Top

Published in:

Open Access 01-12-2017 | Short Communication

Oleic acid induces down-regulation of the granulosa cell identity marker FOXL2, and up-regulation of the Sertoli cell marker SOX9 in bovine granulosa cells

Authors: Vengala Rao Yenuganti, Jens Vanselow

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

Abstract

During negative energy balance, the concentration of different fatty acids, especially of oleic acid (OA) increases in the follicular fluid of cattle. Previously, we showed that OA induced morphological, physiological and molecular changes in cultured bovine granulosa cells. In our present study we analyzed effects of OA on the expression of markers for granulosa and Sertoli cell identity, FOXL2 and SOX9, respectively, in addition to effects on the FOXL2 regulated genes ESR2, FST, PTGS2 and PPARG. The results showed that OA down-regulated FOXL2, ESR2, FST and PPARG but up-regulated PTGS2 and SOX9. From these data we conclude that OA can compromise granulosa cell functionality and may initiate trans-differentiation processes in bovine granulosa cells. This novel mechanism may be causally involved in postpartum fertility problems of lactating dairy cows.

Beam SW, Butler WR. Effects of energy balance on follicular development and first ovulation in postpartum dairy cows. J Reprod Fertil Suppl. 1999;54:411–24.PubMed

Opsomer G, Grohn YT, Hertl J, Coryn M. Deluyker H, de KA: risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology. 2000;53:841–57.CrossRefPubMed

Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, De KA, Genicot G, Van SA. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction. 2005;130:485–95.CrossRefPubMed

Rukkwamsuk T, Geelen MJ, Kruip TA, Wensing T. Interrelation of fatty acid composition in adipose tissue, serum, and liver of dairy cows during the development of fatty liver postpartum. J Dairy Sci. 2000;83:52–9.CrossRefPubMed

Aardema H, Lolicato F, van de Lest CH, Brouwers JF, Vaandrager AB, van Tol HT, Roelen BA, Vos PL, Helms JB, Gadella BM. Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage. Biol Reprod. 2013;88:164.CrossRefPubMed

Yenuganti VR, Viergutz T, Vanselow J. Oleic acid induces specific alterations in the morphology, gene expression and steroid hormone production of cultured bovine granulosa cells. Gen Comp Endocrinol. 2016;232:134–44.CrossRefPubMed

Sahmi F, Nicola ES, Zamberlam GO, Goncalves PD, Vanselow J, Price CA. Factors regulating the bovine, caprine, rat and human ovarian aromatase promoters in a bovine granulosa cell model. Gen Comp Endocrinol. 2014;200:10–7.CrossRefPubMed

Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, Forabosco A, Pilia G, Schlessinger D. Foxl2 is required for commitment to ovary differentiation. Hum Mol Genet. 2005;14:2053–62.CrossRefPubMed

Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet. 2007;16:2795–804.CrossRefPubMed

10.

Garcia-Ortiz JE, Pelosi E, Omari S, Nedorezov T, Piao Y, Karmazin J, Uda M, Cao A, Cole SW, Forabosco A, et al. Foxl2 functions in sex determination and histogenesis throughout mouse ovary development. BMC Dev Biol. 2009;9:36. doi:10.1186/1471-213X-9-36.:36-39.CrossRefPubMedPubMedCentral

11.

Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier AC, Klugmann C, Klasen C, Holter NI, et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell. 2009;139:1130–42.CrossRefPubMed

12.

Georges A, L'Hote D, Todeschini AL, Auguste A, Legois B, Zider A, Veitia RA. The transcription factor FOXL2 mobilizes estrogen signaling to maintain the identity of ovarian granulosa cells. elife. 2014;3. doi:10.7554/eLife.04207.:10.

13.

Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000;127:4277–91.PubMed

14.

Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci U S A. 1998;95:6965–70.CrossRefPubMedPubMedCentral

15.

Kim SY, Weiss J, Tong M, Laronda MM, Lee EJ, Jameson JL. Foxl2, a forkhead transcription factor, modulates nonclassical activity of the estrogen receptor-alpha. Endocrinology. 2009;150:5085–93.CrossRefPubMedPubMedCentral

16.

Cheng JC, Chang HM, Qiu X, Fang L, Leung PC. FOXL2-induced follistatin attenuates activin A-stimulated cell proliferation in human granulosa cell tumors. Biochem Biophys Res Commun. 2014;443:537–42.CrossRefPubMed

17.

Sirois J. Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology. 1994;135:841–8.CrossRefPubMed

18.

Glister C, Satchell L, Knight PG. Granulosal and thecal expression of bone morphogenetic protein- and activin-binding protein mRNA transcripts during bovine follicle development and factors modulating their expression in vitro. Reproduction. 2011;142:581–91.CrossRefPubMed

19.

Rosenfeld CS, Yuan X, Manikkam M, Calder MD, Garverick HA, Lubahn DB. Cloning, sequencing, and localization of bovine estrogen receptor-beta within the ovarian follicle. Biol Reprod. 1999;60:691–7.CrossRefPubMed

20.

Froment P, Fabre S, Dupont J, Pisselet C, Chesneau D, Staels B, Monget P. Expression and functional role of peroxisome proliferator-activated receptor-gamma in ovarian folliculogenesis in the sheep. Biol Reprod. 2003;69:1665–74.CrossRefPubMed

21.

Zhang H, Li Q, Lin H, Yang Q, Wang H, Zhu C. Role of PPARgamma and its gonadotrophic regulation in rat ovarian granulosa cells in vitro. Neuro Endocrinol Lett. 2007;28:289–94.PubMed

22.

Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R: Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet. 1996;14:62-68.

23.

Jakob S, Lovell-Badge R. Sex determination and the control of Sox9 expression in mammals. FEBS J. 2011;278:1002–9.CrossRefPubMed

24.

Wilhelm D, Palmer S, Koopman P. Sex determination and gonadal development in mammals. Physiol Rev. 2007;87:1–28.CrossRefPubMed

25.

Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development. 1996;122:2813–22.PubMed

26.

Chaboissier MC, Kobayashi A, Vidal VI, Lutzkendorf S, van de Kant HJ, Wegner M, De Rooij DG, Behringer RR, Schedl A. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development. 2004;131:1891–901.CrossRefPubMed

27.

Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C, Scherer G. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod. 2006;74:195–201.CrossRefPubMed

28.

Vidal VP, Chaboissier MC, De Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet. 2001;28:216–7.CrossRefPubMed

29.

Harikae K, Miura K, Shinomura M, Matoba S, Hiramatsu R, Tsunekawa N, Kanai-Azuma M, Kurohmaru M, Morohashi K, Kanai Y. Heterogeneity in sexual bipotentiality and plasticity of granulosa cells in developing mouse ovaries. J Cell Sci. 2013;126:2834–44.CrossRefPubMed

30.

Baufeld A, Vanselow J. Increasing cell plating density mimics an early post-LH stage in cultured bovine granulosa cells. Cell Tissue Res. 2013;354:869–80.CrossRefPubMed

31.

Yenuganti VR, Vanselow J. Cultured bovine granulosa cells rapidly lose important features of their identity and functionality, but partially recover under long term culture conditions. Cell & Tissue Research. 2017.

32.

Baddela VS, Baufeld A, Yenuganti VR, Vanselow J, Singh D. Suitable housekeeping genes for normalization of transcript abundance analysis by real-time RT-PCR in cultured bovine granulosa cells during hypoxia and differential cell plating density. Reprod Biol Endocrinol. 2014;12:118.CrossRefPubMedPubMedCentral

Title: Oleic acid induces down-regulation of the granulosa cell identity marker FOXL2, and up-regulation of the Sertoli cell marker SOX9 in bovine granulosa cells
Authors: Vengala Rao Yenuganti
Jens Vanselow
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/s12958-017-0276-z

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Oleic acid induces down-regulation of the granulosa cell identity marker FOXL2, and up-regulation of the Sertoli cell marker SOX9 in bovine granulosa cells

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2017

Evaluation of three-dimensional SonoAVC ultrasound for antral follicle count in infertile women: its agreement with conventional two-dimensional ultrasound and serum levels of anti-Müllerian hormone

Influence of endometrial thickness on treatment outcomes following in vitro fertilization/intracytoplasmic sperm injection

The regulation of ovary and conceptus on the uterine natural killer cells during early pregnancy

p,p’-DDT induces testicular oxidative stress-induced apoptosis in adult rats

Natriuretic peptides improve the developmental competence of in vitro cultured porcine oocytes

Role of microRNAs in premature ovarian insufficiency