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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Localisation and endocrine control of hyaluronan synthase (HAS) 2, HAS3 and CD44 expression in sheep granulosa cells

R. Chavoshinejad A B , W. F. A. Marei A C , G. M. Hartshorne B and A. A. Fouladi-Nashta A D
+ Author Affiliations
- Author Affiliations

A Reproduction Research Group, Royal Veterinary College, Hawkshead Campus, Hawkshead Lane, Hatfield, AL9 7TA, UK.

B Warwick Medical School, University of Warwick, Coventry, CV2 2DX, UK.

C Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt.

D Corresponding author. Email: afouladi@rvc.ac.uk

Reproduction, Fertility and Development 28(6) 765-775 https://doi.org/10.1071/RD14294
Submitted: 10 August 2014  Accepted: 23 September 2014   Published: 27 November 2014

Abstract

The aim of the present study was to investigate the hormonal regulation of hyaluronan (HA) components in sheep granulosa cells. HA components are present in the reproductive tract and have a range of physical and signalling properties related to reproductive function in several species. First, abattoir-derived ovaries of sheep were used to determine the localisation of HA synthase (HAS) 1–3 and CD44 proteins in antral follicles. Staining for HAS1–3 and CD44 proteins was most intense in the granulosa layer. Accordingly, the expression of HAS2, HAS3 and CD44 mRNA was measured in cultured granulosa cells exposed to 0–50 ng mL–1 of 17β-oestradiol and different combinations of oestradiol, gonadotropins, insulin-like growth factor (IGF)-1 and insulin for 48–96 h (1 ng mL–1 FSH, 10 ng mL–1 insulin, 10 ng mL–1 IGF-1, 40 ng mL–1 E2 and 25 ng mL–1 LH.). mRNA expression was quantified by real-time polymerase chain reaction using a fold induction method. The results revealed that the hormones tested generally stimulated mRNA expression of the genes of interest in cultured granulosa cells. Specifically, oestradiol, when combined with IGF-1, insulin and FSH, stimulated HAS2 mRNA expression. Oestradiol and LH had synergistic effects in increasing HAS3 mRNA expression. In conclusion, we suggest that the hormones studied differentially regulate HAS2, HAS3 and CD44 in ovine granulosa cells in vitro. Further work is needed to address the signalling pathways involved.

Additional keywords: follicle, ovary, ovine.


References

Adamia, S., Maxwell, C. A., and Pilarski, L. M. (2005). Hyaluronan and hyaluronan synthases: potential therapeutic targets in cancer. Curr. Drug Targets Cardiovasc. Haematol. Disord. 5, 3–14.
Hyaluronan and hyaluronan synthases: potential therapeutic targets in cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsFeksL0%3D&md5=1cefbbd778821d8efb4937c9bc90ebe8CAS | 15720220PubMed |

Allegrucci, C., Hunter, M. G., Webb, R., and Luck, M. R. (2003). Interaction of bovine granulosa and theca cells in a novel serum-free co-culture system. Reproduction 126, 527–538.
Interaction of bovine granulosa and theca cells in a novel serum-free co-culture system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Cksrw%3D&md5=ced892764efab1d16f125065fee757d4CAS | 14525535PubMed |

Baerwald, A. R., Adams, G. P., and Pierson, R. A. (2012). Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum. Reprod. Update 18, 73–91.
Ovarian antral folliculogenesis during the human menstrual cycle: a review.Crossref | GoogleScholarGoogle Scholar | 22068695PubMed |

Bernert, B. (2013). Importance of hyaluronan metabolism and signalling in tumour progression. Doctorate thesis, Uppsala University.

Bodevin-Authelet, S., Kusche-Gullberg, M., Pummill, P. E., DeAngelis, P. L., and Lindahl, U. (2005). Biosynthesis of hyaluronan: direction of chain elongation. J. Biol. Chem. 280, 8813–8818.
Biosynthesis of hyaluronan: direction of chain elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVCisLc%3D&md5=62603842e3b670d74d0a317d24440a25CAS | 15623518PubMed |

Camenisch, T. D., Spicer, A. P., Brehm-Gibson, T., Biesterfeldt, J., Augustine, M. L., Calabro, A., Kubalak, S., Klewer, S. E., and McDonald, J. A. (2000). Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J. Clin. Invest. 106, 349–360.
Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFOrtLw%3D&md5=394c71f6dc8d85cd9c9a8ce6639785aaCAS | 10930438PubMed |

Campbell, B. K., Scaramuzzi, R. J., and Webb, R. (1996). Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media. J. Reprod. Fertil. 106, 7–16.
Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVCnsw%3D%3D&md5=9f5beaef671ec6649a2cff78234f338bCAS | 8667349PubMed |

Campbell, B. K., Dobson, H., Baird, D. T., and Scaramuzzi, R. J. (1999). Examination of the relative role of FSH and LH in the mechanism of ovulatory follicle selection in sheep. J. Reprod. Fertil. 117, 355–367.
Examination of the relative role of FSH and LH in the mechanism of ovulatory follicle selection in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvFOqtr4%3D&md5=967faeeeeaa8b053838cabe9181fbd13CAS | 10690204PubMed |

Deroo, B. J., Rodriguez, K. F., Couse, J. F., Hamilton, K. J., Collins, J. B., Grissom, S. F., and Korach, K. S. (2009). Estrogen receptor β is required for optimal cAMP production in mouse granulosa cells. Mol. Endocrinol. 23, 955–965.
Estrogen receptor β is required for optimal cAMP production in mouse granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlGjuro%3D&md5=552f81ad36f999f1104d27619482749eCAS | 19324971PubMed |

El Maradny, E., Kanayama, N., Kobayashi, H., Hossain, B., Khatun, S., Liping, S., Kobayashi, T., and Terao, T. (1997). The role of hyaluronic acid as a mediator and regulator of cervical ripening. Hum. Reprod. 12, 1080–1088.
The role of hyaluronic acid as a mediator and regulator of cervical ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktlyltbo%3D&md5=8978c46fe62b5d5401a9fb7e75366434CAS | 9194670PubMed |

Erickson, M., and Stern, R. (2012). Chain gangs: new aspects of hyaluronan metabolism. Biochem. Res. Int. 2012, Article ID 893947.
Chain gangs: new aspects of hyaluronan metabolism.Crossref | GoogleScholarGoogle Scholar |

Fortune, J. E., Rivera, G. M., and Yang, M. Y. (2004). Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. Anim. Reprod. Sci. 82–83, 109–126.
Follicular development: the role of the follicular microenvironment in selection of the dominant follicle.Crossref | GoogleScholarGoogle Scholar | 15271447PubMed |

Freudenberger, T., Rack, K., Dai, G., Dorn, S., Mayer, P., Heim, H.-K., and Fischer, J. W. (2011). Estradiol inhibits hyaluronic acid synthase 1 expression in human vascular smooth muscle cells. Basic Res. Cardiol. 106, 1099–1109.
Estradiol inhibits hyaluronic acid synthase 1 expression in human vascular smooth muscle cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOnsL%2FN&md5=3bd9c0320fca7ea4c78b22cbd52c643eCAS | 21901291PubMed |

Galluzzo, P., Caiazza, F., Moreno, S., and Marino, M. (2007). Role of ERβ palmitoylation in the inhibition of human colon cancer cell proliferation. Endocr. Relat. Cancer 14, 153–167.
Role of ERβ palmitoylation in the inhibition of human colon cancer cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaksbnE&md5=8faf12125b05af151dce5624074c7b76CAS | 17395984PubMed |

Hall, J. M., Couse, J. F., and Korach, K. S. (2001). The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276, 36 869–36 872.
The multifaceted mechanisms of estradiol and estrogen receptor signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1eltr4%3D&md5=24f38564fc106fff8464fb6143492f1aCAS |

Hettinger, A. M., Allen, M. R., Zhang, B. R., Goad, D. W., Malayer, J. R., and Geisert, R. D. (2001). Presence of the acute phase protein, bikunin, in the endometrium of gilts during estrous cycle and early pregnancy. Biol. Reprod. 65, 507–513.
Presence of the acute phase protein, bikunin, in the endometrium of gilts during estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Wnsrs%3D&md5=189b8a47958a98d96935b5199e0e074dCAS | 11466219PubMed |

Hunter, M. G., Robinson, R. S., Mann, G. E., and Webb, R. (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim. Reprod. Sci. 82–83, 461–477.
Endocrine and paracrine control of follicular development and ovulation rate in farm species.Crossref | GoogleScholarGoogle Scholar | 15271473PubMed |

Itano, N. (2008). Simple primary structure, complex turnover regulation and multiple roles of hyaluronan. J. Biochem. 144, 131–137.
Simple primary structure, complex turnover regulation and multiple roles of hyaluronan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyrsrjL&md5=b96fc3e82d653cd5a0972ec7237603efCAS | 18390876PubMed |

Itano, N., and Kimata, K. (2002). Mammalian hyaluronan synthases. IUBMB Life 54, 195–199.
Mammalian hyaluronan synthases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVygu7o%3D&md5=e4f5b693b598eaaa71b69c15ae2446f0CAS | 12512858PubMed |

Itano, N., Sawai, T., Yoshida, M., Lenas, P., Yamada, Y., Imagawa, M., Shinomura, T., Hamaguchi, M., Yoshida, Y., Ohnuki, Y., Miyauchi, S., Spicer, A. P., McDonald, J. A., and Kimata, K. (1999). Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 274, 25 085–25 092.
Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1ymur8%3D&md5=f7af94bbda4c5d7747da1283a6b96157CAS |

Jacob, J., Sebastian, K. S., Devassy, S., Priyadarsini, L., Farook, M. F., Shameem, A., Mathew, D., Sreeja, S., and Thampan, R. V. (2006). Membrane estrogen receptors: genomic actions and post transcriptional regulation. Mol. Cell. Endocrinol. 246, 34–41.
Membrane estrogen receptors: genomic actions and post transcriptional regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsF2gtLo%3D&md5=d98046d75727ab711d54123e8c8528b8CAS | 16423448PubMed |

Jain, M., He, Q., Lee, W.-S., Kashiki, S., Foster, L. C., Tsai, J.-C., Lee, M.-E., and Haber, E. (1996). Role of CD44 in the reaction of vascular smooth muscle cells to arterial wall injury. J. Clin. Invest. 97, 596–603.
Role of CD44 in the reaction of vascular smooth muscle cells to arterial wall injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvVOktLs%3D&md5=352c685cc42f2b3537caeff7159a4c6dCAS | 8609213PubMed |

Juengel, J. L., Heath, D. A., Quirke, L. D., and McNatty, K. P. (2006). Oestrogen receptor α and β, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reproduction 131, 81–92.
Oestrogen receptor α and β, androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFegsr0%3D&md5=8b7f88817f178f699c0aa6dc4a068493CAS | 16388012PubMed |

Koehler, K. F., Helguero, L. A., Haldosén, L.-A., Warner, M., and Gustafsson, J.-A. (2005). Reflections on the discovery and significance of estrogen receptor β. Endocr. Rev. 26, 465–478.
Reflections on the discovery and significance of estrogen receptor β.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWqsr8%3D&md5=eeca0872b460525fee5b14de9b468547CAS | 15857973PubMed |

Kosaki, R., Watanabe, K., and Yamaguchi, Y. (1999). Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenicity. Cancer Res. 59, 1141–1145.
| 1:CAS:528:DyaK1MXhslelt7w%3D&md5=51ea51e2d58b561b86347b9d2b45cfbaCAS | 10070975PubMed |

Kultti, A., Pasonen-Seppanen, S., Jauhiainen, M., Rilla, K. J., Karna, R., Pyoria, E., Tammi, R. H., and Tammi, M. I. (2009). 4-Methylumbelliferone inhibits hyaluronan synthesis by depletion of cellular UDP–glucuronic acid and downregulation of hyaluronan synthase 2 and 3. Exp. Cell Res. 315, 1914–1923.
4-Methylumbelliferone inhibits hyaluronan synthesis by depletion of cellular UDP–glucuronic acid and downregulation of hyaluronan synthase 2 and 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1Oqu78%3D&md5=94b12ef0d8afc884e0433da692b006dcCAS | 19285976PubMed |

Laurent, T. C., Laurent, U. B., and Fraser, J. R. (1995). Functions of hyaluronan. Ann. Rheum. Dis. 54, 429.
Functions of hyaluronan.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzhsVequw%3D%3D&md5=22eb09bc7fac8fcf0f85ea5c2ffceabaCAS | 7794055PubMed |

Lee, J. Y., and Spicer, A. P. (2000). Hyaluronan: a multifunctional, megaDalton, stealth molecule. Curr. Opin. Cell Biol. 12, 581–586.
Hyaluronan: a multifunctional, megaDalton, stealth molecule.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Chtbw%3D&md5=8c0e89def81a032b9bdd5973c1e8ffd9CAS | 10978893PubMed |

Luo, W., and Wiltbank, M. C. (2006). Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells. Biol. Reprod. 75, 217.
Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVWgsLg%3D&md5=02fe5975d70ce6fca7b792b1df8645d8CAS | 16641147PubMed |

Manna, P. R., and Stocco, D. M. (2011). The role of specific mitogen-activated protein kinase signaling cascades in the regulation of steroidogenesis. J. Signal Transduct. 2011, Article ID 821615.
The role of specific mitogen-activated protein kinase signaling cascades in the regulation of steroidogenesis.Crossref | GoogleScholarGoogle Scholar |

Marei, W. F., Ghafari, F., and Fouladi-Nashta, A. A. (2012). Role of hyaluronic acid in maturation and further early embryo development of bovine oocytes. Theriogenology 78, 670–677.
Role of hyaluronic acid in maturation and further early embryo development of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1GqsL4%3D&md5=4d10e6fb33ba1890362b19b1d5bf746fCAS | 22541325PubMed |

Marei, W. F. A., Salavati, M., and Fouladi-Nashta, A. A. (2013). Critical role of hyaluronidase-2 during preimplantation embryo development. Mol. Hum. Reprod. 19, 590–599.
Critical role of hyaluronidase-2 during preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGmt7vJ&md5=a2e9f8d5130ea97ce161dd8efe4a9617CAS |

Marzioni, D., Crescimanno, C., Zaccheo, D., Coppari, R., Underhill, C. B., and Castellucci, M. (2001). Hyaluronate and CD44 expression patterns in the human placenta throughout pregnancy. Eur. J. Histochem. 45, 131–140.
| 1:STN:280:DC%2BD3MvmvVentg%3D%3D&md5=b70305dac4b604de37c112fc709cb676CAS | 11512634PubMed |

Miyake, Y., Matsumoto, H., Yokoo, M., Miyazawa, K., Kimura, N., Tunjung, W. A. S., Shimizu, T., Sasada, H., Aso, H., and Yamaguchi, T. (2006). Expression and glycosylation with polylactosamine of CD44 antigen on macrophages during follicular atresia in pig ovaries. Biol. Reprod. 74, 501–510.
Expression and glycosylation with polylactosamine of CD44 antigen on macrophages during follicular atresia in pig ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhslejs7g%3D&md5=d9e6513a0a1b6483db82a96161a43e35CAS | 16306424PubMed |

Miyake, Y., Sakurai, M., Tanaka, S., Tunjung, W. A. S., Yokoo, M., Matsumoto, H., Aso, H., Yamaguchi, T., and Sato, E. (2009). Expression of hyaluronan synthase 1 and distribution of hyaluronan during follicular atresia in pig ovaries. Biol. Reprod. 80, 249–257.
Expression of hyaluronan synthase 1 and distribution of hyaluronan during follicular atresia in pig ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOitLo%3D&md5=177a932527d9da6709ddd70e471402e7CAS | 18923162PubMed |

Moriarty, K., Kim, K. H., and Bender, J. R. (2006). Estrogen receptor-mediated rapid signaling. Endocrinology 147, 5557–5563.
Estrogen receptor-mediated rapid signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yqsbfE&md5=4c259fd2ccc9106e7f30029ae9f39eecCAS | 16946015PubMed |

Necas, J., Bartosikova, L., Brauner, P., and Kolar, J. (2008). Hyaluronic acid (hyaluronan): a review. Vet. Med. (Praha) 53, 397–411.
| 1:CAS:528:DC%2BD1cXhtlahu7nO&md5=5af93c9fbde1b098818d24bba1bb9bd4CAS |

Nykopp, T. K., Rilla, K., Sironen, R., Tammi, M. I., Tammi, R. H., Hamalainen, K., Heikkinen, A.-M., Komulainen, M., Kosma, V.-M., and Anttila, M. (2009). Expression of hyaluronan synthases (HAS1–3) and hyaluronidases (HYAL1–2) in serous ovarian carcinomas: inverse correlation between HYAL1 and hyaluronan content. BMC Cancer 9, 143.
Expression of hyaluronan synthases (HAS1–3) and hyaluronidases (HYAL1–2) in serous ovarian carcinomas: inverse correlation between HYAL1 and hyaluronan content.Crossref | GoogleScholarGoogle Scholar | 19435493PubMed |

Nykopp, T. K., Rilla, K., Tammi, M. I., Tammi, R. H., Sironen, R., Hamalainen, K., Kosma, V.-M., Heinonen, S., and Anttila, M. (2010). Hyaluronan synthases (HAS1–3) and hyaluronidases (HYAL1–2) in the accumulation of hyaluronan in endometrioid endometrial carcinoma. BMC Cancer 10, 512.
Hyaluronan synthases (HAS1–3) and hyaluronidases (HYAL1–2) in the accumulation of hyaluronan in endometrioid endometrial carcinoma.Crossref | GoogleScholarGoogle Scholar | 20875124PubMed |

Ohta, N., Saito, H., Kuzumaki, T., Takahashi, T., Ito, M. M., Saito, T., Nakahara, K., and Hiroi, M. (1999). Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes. Mol. Hum. Reprod. 5, 22–28.
Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7lsl2ntw%3D%3D&md5=9574e8b6ec26ec06ed76a14bf00a85c8CAS | 10050658PubMed |

Ohta, N., Saito, H., Kaneko, T., Yoshida, M., Takahashi, T., Saito, T., Nakahara, K., and Hiroi, M. (2001). Soluble CD44 in human ovarian follicular fluid. J. Assist. Reprod. Genet. 18, 21–25.
Soluble CD44 in human ovarian follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvkslGmtw%3D%3D&md5=e70524e4ffe43a92cd76071d0b70eb55CAS | 11292991PubMed |

Perry, K., Haresign, W., Wathes, D. C., and Khalid, M. (2010). Hyaluronan (HA) content, the ratio of HA fragments and the expression of CD44 in the ovine cervix vary with the stage of the oestrous cycle. Reproduction 140, 133–141.
Hyaluronan (HA) content, the ratio of HA fragments and the expression of CD44 in the ovine cervix vary with the stage of the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVWls77L&md5=94205c69d3f95c3185469f5c4daa50b3CAS | 20413624PubMed |

Perry, K., Haresign, W., Wathes, D. C., Pitsillides, A. A., and Khalid, M. (2012). Cervical expression of hyaluronan synthases varies with the stage of the estrous cycle in the ewe. Theriogenology 77, 1100–1110.
Cervical expression of hyaluronan synthases varies with the stage of the estrous cycle in the ewe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1ags70%3D&md5=59828c851e15512f1fa8bed85e0b79c9CAS | 22225684PubMed |

Pettersson, K., Grandien, K., Kuiper, G. G. J. M., and Gustafsson, J.-A. k. (1997). Mouse estrogen receptor β forms estrogen response element-binding heterodimers with estrogen receptor α. Mol. Endocrinol. 11, 1486–1496.
| 1:CAS:528:DyaK2sXlsF2ms7o%3D&md5=81258cbd87497e0debe63f48bb1271bdCAS | 9280064PubMed |

Raheem, K. A., Marei, W. F., Mifsud, K., Khalid, M., Wathes, D. C., and Fouladi-Nashta, A. A. (2013). Regulation of the hyaluronan system in ovine endometrium by ovarian steroids. Reproduction 145, 491–504.
Regulation of the hyaluronan system in ovine endometrium by ovarian steroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVejsb4%3D&md5=bae231d3678d4a9b605ceaa136daf9afCAS | 23630333PubMed |

Rilla, K., Oikari, S., Jokela, T. A., Hyttinen, J. M. T., Karna, R., Tammi, R. H., and Tammi, M. I. (2013). Hyaluronan synthase 1 (HAS1) requires higher cellular UDP-GlcNAc concentration than HAS2 and HAS3. J. Biol. Chem. 288, 5973–5983.
Hyaluronan synthase 1 (HAS1) requires higher cellular UDP-GlcNAc concentration than HAS2 and HAS3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtVGmsbk%3D&md5=a0c88b7b98d927450f55e00bfe6add02CAS | 23303191PubMed |

Robinson, R. S., Pushpakumara, P. G., Cheng, Z., Peters, A. R., Abayasekara, D. R., and Wathes, D. C. (2002). Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124, 119–131.
Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtFaksLo%3D&md5=3990b96051a5ded8d7cec87d6997251dCAS | 12090925PubMed |

Sainio, A., Jokela, T., Tammi, M. I., and Järveläinen, H. (2010). Hyperglycemic conditions modulate connective tissue reorganization by human vascular smooth muscle cells through stimulation of hyaluronan synthesis. Glycobiology 20, 1117–1126.
Hyperglycemic conditions modulate connective tissue reorganization by human vascular smooth muscle cells through stimulation of hyaluronan synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFSqsbc%3D&md5=650cd6de0cdc8af6fd0a76d3d23ba8ebCAS | 20488939PubMed |

Saito, H., Kaneko, T., Takahashi, T., Kawachiya, S., Saito, T., and Hiroi, M. (2000). Hyaluronan in follicular fluids and fertilization of oocytes. Fertil. Steril. 74, 1148–1152.
Hyaluronan in follicular fluids and fertilization of oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FotVGmuw%3D%3D&md5=9e0e4452fc616f5ef32feb0ac4009e81CAS | 11119742PubMed |

Scaramuzzi, R. J., Baird, D. T., Campbell, B. K., Driancourt, M. A., Dupont, J., Fortune, J. E., Gilchrist, R. B., Martin, G. B., McNatty, K. P., McNeilly, A. S., Monget, P., Monniaux, D., Vinoles, C., and Webb, R. (2011). Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod. Fertil. Dev. 23, 444–467.
Regulation of folliculogenesis and the determination of ovulation rate in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt12ntLg%3D&md5=74cb3d30f5c858a605318a3ffb0064ffCAS | 21426863PubMed |

Schoenfelder, M., and Einspanier, R. (2003). Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol. Reprod. 69, 269–277.
Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvFCntbw%3D&md5=c91151711b3ed5e761be0764438be71aCAS | 12620932PubMed |

Silva, J. R. V., Figueiredo, J. R., and van den Hurk, R. (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–1208.
Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktF2nur0%3D&md5=c3d2d598bc7afb1348805ab99ccd8135CAS |

Stern, R. (2004). Hyaluronan catabolism: a new metabolic pathway. Eur. J. Cell Biol. 83, 317–325.
Hyaluronan catabolism: a new metabolic pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGgu7rL&md5=1df1b064062b3ce5f34474b06f3f494eCAS | 15503855PubMed |

Tempel, C., Gilead, A., and Neeman, M. (2000). Hyaluronic acid as an anti-angiogenic shield in the preovulatory rat follicle. Biol. Reprod. 63, 134–140.
Hyaluronic acid as an anti-angiogenic shield in the preovulatory rat follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2rs7o%3D&md5=fc9f5f5dbaadd0bfe01fe726d893cce2CAS | 10859252PubMed |

Tienthai, P., Yokoo, M., Kimura, N., Heldin, P., Sato, E., and Rodriguez-Martinez, H. (2003). Immunohistochemical localization and expression of the hyaluronan receptor CD44 in the epithelium of the pig oviduct during oestrus. Reproduction 125, 119–132.
Immunohistochemical localization and expression of the hyaluronan receptor CD44 in the epithelium of the pig oviduct during oestrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFGlsL8%3D&md5=d5bb2f831a35809cea4a4649cefbbf7fCAS | 12622702PubMed |

Toole, B. P. (2001). Hyaluronan in morphogenesis. Semin. Cell Dev. Biol. 12, 79–87.
Hyaluronan in morphogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1SisLY%3D&md5=30a4d4e8f51b1721dfc63dd65c0bc551CAS | 11292373PubMed |

Toole, B. P. (2004). Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4, 528–539.
Hyaluronan: from extracellular glue to pericellular cue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1OktrY%3D&md5=d01b928020a1d6ebb1aec42960037f77CAS | 15229478PubMed |

Toole, B. P., Wight, T. N., and Tammi, M. I. (2002). Hyaluronan–cell interactions in cancer and vascular disease. J. Biol. Chem. 277, 4593–4596.
Hyaluronan–cell interactions in cancer and vascular disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFeqsbs%3D&md5=3763a2d2bc044dc5d072bdfafe2fd769CAS | 11717318PubMed |

Tsonis, C. G., Carson, R. S., and Findlay, J. K. (1984). Relationships between aromatase activity, follicular fluid oestradiol-17 beta and testosterone concentrations, and diameter and atresia of individual ovine follicles. J. Reprod. Fertil. 72, 153–163.
Relationships between aromatase activity, follicular fluid oestradiol-17 beta and testosterone concentrations, and diameter and atresia of individual ovine follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmt1aqu7s%3D&md5=1069e4197dabc6f80bf73b971f15d1bfCAS | 6471045PubMed |

Ulbrich, S. E., Schoenfelder, M., Thoene, S., and Einspanier, R. (2004). Hyaluronan in the bovine oviduct: modulation of synthases and receptors during the estrous cycle. Mol. Cell. Endocrinol. 214, 9–18.
Hyaluronan in the bovine oviduct: modulation of synthases and receptors during the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFWgsr4%3D&md5=d8aea01acfb965b2e169c912005ce0fdCAS | 15062540PubMed |

Watson, C. S., Jeng, Y.-J., Hu, G., Wozniak, A., Bulayeva, N., and Guptarak, J. (2012). Estrogen- and xenoestrogen-induced ERK signaling in pituitary tumor cells involves estrogen receptor-α interactions with G protein-αi and caveolin I. Steroids 77, 424–432.
Estrogen- and xenoestrogen-induced ERK signaling in pituitary tumor cells involves estrogen receptor-α interactions with G protein-αi and caveolin I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1yjtro%3D&md5=974c964bac9ae91398b9a66d6518de39CAS | 22230296PubMed |

Weigel, P. H., and DeAngelis, P. L. (2007). Hyaluronan synthases: a decade-plus of novel glycosyltransferases. J. Biol. Chem. 282, 36 777–36 781.
Hyaluronan synthases: a decade-plus of novel glycosyltransferases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVamur%2FP&md5=fdfa13432922906ec2865fecc614f495CAS |

Zhao, C., Dahlman-Wright, K., and Gustafsson, J.-A. (2008). Estrogen receptor β: an overview and update. Nucl. Recept. Signal. 6, e003.
| 18301783PubMed |