Skip to main content Accessibility help
×
Home
Hostname: page-component-55b6f6c457-rq6d8 Total loading time: 0.387 Render date: 2021-09-26T14:02:31.593Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

A pilot study on transcriptome data analysis of folliculogenesis in pigs

Published online by Cambridge University Press:  01 March 2009

G. Tosser-Klopp*
Affiliation:
Laboratoire de Génétique Cellulaire, Institut National de la Recherche Agronomique, UMR444, BP 52627, 31326 Castanet Tolosan Cedex, France
K.-A. Lê Cao
Affiliation:
Station d’Amélioration Génétique des Animaux, Institut National de la Recherche Agronomique (UR631), BP 52627, 31326 Castanet Tolosan Cedex, France Institut de Mathématiques, Université de Toulouse et Centre National de la Recherche Scientifique (UMR5219), 31062 Toulouse Cedex 9, France
A. Bonnet
Affiliation:
Laboratoire de Génétique Cellulaire, Institut National de la Recherche Agronomique, UMR444, BP 52627, 31326 Castanet Tolosan Cedex, France
N. Gobert
Affiliation:
Laboratoire de Génétique Cellulaire, Institut National de la Recherche Agronomique, UMR444, BP 52627, 31326 Castanet Tolosan Cedex, France
F. Hatey
Affiliation:
Laboratoire de Génétique Cellulaire, Institut National de la Recherche Agronomique, UMR444, BP 52627, 31326 Castanet Tolosan Cedex, France
C. Robert-Granié
Affiliation:
Station d’Amélioration Génétique des Animaux, Institut National de la Recherche Agronomique (UR631), BP 52627, 31326 Castanet Tolosan Cedex, France
S. Déjean
Affiliation:
Institut de Mathématiques, Université de Toulouse et Centre National de la Recherche Scientifique (UMR5219), 31062 Toulouse Cedex 9, France
J. Antic
Affiliation:
Département de Génie Mathématique et Modélisation, INSA, 135, Avenue de Rangueil, 31077 Toulouse Cedex 4, France
L. Baschet
Affiliation:
Département de Génie Mathématique et Modélisation, INSA, 135, Avenue de Rangueil, 31077 Toulouse Cedex 4, France
M. SanCristobal
Affiliation:
Laboratoire de Génétique Cellulaire, Institut National de la Recherche Agronomique, UMR444, BP 52627, 31326 Castanet Tolosan Cedex, France
Get access

Abstract

Three different stages of pig antral follicles have been studied in a granulosa-cell transcriptome analysis on nylon microarrays (1152 clones). The data have been generated from seven RNA follicle pools and several technical replicates were made. The objective of this paper was to state the feasibility of a transcriptomic protocol for the study of folliculogenesis in the pig. A statistical analysis was chosen, relying on the linear mixed model (LMM) paradigm. Low variability within technical replicates was hence checked with a LMM. Relevant genes that might be involved in the studied process were then selected. For the most significant genes, statistical methods such as principal component analysis and unsupervised hierarchical clustering were applied to assess their relevance, and a random forest analysis proved their predictive value. The selection of genes was consistent with previous studies and also allowed the identification of new genes whose role in pig folliculogenesis will be further investigated.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

These authors have contributed equally to this work.

References

Agca, C, Ries, JE, Kolath, SJ, Kim, JH, Forrester, LJ, Antoniou, E, Whitworth, KM, Mathialagan, N, Springer, GK, Prather, RS, Lucy, MC 2006. Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132, 133145.CrossRefGoogle ScholarPubMed
Algers, B, Uvnas-Moberg, K 2007. Maternal behavior in pigs. Hormones and Behavior 52, 7885.CrossRefGoogle ScholarPubMed
Benjamini, Y, Hochberg, Y 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289300.Google Scholar
Bertucci, F, Bernard, K, Loriod, B, Chang, YC, Granjeaud, S, Birnbaum, D, Nguyen, C, Peck, K, Jordan, BR 1999. Sensitivity issues in DNA array-based expression measurements and performance of nylon microarrays for small samples. Human Molecular Genetics 8, 17151722.CrossRefGoogle ScholarPubMed
Besnard, N, Pisselet, C, Monniaux, D, Locatelli, A, Benne, F, Gasser, F, Hatey, F, Monget, P 1996. Expression of messenger ribonucleic acids of insulin-like growth factor binding protein-2, -4, and -5 in the ovine ovary: localization and changes during growth and atresia of antral follicles. Biology of Reproduction 55, 13561367.CrossRefGoogle ScholarPubMed
Bichard, M, David, PJ 1985. Effectiveness of genetic selection for prolificacy in pigs. Journal of Reproduction and Fertility. Supplement 33, 127138.Google ScholarPubMed
Bonnet, A, Frappart, PO, Dehais, P, Tosser-Klopp, G, Hatey, F 2006. Identification of differential gene expression in in vitro FSH treated pig granulosa cells using suppression subtractive hybridization. Reproductive Biology and Endocrinology 4, 3510.1186/1477-7827-4-35.CrossRefGoogle ScholarPubMed
Bonnet, A, Iannuccelli, E, Hugot, K, Benne, F, Bonaldo, MF, Soares, MB, Hatey, F, Tosser-Klopp, G 2008a. A pig multi-tissue normalised cDNA library: large-scale sequencing, cluster analysis and 9 K micro-array resource generation. BMC Genomics 9, 1710.1186/1471-2164-9-17.CrossRefGoogle Scholar
Bonnet, A, Le Cao, KA, San Cristobal, M, Benne, F, Robert-Granié, C, Law-So, G, Fabre, S, Besse, P, De Billy, E, Quesnel, H, Hatey, F, Tosser-Klopp, G 2008b. In vivo gene expression in granulosa cells during pig terminal follicular development. Reproduction 136, 211224.CrossRefGoogle ScholarPubMed
Breiman, L 2001. Random forests. Machine Learning 45, 532.CrossRefGoogle Scholar
Buske, B, Sternstein, I, Brockmann, G 2006. QTL and candidate genes for fecundity in sows. Animal Reproduction Science 95, 167183.CrossRefGoogle ScholarPubMed
Caetano, AR, Johnson, RK, Ford, JJ, Pomp, D 2004. Microarray profiling for differential gene expression in ovaries and ovarian follicles of pigs selected for increased ovulation rate. Genetics 168, 15291537.CrossRefGoogle ScholarPubMed
Churchill, GA, Oliver, B 2001. Sex, flies and microarrays. Nature Genetics 29, 355356.CrossRefGoogle ScholarPubMed
Diaz-Uriarte, R, Alvarez de Andres, S 2006. Gene selection and classification of microarray data using random forest. BMC Bioinformatics 7, 310.1186/1471-2105-7-3.CrossRefGoogle ScholarPubMed
Duda, M 1997. The influence of FSH, LH and testosterone on steroidsecretion by two subpopulations of porcine granulosa cells. Journal of Physiology and Pharmacology 48, 8996.Google ScholarPubMed
Eisen, MB, Spellman, PT, Brown, PO, Botstein, D 1998. Cluster analysis and display of genome-wide expression patterns. The Proceedings of the National Academy of Sciences of the United States of America 95, 1486314868.CrossRefGoogle ScholarPubMed
Erickson, GF, Magoffin, DA, Dyer, CA, Hofeditz, C 1985. The ovarian androgen producing cells: a review of structure/function relationships. Endocrine Reviews 6, 371399.CrossRefGoogle ScholarPubMed
Fayad, T, Levesque, V, Sirois, J, Silversides, DW, Lussier, JG 2004. Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive hybridization. Biology of Reproduction 70, 523533.CrossRefGoogle ScholarPubMed
Ferré, PJ, Liaubet, L, Concordet, D, Sancristobal, M, Uro-Coste, E, Tosser-Klopp, G, Bonnet, A, Toutain, PL, Hatey, F, Lefebvre, HP 2007. Longitudinal analysis of gene expression in porcine skeletal muscle after post-injection local injury. Pharmaceutical Research 24, 14801489.CrossRefGoogle ScholarPubMed
Foxcroft, GR, Hunter, MG 1985. Basic physiology of follicular maturation in the pig. Journal of Reproduction and Fertility. Supplement 33, 119.Google ScholarPubMed
Foxcroft, GR, Hunter, MG, Grant, SA 1989. The physiology of follicular maturation in the pig. Acta Physiologica Polonica 40, 5363.Google ScholarPubMed
Fricke, PM, Ford, JJ, Reynolds, LP, Redmer, DA 1996. Growth and cellular proliferation of antral follicles throughout the follicular phase of the estrous cycle in Meishan gilts. Biology of Reproduction 54, 879887.CrossRefGoogle ScholarPubMed
Garrett, WM, Mack, SO, Rohan, RM, Guthrie, HD 2000. In situ analysis of the changes in expression of ovarian inhibin subunit mRNAs during follicle recruitment after ovulation in pigs. Journal of Reproduction and Fertility 118, 235242.Google ScholarPubMed
Gasser, F, Mulsant, P, Gillois, M 1985. Long-term multiplication of the Chinese hamster ovary (CHO) cell line in a serum-free medium. In Vitro Cellular and Developmental Biology 21, 588592.CrossRefGoogle Scholar
Guthrie, HD, Barber, JA, Leighton, JK, Hammond, JM 1994. Steroidogenic cytochrome P450 enzyme messenger ribonucleic acids and follicular fluid steroids in individual follicles during preovulatory maturation in the pig. Biology of Reproduction 51, 465471.CrossRefGoogle ScholarPubMed
Hirshfield, AN 1986. Patterns of [3H] thymidine incorporation differ in immature rats and mature, cycling rats. Biology of Reproduction 34, 229235.CrossRefGoogle Scholar
Jin, W, Riley, RM, Wolfinger, RD, White, KP, Passador-Gurgel, G, Gibson, G 2001. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nature Genetics 29, 389395.CrossRefGoogle ScholarPubMed
Kao, LC, Germeyer, A, Tulac, S, Lobo, S, Yang, JP, Taylor, RN, Osteen, K, Lessey, BA, Giudice, LC 2003. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 144, 28702881.CrossRefGoogle ScholarPubMed
Kerr, MK, Churchill, GA 2001. Experimental design for gene expression microarrays. Biostatistics 2, 183201.CrossRefGoogle ScholarPubMed
Knox, RV 2005. Recruitment and selection of ovarian follicles for determination of ovulation rate in the pig. Domestic Animal Endocrinology 29, 385397.CrossRefGoogle ScholarPubMed
Le Cao, KA, Goncalves, O, Besse, P, Gadat, S 2007. Selection of biologically relevant genes with a wrapper stochastic algorithm. Statistical Applications in Genetics and Molecular Biology 6, Article 29.CrossRefGoogle ScholarPubMed
Liaw, A, Wiener, M 2002. Classification and regression by random Forest. The Newspaper of R Project 2, 1822.Google Scholar
Lopez, F, Rougemont, J, Loriod, B, Bourgeois, A, Loi, L, Bertucci, F, Hingamp, P, Houlgatte, R, Granjeaud, S 2004. Feature extraction and signal processing for nylon DNA microarrays. BMC Genomics 5, 38.CrossRefGoogle ScholarPubMed
May, JV, Schomberg, DW 1984. Developmental coordination of luteinizing hormone/human chorionic gonadotropin (hCG) receptors and acute hCG responsiveness in cultured and freshly harvested porcine granulosa cells. Endocrinology 114, 153163.CrossRefGoogle ScholarPubMed
Monniaux, D 1987. Short-term effects of FSH in vitro on granulosa cells of individual sheep follicles. Journal of Reproduction and Fertility 79, 505515.CrossRefGoogle ScholarPubMed
Muller, C, Denis, M, Gentzbittel, L, Faraut, T 2004. The Iccare web server: an attempt to merge sequence and mapping information for plant and animal species. Nucleic Acids Research 32, W429W434.CrossRefGoogle ScholarPubMed
Patterson, HD, Thompson, R 1971. Recovery of inter-block information when block sizes are unequal. Biometrika 58, 545554.CrossRefGoogle Scholar
Pisselet, C, Clement, F, Monniaux, D 2000. Fraction of proliferating cells in granulosa during terminal follicular development in high and low prolific sheep breeds. Reproduction, Nutrition, Development 40, 295304.CrossRefGoogle ScholarPubMed
Raychaudhuri, S, Stuart, JM, Altman, RB 2000. Principal components analysis to summarize microarray experiments: application to sporulation time series. Pacific Symposium on Biocomputing 5, 452463.Google Scholar
Seber, G 1984. Multivariate observations. Wiley, New York, NY.CrossRefGoogle Scholar
Statistical Analysis Systems Institute 1999. SAS/STAT Software, version 8. SAS Institute Inc., Cary, NC.Google Scholar
Tosser-Klopp, G, Benne, F, Bonnet, A, Mulsant, P, Gasser, F, Hatey, F 1997. A first catalog of genes involved in pig ovarian follicular differentiation. Mammalian Genome 8, 250254.CrossRefGoogle ScholarPubMed
van der Lende, T, Knol, EF, Leenhouwers, JI 2001. Prenatal development as a predisposing factor for perinatal losses in pigs. Reproduction 58(suppl.), 247261.Google Scholar
Varani, S, Elvin, JA, Yan, C, DeMayo, J, DeMayo, FJ, Horton, HF, Byrne, MC, Matzuk, MM 2002. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Molecular Endocrinology 16, 11541167.CrossRefGoogle ScholarPubMed
Vizirianakis, IS, Pappas, IS, Gougoumas, D, Tsiftsoglou, AS 1999. Expression of ribosomal protein S5 cloned gene during differentiation and apoptosis in murine erythroleukemia (MEL) cells. Oncology Research 11, 409419.Google ScholarPubMed
Whitworth, KM, Agca, C, Kim, JG, Patel, RV, Springer, GK, Bivens, N, Forrester, LJ, Mathialagan, N, Green, JA, Prather, RS 2005. Transcriptional profiling of pig embryogenesis by using a 15k member unigene set specific for pig reproductive tissues and embryos. Biology of Reproduction 72, 14371451.CrossRefGoogle Scholar
Wu, H, Kerr, MK, Cui, X, Churchill, GA 2003. MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. In The analysis of gene expression data: methods and software (ed. G Parmigiani, ES Garrett, RA Irizarry and SL Zeger). Springer, New York, NY.Google Scholar
Yeung, KY, Ruzzo, WL 2001. Principal component analysis for clustering gene expression data. Bioinformatics 17, 763774.CrossRefGoogle ScholarPubMed

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

A pilot study on transcriptome data analysis of folliculogenesis in pigs
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

A pilot study on transcriptome data analysis of folliculogenesis in pigs
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

A pilot study on transcriptome data analysis of folliculogenesis in pigs
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *