Gender inequality persists in all sectors of society, including science and medicine disciplines. While female clinicians and researchers are increasing in number[1], they remain underrepresented in scholarly publications and academic positions[2]. Although nearly 50% of medical school graduates are women, they continue to hold fewer senior academic positions and tenured faculty posts than their male counterparts, and receive less federal grant money than men[3].
Endocrinology combines fundamental scientific discovery and medical care that greatly influence human health. Publication of research is necessary to advance our understanding of endocrine science; however, women remain a minority as first and senior authors in endocrinology publications. This special thematic issue focuses on recent research performed and published by women in endocrinology and highlights the influence that their work has had on fellow scientists and clinicians today.
All papers were nominated by members of the scientific community and are from current, early-career or established, well-known or up-and-coming academics from the US or international research community. These studies were published by laboratory groups led by established female researchers or were projects spearheaded by women just starting out in their scientific careers. Over 30 articles were nominated, and the 12 most influential, high-impact research papers were selected to represent the spectrum of basic through clinical research, geographical diversity, and career stage.
Topics covered include ground-breaking studies of single-cell RNA sequencing in the pituitary gland, innovative technology used to record neuronal activity in free moving animals, the impact of gut microbes on PCOS, and much more. We hope you enjoy this collection of papers celebrating female researchers and their achievements in endocrinology.
Thank you to the Selection Panel for their time and attention in putting together this inspiring collection of papers:
Zane Andrews, PhD, Monash University
Kristy A. Brown, PhD, Cornell University
Ghada El-Hajj Fuleihan, MD, MPH, American University of Beirut
Ana Claudia Latronico, MD, PhD, University of Sao Paulo
Daniel I. Spratt, MD, MaineHealth
Jenny Visser, PhD, Erasmus MC
Whitney Woodmansee, MD, University of Florida Health
Joy Wu, MD, PhD, Stanford University
Top 12 Papers
Su Young Han, Grace Kane, Isaiah Cheong, Allan E Herbison; Characterization of GnRH Pulse Generator Activity in Male Mice Using GCaMP Fiber Photometry, Endocrinology, Volume 160, Issue 3, 1 March 2019, Pages 557–567, https://doi.org/10.1210/en.2018-01047
“The first author of this paper, Su Han, has pioneered the use of fibre photometry to measure activity of kisspeptin neurons in vivo in conscious, freely behaving animals. This paper documents some of that work, and is a really excellent example of how technical innovation is revolutionising our ability to study classical neuroendocrine systems.”
Arthi Thirumalai, Jonas Ceponis, John K Amory, Ronald Swerdloff, Vijaya Surampudi, Peter Y Liu, William J Bremner, Eric Harvey, Diana L Blithe, Min S Lee, Laura Hull, Christina Wang, Stephanie T Page; Effects of 28 Days of Oral Dimethandrolone Undecanoate in Healthy Men: A Prototype Male Pill, The Journal of Clinical Endocrinology & Metabolism, Volume 104, Issue 2, 1 February 2019, Pages 423–432, https://doi.org/10.1210/jc.2018-01452
“Drs. Stephanie Page and Christina Wang are international leaders in the area of hormonal male contraception…(this paper) reports on promising novel compounds as potential hormonal male contraceptive agents.”
Thu H Truong, Amy R Dwyer, Caroline H Diep, Hsiangyu Hu, Kyla M Hagen, Carol A Lange; Phosphorylated Progesterone Receptor Isoforms Mediate Opposing Stem Cell and Proliferative Breast Cancer Cell Fates, Endocrinology, Volume 160, Issue 2, 1 February 2019, Pages 430–446, https://doi.org/10.1210/en.2018-00990
Leonard Y M Cheung, Akima S George, Stacey R McGee, Alexandre Z Daly, Michelle L Brinkmeier, Buffy S Ellsworth, Sally A Camper; Single-Cell RNA Sequencing Reveals Novel Markers of Male Pituitary Stem Cells and Hormone-Producing Cell Types, Endocrinology, Volume 159, Issue 12, 1 December 2018, Pages 3910–3924, https://doi.org/10.1210/en.2018-00750
“This is the first paper describing single cell RNA sequencing in the pituitary. It is groundbreaking work that will serve as the backbone for new cell type identification and should become a highly cited publication. I have looked at it weekly since it was published and get something new from it each time.”
Edgar D Torres Fernandez, Kristen V Adams, Maryam Syed, Rodrigo O Maranon, Damian G Romero, Licy L Yanes Cardozo; Long-Lasting Androgen-Induced Cardiometabolic Effects in Polycystic Ovary Syndrome, Journal of the Endocrine Society, Volume 2, Issue 8, 1 August 2018, Pages 949–964, https://doi.org/10.1210/js.2018-00131
“This manuscript strongly suggests that time is of the essence to normalize androgen levels in PCOS and other androgen excess pathological conditions because, once cardiometabolic dysregulations have been established, normalization of the androgenic profile may have little beneficial effect.”
Katja Kiseljak-Vassiliades, Yu Zhang, Adwitiya Kar, Raud Razzaghi, Mei Xu, Katherine Gowan, Christopher D Raeburn, Maria Albuja-Cruz, Kenneth L Jones, Hilary Somerset, Lauren Fishbein, Stephen Leong, Margaret E Wierman; Elucidating the Role of the Maternal Embryonic Leucine Zipper Kinase in Adrenocortical Carcinoma, Endocrinology, Volume 159, Issue 7, 1 July 2018, Pages 2532–2544, https://doi.org/10.1210/en.2018-00310
Marjoleine F Broekema, Danielle A A Hollman, Arjen Koppen, Henk-Jan van den Ham, Diana Melchers, Dirk Pijnenburg, Rob Ruijtenbeek, Saskia W C van Mil, René Houtman, Eric Kalkhoven; Profiling of 3696 Nuclear Receptor–Coregulator Interactions: A Resource for Biological and Clinical Discovery, Endocrinology, Volume 159, Issue 6, 1 June 2018, Pages 2397–2407, https://doi.org/10.1210/en.2018-00149
Pedro J Torres, Martyna Siakowska, Beata Banaszewska, Leszek Pawelczyk, Antoni J Duleba, Scott T Kelley, Varykina G Thackray; Gut Microbial Diversity in Women With Polycystic Ovary Syndrome Correlates With Hyperandrogenism, The Journal of Clinical Endocrinology & Metabolism, Volume 103, Issue 4, 1 April 2018, Pages 1502–1511, https://doi.org/10.1210/jc.2017-02153
“This paper showed that women who have polycystic ovary syndrome (PCOS), a common hormone condition that contributes to infertility and metabolic problems, have less diverse gut bacteria than women who do not have the condition and that this trend is linked with elevated testosterone levels. This study is impactful because it suggests that testosterone may alter the gut microbiome in women with PCOS, and these changes may influence the development of PCOS and the impact it has on a women’s health and quality of life. This study highlights the intriguing possibility that gut microbes may be involved in the pathophysiology of PCOS and that modulation of the gut microbiome may offer a potential pathway to develop novel treatments for PCOS.”
Cetewayo S Rashid, Yu-Chin Lien, Amita Bansal, Lane J Jaeckle-Santos, Changhong Li, Kyoung-Jae Won, Rebecca A Simmons; Transcriptomic Analysis Reveals Novel Mechanisms Mediating Islet Dysfunction in the Intrauterine Growth–Restricted Rat, Endocrinology, Volume 159, Issue 2, 1 February 2018, Pages 1035–1049, https://doi.org/10.1210/en.2017-00888
“This is a very nice approach to develop hypotheses regarding the developmental origins of adult metabolic disease, as confirmed in islets from human patients with type 2 diabetes.”
Tamara J Vokes, Michael Mannstadt, Michael A Levine, Bart L Clarke, Peter Lakatos, Kristina Chen, Rebecca Piccolo, Alan Krasner, Dolores M Shoback, John P Bilezikian; Recombinant Human Parathyroid Hormone Effect on Health-Related Quality of Life in Adults With Chronic Hypoparathyroidism, The Journal of Clinical Endocrinology & Metabolism, Volume 103, Issue 2, 1 February 2018, Pages 722–731, https://doi.org/10.1210/jc.2017-01471
“I believe this is very important work on a rare endocrine disease and for patients who often suffer from poor quality of life. Clinicians, including myself, struggle with who are the best candidates for rhPTH. This paper lends very important insights that are likely much more important to patients than simple biochemical variables.”
Stina Rikke Jensen, Sarah E Wheeler, Henning Hvid, Jonas Ahnfelt-Rønne, Bo Falck Hansen, Erica Nishimura, Grith Skytte Olsen, Patricia L Brubaker; Elucidating the Biological Roles of Insulin and Its Receptor in Murine Intestinal Growth and Function, Endocrinology, Volume 158, Issue 8, 1 August 2017, Pages 2453–2469, https://doi.org/10.1210/en.2017-00195
“(This paper) showed for the first time that the villin-cre construct used to generate the mouse line demonstrated a phenotype that was independent of the knockout – others have since gone on to show this but, in the meantime, many labs continue to exclude the villin-cre mice alone as controls, which is wrong!”
Nayara S. S. Aquino, Roberta Araujo-Lopes, Patricia C. Henriques, Felipe E. F. Lopes, Daniela O. Gusmao, Candido C. Coimbra, Celso R. Franci, Adelina M. Reis, Raphael E. Szawka; α-Estrogen and Progesterone Receptors Modulate Kisspeptin Effects on Prolactin: Role in Estradiol-Induced Prolactin Surge in Female Rats, Endocrinology, Volume 158, Issue 6, 1 June 2017, Pages 1812–1826, https://doi.org/10.1210/en.2016-1855
“The first author in this paper, Nayara Aquino, was a PhD student at the time of writing it…this work characterises a little known additional function of kisspeptin, contributing to the control of prolactin secretion. It highlights that this population of neurons has a wider range of functions than is currently appreciated.”
All Nominated Papers
Mariana Quiroz-Munoz, Sudeh Izadmehr, Dushyanthy Arumugam, Beatrice Wong, Alexander Kirschenbaum, Alice C Levine; Mechanisms of Osteoblastic Bone Metastasis in Prostate Cancer: Role of Prostatic Acid Phosphatase, Journal of the Endocrine Society, https://doi.org/10.1210/js.2018-00425
Irene T Lee, Alexandria Atuahene, Hale Ergin Egritag, Ling Wang, Michael Donovan, Christoph Buettner, Eliza B Geer; Active Cushing’s Disease is Characterized by Increased Adipose Tissue Macrophage Presence, The Journal of Clinical Endocrinology & Metabolism, https://doi.org/10.1210/jc.2018-02552
Jerilynn C Prior; Progesterone Is Important for Transgender Women’s Therapy—Applying Evidence for the Benefits of Progesterone in Ciswomen, The Journal of Clinical Endocrinology & Metabolism, Volume 104, Issue 4, 1 April 2019, Pages 1181–1186, https://doi.org/10.1210/jc.2018-01777
Aya T Nanba, Taweesak Wannachalee, James J Shields, James B Byrd, William E Rainey, Richard J Auchus, Adina F Turcu; Adrenal Vein Sampling Lateralization Despite Mineralocorticoid Receptor Antagonists Exposure in Primary Aldosteronism, The Journal of Clinical Endocrinology & Metabolism, Volume 104, Issue 2, 1 February 2019, Pages 487–492, https://doi.org/10.1210/jc.2018-01299
Bob Z Sun, Tairmae Kangarloo, Judith M Adams, Patrick M Sluss, Corrine K Welt, Donald W Chandler, David T Zava, John A McGrath, David M Umbach, Janet E Hall, Natalie D Shaw; Healthy Post-Menarchal Adolescent Girls Demonstrate Multi-Level Reproductive Axis Immaturity, The Journal of Clinical Endocrinology & Metabolism, Volume 104, Issue 2, 1 February 2019, Pages 613–623, https://doi.org/10.1210/jc.2018-00595
“This was a remarkable paper that is slated to be a landmark study of adolescent anovulation for many reasons. 1) This paper convincingly teaches us that many menstrual cycles that would have been labeled anovulatory by previous studies are actually ovulatory cycles with a short luteal phase… 2) The methodology was exemplary and meticulous: ovulatory cycles were defined by rigorous, exemplary experimentally determined criteria involving LH, E2, and ultrasound, and the day of ovulation was defined by rigorous criteria… 3) They report, for the first time, 2 cases of unruptured corpus lutea among the anovulatory adolescents, which places this abnormality at the extreme end of the luteal insufficiency spectrum. 4) Salivary progesterone was found to be an unreliable method for classifying cycles as ovulatory when compared to sensitive serum progesterone assay results.”
Mita Varghese, Cameron Griffin, Kaitlin McKernan, Leila Eter, Nicholas Lanzetta, Devyani Agarwal, Simin Abrishami, Kanakadurga Singer; Sex Differences in Inflammatory Responses to Adipose Tissue Lipolysis in Diet-Induced Obesity, Endocrinology, Volume 160, Issue 2, 1 February 2019, Pages 293–312, https://doi.org/10.1210/en.2018-00797
Natalie M Hohos, Kirstin J Cho, Delaney C Swindle, Amanda A Allshouse, Michael C Rudolph, Malgorzata E Skaznik-Wikiel; Fat-1 Transgene Is Associated With Improved Reproductive Outcomes, Endocrinology, Volume 159, Issue 12, 1 December 2018, Pages 3981–3992, https://doi.org/10.1210/en.2018-00723
Emily Qualls-Creekmore, Heike Münzberg; Modulation of Feeding and Associated Behaviors by Lateral Hypothalamic Circuits, Endocrinology, Volume 159, Issue 11, 1 November 2018, Pages 3631–3642, https://doi.org/10.1210/en.2018-00449
Aleisha M Moore, Mel Prescott, Katja Czieselsky, Elodie Desroziers, Siew Hoong Yip, Rebecca E Campbell, Allan E Herbison; Synaptic Innervation of the GnRH Neuron Distal Dendron in Female Mice, Endocrinology, Volume 159, Issue 9, 1 September 2018, Pages 3200–3208, https://doi.org/10.1210/en.2018-00505
“The first author in this paper, Aleisha Moore, was a Ph.D. student working with Rebecca Campbell at the University of Otago. This paper provided the anatomical proof that GnRH neurons can be regulated by synaptic inputs very near the nerve terminal (as opposed to inputs onto classical dendrites or cell bodies), changing the way that we think about the anatomy of these unusual neurosecretory neurons. Rebecca Campbell, the co-senior author, is an emerging leader in the PCOS field.”
Yuhan Bi, Mengxi Jiang, Weiwei Guo, Xiudong Guan, Meishu Xu, Songrong Ren, Da Yang, Nilesh W Gaikwad, Kyle W Selcer, Wen Xie; Sex-Dimorphic and Sex Hormone–Dependent Role of Steroid Sulfatase in Adipose Inflammation and Energy Homeostasis, Endocrinology, Volume 159, Issue 9, 1 September 2018, Pages 3365–3377, https://doi.org/10.1210/en.2018-00531
Sharon Rachel Ladyman, Zin Khant Aung, David Ross Grattan; Impact of Pregnancy and Lactation on the Long-Term Regulation of Energy Balance in Female Mice, Endocrinology, Volume 159, Issue 6, 1 June 2018, Pages 2324–2336, https://doi.org/10.1210/en.2018-00057
“Most work in this field focuses on the impact of maternal metabolism on the fetus, but Sharon is one of a few whose focus is on the impact of reproduction on metabolic health in the mother. This paper shows that the experience of pregnancy and lactation exerts long term effects on body-weight homeostasis and physical activity in a female. This provides a biological basis to help explain why many mothers report that they gain weight after the birth of their children, and struggle to return to pre-pregnancy body weight.”
Noelle E Gillis, Thomas H Taber, Eric L Bolf, Caitlin M Beaudet, Jennifer A Tomczak, Jeffrey H White, Janet L Stein, Gary S Stein, Jane B Lian, Seth Frietze, Frances E Carr; Thyroid Hormone Receptor β Suppression of RUNX2 Is Mediated by Brahma-Related Gene 1–Dependent Chromatin Remodeling, Endocrinology, Volume 159, Issue 6, 1 June 2018, Pages 2484–2494, https://doi.org/10.1210/en.2018-00128
Laurie L Baggio, Bernardo Yusta, Erin E Mulvihill, Xiemin Cao, Catherine J Streutker, Jagdish Butany, Thomas P Cappola, Kenneth B Margulies, Daniel J Drucker; GLP-1 Receptor Expression Within the Human Heart, Endocrinology, Volume 159, Issue 4, 1 April 2018, Pages 1570–1584, https://doi.org/10.1210/en.2018-00004
“This paper represents the first comprehensive and complete analysis of GLP-1 receptor expression in the human heart, of great clinical interest given findings that GLP-1 receptor agonists are cardioprotective!”
Laura L Burger, Charlotte Vanacker, Chayarndorn Phumsatitpong, Elizabeth R Wagenmaker, Luhong Wang, David P Olson, Suzanne M Moenter; Identification of Genes Enriched in GnRH Neurons by Translating Ribosome Affinity Purification and RNAseq in Mice, Endocrinology, Volume 159, Issue 4, 1 April 2018, Pages 1922–1940, https://doi.org/10.1210/en.2018-00001
“This paper is the first to look at the complement of mRNAs that are translated in GnRH neurons and the response to gonad removal. In addition to finding differences in the way GnRH neurons use fuel with and without gonadal hormones. The data set generated is also a valuable resource for the research community.”
Miriam A Bredella, Melanie Schorr, Laura E Dichtel, Anu V Gerweck, Brian J Young, Whitney W Woodmansee, Brooke Swearingen, Karen K Miller; Body Composition and Ectopic Lipid Changes With Biochemical Control of Acromegaly, The Journal of Clinical Endocrinology & Metabolism, Volume 102, Issue 11, 1 November 2017, Pages 4218–4225, https://doi.org/10.1210/jc.2017-01210
Jennifer A Yang, Christopher I Song, Jessica K Hughes, Michael J Kreisman, Ruby A Parra, Daniel J Haisenleder, Alexander S Kauffman, Kellie M Breen; Acute Psychosocial Stress Inhibits LH Pulsatility and Kiss1 Neuronal Activation in Female Mice, Endocrinology, Volume 158, Issue 11, 1 November 2017, Pages 3716–3723, https://doi.org/10.1210/en.2017-00301
“Dr. Kellie Breen’s research group is making significant advances to our understanding of how stress disrupts reproductive function and fertility… they are the first to demonstrate that acute physiologic challenges, such as stress, can rapidly change luteinizing hormone secretion in the mouse. (This paper) showed that psychosocial stress rapidly inhibits pulsatile LH secretion in female mice and that this suppression is associated with a diminishment in KNDy neural activity and function. These data provide the foundation for examining the anatomical and functional circuits activated by stress as understanding will influence the management of treatments for compromised fertility associated with stress.”
Charlotte Vanacker, Manuel Ricu Moya, R. Anthony DeFazio, Michael L Johnson, Suzanne M Moenter; Long-Term Recordings of Arcuate Nucleus Kisspeptin Neurons Reveal Patterned Activity That Is Modulated by Gonadal Steroids in Male Mice, Endocrinology, Volume 158, Issue 10, 1 October 2017, Pages 3553–3564, https://doi.org/10.1210/en.2017-00382
Tina Constantin, Vin Tangpricha, Reshma Shah, Nelson M. Oyesiku, Octavian C. Ioachimescu, James Ritchie, Adriana G. Ioachimescu; Calcium and Bone Turnover Markers in Acromegaly: A Prospective, Controlled Study, The Journal of Clinical Endocrinology & Metabolism, Volume 102, Issue 7, 1 July 2017, Pages 2416–2424, https://doi.org/10.1210/jc.2016-3693
Rachel J. Fenske, Mark T. Cadena, Quincy E. Harenda, Haley N. Wienkes, Kathryn Carbajal, Michael D. Schaid, Erin Laundre, Allison L. Brill, Nathan A. Truchan, Harpreet Brar, Jaclyn Wisinski, Jinjin Cai, Timothy E. Graham, Feyza Engin, Michelle E. Kimple; The Inhibitory G Protein α-Subunit, Gαz, Promotes Type 1 Diabetes-Like Pathophysiology in NOD Mice, Endocrinology, Volume 158, Issue 6, 1 June 2017, Pages 1645–1658, https://doi.org/10.1210/en.2016-1700
“Rachel’s comprehensive work, which serves as the basis for her PhD thesis project, has great translational potential and impact to the field of beta-cell adjuvant therapies for T1D, as it suggests targeting the Gαz signaling pathway might improve T1D outcomes regardless of auto-immune infiltration …Rachel blogs for the diabetes advocacy groups YOUglycemia and BeyondType1.org. YOUglycemia is an organization of professionals in diabetes education, dietetics, exercise physiology, and immunology who are passionate about providing evidence-based recommendations regarding exercise and nutritional strategies for managing the disease.”
*All papers are listed in chronological order
[1] https://academic.oup.com/jcem/article/101/1/16/2806435
[2] https://www.sciencemag.org/careers/2017/03/more-female-researchers-globally-challenges-remain
[3] https://www.nytimes.com/2019/03/05/science/women-scientists-grants.html
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