Reproductive health research in Australia and New Zealand: highlights from the Annual Meeting of the Society for Reproductive Biology, 2019
Amy Winship A , Jacqueline Donoghue B , Brendan J. Houston C , Jacinta H. Martin D , Tessa Lord D E , Alaknanda Adwal F , Macarena Gonzalez F , Elodie Desroziers G H , Gulfam Ahmad I , Dulama Richani J and Elizabeth G. Bromfield
E K L
+ Author Affiliations
- Author Affiliations
A Biomedicine Discovery Institute, Department of Anatomy and Developmental Biology, Stem Cells and Development Program, Monash University, 19 Innovation Walk, Clayton, Vic. 3800, Australia.
B The University of Melbourne, Department of Obstetrics and Gynaecology, Gynaecology Research Centre, Royal Women’s Hospital, 20 Flemington Rd, Parkville, Vic. 3052, Australia.
C School of Biological Sciences, Monash University, 25 Rainforest Walk, Clayton, Vic. 3800, Australia.
D Hunter Medical Research Institute, Pregnancy and Reproduction Program, Lot 1 Kookaburra Cct, New Lambton Heights, NSW 2305, Australia.
E Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, The University of Newcastle, Callaghan, NSW 2300, Australia.
F School of Medicine, Robinson Research Institute, The University of Adelaide, Adelaide, SA 5005, Australia.
G Department of Physiology, University of Otago, PO Box 56, Dunedin 9054, New Zealand.
H Centre for Neuroendocrinology, University of Otago, PO Box 913, Dunedin 9054, New Zealand.
I The University of Sydney Medical School, Discipline of Pathology, School of Medical Sciences, Sydney, NSW 2006, Australia.
J School of Women’s and Children’s Health, Fertility & Research Centre, University of New South Wales Medicine, Sydney, NSW 2052 Australia.
K Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, Netherlands.
L Corresponding author: Elizabeth.bromfield@newcastle.edu.au
Reproduction, Fertility and Development 32(7) 637-647 https://doi.org/10.1071/RD19449
Submitted: 9 December 2019 Accepted: 13 December 2019 Published: 1 April 2020
Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND
Abstract
The 2019 meeting of the Society for Reproductive Biology (SRB) provided a platform for the dissemination of new knowledge and innovations to improve reproductive health in humans, enhance animal breeding efficiency and understand the effect of the environment on reproductive processes. The effects of environment and lifestyle on fertility and animal behaviour are emerging as the most important modern issues facing reproductive health. Here, we summarise key highlights from recent work on endocrine-disrupting chemicals and diet- and lifestyle-induced metabolic changes and how these factors affect reproduction. This is particularly important to discuss in the context of potential effects on the reproductive potential that may be imparted to future generations of humans and animals. In addition to key summaries of new work in the male and female reproductive tract and on the health of the placenta, for the first time the SRB meeting included a workshop on endometriosis. This was an important opportunity for researchers, healthcare professionals and patient advocates to unite and provide critical updates on efforts to reduce the effect of this chronic disease and to improve the welfare of the women it affects. These new findings and directions are captured in this review.
References
AbdelHafez, F. F., Desai, N., Abou-Setta, A. M., Falcone, T., and Goldfarb, J. (2010). Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis. Reprod. Biomed. Online 20, 209–222.| Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 20113959PubMed |
Alshahrani, S., Ahmed, A. F., Gabr, A. H., Abalhassan, M., and Ahmad, G. (2016). The impact of body mass index on semen parameters in infertile men. Andrologia 48, 1125–1129.
| The impact of body mass index on semen parameters in infertile men.Crossref | GoogleScholarGoogle Scholar | 26847036PubMed |
Anglesio, M. S., and Yong, P. J. (2017). Endometriosis-associated ovarian cancers. Clin. Obstet. Gynecol. 60, 711–727.
| Endometriosis-associated ovarian cancers.Crossref | GoogleScholarGoogle Scholar | 28990985PubMed |
Anglesio, M. S., Bashashati, A., Wang, Y. K., Senz, J., Ha, G., Yang, W., Aniba, M. R., Prentice, L. M., Farahani, H., Li Chang, H., Karnezis, A. N., Marra, M. A., Yong, P. J., Hirst, M., Gilks, B., Shah, S. P., and Huntsman, D. G. (2015). Multifocal endometriotic lesions associated with cancer are clonal and carry a high mutation burden. J. Pathol. 236, 201–209.
| Multifocal endometriotic lesions associated with cancer are clonal and carry a high mutation burden.Crossref | GoogleScholarGoogle Scholar | 25692284PubMed |
Armour, M., Lawson, K., Wood, A., Smith, C. A., and Abbott, J. (2019). The cost of illness and economic burden of endometriosis and chronic pelvic pain in Australia: a national online survey. PLoS One 14, e0223316.
| The cost of illness and economic burden of endometriosis and chronic pelvic pain in Australia: a national online survey.Crossref | GoogleScholarGoogle Scholar | 31600241PubMed |
As-Sanie, S., Black, R., Giudice, L. C., Gray Valbrun, T., Gupta, J., Jones, B., Laufer, M. R., Milspaw, A. T., Missmer, S. A., Norman, A., Taylor, R. N., Wallace, K., Williams, Z., Yong, P. J., and Nebel, R. A. (2019). Assessing research gaps and unmet needs in endometriosis. Am. J. Obstet. Gynecol. 221, 86–94.
| Assessing research gaps and unmet needs in endometriosis.Crossref | GoogleScholarGoogle Scholar | 30790565PubMed |
Bhargava, A., Pathak, N., Sharma, R. S., Lohiya, N. K., and Mishra, P. K. (2017). Environmental impact on reproductive health: can biomarkers offer any help? J. Reprod. Infertil. 18, 336–340.
| 29062799PubMed |
Boretto, M., Cox, B., Noben, M., Hendriks, N., Fassbender, A., Roose, H., Amant, F., Timmerman, D., Tomassetti, C., Vanhie, A., Meuleman, C., Ferrante, M., and Vankelecom, H. (2017). Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development 144, 1775–1786.
| Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability.Crossref | GoogleScholarGoogle Scholar | 28442471PubMed |
Boretto, M., Maenhoudt, N., Luo, X., Hennes, A., Boeckx, B., Bui, B., Heremans, R., Perneel, L., Kobayashi, H., Van Zundert, I., Brems, H., Cox, B., Ferrante, M., Uji, I. H., Koh, K. P., D’Hooghe, T., Vanhie, A., Vergote, I., Meuleman, C., Tomassetti, C., Lambrechts, D., Vriens, J., Timmerman, D., and Vankelecom, H. (2019). Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat. Cell Biol. 21, 1041–1051.
| Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening.Crossref | GoogleScholarGoogle Scholar | 31371824PubMed |
Bouty, A., Ayers, K. L., Pask, A., Heloury, Y., and Sinclair, A. H. (2015). The genetic and environmental factors underlying hypospadias. Sex Dev. 9, 239–259.
| The genetic and environmental factors underlying hypospadias.Crossref | GoogleScholarGoogle Scholar | 26613581PubMed |
Burton, G. J., Fowden, A. L., and Thornburg, K. L. (2016). Placental origins of chronic disease. Physiol. Rev. 96, 1509–1565.
| Placental origins of chronic disease.Crossref | GoogleScholarGoogle Scholar | 27604528PubMed |
Chatterjee, A., Macaulay, E. C., Rodger, E. J., Stockwell, P. A., Parry, M. F., Roberts, H. E., Slatter, T. L., Hung, N. A., Devenish, C. J., and Morison, I. M. (2016). Placental hypomethylation is more pronounced in genomic loci devoid of retroelements. G3 (Bethesda) 6, 1911–1921.
| Placental hypomethylation is more pronounced in genomic loci devoid of retroelements.Crossref | GoogleScholarGoogle Scholar | 27172225PubMed |
Chung, S. H., Franceschi, S., and Lambert, P. F. (2010). Estrogen and ERalpha: culprits in cervical cancer? Trends Endocrinol. Metab. 21, 504–511.
| Estrogen and ERalpha: culprits in cervical cancer?Crossref | GoogleScholarGoogle Scholar | 20456973PubMed |
Clark, A. R., James, J. L., Stevenson, G. N., and Collins, S. L. (2018). Understanding abnormal uterine artery Doppler waveforms: a novel computational model to explore potential causes within the utero-placental vasculature. Placenta 66, 74–81.
| Understanding abnormal uterine artery Doppler waveforms: a novel computational model to explore potential causes within the utero-placental vasculature.Crossref | GoogleScholarGoogle Scholar | 29884305PubMed |
Coughlan, C., Ledger, W., Wang, Q., Liu, F., Demirol, A., Gurgan, T., Cutting, R., Ong, K., Sallam, H., and Li, T. C. (2014). Recurrent implantation failure: definition and management. Reprod. Biomed. Online 28, 14–38.
| Recurrent implantation failure: definition and management.Crossref | GoogleScholarGoogle Scholar | 24269084PubMed |
Cousins, F. L., Msc, D. F. O, and Gargett, C. E. (2018). Endometrial stem/progenitor cells and their role in the pathogenesis of endometriosis. Best Pract. Res. Clin. Obstet. Gynaecol. 50, 27–38.
| Endometrial stem/progenitor cells and their role in the pathogenesis of endometriosis.Crossref | GoogleScholarGoogle Scholar | 29503126PubMed |
Cripps, S. M., Mattiske, D. M., Black, J. R., Risbridger, G. P., Govers, L. C., Phillips, T. R., and Pask, A. J. (2019). A loss of estrogen signaling in the aromatase deficient mouse penis results in mild hypospadias. Differentiation 109, 42–52.
| A loss of estrogen signaling in the aromatase deficient mouse penis results in mild hypospadias.Crossref | GoogleScholarGoogle Scholar | 31520742PubMed |
Croft, B., Ayers, K., Sinclair, A., and Ohnesorg, T. (2016). Review disorders of sex development: the evolving role of genomics in diagnosis and gene discovery. Birth Defects Res. C Embryo Today 108, 337–350.
| 28033663PubMed |
Cuman, C., Van Sinderen, M., Gantier, M. P., Rainczuk, K., Sorby, K., Rombauts, L., Osianlis, T., and Dimitriadis, E. (2015). Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion. EBioMedicine 2, 1528–1535.
| Human blastocyst secreted microRNA regulate endometrial epithelial cell adhesion.Crossref | GoogleScholarGoogle Scholar | 26629549PubMed |
Délot, E. C., Papp, J. C., The DSD-TRN Genetics Workgroup Sandberg, D. E., and Vilain, E. (2017). Genetics of disorders of sex development: the DSD-TRN experience. Endocrinol. Metab. Clin. North Am. 46, 519–537.
| Genetics of disorders of sex development: the DSD-TRN experience.Crossref | GoogleScholarGoogle Scholar | 28476235PubMed |
Dior, U. P., Kogan, L., Chill, H. H., Eizenberg, N., Simon, A., and Revel, A. (2014). Emerging roles of microRNA in the embryo–endometrium cross talk. Semin. Reprod. Med. 32, 402–409.
| Emerging roles of microRNA in the embryo–endometrium cross talk.Crossref | GoogleScholarGoogle Scholar | 24959822PubMed |
Evans, S. F., Brooks, T. A., Esterman, A. J., Hull, M. L., and Rolan, P. E. (2018). The comorbidities of dysmenorrhea: a clinical survey comparing symptom profile in women with and without endometriosis. J. Pain Res. 11, 3181–3194.
| The comorbidities of dysmenorrhea: a clinical survey comparing symptom profile in women with and without endometriosis.Crossref | GoogleScholarGoogle Scholar | 30588070PubMed |
Folmes, C. D., Nelson, T. J., Dzeja, P. P., and Terzic, A. (2012). Energy metabolism plasticity enables stemness programs. Ann. N. Y. Acad. Sci. 1254, 82–89.
| Energy metabolism plasticity enables stemness programs.Crossref | GoogleScholarGoogle Scholar | 22548573PubMed |
Ford, H. B., and Schust, D. J. (2009). Recurrent pregnancy loss: etiology, diagnosis, and therapy. Rev. Obstet. Gynecol. 2, 76–83.
| 19609401PubMed |
Fung, J. N., and Montgomery, G. W. (2018). Genetics of endometriosis: state of the art on genetic risk factors for endometriosis. Best Pract. Res. Clin. Obstet. Gynaecol. 50, 61–71.
| Genetics of endometriosis: state of the art on genetic risk factors for endometriosis.Crossref | GoogleScholarGoogle Scholar | 29506960PubMed |
Fung, J. N., Rogers, P. A., and Montgomery, G. W. (2015). Identifying the biological basis of GWAS hits for endometriosis. Biol. Reprod. 92, 87.
| Identifying the biological basis of GWAS hits for endometriosis.Crossref | GoogleScholarGoogle Scholar | 25695719PubMed |
Gardner, D. K., and Schoolcraft, W. B. (1999). In vitro culture of human blastocysts. In ‘Towards Reproductive Certainty: Fertility and Genetics Beyond 1999’, (Eds R. Jansen and D. Mortimer.) pp. 378–388. (CRC Press: Boca Raton)
Gardner, D. K. (2016). The impact of physiological oxygen during culture, and vitrification for cryopreservation, on the outcome of extended culture in human IVF. Reprod. Biomed. Online 32, 137–141.
| The impact of physiological oxygen during culture, and vitrification for cryopreservation, on the outcome of extended culture in human IVF.Crossref | GoogleScholarGoogle Scholar | 26687905PubMed |
Gardner, D. K., and Harvey, A. J. (2015). Blastocyst metabolism. Reprod. Fertil. Dev. 27, 638–654.
| Blastocyst metabolism.Crossref | GoogleScholarGoogle Scholar | 25751298PubMed |
Gardner, D. K., and Leese, H. J. (1987). Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake. J. Exp. Zool. 242, 103–105.
| Assessment of embryo viability prior to transfer by the noninvasive measurement of glucose uptake.Crossref | GoogleScholarGoogle Scholar | 3598508PubMed |
Gardner, D. K., and Wale, P. L. (2013). Analysis of metabolism to select viable human embryos for transfer. Fertil. Steril. 99, 1062–1072.
| Analysis of metabolism to select viable human embryos for transfer.Crossref | GoogleScholarGoogle Scholar | 23312219PubMed |
Gardner, D. K., Lane, M., and Schoolcraft, W. B. (2002). Physiology and culture of the human blastocyst. J. Reprod. Immunol. 55, 85–100.
| Physiology and culture of the human blastocyst.Crossref | GoogleScholarGoogle Scholar | 12062824PubMed |
Gardner, D. K., Wale, P. L., Collins, R., and Lane, M. (2011). Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome. Hum. Reprod. 26, 1981–1986.
| Glucose consumption of single post-compaction human embryos is predictive of embryo sex and live birth outcome.Crossref | GoogleScholarGoogle Scholar | 21572086PubMed |
Gargett, C. E., Schwab, K. E., Brosens, J. J., Puttemans, P., Benagiano, G., and Brosens, I. (2014). Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol. Hum. Reprod. 20, 591–598.
| Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis.Crossref | GoogleScholarGoogle Scholar | 24674992PubMed |
Ge, P., Ren, J., Harrington, A. M., Grundy, L., Castro, J., Brierley, S. M., and Hannig, G. (2019). Linaclotide treatment reduces endometriosis-associated vaginal hyperalgesia and mechanical allodynia through viscerovisceral cross-talk. Pain 160, 2566–2579.
| Linaclotide treatment reduces endometriosis-associated vaginal hyperalgesia and mechanical allodynia through viscerovisceral cross-talk.Crossref | GoogleScholarGoogle Scholar | 31335750PubMed |
Govers, L. C., Phillips, T. R., Mattiske, D. M., Rashoo, N., Black, J. R., Sinclair, A., Baskin, L. S., Risbridger, G. P., and Pask, A. J. (2019). A critical role for estrogen signaling in penis development. FASEB J. 33, 10383–10392.
| A critical role for estrogen signaling in penis development.Crossref | GoogleScholarGoogle Scholar | 31225966PubMed |
Grundy, L., Erickson, A., and Brierley, S. M. (2019). Visceral pain. Annu. Rev. Physiol. 81, 261–284.
| Visceral pain.Crossref | GoogleScholarGoogle Scholar | 30379615PubMed |
Gu, W., Gaeta, X., Sahakyan, A., Chan, A. B., Hong, C. S., Kim, R., Braas, D., Plath, K., Lowry, W. E., and Christofk, H. R. (2016). Glycolytic metabolism plays a functional role in regulating human pluripotent stem cell state. Cell Stem Cell 19, 476–490.
| Glycolytic metabolism plays a functional role in regulating human pluripotent stem cell state.Crossref | GoogleScholarGoogle Scholar | 27618217PubMed |
Ha, M., and Kim, V. N. (2014). Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15, 509–524.
| Regulation of microRNA biogenesis.Crossref | GoogleScholarGoogle Scholar | 25027649PubMed |
Hahn, F., Hutterer, C., Henry, C., Hamilton, S. T., Strojan, H., Kraut, A., Schulte, U., Schutz, M., Kohrt, S., Wangen, C., Pfizer, J., Coute, Y., Rawlinson, W. D., Strobl, S., and Marschall, M. (2018). Novel cytomegalovirus-inhibitory compounds of the class pyrrolopyridines show a complex pattern of target binding that suggests an unusual mechanism of antiviral activity. Antiviral Res. 159, 84–94.
| Novel cytomegalovirus-inhibitory compounds of the class pyrrolopyridines show a complex pattern of target binding that suggests an unusual mechanism of antiviral activity.Crossref | GoogleScholarGoogle Scholar | 30268914PubMed |
Hamilton, S. T., Scott, G., Naing, Z., Iwasenko, J., Hall, B., Graf, N., Arbuckle, S., Craig, M. E., and Rawlinson, W. D. (2012). Human cytomegalovirus-induces cytokine changes in the placenta with implications for adverse pregnancy outcomes. PLoS One 7, e52899.
| Human cytomegalovirus-induces cytokine changes in the placenta with implications for adverse pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 23300810PubMed |
Hamilton, S. T., Hutterer, C., Egilmezer, E., Steingruber, M., Milbradt, J., Marschall, M., and Rawlinson, W. D. (2018). Human cytomegalovirus utilises cellular dual-specificity tyrosine phosphorylation-regulated kinases during placental replication. Placenta 72–73, 10–19.
| Human cytomegalovirus utilises cellular dual-specificity tyrosine phosphorylation-regulated kinases during placental replication.Crossref | GoogleScholarGoogle Scholar | 30501876PubMed |
Harvey, A. J., Kind, K. L., Pantaleon, M., Armstrong, D. T., and Thompson, J. G. (2004). Oxygen-regulated gene expression in bovine blastocysts. Biol. Reprod. 71, 1108–1119.
| Oxygen-regulated gene expression in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 15163614PubMed |
Harvey, A. J., Rathjen, J., and Gardner, D. K. (2016a). Metaboloepigenetic regulation of pluripotent stem cells. Stem Cells Int. 2016, 1816525.
| Metaboloepigenetic regulation of pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 26839556PubMed |
Harvey, A. J., Rathjen, J., Yu, L. J., and Gardner, D. K. (2016b). Oxygen modulates human embryonic stem cell metabolism in the absence of changes in self-renewal. Reprod. Fertil. Dev. 28, 446–458.
| Oxygen modulates human embryonic stem cell metabolism in the absence of changes in self-renewal.Crossref | GoogleScholarGoogle Scholar | 25145274PubMed |
Harvey, A. J., O’Brien, C., Lambshead, J., Sheedy, J. R., Rathjen, J., Laslett, A. L., and Gardner, D. K. (2018). Physiological oxygen culture reveals retention of metabolic memory in human induced pluripotent stem cells. PLoS One 13, e0193949.
| Physiological oxygen culture reveals retention of metabolic memory in human induced pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 29543848PubMed |
Higgins, J. S., Vaughan, O. R., Fernandez de Liger, E., Fowden, A. L., and Sferruzzi-Perri, A. N. (2016). Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy. J. Physiol. 594, 1341–1356.
| Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy.Crossref | GoogleScholarGoogle Scholar | 26377136PubMed |
Horne, A. W., Saunders, P. T. K., Abokhrais, I. M., Hogg, L., Group Endometriosis Priority Setting Partnership Steering (2017). Top ten endometriosis research priorities in the UK and Ireland. Lancet 389, 2191–2192.
| Top ten endometriosis research priorities in the UK and Ireland.Crossref | GoogleScholarGoogle Scholar | 28528751PubMed |
Hutterer, C., Hamilton, S., Steingruber, M., Zeittrager, I., Bahsi, H., Thuma, N., Naing, Z., Orfi, Z., Orfi, L., Socher, E., Sticht, H., Rawlinson, W., Chou, S., Haupt, V. J., and Marschall, M. (2016). The chemical class of quinazoline compounds provides a core structure for the design of anticytomegaloviral kinase inhibitors. Antiviral Res. 134, 130–143.
| The chemical class of quinazoline compounds provides a core structure for the design of anticytomegaloviral kinase inhibitors.Crossref | GoogleScholarGoogle Scholar | 27515131PubMed |
Huynh, K. T., van Zuylen, W. J., Ford, C. E., and Rawlinson, W. D. (2019). Selective modulation of Wnt-binding receptor tyrosine kinase ROR2 expression by human cytomegalovirus regulates trophoblast migration. J. Gen. Virol. 100, 99–104.
| Selective modulation of Wnt-binding receptor tyrosine kinase ROR2 expression by human cytomegalovirus regulates trophoblast migration.Crossref | GoogleScholarGoogle Scholar | 30431423PubMed |
James, J. L., Saghian, R., Perwick, R., and Clark, A. R. (2018). Trophoblast plugs: impact on utero-placental haemodynamics and spiral artery remodelling. Hum. Reprod. 33, 1430–1441.
| Trophoblast plugs: impact on utero-placental haemodynamics and spiral artery remodelling.Crossref | GoogleScholarGoogle Scholar | 29955830PubMed |
Jeng, H. A. (2014). Exposure to endocrine disrupting chemicals and male reproductive health. Front. Public Health 2, 55.
| Exposure to endocrine disrupting chemicals and male reproductive health.Crossref | GoogleScholarGoogle Scholar | 24926476PubMed |
Kenneson, A., and Cannon, M. J. (2007). Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev. Med. Virol. 17, 253–276.
| Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection.Crossref | GoogleScholarGoogle Scholar | 17579921PubMed |
Koot, Y. E. M., Teklenburg, G., Salker, M. S., Brosens, J. J., and Macklon, N. S. (2012). Molecular aspects of implantation failure. Biochim Biophys Acta. 1822, 1943–1950.
| Molecular aspects of implantation failure.Crossref | GoogleScholarGoogle Scholar |
Kropp, J., Salih, S. M., and Khatib, H. (2014). Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front. Genet. 5, 91.
| Expression of microRNAs in bovine and human pre-implantation embryo culture media.Crossref | GoogleScholarGoogle Scholar | 24795753PubMed |
Lagesson, A., Saaristo, M., Brodin, T., Fick, J., Klaminder, J., Martin, J. M., and Wong, B. B. M. (2019). Fish on steroids: temperature-dependent effects of 17beta-trenbolone on predator escape, boldness, and exploratory behaviors. Environ. Pollut. 245, 243–252.
| Fish on steroids: temperature-dependent effects of 17beta-trenbolone on predator escape, boldness, and exploratory behaviors.Crossref | GoogleScholarGoogle Scholar | 30423539PubMed |
Lane, M., and Gardner, D. K. (1996). Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum. Reprod. 11, 1975–1978.
| Selection of viable mouse blastocysts prior to transfer using a metabolic criterion.Crossref | GoogleScholarGoogle Scholar | 8921074PubMed |
Lees, J. G., Rathjen, J., Sheedy, J. R., Gardner, D. K., and Harvey, A. J. (2015). Distinct profiles of human embryonic stem cell metabolism and mitochondria identified by oxygen. Reproduction 150, 367–382.
| Distinct profiles of human embryonic stem cell metabolism and mitochondria identified by oxygen.Crossref | GoogleScholarGoogle Scholar | 26159831PubMed |
Lees, J. G., Gardner, D. K., and Harvey, A. J. (2017). Pluripotent stem cell metabolism and mitochondria: beyond ATP. Stem Cells Int. 2017, 2874283.
| Pluripotent stem cell metabolism and mitochondria: beyond ATP.Crossref | GoogleScholarGoogle Scholar | 28804500PubMed |
Lees, J. G., Gardner, D. K., and Harvey, A. J. (2018). Mitochondrial and glycolytic remodeling during nascent neural differentiation of human pluripotent stem cells. Development 145, dev168997.
| Mitochondrial and glycolytic remodeling during nascent neural differentiation of human pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 30266828PubMed |
Lees, J. G., Cliff, T. S., Gammilonghi, A., Ryall, J. G., Dalton, S., Gardner, D. K., and Harvey, A. J. (2019). Oxygen regulates human pluripotent stem cell metabolic flux. Stem Cells Int. 2019, 8195614.
| Oxygen regulates human pluripotent stem cell metabolic flux.Crossref | GoogleScholarGoogle Scholar | 31641358PubMed |
Manikkam, M., Tracey, R., Guerrero-Bosagna, C., and Skinner, M. K. (2012). Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS One 7, e46249.
| Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations.Crossref | GoogleScholarGoogle Scholar | 23049995PubMed |
Maxwell, S. M., Colls, P., Hodes-Wertz, B., McCulloh, D. H., McCaffrey, C., Wells, D., Munne, S., and Grifo, J. A. (2016). Why do euploid embryos miscarry? A case-control study comparing the rate of aneuploidy within presumed euploid embryos that resulted in miscarriage or live birth using next-generation sequencing. Fertil. Steril. 106, 1414–1419e5.
| Why do euploid embryos miscarry? A case-control study comparing the rate of aneuploidy within presumed euploid embryos that resulted in miscarriage or live birth using next-generation sequencing.Crossref | GoogleScholarGoogle Scholar | 27692437PubMed |
McPherson, N. O., and Lane, M. (2015). Male obesity and subfertility, is it really about increased adiposity? Asian J. Androl. 17, 450–458.
| 25652636PubMed |
Meseguer, M., Herrero, J., Tejera, A., Hilligsoe, K. M., Ramsing, N. B., and Remohi, J. (2011). The use of morphokinetics as a predictor of embryo implantation. Hum. Reprod. 26, 2658–2671.
| The use of morphokinetics as a predictor of embryo implantation.Crossref | GoogleScholarGoogle Scholar | 21828117PubMed |
Morris, S. A., Grewal, S., Barrios, F., Patankar, S. N., Strauss, B., Buttery, L., Alexander, M., Shakesheff, K. M., and Zernicka-Goetz, M. (2012). Dynamics of anterior–posterior axis formation in the developing mouse embryo. Nat. Commun. 3, 673.
| Dynamics of anterior–posterior axis formation in the developing mouse embryo.Crossref | GoogleScholarGoogle Scholar | 22334076PubMed |
Mortlock, S., Restuadi, R., Levien, R., Girling, J. E., Holdsworth-Carson, S. J., Healey, M., Zhu, Z., Qi, T., Wu, Y., Lukowski, S. W., Rogers, P. A. W., Yang, J., McRae, A. F., Fung, J. N., and Montgomery, G. W. (2019). Genetic regulation of methylation in human endometrium and blood and gene targets for reproductive diseases. Clin. Epigenetics 11, 49.
| Genetic regulation of methylation in human endometrium and blood and gene targets for reproductive diseases.Crossref | GoogleScholarGoogle Scholar | 30871624PubMed |
Moussaieff, A., Kogan, N. M., and Aberdam, D. (2015). Concise review: energy metabolites: key mediators of the epigenetic state of pluripotency. Stem Cells 33, 2374–2380.
| Concise review: energy metabolites: key mediators of the epigenetic state of pluripotency.Crossref | GoogleScholarGoogle Scholar | 25873344PubMed |
Nguyen, H. P. T., Xiao, L., Deane, J. A., Tan, K. S., Cousins, F. L., Masuda, H., Sprung, C. N., Rosamilia, A., and Gargett, C. E. (2017). N-Cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays. Hum. Reprod. 32, 2254–2268.
| N-Cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays.Crossref | GoogleScholarGoogle Scholar |
Niakan, K. K., Han, J., Pedersen, R. A., Simon, C., and Pera, R. A. (2012). Human pre-implantation embryo development. Development 139, 829–841.
| Human pre-implantation embryo development.Crossref | GoogleScholarGoogle Scholar | 22318624PubMed |
Nilsson, E. E., Sadler-Riggleman, I., and Skinner, M. K. (2018). Environmentally induced epigenetic transgenerational inheritance of disease. Environ. Epigenet. 4, dvy016.
| Environmentally induced epigenetic transgenerational inheritance of disease.Crossref | GoogleScholarGoogle Scholar | 30038800PubMed |
Norwitz, E. R., Schust, D. J., and Fisher, S. J. (2001). Implantation and the survival of early pregnancy. N. Engl. J. Med. 345, 1400–1408.
| Implantation and the survival of early pregnancy.Crossref | GoogleScholarGoogle Scholar | 11794174PubMed |
Ohnesorg, T., Vilain, E., and Sinclair, A. H. (2014). The genetics of disorders of sex development in humans. Sex Dev. 8, 262–272.
| The genetics of disorders of sex development in humans.Crossref | GoogleScholarGoogle Scholar | 24504012PubMed |
Oud, M. S., Ramos, L., O’Bryan, M. K., McLachlan, R. I., Okutman, Ö., Viville, S., de Vries, P. F., Smeets, D. F. C. M., Lugtenberg, D., Hehir-Kwa, J. Y., Gilissen, C., van de Vorst, M., Vissers, L. E. L. M., Hoischen, A., Meijerink, A. M., Fleischer, K., Veltman, J. A., and Noordam, M. J. (2017). Validation and application of a novel integrated genetic screening method to a cohort of 1,112 men with idiopathic azoospermia or severe oligozoospermia. Hum. Mutat. 38, 1592–1605.
| Validation and application of a novel integrated genetic screening method to a cohort of 1,112 men with idiopathic azoospermia or severe oligozoospermia.Crossref | GoogleScholarGoogle Scholar | 28801929PubMed |
Palmer, N. O., Bakos, H. W., Owens, J. A., Setchell, B. P., and Lane, M. (2012). Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am. J. Physiol. Endocrinol. Metab. 302, E768–E780.
| Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function.Crossref | GoogleScholarGoogle Scholar | 22252945PubMed |
Pauli, E. M., Legro, R. S., Demers, L. M., Kunselman, A. R., Dodson, W. C., and Lee, P. A. (2008). Diminished paternity and gonadal function with increasing obesity in men. Fertil. Steril. 90, 346–351.
| Diminished paternity and gonadal function with increasing obesity in men.Crossref | GoogleScholarGoogle Scholar | 18291378PubMed |
Paulozzi, L. J., Erickson, J. D., and Jackson, R. J. (1997). Hypospadias trends in two US surveillance systems. Pediatrics 100, 831–834.
| Hypospadias trends in two US surveillance systems.Crossref | GoogleScholarGoogle Scholar | 9346983PubMed |
Rawlinson, W. D., Boppana, S. B., Fowler, K. B., Kimberlin, D. W., Lazzarotto, T., Alain, S., Daly, K., Doutre, S., Gibson, L., Giles, M. L., Greenlee, J., Hamilton, S. T., Harrison, G. J., Hui, L., Jones, C. A., Palasanthiran, P., Schleiss, M. R., Shand, A. W., and van Zuylen, W. J. (2017). Congenital cytomegalovirus infection in pregnancy and the neonate: consensus recommendations for prevention, diagnosis, and therapy. Lancet Infect. Dis. 17, e177–e188.
| Congenital cytomegalovirus infection in pregnancy and the neonate: consensus recommendations for prevention, diagnosis, and therapy.Crossref | GoogleScholarGoogle Scholar | 28291720PubMed |
Rehman, S., Usman, Z., Rehman, S., AlDraihem, M., Rehman, N., Rehman, I., and Ahmad, G. (2018). Endocrine disrupting chemicals and impact on male reproductive health. Transl. Androl. Urol. 7, 490–503.
| Endocrine disrupting chemicals and impact on male reproductive health.Crossref | GoogleScholarGoogle Scholar | 30050807PubMed |
Revel, A., Achache, H., Stevens, J., Smith, Y., and Reich, R. (2011). MicroRNAs are associated with human embryo implantation defects. Hum. Reprod. 26, 2830–2840.
| MicroRNAs are associated with human embryo implantation defects.Crossref | GoogleScholarGoogle Scholar | 21849299PubMed |
Rier, S., and Foster, W. G. (2002). Environmental dioxins and endometriosis. Toxicol. Sci. 70, 161–170.
| Environmental dioxins and endometriosis.Crossref | GoogleScholarGoogle Scholar | 12441361PubMed |
Rogers, P. A., Adamson, G. D., Al-Jefout, M., Becker, C. M., D’Hooghe, T. M., Dunselman, G. A., Fazleabas, A., Giudice, L. C., Horne, A. W., Hull, M. L., Hummelshoj, L., Missmer, S. A., Montgomery, G. W., Stratton, P., Taylor, R. N., Rombauts, L., Saunders, P. T., Vincent, K., Zondervan, K. T., Wes Werf Consortium for Research Priorities in Endometriosis (2017). Research priorities for endometriosis. Reprod. Sci. 24, 202–226.
| Research priorities for endometriosis.Crossref | GoogleScholarGoogle Scholar | 27368878PubMed |
Rosenbluth, E. M., Shelton, D. N., Wells, L. M., Sparks, A. E., and Van Voorhis, B. J. (2014). Human embryos secrete microRNAs into culture media – a potential biomarker for implantation. Fertil. Steril. 101, 1493–1500.
| Human embryos secrete microRNAs into culture media – a potential biomarker for implantation.Crossref | GoogleScholarGoogle Scholar | 24786747PubMed |
Saghian, R., Bogle, G., James, J. L., and Clark, A. R. (2019). Establishment of maternal blood supply to the placenta: insights into plugging, unplugging and trophoblast behaviour from an agent-based model. Interface Focus 9, 20190019.
| Establishment of maternal blood supply to the placenta: insights into plugging, unplugging and trophoblast behaviour from an agent-based model.Crossref | GoogleScholarGoogle Scholar | 31485310PubMed |
Sferruzzi-Perri, A. N., Lopez-Tello, J., Fowden, A. L., and Constancia, M. (2016). Maternal and fetal genomes interplay through phosphoinositol 3-kinase(PI3K)–p110alpha signaling to modify placental resource allocation. Proc. Natl Acad. Sci. USA 113, 11255–11260.
| Maternal and fetal genomes interplay through phosphoinositol 3-kinase(PI3K)–p110alpha signaling to modify placental resource allocation.Crossref | GoogleScholarGoogle Scholar | 27621448PubMed |
Sferruzzi-Perri, A. N., Sandovici, I., Constancia, M., and Fowden, A. L. (2017). Placental phenotype and the insulin-like growth factors: resource allocation to fetal growth. J. Physiol. 595, 5057–5093.
| Placental phenotype and the insulin-like growth factors: resource allocation to fetal growth.Crossref | GoogleScholarGoogle Scholar | 28337745PubMed |
Sferruzzi-Perri, A. N., Higgins, J. S., Vaughan, O. R., Murray, A. J., and Fowden, A. L. (2019). Placental mitochondria adapt developmentally and in response to hypoxia to support fetal growth. Proc. Natl Acad. Sci. USA 116, 1621–1626.
| Placental mitochondria adapt developmentally and in response to hypoxia to support fetal growth.Crossref | GoogleScholarGoogle Scholar | 30655345PubMed |
Shayeb, A. G., Harrild, K., Mathers, E., and Bhattacharya, S. (2011). An exploration of the association between male body mass index and semen quality. Reprod. Biomed. Online 23, 717–723.
| An exploration of the association between male body mass index and semen quality.Crossref | GoogleScholarGoogle Scholar | 22019618PubMed |
Shyh-Chang, N., and Daley, G. Q. (2015). Metabolic switches linked to pluripotency and embryonic stem cell differentiation. Cell Metab. 21, 349–350.
| Metabolic switches linked to pluripotency and embryonic stem cell differentiation.Crossref | GoogleScholarGoogle Scholar | 25738450PubMed |
Simon, A., and Laufer, N. (2012). Assessment and treatment of repeated implantation failure (RIF). J. Assist. Reprod. Genet. 29, 1227–1239.
| Assessment and treatment of repeated implantation failure (RIF).Crossref | GoogleScholarGoogle Scholar | 22976427PubMed |
Simsa, P., Mihalyi, A., Schoeters, G., Koppen, G., Kyama, C. M., Den Hond, E. M., Fulop, V., and D’Hooghe, T. M. (2010). Increased exposure to dioxin-like compounds is associated with endometriosis in a case-control study in women. Reprod. Biomed. Online 20, 681–688.
| Increased exposure to dioxin-like compounds is associated with endometriosis in a case-control study in women.Crossref | GoogleScholarGoogle Scholar | 20211585PubMed |
Spyrou, J., Gardner, D. K., and Harvey, A. J. (2019). Metabolomic and transcriptional analyses reveal atmospheric oxygen during human induced pluripotent stem cell generation impairs metabolic reprogramming. Stem Cells 37, 1042–1056.
| Metabolomic and transcriptional analyses reveal atmospheric oxygen during human induced pluripotent stem cell generation impairs metabolic reprogramming.Crossref | GoogleScholarGoogle Scholar | 31042329PubMed |
Stewart, T. M., Liu, D. Y., Garrett, C., Jorgensen, N., Brown, E. H., and Baker, H. W. (2009). Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum. Reprod. 24, 1561–1568.
| Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output.Crossref | GoogleScholarGoogle Scholar | 19351657PubMed |
Suda, K., Nakaoka, H., Yoshihara, K., Ishiguro, T., Tamura, R., Mori, Y., Yamawaki, K., Adachi, S., Takahashi, T., Kase, H., Tanaka, K., Yamamoto, T., Motoyama, T., Inoue, I., and Enomoto, T. (2018). Clonal expansion and diversification of cancer-associated mutations in endometriosis and normal endometrium. Cell Rep. 24, 1777–1789.
| Clonal expansion and diversification of cancer-associated mutations in endometriosis and normal endometrium.Crossref | GoogleScholarGoogle Scholar | 30110635PubMed |
Takai, Y., and Nakanishi, H. (2003). Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116, 17–27.
| Nectin and afadin: novel organizers of intercellular junctions.Crossref | GoogleScholarGoogle Scholar | 12456712PubMed |
Takai, Y., Irie, K., Shimizu, K., Sakisaka, T., and Ikeda, W. (2003). Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci. 94, 655–667.
| Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization.Crossref | GoogleScholarGoogle Scholar | 12901789PubMed |
Takai, Y., Miyoshi, J., Ikeda, W., and Ogita, H. (2008). Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 9, 603.
| Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation.Crossref | GoogleScholarGoogle Scholar | 18648374PubMed |
Tan, B. K., Vandekerckhove, P., Kennedy, R., and Keay, S. D. (2005). Investigation and current management of recurrent IVF treatment failure in the UK. BJOG 112, 773–780.
| Investigation and current management of recurrent IVF treatment failure in the UK.Crossref | GoogleScholarGoogle Scholar | 15924536PubMed |
Tarrade, A., Panchenko, P., Junien, C., and Gabory, A. (2015). Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J. Exp. Biol. 218, 50–58.
| Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism.Crossref | GoogleScholarGoogle Scholar | 25568451PubMed |
Tomkins, P., Saaristo, M., Allinson, M., and Wong, B. B. M. (2016). Exposure to an agricultural contaminant, 17beta-trenbolone, impairs female mate choice in a freshwater fish. Aquat. Toxicol. 170, 365–370.
| Exposure to an agricultural contaminant, 17beta-trenbolone, impairs female mate choice in a freshwater fish.Crossref | GoogleScholarGoogle Scholar | 26466515PubMed |
Turco, M. Y., Gardner, L., Hughes, J., Cindrova-Davies, T., Gomez, M. J., Farrell, L., Hollinshead, M., Marsh, S. G. E., Brosens, J. J., Critchley, H. O., Simons, B. D., Hemberger, M., Koo, B. K., Moffett, A., and Burton, G. J. (2017). Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat. Cell Biol. 19, 568–577.
| Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium.Crossref | GoogleScholarGoogle Scholar | 28394884PubMed |
Valentijn, A. J., Palial, K., Al-Lamee, H., Tempest, N., Drury, J., Von Zglinicki, T., Saretzki, G., Murray, P., Gargett, C. E., and Hapangama, D. K. (2013). SSEA-1 isolates human endometrial basal glandular epithelial cells: phenotypic and functional characterization and implications in the pathogenesis of endometriosis. Hum. Reprod. 28, 2695–2708.
| SSEA-1 isolates human endometrial basal glandular epithelial cells: phenotypic and functional characterization and implications in the pathogenesis of endometriosis.Crossref | GoogleScholarGoogle Scholar | 23847113PubMed |
Walker, K. F., Cohen, A. L., Walker, S. H., Allen, K. M., Baines, D. L., and Thornton, J. G. (2014). The dangers of the day of birth. BJOG 121, 714–718.
| The dangers of the day of birth.Crossref | GoogleScholarGoogle Scholar | 24521517PubMed |
Winship, A., Ton, A., Van Sinderen, M., Menkhorst, E., Rainczuk, K., Griffiths, M., Cuman, C., and Dimitriadis, E. (2018). Mouse double minute homologue 2 (MDM2) downregulation by miR-661 impairs human endometrial epithelial cell adhesive capacity. Reprod. Fertil. Dev. 30, 477–486.
| Mouse double minute homologue 2 (MDM2) downregulation by miR-661 impairs human endometrial epithelial cell adhesive capacity.Crossref | GoogleScholarGoogle Scholar | 28847363PubMed |
Yang, B., Chen, R., Liang, X., Shi, J., Wu, X., Zhang, Z., and Chen, X. (2019). Estrogen enhances endometrial cancer cells proliferation by upregulation of prohibitin. J. Cancer 10, 1616–1621.
| Estrogen enhances endometrial cancer cells proliferation by upregulation of prohibitin.Crossref | GoogleScholarGoogle Scholar | 31205517PubMed |
Zhang, J., Khvorostov, I., Hong, J. S., Oktay, Y., Vergnes, L., Nuebel, E., Wahjudi, P. N., Setoguchi, K., Wang, G., Do, A., Jung, H. J., McCaffery, J. M., Kurland, I. J., Reue, K., Lee, W. N., Koehler, C. M., and Teitell, M. A. (2011). UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 30, 4860–4873.
| UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 22085932PubMed |
Zhao, Y., Zacur, H., Cheadle, C., Ning, N., Fan, J., and Vlahos, N. F. (2012). Effect of luteal-phase support on endometrial microRNA expression following controlled ovarian stimulation. Reprod. Biol. Endocrinol. 10, 72.
| Effect of luteal-phase support on endometrial microRNA expression following controlled ovarian stimulation.Crossref | GoogleScholarGoogle Scholar | 22950660PubMed |
Zinaman, M. J., Clegg, E. D., Brown, C. C., O’Connor, J., and Selevan, S. G. (1996). Estimates of human fertility and pregnancy loss. Fertil. Steril. 65, 503–509.
| Estimates of human fertility and pregnancy loss.Crossref | GoogleScholarGoogle Scholar | 8774277PubMed |
