1986, 83:8477-8481.
52. Tuiskunen A., Leparc-Goffart I., Boubis L., Monteil V., Klingström J., Tolou H.J., Lundkvist A., Plomet S. Self-priming of reverse transcriptase impairs strand-specific detection of dengue virus RNA. J. Gen. Virol. 2010, 91:1019-1027.
53. Untergasser A., Nijveen H., Rao X., Bisseling T., Geurts R., Leunissen J.A.M. Primer3Plus, an enhanced web interface to primer3. Nucleic Acids Res. 2007, 35:W71-W74.
54. Vandesompele J., Preter K.D., Pattyn F., Poppe B., Roy N.V., Paepe A.D., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (research0034.1-0034.11).
55. Xue J.-L., Salem T.Z., Turney C.M., Cheng X.-W. Strategy of the use of 28S rRNA as a housekeeping gene in real-time quantitative PCR analysis of gene transcription in insect cells infected by viruses. J. Gen. Virol. 2010, 163:210-215.
56. Zhong Q., Zhang Q., Wang Z., Qi J., Chen Y., Li S. Expression profiling and validation of potential reference genes during Paralichthys olivaceus embryogenesis. Mar. Biotechnol. 2008, 10:310-318.
57. Zhu L.J., Altmann S.W. mRNA and 18S-RNA coapplication-reverse transcription for quantitative gene expression analysis. Anal. Biochem. 2005, 345:102-109.
58. Zimowska G.J., Nirmala X., Handler A.M. The β2-tubulin gene from three tephritid fruit fly species and use of its promoter for sperm marking. Insect Biochem. Mol. Biol. 2009, 39:508-515.