Skip to main content
SpringerLink
Log in

Differential Expression of RNAseq Imprinted Genes from Bovine Females Before and After Puberty

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

The productivity of beef cows depends on early reproduction traits such as puberty and has an economic impact on the efficiency of production system. Imprinted genes modulate many important endocrine processes such as growth, the onset of puberty and maternal reproductive and behavior. The role of imprinted genes in puberty is a challenging subject since they show the reciprocal role of maternal and paternal genomes in progeny. Although, there are evidences of the involvement of imprint genes in puberty in human, the role of this type of genes in the onset of puberty in cattle has not been studied yet. Here we examined the expression of 27 imprinted genes in pre and post puberty in a bovine model to find differentially expressed imprinted genes in maternal-paternal purebreds and reciprocal crosses across eight tissues and discussed the task of these genes in this crucial process of development and in onset of puberty. DLK1 and MKRN3 that previously described as cause of the central precocious puberty (CPP) in human were differentially expressed in this study. Functional annotation analysis of differentially imprinted genes in different tissues showed significant biological processes of cellular response to growth factor stimulus, response to growth factor, response to parathyroid hormone, developmental growth and the importance of alternative splicing. The results of this study have implications in understanding the role of imprinted genes in the onset of puberty in cattle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abreu AP, Kaiser UB (2016) Pubertal development and regulation. Lancet Diabetes Endocrinol 4(3):254–264

    PubMed  PubMed Central  Google Scholar 

  • Abreu AP, Dauber A, Macedo DB, Noel SD, Brito VN, Gill JC, Cukier P, Thompson IR, Navarro VM, Gagliardi PC (2013) Central precocious puberty caused by mutations in the imprinted gene MKRN3. N Engl J Med 368:2467–2475

    CAS  PubMed  Google Scholar 

  • Afgan E, Baker D, Batut B, Van Den Beek M, Bouvier D, Čech M, Chilton J, Clements D, Coraor N, Grüning BA (2018) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46:W537–W544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baralle FE, Giudice J (2017) Alternative splicing as a regulator of development and tissue identity. Nat Rev Mol Cell Biol 18(7):437–451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brionne A, Juanchich A, Hennequet-Antier C (2019) ViSEAGO: a bioconductor package for clustering biological functions using gene ontology and semantic similarity. BioData Min 12(1):1–13

    CAS  Google Scholar 

  • Cánovas A, Reverter A, DeAtley KL, Ashley RL, Colgrave ML, Fortes MR, Islas-Trejo A, Lehnert S, Porto-Neto L, Rincón G, Silver GA, Thomas MG (2014) Multi-tissue omics analyses reveal molecular regulatory networks for puberty in composite beef cattle. PLoS ONE 9(7):e102551

    PubMed  PubMed Central  Google Scholar 

  • Cao G, Liu Q, Chu M, Di R, Fang L, Feng T, Li N (2013) Analysis on cDNA sequence, alternative splicing and polymorphisms associated with timing of puberty of Lin28B gene in goats. Mol Biol Rep 40:4675–4683

    CAS  PubMed  Google Scholar 

  • Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A (2003) Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc Natl Acad Sci 100:8292–8297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Hagen DE, Wang J, Elsik CG, Ji T, Siqueira LG, Hansen PJ, Rivera RM (2016) Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing. Epigenetics 11:501–516

    PubMed  PubMed Central  Google Scholar 

  • Curley J, Pinnock S, Dickson S, Thresher R, Miyoshi N, Surani M, Keverne E (2005) Increased body fat in mice with a targeted mutation of the paternally expressed imprinted gene Peg3. FASEB J 19:1302–1304

    CAS  PubMed  Google Scholar 

  • Dauber A, Cunha-Silva M, Macedo DB, Brito VN, Abreu AP, Roberts SA, Montenegro LR, Andrew M, Kirby A, Weirauch MT (2017) Paternally inherited DLK1 deletion associated with familial central precocious puberty. J Clin Endocrinol Metab 102:1557–1567

    PubMed  PubMed Central  Google Scholar 

  • DeChiara TM, Robertson EJ, Efstratiadis A (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–859

    CAS  PubMed  Google Scholar 

  • Erdmann VA, Szymanski M, Hochberg A, Groot ND, Barciszewski J (2000) Non-coding, mRNA-like RNAs database Y2K. Nucleic Acids Res 28(1):197–200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grandone A, Capristo C, Cirillo G, Sasso M, Umano GR, Mariani M, Del Giudice EM, Perrone L (2017) Molecular screening of MKRN3, DLK1, and KCNK9 genes in girls with idiopathic central precocious puberty. Horm Res Paediatr 88:194–200

    CAS  PubMed  Google Scholar 

  • Howard SR (2019) The genetic basis of delayed puberty. Front Endocrinol 10:423

    Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57

    CAS  PubMed  Google Scholar 

  • Ioannides Y, Lokulo-Sodipe K, Mackay DJ, Davies JH, Temple IK (2014) Temple syndrome: improving the recognition of an underdiagnosed chromosome 14 imprinting disorder: an analysis of 51 published cases. J Med Genet 51:495–501

    CAS  PubMed  Google Scholar 

  • Isles AR, Davies W, Wilkinson LS (2006) Genomic imprinting and the social brain. Phil Trans R Soc B 361:2229–2237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kagami M, O’Sullivan MJ, Green AJ, Watabe Y, Arisaka O, Masawa N, Matsuoka K, Fukami M, Matsubara K, Kato F, Ferguson-Smith AC, Ogata T (2010) The IG-DMR and the MEG3-DMR at human chromosome 14q32 2: hierarchical interaction and distinct functional properties as imprinting control centers. PLoS Genet 6(6):e1000992

    PubMed  PubMed Central  Google Scholar 

  • Karami K, Zerehdaran S, Javadmanesh A, Shariati MM (2019a) Assessment of maternal and parent of origin effects in genetic variation of economic traits in Iranian native fowl. Br Poult Sci 60:486–492

    CAS  PubMed  Google Scholar 

  • Karami K, Zerehdaran S, Javadmanesh A, Shariati MM, Fallahi H (2019b) Characterization of bovine (Bos taurus) imprinted genes from genomic to amino acid attributes by data mining approaches. PLoS ONE 14:e0217813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelberman D, Rizzoti K, Lovell-Badge R, Robinson IC, Dattani MT (2009) Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 30(7):790–829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kenny DA, Heslin J, Byrne CJ (2018) Early onset of puberty in cattle: implications for gamete quality and embryo survival. Reprod Fertil Dev 30(1):101–117

    CAS  Google Scholar 

  • Kotler J, Haig D (2018) The tempo of human childhood: a maternal foot on the accelerator, a paternal foot on the brake. Evol Anthropol 27:80–91

    PubMed  PubMed Central  Google Scholar 

  • Lee Y, Rio DC (2015) Mechanisms and regulation of alternative pre-mRNA splicing. Annu Rev Biochem 84:291–323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li L-L, Keverne E, Aparicio S, Ishino F, Barton S, Surani M (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284:330–334

    CAS  PubMed  Google Scholar 

  • Li J, Shen H, Xie H, Ying Y, Jin K, Yan H, Wang S, Xu M, Wang X, Xu X, Xie L (2019) Dysregulation of ncRNAs located at the DLK1 DiO3 imprinted domain: involvement in urological cancers. Cancer Manag Res 11:777

    CAS  PubMed  PubMed Central  Google Scholar 

  • Macedo DB, Brito VN, Latronico AC (2014) New causes of central precocious puberty: the role of genetic factors. Neuroendocrinology 100:1–8

    CAS  Google Scholar 

  • Magee DA, Berry DP, Berkowicz EW, Sikora KM, Howard DJ, Mullen MP, Evans RD, Spillane C, MacHugh DE (2011) Single nucleotide polymorphisms within the bovine DLK1-DIO3 imprinted domain are associated with economically important production traits in cattle. J Hered 102(1):94–101

    CAS  PubMed  Google Scholar 

  • Masoudzadeh S, Mohammadabadi M, Khezri A, Kochuk-Yashchenko O, Kucher D, Babenko O, Bushtruk M, Tkachenko S, Stavetska R, Klopenko N (2020) Dlk1 gene expression in different tissues of lamb. Iran J Appl Anim Sci 10(4):669–677

    CAS  Google Scholar 

  • McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183

    CAS  PubMed  Google Scholar 

  • Mechaly AS, Viñas J, Piferrer F (2009) Identification of two isoforms of the Kisspeptin-1 receptor (kiss1r) generated by alternative splicing in a modern teleost, the Senegalese sole (Solea senegalensis). Biol Reprod 80:60–69

    CAS  PubMed  Google Scholar 

  • Naulé L, Maione L, Kaiser UB (2021) Puberty, a sensitive window of hypothalamic development and plasticity. Endocrinology 162(1):bqaa209

    PubMed  Google Scholar 

  • Ojeda SR, Hill J, Hill DF, Costa ME, Tapia V, Cornea A, Ma YJ (1999) The Oct-2 POU domain gene in the neuroendocrine brain: a transcriptional regulator of mammalian puberty. Endocrinology 140:3774–3789

    CAS  PubMed  Google Scholar 

  • Palmert MR, Boepple PA (2001) Variation in the timing of puberty: clinical spectrum and genetic investigation. J Clin Endocrinol Metab 86(6):2364–2368

    CAS  PubMed  Google Scholar 

  • Pan X, Li Q, Chen D, Gong W, Li N, Jiang Y, Zhang H, Chen Y, Yuan X (2021) Alternative splicing dynamics of the hypothalamus–pituitary–ovary axis during pubertal transition in gilts. Front Genet. https://doi.org/10.3389/fgene.2021.592669

    Article  PubMed  PubMed Central  Google Scholar 

  • Park C-H, Uh K-J, Mulligan BP, Jeung E-B, Hyun S-H, Shin T, Ka H, Lee C-K (2011) Analysis of imprinted gene expression in normal fertilized and uniparental preimplantation porcine embryos. PLoS ONE 6:e22216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira GR, Barcellos JOJ, Sessim AG, Tarouco JU, Feijó FD, Braccini J, Prates ÊR, Canozzi MEA (2017) Relationship of post-weaning growth and age at puberty in crossbred beef heifers. Revista Brasileira De Zootecnia 46:413–420

    Google Scholar 

  • Perry JR, Day F, Elks CE, Sulem P, Thompson DJ, Ferreira T, He C, Chasman DI, Esko T, Thorleifsson G (2014) Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche. Nature 514:92–97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peters J (2014) The role of genomic imprinting in biology and disease: an expanding view. Nat Rev Genet 15:517–530

    CAS  PubMed  Google Scholar 

  • Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2:21–32

    CAS  PubMed  Google Scholar 

  • Roberts SA, Kaiser UB (2020) Genetics in endocrinology: Genetic etiologies of central precocious puberty and the role of imprinted genes. Eur J Endocrinol 183:R107–R117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez JM, Keogh K, Kelly AK, Byrne CJ, Lonergan P, Kenny DA (2021) A high plane of nutrition during early life alters the hypothalamic transcriptome of heifer calves. Sci Rep 11:1–13

    Google Scholar 

  • Scagliotti V, Costa Fernandes Esse R, Willis TL, Howard M, Carrus I, Lodge E, Andoniadou CL, Charalambous M (2021) Dynamic expression of imprinted genes in the developing and postnatal pituitary gland. Genes 12:509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spaziani M, Tarantino C, Tahani N, Gianfrilli D, Sbardella E, Lenzi A, Radicioni AF (2021) Hypothalamo-pituitary axis and puberty. Mol Cell Endocrinol 520:111094

    CAS  PubMed  Google Scholar 

  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering CV (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1):D607–D613

    CAS  PubMed  Google Scholar 

  • Tahir MS, Porto-Neto LR, Gondro C, Shittu OB, Wockner K, Tan AW, Smith HR, Gouveia GC, Kour J, Fortes MR (2021) Meta-analysis of heifer traits identified reproductive pathways in bos indicus cattle. Genes 12:768

    CAS  PubMed  PubMed Central  Google Scholar 

  • Terasawa E, Fernandez DL (2001) Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 22:111–151

    CAS  PubMed  Google Scholar 

  • Trivers RL (1974) Parent-offspring conflict. Integr Comp Biol 14:249–264

    Google Scholar 

  • Xiang R, Ghanipoor-Samami M, Johns WH, Eindorf T, Rutley DL, Kruk ZA, Fitzsimmons CJ, Thomsen DA, Roberts CT, Burns BM (2013) Maternal and paternal genomes differentially affect myofibre characteristics and muscle weights of bovine fetuses at midgestation. PLoS ONE 8:e53402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang R, Lee AM, Eindorf T, Javadmanesh A, Ghanipoor-Samami M, Gugger M, Fitzsimmons CJ, Kruk ZA, Pitchford WS, Leviton AJ (2014) Widespread differential maternal and paternal genome effects on fetal bone phenotype at mid-gestation. J Bone Miner Res 29:2392–2404

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Ferdowsi University of Mashhad for providing research facilities to conduct this study.

Funding

This study was funded by Ferdowsi University of Mashhad.

Author information

Authors and Affiliations

  1. Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Keyvan Karami, Saeed Zerehdaran & Ali Javadmanesh

Authors
  1. Keyvan Karami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saeed Zerehdaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ali Javadmanesh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KK: did the analysis and wrote the manuscript. SZ: check the results and wrote the manuscript. AJ: made some comments during analysis and writing the manuscript.

Corresponding authors

Correspondence to Saeed Zerehdaran or Ali Javadmanesh.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 220 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karami, K., Zerehdaran, S. & Javadmanesh, A. Differential Expression of RNAseq Imprinted Genes from Bovine Females Before and After Puberty. Biochem Genet 61, 2633–2649 (2023). https://doi.org/10.1007/s10528-023-10395-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-023-10395-9

Keywords

Search

Navigation