Transcriptome analysis of differentially expressed genes in rabbits’ ovaries by digital gene-expression profiling

  • Tao Huang
  • Ya-dong Wang
  • Ming-ming Xue
  • Xue Feng
  • Cai-Xia Sun
  • An-si Wang
  • Shu-yu Xie
  • Meng Zhang
  • Gui-Rong Sun
  • Ming Li
Research Article
  • 20 Downloads

Abstract

Reproduction is a complex physiological process that is regulated by multiple genes and pathways. Compared with studies of common livestock, fewer studies of genes related to the fertility of rabbits (Oryctolagus cuniculus) have been reported, and the molecular mechanism of their high productivity is still poorly understood. To identify candidate genes associated with development and prolificacy in rabbits, we analyzed gene expression differences among the ovaries of mature Californian rabbit (LC), and mature (HH) and immature Harbin white rabbit (IH) using digital gene expression technology. We detected 885 and 321 genes that were significantly differentially expressed in comparisons between HH/IH and HH/LC, respectively. The functions of the differentially expressed genes (DEGs) were determined by GO classification and KEGG pathway analysis. The results suggest that most of the DEGs between the mature and immature developmental stages were predominantly associated with DNA replication, cell cycle, and progesterone-mediated oocyte maturation, and most were up-regulated in the IH group compared with the HH group. The DEGs involved in disparate fecundities between HH and LC were associated with reproduction, fructose and mannose metabolism, steroid hormone biosynthesis, and pyruvate metabolism. Our results will contribute to a better understanding of changes in the regulatory network in ovary at different developmental stages and in different fertility of rabbit.

Keywords

Rabbit Ovary Gene expression Reproduction 

Notes

Acknowledgements

This work was supported by Modern Agricultural Industry Technology System of Henan Province (2013–14). We thank Margaret Biswas, PhD, from Liwen Bianji, Edanz Group China (http://www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Compliance with ethical standards

Conflict of interest

Tao Huang, Ya-dong Wang, Ming-ming Xue, Xue Feng, Cai-Xia Sun, An-si Wang, Shu-yu Xie, Meng Zhang, Gui-Rong Sun, Ming Li declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human subjects and the study was in full compliance with ethical standards of institutional regulation.

Supplementary material

13258_2018_651_MOESM1_ESM.xls (10 kb)
Supplementary material 1 (XLS 10 KB)
13258_2018_651_MOESM2_ESM.xls (772 kb)
Supplementary material 2 (XLS 772 KB)
13258_2018_651_MOESM3_ESM.xls (502 kb)
Supplementary material 3 (XLS 502 KB)
13258_2018_651_MOESM4_ESM.xls (34 kb)
Supplementary material 4 (XLS 34 KB)
13258_2018_651_MOESM5_ESM.xls (86 kb)
Supplementary material 5 (XLS 85 KB)

References

  1. Aardema H, Vos PL, Lolicato F, Roelen BA, Knijn HM, Vaandrager AB, Helms JB, Gadella BM (2011) Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol Reprod 85:62–69CrossRefPubMedGoogle Scholar
  2. Abdennebi L, Monget P, Pisselet C, Remy JJ, Salesse R, Monniaux D (1999) Comparative expression of luteinizing hormone and follicle-stimulating hormone receptors in ovarian follicles from high and low prolific sheep breeds. Biol Reprod 60:845–854CrossRefPubMedGoogle Scholar
  3. Antonov AV, Dietmann S, Mewes HW (2008) KEGG spider: interpretation of genomics data in the context of the global gene metabolic network. Genome Biol 9:R179CrossRefPubMedPubMedCentralGoogle Scholar
  4. Araújo VR, Lima-verde IB, Báo SN, Campello CC, Silva JRV, et al (2010) Bone morphogenetic protein-6 (BMP-6) induces atresia in goat primordial follicles cultured in vitro. Pesqui Vet Bras 30:770–781CrossRefGoogle Scholar
  5. Bleil JD, Wassarman PM (1980) Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro. Proc Natl Acad Sci USA 77:1029CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brankin V, Quinn RL, Webb R, Hunter MG (2005) BMP-2 and -6 modulate porcine theca cell function alone and co-cultured with granulosa cells. Domest Anim Endocrinol 29:593–604CrossRefPubMedGoogle Scholar
  7. Carneiro M, Rubin CJ, Di Palma F, Albert FW, Alföldi J, Barrio AM, Pielberg G, Rafati N, Sayyab S, Turner-Maier J et al (2014) Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345:1074CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chang YS, Wang SC, Tsao CC, Huang FL (1997) Molecular cloning, structural analysis, and expression of carp ZP3 gene. Mol Reprod 44:295–304CrossRefGoogle Scholar
  9. Chávez B, Ramos L, García-Becerra R, Vilchis F (2015) Hamster SRD5A3 lacks steroid 5α-reductase activity in vitro. Steroids 94:41CrossRefPubMedGoogle Scholar
  10. Christodoulides C, Vidalpuig A (2010) PPARs and adipocyte function. Mol Cell Endocrinol 318:61–68CrossRefPubMedGoogle Scholar
  11. Duckworth JA, Cui X, Scobie S, Arrow J, Cowan PE (2008) Development of a contraceptive vaccine for the marsupial brushtail possum (Trichosurus vulpecula): lack of effects in mice and chickens immunised with an anti-fertility epitope of possum ZP3 protein. CSIRO Wildl Res 35:563–572CrossRefGoogle Scholar
  12. Epifano O, Liang LF, Familari M, Moos MC Jr, Dean J (1995) Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 121:1947–1956PubMedGoogle Scholar
  13. Fournier A, Rychen G, Marchand P, Toussaint H, Le Bizec B, Feidt C (2013) Polychlorinated biphenyl (PCB) decontamination kinetics in lactating goats (Capra hircus) following a contaminated corn silage exposure. J Agric Food Chem 61:7156–7164CrossRefPubMedGoogle Scholar
  14. Fry RC, Clarke IJ, Cummins JT, Bindon BM, Piper LR, Cahill LP (1988) Induction of ovulation in chronically hypophysectomized Booroola ewes. J Reprod Fertil 82:711–715CrossRefPubMedGoogle Scholar
  15. Ganguly A, Meur SK, Ganguly I (2013) Changes in circulatory FSH of Barbari goats following treatment with high molecular weight inhibin isolated from buffalo follicular fluid. Res Vet Sci 95:374–380CrossRefPubMedGoogle Scholar
  16. Garcia A, Masot J, Franco A, Gazquez A, Redondo E (2013) Histomorphometric and immunohistochemical study of the goat abomasum during prenatal development. Histol Histopathol 28:1369–1381PubMedGoogle Scholar
  17. Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM (2004) Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod 70:900–909CrossRefPubMedGoogle Scholar
  18. Hardy CM, ten Have JF, Pekin J, Beaton S, Jackson RJ, Clydesdale G (2003) Contraceptive responses of mice immunized with purified recombinant mouse zona pellucida subunit 3 (mZP3) proteins. Reproduction 126:49–59CrossRefPubMedGoogle Scholar
  19. Honda R, Ohba Y, Nagata A, Okayama H, Yasuda H (1993) Dephosphorylation of human p34cdc2 kinase on both Thr-14 and Tyr-15 by human cdc25B phosphatase. FEBS Lett 318:331–334CrossRefPubMedGoogle Scholar
  20. Huang HL, Lv C, Zhao YC, Li W, Lu GX, Li P, Sha AG, Tian X, Papasian CJ, Deng HW et al (2014) Mutant ZP1 in familial infertility. N Engl J Med 370:1220–1226CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB (2005) Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci 118:5257–5268CrossRefPubMedGoogle Scholar
  22. Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, Okayama H (1994) Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J 13:1549–1556PubMedPubMedCentralGoogle Scholar
  23. Jorritsma R, César ML, Hermans JT, Kruitwagen CL, Vos PL, Kruip TA (2004) Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim Reprod Sci 81:225–235CrossRefPubMedGoogle Scholar
  24. Kanehisa M, Goto S, Kawashima S, Nakaya A (2002) The KEGG databases at GenomeNet. Nucleic Acids Res 30:42–46CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kaul R, Afzalpurkar A, Gupta SK (1997) Expression of bonnet monkey (Macaca radiata) zona pellucida-3 (ZP3) in a prokaryotic system and its immunogenicity. Mol Reprod Dev 47:140–147CrossRefPubMedGoogle Scholar
  26. Kerr PJ, Jackson RJ, Robinson AJ, Swan J, Silvers L, French N, Clarke H, Hall DF, Holland MK (1999) Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biol Reprod 61:606–613CrossRefPubMedGoogle Scholar
  27. Kitchener AL, Kay DJ, Walters B, Menkhorst P, McCartney CA, Buist JA, Mate KE, Rodger JC (2009) The immune response and fertility of koalas (Phascolarctos cinereus) immunised with porcine zonae pellucidae or recombinant brushtail possum ZP3 protein. J Reprod Immunol 82:40–47CrossRefPubMedGoogle Scholar
  28. Krens SF, Spaink HP, Snaar-Jagalska BE (2006) Functions of the MAPK family in vertebrate-development. FEBS Lett 580:4984–4990CrossRefPubMedGoogle Scholar
  29. Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A (2005) Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130:485–495CrossRefPubMedGoogle Scholar
  30. Liu C, Litscher ES, Mortillo S, Sakai Y, Kinloch RA, Stewart CL, Wassarman PM (1996) Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. Proc Natl Acad Sci USA 93:5431–5436CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mazerbourg S, Hsueh AJ (2003) Growth differentiation factor-9 signaling in the ovary. Mol Cell Endocrinol 202:31–36CrossRefPubMedGoogle Scholar
  32. McGrath SA, Esquela AF, Lee SJ (1995) Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 9:131–136PubMedGoogle Scholar
  33. Meng XL, Liu P, Jia FL, Li J, Gao BQ (2015) De novo transcriptome analysis of Portunus trituberculatus ovary and testis by RNA-Seq: identification of genes involved in gonadal development. PLoS ONE 10:e0128659CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mi H, Lazareva-Ulitsky B, Loo R, Kejariwal A, Vandergriff J, Rabkin S, Guo N, Muruganujan A, Doremieux O, Campbell MJ et al (2005) The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res 33:D284-288Google Scholar
  35. Nagata A, Igarashi M, Jinno S, Suto K, Okayama H (1991) An additional homolog of the fission yeast cdc25+ gene occurs in humans and is highly expressed in some cancer cells. New Biol 3:959–968PubMedGoogle Scholar
  36. Peng JY, Xin HY, Han P, Zhao HB, Bai L, An XP, Cao BY (2013) Identification and gene expression analyses of natriuretic peptide system in the ovary of goat (Capra hircus). Gene 524:105–113CrossRefPubMedGoogle Scholar
  37. Persani L, Rossetti R, Pasquale ED, Cacciatore C, Fabre S (2014) The fundamental role of bone morphogenetic protein 15 in ovarian function and its involvement in female fertility disorders. Hum Reprod Update 20:869–883CrossRefPubMedGoogle Scholar
  38. Ranjan R, Singh RK, Yasotha T, Kumar M, Puri G, Kumar K, Singh R, Bhure S, Malakar D, Bhanja SK et al (2013) Effect of actin polymerization inhibitor during oocyte maturation on parthenogenetic embryo development and ploidy in Capra hircus. Biochem Genet 51:944–953CrossRefPubMedGoogle Scholar
  39. Rankin TL, O’Brien M, Lee E, Wigglesworth K, Eppig J, Dean J (2001) Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Development 128:1119–1126PubMedGoogle Scholar
  40. Rannikki AS, Zhang FP, Huhtaniemi IT (1995) Ontogeny of follicle-stimulating hormone receptor gene expression in the rat testis and ovary. Mol Cell Endocrinol 107:199–208CrossRefPubMedGoogle Scholar
  41. Rath A, Choudhury S, Hasegawa A, Koyama K, Gupta SK (2002) Antibodies generated in response to plasmid DNA encoding zona pellucida glycoprotein-B inhibit in vitro human sperm-egg binding. Mol Reprod Dev 62:525–533CrossRefPubMedGoogle Scholar
  42. Santhanam R, Panda AK, Kumar VS, Gupta SK (1998) Dog zona pellucida glycoprotein-3 (ZP3): expression in Escherichia coli and immunological characterization. Protein Expr Purif 12:331–339CrossRefPubMedGoogle Scholar
  43. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C-T method. Nat Protoc 3:1101–1108CrossRefPubMedGoogle Scholar
  44. Sharma RK, Singh R, Bhardwaj JK, Saini S (2013) Topographic and ultrastructural variations in isthmus segment of oviduct during oestrous cycle in Caprines. Scanning 35:344–348CrossRefPubMedGoogle Scholar
  45. Shimasaki S, Moore RK, Otsuka F, Erickson GF (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72–101CrossRefPubMedGoogle Scholar
  46. Souza-Fabjan JMG, Pereira AF, Melo CH, Sanchez DJ, Oba E, Mermillod P, Melo LM, Teixeira DI, Freitas VJ (2013) Assessment of the reproductive parameters, laparoscopic oocyte recovery and the first embryos produced in vitro, from endangered Canindé goats (Capra hircus). Reprod Biol 13:325–332CrossRefPubMedGoogle Scholar
  47. Sun C, Xie S, Tao H, Zhang W, Wang A, Wang D, Li M, Sun G (2017) Molecular characterization and expression of the GDF9, gene in New Zealand white rabbits. J Genet 96:313–318CrossRefPubMedGoogle Scholar
  48. Zhang AL, Zhao G, Wang B, Zhang FC (2004) Expression of Lagurus ZP3 fusion protein in prokaryotic cells and preparation of its antiserum. J Cell Mol Immunol 20:168–170Google Scholar
  49. Zi XD, Mu XK, Wang Y (2013) Variation in sequences and mRNA expression levels of growth hormone (GH), insulin-like growth factor I (IGF-I) and II (IGF-II) genes between prolific Lezhi black goat and non-prolific Tibetan goat (Capra hircus). Gen Comp Endocrinol 187:1–5CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Tao Huang
    • 1
  • Ya-dong Wang
    • 1
  • Ming-ming Xue
    • 1
  • Xue Feng
    • 1
  • Cai-Xia Sun
    • 1
  • An-si Wang
    • 1
  • Shu-yu Xie
    • 1
  • Meng Zhang
    • 1
  • Gui-Rong Sun
    • 1
  • Ming Li
    • 1
  1. 1.College of Animal Science and Veterinary MedicineHenan Agricultural UniversityZhengzhouPeople’s Republic of China

Personalised recommendations