Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Unique oestrogen receptor ligand-binding domain sequence of native parrots: a possible link between phytoestrogens and breeding success

Catherine E. J. Davis A , Adrian H. Bibby A , Kevin M. Buckley A , Kenneth P. McNatty A and Janet L. Pitman A B
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington 6140, New Zealand.

B Corresponding author. Email: janet.pitman@vuw.ac.nz

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17045
Submitted: 7 February 2017  Accepted: 1 June 2017   Published online: 11 July 2017

Abstract

The New Zealand (NZ) native parrots kākāpō, kākā and kea are classified as critically endangered, endangered and vulnerable respectively. Successful reproduction of kākāpō and kākā is linked to years of high levels of fruiting in native flora (mast years). To assess a possible hormonal link between native plants and reproductive success in these parrots in mast years, we examined the ligand-binding domains (LBD) of the progesterone receptor (PR), androgen receptor (AR), estrogen receptor 1 (ESR1) and estrogen receptor 2 (ESR2) in NZ native (kākāpō, kākā, kea and kākāriki) and non-native (Australian cockatiel) parrots and compared them with those in the chicken. The amino acid sequences for PR, AR, ESR1 and ESR2 shared >90% homology among the NZ parrots, the cockatiel and, in most cases, the chicken. The exception was for the ESR1 LBD, which contained an extra eight amino acids at the C-terminal in all the parrots compared with the chicken and with published sequences of non-parrot species. These results support the notion that the ESR1 LBD of parrots responds differently to putative oestrogenic compounds in native trees in NZ during times of intermittent masting. In turn, this may provide important information for generating parrot-specific bioassays and linkages to steroidogenic activity in native plants.

Additional keywords: kākāpō, masting, steroid receptor.


References

Atkinson, I. A. E., and Merton, D. V. (2006). Habitat and diet of kākāpō (Strigops habroptilus) in the Esperance Valley, Fiordland, New Zealand. Notornis 53, 37–54. open url image1

Bai, W., and Weigel, N. L. (1996). Phosphorylation of Ser211 in the chicken progesterone receptor modulates its transcriptional activity. J. Biol. Chem. 271, 12801–12806.
| 1:CAS:528:DyaK28XjtlGjtLk%3D&md5=a4a055a74d9ed86eac62866af02577f7CAS | open url image1

Butler, D. J. (2006). The habitat, food and feeding ecology of kakapo. Notornis 53, 55–79. open url image1

Cockrem, J. F. (2006). The timing of breeding in the kakapo (Strigops habroptilus). Notornis 53, 153–159. open url image1

Conneely, O. M., Mulac-Jericevic, B., Lydon, J. P., and De Mayo, F. J. (2001). Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol. Cell. Endocrinol. 179, 97–103.
Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice.CrossRef | 1:CAS:528:DC%2BD3MXksVylsb0%3D&md5=86b8651810682fbdbc790a9d5930fdbdCAS | open url image1

Conneely, O. M., Mulac-Jericevic, B., and Lydon, J. P. (2003). Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 68, 771–778.
Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms.CrossRef | 1:CAS:528:DC%2BD3sXps1Oltb8%3D&md5=fdda99383026ad29838f4aa46413f4aeCAS | open url image1

Davis, C. E. J. (2013). Kākāpō reproduction: identification of steroid receptors and oestrogenic activity in native flora. Ph.D. thesis, Victoria University of Wellington, Wellington, New Zealand.

Department of Conservation National Office (2017). Kākāpō Recovery Programme Update – Newsletter April 2017. Available at http://kakaporecovery.org.nz/science-update-newsletter/

Deroo, B. J., and Korach, K. S. (2006). Estrogen receptors and human disease. J. Clin. Invest. 116, 561–570.
Estrogen receptors and human disease.CrossRef | 1:CAS:528:DC%2BD28XitlGktrc%3D&md5=46f0fae0732183f236257c051d2d3adeCAS | open url image1

Drummond, A. E., Britt, K. L., Dyson, M., Jones, M. E., Kerr, J. B., O’Donnell, L., Simpson, E. R., and Findlay, J. K. (2002). Ovarian steroid receptors and their role in ovarian function. Mol. Cell. Endocrinol. 191, 27–33.
Ovarian steroid receptors and their role in ovarian function.CrossRef | 1:CAS:528:DC%2BD38XktFKhurg%3D&md5=5309da7abb430d3e61939c40e6712f5fCAS | open url image1

Dupont, S., Krust, A., Gansmuller, A., Dierich, A., Chambon, P., and Mark, M. (2000). Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127, 4277–4291.
| 1:CAS:528:DC%2BD3cXotVWisbY%3D&md5=28f168e0b4187e81281daac982e0cc66CAS | open url image1

Elliott, G. P., and Kemp, J. (1999). Conservation ecology of kea (Nestor notabilis). WWF–New Zealand final report, World Wide Fund for Nature, Wellington, New Zealand.

Elliott, G. P., Dilks, P. J., and O’Donnell, C. F. J. (1996). Nest site selection by mohua and yellow-crowned parakeets in beech forest in Fiordland, New Zealand. N.Z. J. Zool. 23, 249–265.
Nest site selection by mohua and yellow-crowned parakeets in beech forest in Fiordland, New Zealand.CrossRef | open url image1

Elliott, G. P., Merton, D. V., and Jansen, P. W. (2001). Intensive management of a critically endangered species: the kakapo. Biol. Conserv. 99, 121–133.
Intensive management of a critically endangered species: the kakapo.CrossRef | open url image1

Fidler, A. E., Zwart, S., Pharis, R., Lawrence, S. B., Elliott, G. P., Merton, D., and McNatty, K. P. (2000). Screening foods of the endangered kakapo parrot (Strigops habroptilus) for oestrogenic activity using a recombinant yeast bioassay. Br. Poult. Sci. 41, 48–49.
Screening foods of the endangered kakapo parrot (Strigops habroptilus) for oestrogenic activity using a recombinant yeast bioassay.CrossRef | open url image1

Fidler, A. E., Lawrence, S. B., and McNatty, K. P. (2008). An hypothesis to explain the linkage between kakapo (Strigops habroptilus) breeding and the mast fruiting of their food trees. Wildl. Res. 35, 1–7.
An hypothesis to explain the linkage between kakapo (Strigops habroptilus) breeding and the mast fruiting of their food trees.CrossRef | open url image1

Greene, T. C., Powlesland, R. G., Dilks, P. J., and Moran, L. R. (2004). Research summary and options for conservation of kaka (Nestor meridionalis). DOC Science Internal Series #178. (Department of Conservation: Wellington, New Zealand.)

Higgins, P. J. (1999). ‘Handbook of Australian, New Zealand and Antarctic Birds.’ (Oxford University Press: Melbourne.)

Horrocks, M., Salter, J., Braggins, S., Nichol, S., Moorhouse, R., and Elliot, G. (2008). Plant microfossil analysis of coprolites of the critically endangered kakapo (Strigops habroptilus) parrot from New Zealand. Rev. Palaeobot. Palynol. 149, 229–245.
Plant microfossil analysis of coprolites of the critically endangered kakapo (Strigops habroptilus) parrot from New Zealand.CrossRef | open url image1

Khorasanizadeh, S., and Rastinejad, F. (2016). Visualizing the architectures and interactions of nuclear receptors. Endocrinology 157, 4212–4221.
Visualizing the architectures and interactions of nuclear receptors.CrossRef | 1:CAS:528:DC%2BC2sXhtlKqt70%3D&md5=3df0777d542609ddd7d45bf9965cf005CAS | open url image1

Leung, Y.-K., Mak, P., Hassan, S., and Ho, S.-M. (2006). Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signalling. Proc. Natl Acad. Sci. USA 103, 13162–13167.
Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signalling.CrossRef | 1:CAS:528:DC%2BD28Xptlelsrk%3D&md5=1c103dec5ba411bbc6fa000afadf12feCAS | open url image1

Li, J., Leghari, I. H., He, B., Zeng, W., Mi, Y., and Zhang, C. (2014). Estrogen stimulates expression of chicken hepatic vitellogenin II and very low-density apolipoprotein II through ER-α. Theriogenology 82, 517–524.
Estrogen stimulates expression of chicken hepatic vitellogenin II and very low-density apolipoprotein II through ER-α.CrossRef | 1:CAS:528:DC%2BC2cXhtVWmtL%2FN&md5=903ba61ea36ca2dbaf98e2deefcf88acCAS | open url image1

Ong, Y. C., Kolatkar, P. R., and Yong, E. L. (2002). Androgen receptor mutations causing human androgen insensitivity syndromes show a key role of residue M807 in Helix 8–Helix 10 interactions and in receptor ligand-binding domain stability. Mol. Hum. Reprod. 8, 101–108.
Androgen receptor mutations causing human androgen insensitivity syndromes show a key role of residue M807 in Helix 8–Helix 10 interactions and in receptor ligand-binding domain stability.CrossRef | 1:CAS:528:DC%2BD38XitFOhu7Y%3D&md5=7518aa5f250fb272b4272d5c096b6224CAS | open url image1

Powlesland, R. G., Lloyd, B. D., Best, H. A., and Merton, D. V. (1992). Breeding biology of the kakapo Strigops habroptilus on Stewart Island, New Zealand. Ibis 134, 361–373.
Breeding biology of the kakapo Strigops habroptilus on Stewart Island, New Zealand.CrossRef | open url image1

Rastinejad, F., Huang, P., Chandra, V., and Khorasanizadeh, S. (2013). Understanding nuclear receptor form and function using structural biology. J. Mol. Endocrinol. 51, T1–T21.
Understanding nuclear receptor form and function using structural biology.CrossRef | 1:CAS:528:DC%2BC2cXivFSnsbc%3D&md5=a65fc9cf434b2e6cf569e2f1c6ea2166CAS | open url image1

Schauber, E. M., Kelly, D., Turchin, P., Simon, C., Lee, W. G., Allen, R. B., Payton, I. J., Wilson, P. R., Cowan, P. E., and Brockie, R. E. (2002). Masting by eighteen New Zealand plant species: the role of temperature as a synchronizing cue. Ecology 83, 1214–1225.
Masting by eighteen New Zealand plant species: the role of temperature as a synchronizing cue.CrossRef | open url image1

Sotoca, A. M., Vervoort, J., Rietjens, I. M. C. M., and Gustafsson, J.-A. (2012). Human ERa and ERb splice variants: Understanding their domain structure in relation to their biological roles in breast cancer cell proliferation. In ‘Biochemistry’. (Ed. D. Ekinci.) pp. 141–160. (InTech: Rijeka, Croatia.)

Terasaki, M., Shiraishi, F., Fukazawa, H., and Makino, M. (2007). Occurrence and estrogenicity of phenolics in paper-recycling process water: pollutants originating from thermal paper in waste paper. Environ. Toxicol. Chem. 26, 2356–2366.
Occurrence and estrogenicity of phenolics in paper-recycling process water: pollutants originating from thermal paper in waste paper.CrossRef | 1:CAS:528:DC%2BD2sXht1eku7rM&md5=05905a2aa5c633b66430e82bd861f98dCAS | open url image1

Wilson, P. R., Karl, B. J., Toft, R. J., Beggs, J. R., and Taylor, R. H. (1998). The role of introduced predators and competitors in the decline of kaka (Nestor meridionalis) populations in New Zealand. Biol. Conserv. 83, 175–185.
The role of introduced predators and competitors in the decline of kaka (Nestor meridionalis) populations in New Zealand.CrossRef | open url image1

Wilson, D. J., Grant, A. D., and Parker, N. (2006). Diet of kākāpō in breeding and non-breeding years on Codfish Island (Whenua Hou) and Stewart Island. Notornis 53, 80–89. open url image1

Zhou, T. B., Qin, Y. H., Su, L. N., Lei, F. Y., Huang, W. F., Zhao, Y. J., and Pang, Y. S. (2011). Insertion/deletion (I/D) polymorphism of angiotensin-converting enzyme gene in steroid-resistant nephrotic syndrome for children: a genetic association study and meta-analysis. Ren. Fail. 33, 741–748.
Insertion/deletion (I/D) polymorphism of angiotensin-converting enzyme gene in steroid-resistant nephrotic syndrome for children: a genetic association study and meta-analysis.CrossRef | 1:CAS:528:DC%2BC3MXptlyrsbg%3D&md5=97e6ea65da19e72da44392ced1711522CAS | open url image1


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