Transcriptome profiling of sheep granulosa cells and oocytes during early follicular development obtained by Laser Capture Microdissection

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作者：Agnes Bonnet (1) Claudia Bevilacqua (2) Francis Benne (1) Loys Bodin (3) Corinne Cotinot (4) Laurence Liaubet (1) Magali Sancristobal (1) Julien Sarry (1) Elena Terenina (1) Patrice Martin (2) Gwenola Tosser-Klopp (1) Beatrice Mandon-Pepin (4)
刊名：BMC Genomics
出版年：2011
出版时间：December 2011
年：2011
卷：12
期：1
全文大小：607KB
参考文献：1. McNatty KP, Smith P, Hudson NL, Heath DA, Tisdall DJ, O WS, Braw-Tal R: Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. / J Reprod Fertil Suppl 1995, 49:123鈥?35. 2. Soyal SM, Amleh A, Dean J: FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. / Development 2000, 127:4645鈥?654. 3. Oktem O, Urman B: Understanding follicle growth in vivo. / Hum Reprod 2010, 25:2944鈥?954. mrep/deq275">CrossRef 4. Hutt KJ, McLaughlin EA, Holland MK: Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. / Mol Hum Reprod 2006, 12:61鈥?9. molehr/gal010">CrossRef 5. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM: Growth differentiation factor-9 is required during early ovarian folliculogenesis. / Nature 1996, 383:531鈥?35. CrossRef 6. McMahon HE, Hashimoto O, Mellon PL, Shimasaki S: Oocyte-specific overexpression of mouse bone morphogenetic protein-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice. / Endocrinology 2008, 149:2807鈥?815. CrossRef 7. McNatty KP, Smith P, Moore LG, Reader K, Lun S, Hanrahan JP, Groome NP, Laitinen M, Ritvos O, Juengel JL: Oocyte-expressed genes affecting ovulation rate. / Mol Cell Endocrinol 2005, 234:57鈥?6. mce.2004.08.013">CrossRef 8. Choi Y, Rajkovic A: Genetics of early mammalian folliculogenesis. / Cell Mol Life Sci 2006, 63:579鈥?90. CrossRef 9. Bodin L, Di Pasquale E, Fabre S, Bontoux M, Monget P, Persani L, Mulsant P: A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. / Endocrinology 2007, 148:393鈥?00. CrossRef 10. Di Pasquale E, Beck-Peccoz P, Persani L: Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. / Am J Hum Genet 2004, 75:106鈥?11. CrossRef 11. Di Pasquale E, Rossetti R, Marozzi A, Bodega B, Borgato S, Cavallo L, Einaudi S, Radetti G, Russo G, Sacco M, / et al.: Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. / J Clin Endocrinol Metab 2006, 91:1976鈥?979. CrossRef 12. Rossetti R, Di Pasquale E, Marozzi A, Bione S, Toniolo D, Grammatico P, Nelson LM, Beck-Peccoz P, Persani L: BMP15 mutations associated with primary ovarian insufficiency cause a defective production of bioactive protein. / Hum Mutat 2009, 30:804鈥?10. mu.20961">CrossRef 13. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, / et al.: Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. / Mol Endocrinol 2001, 15:854鈥?66. me.15.6.854">CrossRef 14. Gallardo TD, John GB, Shirley L, Contreras CM, Akbay EA, Haynie JM, Ward SE, Shidler MJ, Castrillon DH: Genomewide discovery and classification of candidate ovarian fertility genes in the mouse. / Genetics 2007, 177:179鈥?94. CrossRef 15. Herrera L, Ottolenghi C, Garcia-Ortiz JE, Pellegrini M, Manini F, Ko MS, Nagaraja R, Forabosco A, Schlessinger D: Mouse ovary developmental RNA and protein markers from gene expression profiling. / Dev Biol 2005, 279:271鈥?90. bio.2004.11.029">CrossRef 16. Yoon SJ, Kim KH, Chung HM, Choi DH, Lee WS, Cha KY, Lee KA: Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. / Fertil Steril 2006, 85:193鈥?03. CrossRef 17. Espina V, Wulfkuhle JD, Calvert VS, VanMeter A, Zhou W, Coukos G, Geho DH, Petricoin EF, Liotta LA: Laser-capture microdissection. / Nat Protoc 2006, 1:586鈥?03. CrossRef 18. Clement-Ziza M, Munnich A, Lyonnet S, Jaubert F, Besmond C: Stabilization of RNA during laser capture microdissection by performing experiments under argon atmosphere or using ethanol as a solvent in staining solutions. / Rna 2008, 14:2698鈥?704. CrossRef 19. Goldsworthy SM, Stockton PS, Trempus CS, Foley JF, Maronpot RR: Effects of fixation on RNA extraction and amplification from laser capture microdissected tissue. / Mol Carcinog 1999, 25:86鈥?1. CrossRef 20. Huang LE, Luzzi V, Ehrig T, Holtschlag V, Watson MA: Optimized tissue processing and staining for laser capture microdissection and nucleic acid retrieval. / Methods Enzymol 2002, 356:49鈥?2. CrossRef 21. Mikulowska-Mennis A, Taylor TB, Vishnu P, Michie SA, Raja R, Horner N, Kunitake ST: High-quality RNA from cells isolated by laser capture microdissection. / Biotechniques 2002, 33:176鈥?79. 22. Mojsilovic-Petrovic J, Nesic M, Pen A, Zhang W, Stanimirovic D: Development of rapid staining protocols for laser-capture microdissection of brain vessels from human and rat coupled to gene expression analyses. / J Neurosci Methods 2004, 133:39鈥?8. meth.2003.09.026">CrossRef 23. Lundy T, Smith P, O'Connell A, Hudson NL, McNatty KP: Populations of granulosa cells in small follicles of the sheep ovary. / J Reprod Fertil 1999, 115:251鈥?62. CrossRef 24. Fleming-Waddell JN, Wilson LM, Olbricht GR, Vuocolo T, Byrne K, Craig BA, Tellam RL, Cockett NE, Bidwell CA: Analysis of gene expression during the onset of muscle hypertrophy in callipyge lambs. / Anim Genet 2007, 38:28鈥?6. CrossRef 25. Cope L, Hartman SM, Gohlmann HW, Tiesman JP, Irizarry RA: Analysis of Affymetrix GeneChip data using amplified RNA. / Biotechniques 2006, 40:165鈥?66, 168, 170. CrossRef 26. King C, Guo N, Frampton GM, Gerry NP, Lenburg ME, Rosenberg CL: Reliability and reproducibility of gene expression measurements using amplified RNA from laser-microdissected primary breast tissue with oligonucleotide arrays. / J Mol Diagn 2005, 7:57鈥?4. CrossRef 27. Hasegawa A, Kumamoto K, Mochida N, Komori S, Koyama K: Gene expression profile during ovarian folliculogenesis. / J Reprod Immunol 2009, 83:40鈥?4. CrossRef 28. Dharma SJ, Modi DN, Nandedkar TD: Gene expression profiling during early folliculogenesis in the mouse ovary. / Fertil Steril 2009, 91:2025鈥?036. CrossRef 29. Arraztoa JA, Zhou J, Marcu D, Cheng C, Bonner R, Chen M, Xiang C, Brownstein M, Maisey K, Imarai M, Bondy C: Identification of genes expressed in primate primordial oocytes. / Hum Reprod 2005, 20:476鈥?83. mrep/deh498">CrossRef 30. Pan H, O'Brien M J, Wigglesworth K, Eppig JJ, Schultz RM: Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. / Dev Biol 2005, 286:493鈥?06. bio.2005.08.023">CrossRef 31. Martinez-Madrid B, Dolmans MM, Langendonckt AV, Defrere S, Van Eyck AS, Donnez J: Ficoll density gradient method for recovery of isolated human ovarian primordial follicles. / Fertil Steril 2004, 82:1648鈥?653. CrossRef 32. Wang H, Owens JD, Shih JH, Li MC, Bonner RF, Mushinski JF: Histological staining methods preparatory to laser capture microdissection significantly affect the integrity of the cellular RNA. / BMC Genomics 2006, 7:97. CrossRef 33. Wang WZ, Oeschger FM, Lee S, Molnar Z: High quality RNA from multiple brain regions simultaneously acquired by laser capture microdissection. / BMC Mol Biol 2009, 10:69. CrossRef 34. Pietersen CY, Lim MP, Woo TU: Obtaining high quality RNA from single cell populations in human postmortem brain tissue. / J Vis Exp 2009. 35. Sluka P, O'Donnell L, McLachlan RI, Stanton PG: Application of laser-capture microdissection to analysis of gene expression in the testis. / Prog Histochem Cytochem 2008, 42:173鈥?01. CrossRef 36. Bevilacqua C, Makhzami S, Helbling JC, Defrenaix P, Martin P: Maintaining RNA integrity in a homogeneous population of mammary epithelial cells isolated by Laser Capture Microdissection. / BMC Cell Biol 2010, 11:95. CrossRef 37. Moore GP, Lintern-Moore S, Peters H, Faber M: RNA synthesis in the mouse oocyte. / J Cell Biol 1974, 60:416鈥?22. b.60.2.416">CrossRef 38. Moore GP, Lintern-Moore S: A correlation between growth and RNA synthesis in the mouse oocyte. / J Reprod Fertil 1974, 39:163鈥?66. CrossRef 39. Bachvarova R: Gene expression during oogenesis and oocyte development in mammals. / Dev Biol (N Y 1985) 1985, 1:453鈥?24. 40. Luzzi V, Mahadevappa M, Raja R, Warrington JA, Watson MA: Accurate and reproducible gene expression profiles from laser capture microdissection, transcript amplification, and high density oligonucleotide microarray analysis. / J Mol Diagn 2003, 5:9鈥?4. CrossRef 41. Feary ES, Juengel JL, Smith P, French MC, O'Connell AR, Lawrence SB, Galloway SM, Davis GH, McNatty KP: Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewes carrying the Woodlands FecX2W mutation. / Biol Reprod 2007, 77:990鈥?98. biolreprod.107.062752">CrossRef 42. Bebbere D, Bogliolo L, Ariu F, Fois S, Leoni GG, Tore S, Succu S, Berlinguer F, Naitana S, Ledda S: Expression pattern of zygote arrest 1 (ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos. / Reprod Fertil Dev 2008, 20:908鈥?15. CrossRef 43. Anderson RA, Fulton N, Cowan G, Coutts S, Saunders PT: Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis. / BMC Dev Biol 2007, 7:136. CrossRef 44. Silva JR, van den Hurk R, van Tol HT, Roelen BA, Figueiredo JR: The Kit ligand/c-Kit receptor system in goat ovaries: gene expression and protein localization. / Zygote 2006, 14:317鈥?28. CrossRef 45. LaVoie HA: The role of GATA in mammalian reproduction. / Exp Biol Med (Maywood) 2003, 228:1282鈥?290. 46. Visser JA, de Jong FH, Laven JS, Themmen AP: Anti-Mullerian hormone: a new marker for ovarian function. / Reproduction 2006, 131:1鈥?. CrossRef 47. Ballow DJ, Xin Y, Choi Y, Pangas SA, Rajkovic A: Sohlh2 is a germ cell-specific bHLH transcription factor. / Gene Expr Patterns 2006, 6:1014鈥?018. modgep.2006.04.007">CrossRef 48. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, Matzuk MM, Rajkovic A: Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. / Proc Natl Acad Sci USA 2006, 103:8090鈥?095. CrossRef 49. Choi Y, Yuan D, Rajkovic A: Germ cell-specific transcriptional regulator sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. / Biol Reprod 2008, 79:1176鈥?182. biolreprod.108.071217">CrossRef 50. Findley SD, Tamanaha M, Clegg NJ, Ruohola-Baker H: Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. / Development 2003, 130:859鈥?71. CrossRef 51. Clegg NJ, Frost DM, Larkin MK, Subrahmanyan L, Bryant Z, Ruohola-Baker H: maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA. / Development 1997, 124:4661鈥?671. 52. Fair T, Carter F, Park S, Evans AC, Lonergan P: Global gene expression analysis during bovine oocyte in vitro maturation. / Theriogenology 2007,68(Suppl 1):S91鈥?7. CrossRef 53. Dade S, Callebaut I, Mermillod P, Monget P: Identification of a new expanding family of genes characterized by atypical LRR domains. Localization of a cluster preferentially expressed in oocyte. / FEBS Lett 2003, 555:533鈥?38. CrossRef 54. Bonnet A, Dalbies-Tran R, Sirard MA: Opportunities and challenges in applying genomics to the study of oogenesis and folliculogenesis in farm animals. / Reproduction 2008, 135:119鈥?28. CrossRef 55. Da Silva-Buttkus P, Jayasooriya GS, Mora JM, Mobberley M, Ryder TA, Baithun M, Stark J, Franks S, Hardy K: Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. / J Cell Sci 2008, 121:3890鈥?900. CrossRef 56. Nilsson EE, Savenkova MI, Schindler R, Zhang B, Schadt EE, Skinner MK: Gene bionetwork analysis of ovarian primordial follicle development. / PLoS One 2010, 5:e11637. CrossRef 57. Liu YX: Interaction and signal transduction between oocyte and samatic cells in the ovary. / Front Biosci 2007, 12:2782鈥?796. 58. Gilchrist RB, Ritter LJ, Armstrong DT: Oocyte-somatic cell interactions during follicle development in mammals. / Anim Reprod Sci 2004, (82鈥?3):431鈥?46. 59. Martoriati A, Gerard N: Interleukin-1 (IL-1) system gene expression in granulosa cells: kinetics during terminal preovulatory follicle maturation in the mare. / Reprod Biol Endocrinol 2003, 1:42. CrossRef 60. Gerard N, Caillaud M, Martoriati A, Goudet G, Lalmanach AC: The interleukin-1 system and female reproduction. / J Endocrinol 2004, 180:203鈥?12. CrossRef 61. Kezele PR, Ague JM, Nilsson E, Skinner MK: Alterations in the ovarian transcriptome during primordial follicle assembly and development. / Biol Reprod 2005, 72:241鈥?55. biolreprod.104.032060">CrossRef 62. Thorrez L, Van Deun K, Tranchevent LC, Van Lommel L, Engelen K, Marchal K, Moreau Y, Van Mechelen I, Schuit F: Using ribosomal protein genes as reference: a tale of caution. / PLoS One 2008, 3:e1854. CrossRef 63. Ge X, Yamamoto S, Tsutsumi S, Midorikawa Y, Ihara S, Wang SM, Aburatani H: Interpreting expression profiles of cancers by genome-wide survey of breadth of expression in normal tissues. / Genomics 2005, 86:127鈥?41. CrossRef 64. Blander G, Guarente L: The Sir2 family of protein deacetylases. / Annu Rev Biochem 2004, 73:417鈥?35. biochem.73.011303.073651">CrossRef 65. Ford E, Voit R, Liszt G, Magin C, Grummt I, Guarente L: Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. / Genes Dev 2006, 20:1075鈥?080. CrossRef 66. Tian Q, Kopf GS, Brown RS, Tseng H: Function of basonuclin in increasing transcription of the ribosomal RNA genes during mouse oogenesis. / Development 2001, 128:407鈥?16. 67. Welt C, Sidis Y, Keutmann H, Schneyer A: Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. / Exp Biol Med (Maywood) 2002, 227:724鈥?52. 68. Li Q, Rajanahally S, Edson MA, Matzuk MM: Stable expression and characterization of N-terminal tagged recombinant human bone morphogenetic protein 15. / Mol Hum Reprod 2009, 15:779鈥?88. molehr/gap062">CrossRef 69. Otsuka F, Moore RK, Iemura S, Ueno N, Shimasaki S: Follistatin inhibits the function of the oocyte-derived factor BMP-15. / Biochem Biophys Res Commun 2001, 289:961鈥?66. bbrc.2001.6103">CrossRef 70. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T: The RIN: an RNA integrity number for assigning integrity values to RNA measurements. / BMC Mol Biol 2006, 7:3. CrossRef 71. Joyce IM, Clark AT, Pendola FL, Eppig JJ: Comparison of recombinant growth differentiation factor-9 and oocyte regulation of KIT ligand messenger ribonucleic acid expression in mouse ovarian follicles. / Biol Reprod 2000, 63:1669鈥?675. biolreprod63.6.1669">CrossRef 72. Shou J, Qian HR, Lin X, Stewart T, Onyia JE, Gelbert LM: Optimization and validation of small quantity RNA profiling for identifying TNF responses in cultured human vascular endothelial cells. / J Pharmacol Toxicol Methods 2006, 53:152鈥?59. CrossRef 73. Muller C, Denis M, Gentzbittel L, Faraut T: The Iccare web server: an attempt to merge sequence and mapping information for plant and animal species. / Nucleic Acids Res 2004, 32:W429鈥?34. CrossRef 74. Bonnet A, Le Cao KA, Sancristobal M, Benne F, Robert-Granie C, Law-So G, Fabre S, Besse P, De Billy E, Quesnel H, / et al.: In vivo gene expression in granulosa cells during pig terminal follicular development. / Reproduction 2008, 136:211鈥?24. CrossRef 75. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. / Nucleic Acids Res 2001, 29:e45. CrossRef 76. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. / Genome Biol 2002, 3:RESEARCH0034. b-2002-3-7-research0034">CrossRef
作者单位：Agnes Bonnet (1) Claudia Bevilacqua (2) Francis Benne (1) Loys Bodin (3) Corinne Cotinot (4) Laurence Liaubet (1) Magali Sancristobal (1) Julien Sarry (1) Elena Terenina (1) Patrice Martin (2) Gwenola Tosser-Klopp (1) Beatrice Mandon-Pepin (4) 1. INRA, UMR444 G茅n茅tique Cellulaire, Auzeville, BP52627, F-31326, Castanet-Tolosan, France 2. INRA, UMR1313 G茅n茅tique Animale et Biologie Int茅grative, Plateforme de Microg茅nomique expressionnelle ICE, F-78350, Jouy-en-Josas, France 3. INRA, UR631 Station d鈥橝m茅lioration G茅n茅tique des Animaux, BP52627, F-31326, Castanet-Tolosan, France 4. INRA, UMR1198 Biologie du D茅veloppement et de la Reproduction, F-78350, Jouy-en-Josas, France

文摘

Background Successful achievement of early folliculogenesis is crucial for female reproductive function. The process is finely regulated by cell-cell interactions and by the coordinated expression of genes in both the oocyte and in granulosa cells. Despite many studies, little is known about the cell-specific gene expression driving early folliculogenesis. The very small size of these follicles and the mixture of types of follicles within the developing ovary make the experimental study of isolated follicular components very difficult. The recently developed laser capture microdissection (LCM) technique coupled with microarray experiments is a promising way to address the molecular profile of pure cell populations. However, one main challenge was to preserve the RNA quality during the isolation of single cells or groups of cells and also to obtain sufficient amounts of RNA. Using a new LCM method, we describe here the separate expression profiles of oocytes and follicular cells during the first stages of sheep folliculogenesis. Results We developed a new tissue fixation protocol ensuring efficient single cell capture and RNA integrity during the microdissection procedure. Enrichment in specific cell types was controlled by qRT-PCR analysis of known genes: six oocyte-specific genes (SOHLH2, MAEL, MATER, VASA, GDF9, BMP15) and three granulosa cell-specific genes (KL, GATA4, AMH). A global gene expression profile for each follicular compartment during early developmental stages was identified here for the first time, using a bovine Affymetrix chip. Most notably, the granulosa cell dataset is unique to date. The comparison of oocyte vs. follicular cell transcriptomes revealed 1050 transcripts specific to the granulosa cell and 759 specific to the oocyte. Functional analyses allowed the characterization of the three main cellular events involved in early folliculogenesis and confirmed the relevance and potential of LCM-derived RNA. Conclusions The ovary is a complex mixture of different cell types. Distinct cell populations need therefore to be analyzed for a better understanding of their potential interactions. LCM and microarray analysis allowed us to identify novel gene expression patterns in follicular cells at different stages and in oocyte populations.

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