Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0038
Animal Reproduction (AR)
Conference Paper

Applications of large-scale molecular profiling techniques to the study of the corpus luteum

Joy L. Pate, Camilla K. Hughes

Downloads: 3
Views: 1321

Abstract

The corpus luteum (CL) is vital for the establishment and maintenance of pregnancy. Throughout the history of luteal biology, cutting-edge technologies have been used to develop a thorough understanding of the functions of specific luteal cell types, the signaling pathways that result in luteal cell stimulation or demise, and the molecules that regulate specific functions of luteal cells. The advent of large-scale profiling technologies such as transcriptomics, proteomics, and metabolomics, has brought with it an interest in discovering novel regulatory molecules that may provide targets for manipulation of luteal function or lifespan. Although the work to date is limited, transcriptomics have been effectively used to provide a global picture of changes in mRNA that relate to luteal development, steroidogenesis, luteolysis or luteal rescue. Some studies have been reported that profile microRNA (miRNA) and proteins, and although not yet published, metabolomics analyses of the CL have been undertaken. Thus far, these profiling studies seem to largely confirm earlier findings using targeted approaches, although previously unstudied molecules have also come to light as important luteal regulators. These molecules can then be studied using traditional mechanistic techniques. Use of profiling technologies has presented physiologists with unique challenges associated with analyses of big data sets. An appropriate technique for balancing the risks associated with type I (false discoveries) and type II (overlooking a real change) statistical error has not yet been developed and many big data studies may have potentially important differences that are overlooked. Also, it is imperative that attempts be made to integrate information from the various -omics studies before drawing conclusions based on expression of only one class of molecule, to better reflect the interdependency of molecular networks in cells. Currently, few analysis programs exist for such integrations. Despite challenges associated with these techniques, they have already provided new information about the biology of the CL, notably allowing identification of a key regulator of acquisition of luteolytic capacity and providing a big-picture view of the subtle changes that occur in the CL during early pregnancy. As these technologies become more accurate and less expensive, and as analysis becomes more user-friendly, their use will become much more widespread and many new discoveries will be made. This review will focus only on relevant studies in which these technologies were used to study the CL of ruminants.

Keywords

bovine, corpus luteum, molecular profiling.

References

Alila HW, Hansel W. 1984. Origin of different cell types in the bovine corpus luteum as characterized by specific monoclonal antibodies. Biol Reprod, 31:1015-1025.

Arianmanesh M, McIntosh RH, Lea RG, Fowler PA, Al-Gubory KH. 2011. Ovine corpus luteum proteins, with functions including oxidative stress and lipid metabolism, show complex alterations during implantation. J Endocrinol, 210:47-58.

Atli MO, Bender RW, Mehta V, Bastos MR, Luo W, Vezina CM, Wiltbank MC. 2012. Patterns of gene expression in the bovine corpus luteum following repeated intrauterine infusions of low doses of prostaglandin F2alpha. Biol Reprod, 86:130. doi: 10.1095/biolreprod.111.094870.

Baddela VS, Onteru SK, Singh D. 2017. A syntenic locus on buffalo chromosome 20: novel genomic hotspot for miRNAs involved in follicular-luteal transition. Funct Integr Genomics, 17:321-334.

Baddela VS, Koczan D, ViergutzT, Vernunft A, Vanselow J. 2018. Global gene expression analysis indicates that small luteal cells are involved in extracellular matrix modulation and immune cell recruitment in the bovine corpus luteum. Mol Cell Endocrinol. doi: 10.1016/j.mce.2018.03.011.

Benjamini Y, Hochberg Y. 1995. Controling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc, 57:289-300.

Bowdridge EC, Goravanahally MP, Inskeep EK, Flores JA. 2015. Activation of adenosine monophosphate-activated protein kinase is an additional mechanism that participates in mediating inhibitory actions of prostaglandin F2alpha in mature, but not developing, bovine corpora lutea. Biol Reprod, 93:7. doi: 10.1095/biolreprod.115.129411.

Catalanotto C, Cogoni C, Zardo G. 2016. MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci, 17(10): pii: E1712. doi: 10.3390/ijms17101712.

Christenson LK. 2010. MicroRNA control of ovarian function. Anim Reprod, 7:129-133.

Chung HJ, Kim KW, Han DW, Lee HC, Yang BC, Chung HK, Shim MR, Choi MS, Jo EB, Jo YM, Oh MY, Jo SJ, Hong SK, Park JK, Chang WK. 2012. Protein profile in corpus luteum during pregnancy in Korean native cows. Asian-Aust J Anim Sci, 25:1540-1545.

Farberov S, Meidan R. 2017. Fibroblast growth factor-2 and transforming growth factor-beta1 oppositely regulate miR-221 that targets thrombospondin-1 in bovine luteal endothelial cells. Biol Reprod, 98:366-375.

Fatima LA, Baruselli PS, Gimenes LU, Binelli M, Renno FP, Murphy BD, Papa PC. 2012. Global gene expression in the bovine corpus luteum is altered after stimulatory and superovulatory treatments. Reprod Fertil Dev, 25:998-1011.

Frobenius W. Ludwig Fraenkel: Spiritus rector of the early progesterone research. Eur J Obstet Gynecol Reprod Biol, 83:115-119.

Gecaj RM, Schanzenbach CI, Kirchner B, Pfaffl MW, Riedmaier I, Tweedie-Cullen RY, Berisha B. 2017. The dynamics of microRNA tramscriptome in bovine corpus luteum during its formation, functoin, and regression. Front Genet, 8:213. doi: 10.3389/fgene.2017.00213.

Goravanahally MP, Salem M, Yao J, Inskeep EK, Flores JA. 2009. Differential gene expression in the bovine corpus luteum during transition from early phase to midphase and its potential role in acquisition of luteolytic sensitivity to prostaglandin F2 alpha. Biol Reprod, 80:980-988.

He L, Hannon GJ. 2004. MicroRNAs: Small RNAs with a big role in gene regulation. Nature Rev Genetics, 5:522-531.

Hossain MM, Ghanem N, Hoelker M, Rings F, Phatsara C, tholen E, Schelander K, Tesfaye D. 2009. Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics, 10:443. doi:10.1186/1471-2164-10-443.

Hossain MM, Sohel MM, Schellander K, Tesfaye D. 2012. Characterization and importance of microRNAs in mammalian gonadal functions. Cell Tissue Res, 349:679-690.

Jocelyn HD, Setchell BP. 1972. Regnier deGraaf on the human reproductive organs: an annotated translation of tractatus de virirum organis generationi inservientibus (1668) and de mulierum organis generationi servientibus tractatus novus (1672). J Reprod Fertil Suppl, 17:1-222.

Kfir S, Basavaraja R, Wigoda N, Ben-Dor S, Orr I, Meidan R. 2018. Genomic profiling of bovine corpus luteum maturation. PLoS One, 13(3):e0194456. doi: 10.1371/journal.pone.0194456.

Li Y, Fang Y, Liu Y, Yang X. 2015. MicroRNAs in ovarian function and disorders. J Ovarian Res, 8:51-58.

Ma T, Jiang H, Gao Y, Zhao Y, Dai L, Xiong Q, Xu Y, Zhao Z, Zhang J. 2011. Microarray analysis of differentially expressed microRNAs in nonregressed and regressed bovine corpus luteum tissue; microRNA-378 may suppress luteal cell apoptosis by targeting the interferon gamma receptor 1 gene. J Appl Genet, 52:481-486

Maalouf SW, Liu W-S, Albert I, Pate, JL. 2014. Regulating life or death: potential role of microRNA in rescue of the corpus luteum. Mol Cell Endocrinol, 398:78-88.

Maalouf SW, Liu WS, Pate JL. 2016a. MicroRNA in ovarian function. Cell Tissue Res, 363:7-18.

Maalouf SW, Smith CL, Pate JL. 2016b. Changes in microRNA expression during maturation of the bovine corpus luteum: regulation of luteal cell proliferation and function by microRNA-34a. Biol Reprod, 94:71. doi: 10.1095/biolreprod.115.135053.

McBride D, Carré W, Sontakke SD, Hogg CO, Law A, Donadeu FX, Clinton M. 2012. Reproduction, 144:221-233

McGinnis LK, Luense LJ, Christenson LK. 2015. MicroRNA in ovarian biology and disease. Cold Spring Harb Perspect Med, 5(9):a022962. doi: 10.1101/cshperspect.a022962.

Miyamoto A, Shirasuna K, Shimizu T, Matsui M. 

2013. Impact of angiogenic and innate immune systems on the corpus luteum function during its formation and maintenance in ruminants. Reprod Biol, 13:272-278.

Mohammed BT, Sontakke SD, Ioannidis J, Duncan WC, Donadeu FX. 2017. The adequate corpus luteum: miR-96 promotes luteal cell survival and progesterone production. J Clin Endocrimol Metab, 102:2188-2198.

Mondal M, Schilling B, Folger J, Steibel JP, Buchnick H, Zalman Y, Ireland JJ, Meidan R, Smith GW. 2011. Deciphering the luteal transcriptome: potential mechanisms mediating stage-specific luteolytic response of the corpus luteum to prostaglandin F2α. Physiol Genomics, 43:447-456.

Moore SG, Pryce JE, Hayes BJ, Chamberlain AJ, Kemper KE, Berry DP, McCabe M, Cormican P, Lonergan P, Fair T, Butler ST. 2016. Differentially expressed genes in endometrium and corpus luteum of holstein cows selected for high and low fertility are enriched for sequence variants associated with fertility. Biol Reprod, 94:19. doi: 10.1095/biolreprod.115.132951.

Mudge JF, Martyniuk CJ, and Houlahan JE. 2017. Optimal alpha reduces error rates in gene expression studies: a meta-analysis approach. BMC Bioinformatics, 18:312. doi: 10.1186/s12859-017-1728-3.

Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW. 2000. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev, 80:1-29. doi: 10.1152/physrev.2000.80.1.1

Ochoa JC, Peñagaricanoc F, Baez GM, Melo LF, Motta JC, Guerra AG, Meidan R, Ferreira JCP, Sartori R, Wiltbank MC. 2018. Mechanisms for rescue of CL during pregnancy: gene expression in bovine CL following intrauterine pulses of prostaglandins E1 and F2α. Biol Reprod. doi: 10.1093/biolre/iox183.

Pate JL, Johnson-Larson CJ, Ottobre JS. 2012. Life or death decisions in the corpus luteum. Reprod Domest Anim, 47(suppl. 4):297-303.

Romereim SM, Summer AF, Pohlmeier WE, Zhang P, Hou X, Talbott HA, Cushman RA, Wood JR, Davis JS, Cupp AS. 2017. Gene expression profiling of bovine ovarian follicular and luteal cells provides insight into cellular identities and functions. Mol Cell Endocrinol, 439:379-394.

Romero JJ, Antoniazzi AQ, Smirnova NP, Webb BT, Yu F, Davis JS, Hansen TR. 2013. Pregnancy-associated genes contribute to antiluteolytic mechanisms in ovine corpus luteum. Physiol Genomics, 45:1095-1108.

Sakumoto R, Hayashi K-G, Hosoe M, Iga, K, Kizaki K, Okuda K. 2015. Gene expression profiles in the bovine corpus luteum (CL) during the estrous cycle and pregnancy: Possible roles of chemokines in regulating CL function during pregnancy. J Reprod Dev, 61:42-48.

Shah KB, Tripathy S, Suganthi H, Rudraiah M. 2014. Profiling of luteal transcriptome during prostaglandin F2-alpha treatment in buffalo cows: analysis of signaling pathways associated with luteolysis. PLOS One, 9(8):e104127. doi:10.1371/journal.pone.0104127.

Simmer HH. 1971. The first experiments to demonstrate an endocrine function of the corpus luteum on the occasion of the 100 th birthday of Ludwig Fraenkel (1870-1951). Sudhoffs Arch, 55:392-417.

Smith GW, Meidan R. 2014. Ever-changing cell interactions during the lifespan of the corpus luteum: relevance to luteal regression. Reprod Biol, 14:75-82.

Talbott H, Hou X, Qiu F, Zhang P, Guda C, Yu F, Cushman RA, Wood JR, Wang C, Cupp AS, Davis JS. 2017. Early transcriptome responses of the bovine midcycle corpus luteum to prostaglandin F2α includes cytokine signaling. Mol Cell Endocrinol, 452:93-109.

Tesfaye D, Gebremedhn S, Salilew-Wondim D, Hailay T, Hoelker M, Grosse-Brinkhaus C, Schellander K. 2018. MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development. Reproduction, 155:R121-R135. Treiber T, Treiber N, Meister G. 2012. Regulation of microRNA biogenesis and function. Thromb Haemost, 107:605-610.

Tsai S-J, Wiltbank MC. 1998. Prostaglandin F2α regulates distinct physiological changes in early and midcycle bovine corpora lutea. Biol Reprod, 58:346-352.

Villa-Godoy A, Ireland JJ, Wortman JA, Ames NK, Highes TL, Fogwell RL. 1985. Effect of ovarian follicles on luteal regression in heifers. J Anim Sci, 60:519-527.

Vlachos IS, Zagganas K, Paraskevopoulou MD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T, Hatzigeorgiou AG. 2015. DIANA-miRPath v3. 0: deciphering microRNA function with experimental support. Nucleic Acids Res, 43:460-466.

Wiltbank JN, Ingalls JE, Rowden WW. 1961. Effects of various forms and levels of estrogens alone or in combination with gonadotropins on the estrous cycle of beef heifers. J Anim Sci, 20:341-346.

Wiltbank MC, Salih SM, Atli MO, Luo W, Bormann CL, Ottobre JS, Vezina CM, Mehta V, Diaz FJ, Tsai SJ, Sartori R. 2012. Comparison of endocrine and cellular mechanisms regulating the corpus luteum of primates and ruminants. Anim Reprod, 9:242-259.

Xia J, Wishart DS. 2016. Using metaboanalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinformatics, 55:14.10.1-14.10.91.

Zalman Y, Klipper E, Farberov S, Mondal M, Wee G, Folger JK, Smith GW, Meidan R. 2012. Regulation of angiogenesis-related prostaglandin F2alpha-induced genes in the bovine corpus luteum. Biol Reprod, 86:92. doi: 10.1095/biolreprod. 111.095067.

5b8e9d2f0e88251f4add6775 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections