The Expression of Hormone Receptors as a Gateway toward Understanding Endocrine Actions in Female Pelvic Floor Muscles

Author(s): Francisco Castelán*, Estela Cuevas-Romero, Margarita Martínez-Gómez.

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
(Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders)

Volume 20 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Objective: To provide an overview of the hormone actions and receptors expressed in the female pelvic floor muscles, relevant for understanding the pelvic floor disorders.

Methods: We performed a literature review focused on the expression of hormone receptors mainly in the pelvic floor muscles of women and female rats and rabbits.

Results: The impairment of the pelvic floor muscles can lead to the onset of pelvic floor dysfunctions, including stress urinary incontinence in women. Hormone milieu is associated with the structure and function alterations of pelvic floor muscles, a notion supported by the fact that these muscles express different hormone receptors. Nuclear receptors, such as steroid receptors, are up till now the most investigated. The present review accounts for the limited studies conducted to elucidate the expression of hormone receptors in pelvic floor muscles in females.

Conclusion: Hormone receptor expression is the cornerstone in some hormone-based therapies, which require further detailed studies on the distribution of receptors in particular pelvic floor muscles, as well as their association with muscle effectors, involved in the alterations relevant for understanding pelvic floor disorders.

Keywords: Androgen receptor, estrogen receptor, levator ani, micturition, reproduction, thyroid hormone receptor.

Elenskaia, K.; Thakar, R.; Sultan, A.H.; Scheer, I.; Beggs, A. The effect of pregnancy and childbirth on pelvic floor muscle function. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2011, 22(11), 1421-1427.
[] [PMID: 21789660]
Martínez Franco, E.; Parés, D.; Lorente Colomé, N.; Méndez Paredes, J.R.; Amat Tardiu, L. Urinary incontinence during pregnancy. Is there a difference between first and third trimester? Eur. J. Obstet. Gynecol. Reprod. Biol., 2014, 182, 86-90.
[] [PMID: 25262291]
Pereira, L.C.; Botelho, S.; Marques, J.; Adami, D.B.; Alves, F.K.; Palma, P.; Riccetto, C. Electromyographic pelvic floor activity: Is there impact during the female life cycle? Neurourol. Urodyn., 2016, 35(2), 230-234.
[] [PMID: 25503578]
Alexander, S.P.; Cidlowski, J.A.; Kelly, E.; Marrion, N.V.; Peters, J.A.; Faccenda, E.; Harding, S.D.; Pawson, A.J.; Sharman, J.L.; Southan, C.; Davies, J.A. CGTP Collaborators. THE CONCISE GUIDE TO PHARMACOLOGY 2017/18: Nuclear hormone receptors. Br. J. Pharmacol., 2017, 174(Suppl. 1), S208-S224.
[] [PMID: 29055032]
Alexander, S.P.; Christopoulos, A.; Davenport, A.P.; Kelly, E.; Marrion, N.V.; Peters, J.A.; Faccenda, E.; Harding, S.D.; Pawson, A.J.; Sharman, J.L.; Southan, C.; Davies, J.A. CGTP Collaborators. THE CONCISE GUIDE TO PHARMACOLOGY 2017/18: G protein-coupled receptors. Br. J. Pharmacol., 2017, 174(Suppl. 1), S17-S129.
[] [PMID: 29055040]
Alexander, S.P.; Fabbro, D.; Kelly, E.; Marrion, N.V.; Peters, J.A.; Faccenda, E.; Harding, S.D.; Pawson, A.J.; Sharman, J.L.; Southan, C.; Davies, J.A. CGTP Collaborators. THE CONCISE GUIDE TO PHARMACOLOGY 2017/18: Catalytic receptors. Br. J. Pharmacol., 2017, 174(Suppl. 1), S225-S271.
[] [PMID: 29055036]
Evans, R.M.; Mangelsdorf, D.J. Nuclear Receptors, RXR, and the Big Bang. Cell, 2014, 157(1), 255-266.
[] [PMID: 24679540]
Cody, J.D.; Jacobs, M.L.; Richardson, K.; Moehrer, B.; Hextall, A. Oestrogen therapy for urinary incontinence in post-menopausal women. Cochrane Database Syst. Rev, 2012, 10, CD001405.
[] [PMID: 23076892]
Ismail, S.I.; Bain, C.; Hagen, S. Oestrogens for treatment or prevention of pelvic organ prolapse in postmenopausal women. Cochrane Database Syst. Rev., 2010, (9) CD007063
[] [PMID: 20824855]
Weber, M.A.; Kleijn, M.H.; Langendam, M.; Limpens, J.; Heineman, M.J.; Roovers, J.P. Local Oestrogen for Pelvic Floor Disorders: A Systematic Review. PLoS One, 2015, 10(9) e0136265
[] [PMID: 26383760]
Tzur, T.; Yohai, D.; Weintraub, A.Y. The role of local estrogen therapy in the management of pelvic floor disorders. Climacteric, 2016, 19(2), 162-171.
[] [PMID: 26830033]
Fritel, X.; Ringa, V.; Quiboeuf, E.; Fauconnier, A. Female urinary incontinence, from pregnancy to menopause: a review of epidemiological and pathophysiological findings. Acta Obstet. Gynecol. Scand., 2012, 91(8), 901-910.
[] [PMID: 22497363]
Deindl, F.M.; Vodusek, D.B.; Hesse, U.; Schüssler, B. Pelvic floor activity patterns: comparison of nulliparous continent and parous urinary stress incontinent women. A kinesiological EMG study. Br. J. Urol., 1994, 73(4), 413-417.
[] [PMID: 8199830]
Shafik, A.; Shafik, A.A.; El Sibai, O.; Shafik, I.A. Effect of micturition on clitoris and cavernosus muscles: an electromyographic study. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2008, 19(4), 531-535.
[] [PMID: 17928933]
Betts, J.G.; Young, K.A.; Wise, J.A. Anatomy and Physiology OpenStax: Houston 2013.
Dieter, A.A.; Wilkins, M.F.; Wu, J.M. Epidemiological trends and future care needs for pelvic floor disorders. Curr. Opin. Obstet. Gynecol., 2015, 27(5), 380-384.
[] [PMID: 26308198]
Lukacz, E.S.; Santiago-Lastra, Y.; Albo, M.E.; Brubaker, L. Urinary Incontinence in Women: A Review. JAMA, 2017, 318(16), 1592-1604.
[] [PMID: 29067433]
Hallock, J.L.; Handa, V.L. The Epidemiology of Pelvic Floor Disorders and Childbirth: An Update. Obstet. Gynecol. Clin. North Am., 2016, 43(1), 1-13.
[] [PMID: 26880504]
Johnston, S.L. Pelvic floor dysfunction in midlife women. Climacteric, 2019, 22(3), 270-276.
[] [PMID: 30857432]
Bump, R.C.; Norton, P.A. Epidemiology and natural history of pelvic floor dysfunction. Obstet. Gynecol. Clin. North Am., 1998, 25(4), 723-746.
[] [PMID: 9921553]
Ben-Shlomo, Y.; Kuh, D. A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int. J. Epidemiol., 2002, 31(2), 285-293.
[] [PMID: 11980781]
Kramer, I.M. Nuclear receptorsSignal Transduction, 3ed.; Kramer IM, Ed; Academic Press: United States of America, 2016.
Levin, E.R.; Hammes, S.R. Nuclear receptors outside the nucleus: extranuclear signalling by steroid receptors. Nat. Rev. Mol. Cell Biol., 2016, 17(12), 783-797.
[] [PMID: 27729652]
Robinson, D.; Toozs-Hobson, P.; Cardozo, L. The effect of hormones on the lower urinary tract. Menopause Int., 2013, 19(4), 155-162.
[] [PMID: 24336244]
Augoulea, A.; Sioutis, D.; Rizos, D.; Panoulis, C.; Triantafyllou, N.; Armeni, E.; Deligeoroglou, E.; Chrelias, C.; Creatsa, M.; Liapis, A.; Lambrinoudaki, I. Stress urinary incontinence and endogenous sex steroids in postmenopausal women. Neurourol. Urodyn., 2017, 36(1), 121-125.
[] [PMID: 26380958]
Bodner-Adler, B.; Bodner, K.; Kimberger, O.; Halpern, K.; Rieken, M.; Koelbl, H.; Umek, W. Role of serum steroid hormones in women with stress urinary incontinence: a case-control study. BJU Int., 2017, 120(3), 416-421.
[] [PMID: 28556379]
Micussi, M.T.; Freitas, R.P.; Angelo, P.H.; Soares, E.M.; Lemos, T.M.; Maranhão, T.M. Is there a difference in the electromyographic activity of the pelvic floor muscles across the phases of the menstrual cycle? J. Phys. Ther. Sci., 2015, 27(7), 2233-2237.
[] [PMID: 26311960]
Micussi, M.T.; Freitas, R.P.; Varella, L.; Soares, E.M.; Lemos, T.M.; Maranhão, T.M. Relationship between pelvic floor muscle and hormone levels in polycystic ovary syndrome. Neurourol. Urodyn., 2016, 35(7), 780-785.
[] [PMID: 26288062]
Hewitt, S.C.; Korach, K.S. Estrogen Receptors: New Directions in the New Millennium. Endocr. Rev., 2018, 39(5), 664-675.
[] [PMID: 29901737]
Pihlajamaa, P.; Sahu, B.; Jänne, O.A. Determinants of receptor- and tissue-specific actions in androgen signaling. Endocr. Rev., 2015, 36(4), 357-384.
[] [PMID: 26052734]
Enns, D.L.; Tiidus, P.M. The influence of estrogen on skeletal muscle: sex matters. Sports Med., 2010, 40(1), 41-58.
[] [PMID: 20020786]
Romano, S.N.; Gorelick, D.A. Crosstalk between nuclear and G protein-coupled estrogen receptors. Gen. Comp. Endocrinol., 2018, 261, 190-197.
[] [PMID: 28450143]
Barton, M.; Filardo, E.J.; Lolait, S.J.; Thomas, P.; Maggiolini, M.; Prossnitz, E.R. Twenty years of the G protein-coupled estrogen receptor GPER: Historical and personal perspectives. J. Steroid Biochem. Mol. Biol., 2018, 176, 4-15.
[] [PMID: 28347854]
Ikeda, K.; Horie-Inoue, K.; Inoue, S. Functions of estrogen and estrogen receptor signaling on skeletal muscle. J. Steroid Biochem. Mol. Biol., 2019, 191105375
[] [PMID: 31067490]
Prossnitz, E.R.; Barton, M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat. Rev. Endocrinol., 2011, 7(12), 715-726.
[] [PMID: 21844907]
Kim, Y.J.; Tamadon, A.; Park, H.T.; Kim, H.; Ku, S.Y. The role of sex steroid hormones in the pathophysiology and treatment of sarcopenia. Osteoporos. Sarcopenia, 2016, 2(3), 140-155.
[] [PMID: 30775480]
Vitale, G.; Cesari, M.; Mari, D. Aging of the endocrine system and its potential impact on sarcopenia. Eur. J. Intern. Med., 2016, 35, 10-15.
[] [PMID: 27484963]
Messier, V.; Rabasa-Lhoret, R.; Barbat-Artigas, S.; Elisha, B.; Karelis, A.D.; Aubertin-Leheudre, M. Menopause and sarcopenia: A potential role for sex hormones. Maturitas, 2011, 68(4), 331-336.
[] [PMID: 21353405]
Kane, D.A.; Lin, C-T.; Anderson, E.J.; Kwak, H.B.; Cox, J.H.; Brophy, P.M.; Hickner, R.C.; Neufer, P.D.; Cortright, R.N. Progesterone increases skeletal muscle mitochondrial H2O2 emission in nonmenopausal women. Am. J. Physiol. Endocrinol. Metab., 2011, 300(3), E528-E535.
[] [PMID: 21189359]
Carrington, L.J.; Bailey, C.J. Effects of natural and synthetic estrogens and progestins on glycogen deposition in female mice. Horm. Res., 1985, 21(3), 199-203.
[] [PMID: 3997066]
Gras, F.; Brunmair, B.; Quarré, L.; Szöcs, Z.; Waldhäusl, W.; Fürnsinn, C. Progesterone impairs cell respiration and suppresses a compensatory increase in glucose transport in isolated rat skeletal muscle: a non-genomic mechanism contributing to metabolic adaptation to late pregnancy? Diabetologia, 2007, 50(12), 2544-2552.
[] [PMID: 17932647]
Smith, G.I.; Yoshino, J.; Reeds, D.N.; Bradley, D.; Burrows, R.E.; Heisey, H.D.; Moseley, A.C.; Mittendorfer, B. Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. J. Clin. Endocrinol. Metab., 2014, 99(1), 256-265.
[] [PMID: 24203065]
Sartori, M.G.; Girão, M.J.; de Jesus Simões, M.; Sartori, J.P.; Baracat, E.C.; Rodrigues de Lima, G. Quantitative evaluation of collagen and muscle fibers in the lower urinary tract of castrated and under-hormone replacement female rats. Clin. Exp. Obstet. Gynecol., 2001, 28(2), 92-96.
[PMID: 11491384]
Mobley, C.B.; Mumford, P.W.; Kephart, W.C.; Conover, C.F.; Beggs, L.A.; Balaez, A.; Yarrow, J.F.; Borst, S.E.; Beck, D.T.; Roberts, M.D. Effects of testosterone treatment on markers of skeletal muscle ribosome biogenesis. Andrologia, 2016, 48(9), 967-977.
[] [PMID: 26781353]
Greising, S.M.; Baltgalvis, K.A.; Lowe, D.A.; Warren, G.L. Hormone therapy and skeletal muscle strength: a meta-analysis. J. Gerontol. A Biol. Sci. Med. Sci., 2009, 64(10), 1071-1081.
[] [PMID: 19561145]
Baltgalvis, K.A.; Greising, S.M.; Warren, G.L.; Lowe, D.A. Estrogen regulates estrogen receptors and antioxidant gene expression in mouse skeletal muscle. PLoS One, 2010, 5(4) e10164
[] [PMID: 20405008]
Alonso, A.; Fernández, R.; Ordóñez, P.; Moreno, M.; Patterson, A.M.; González, C. Regulation of estrogen receptor alpha by estradiol in pregnant and estradiol treated rats. Steroids, 2006, 71(13-14), 1052-1061.
[] [PMID: 17030051]
Velders, M.; Diel, P. How sex hormones promote skeletal muscle regeneration. Sports Med., 2013, 43(11), 1089-1100.
[] [PMID: 23888432]
Barros, R.P.A.; Gustafsson, J-Å. Estrogen receptors and the metabolic network. Cell Metab., 2011, 14(3), 289-299.
[] [PMID: 21907136]
Barros, R.P.A.; Machado, U.F.; Warner, M.; Gustafsson, J.A. Muscle GLUT4 regulation by estrogen receptors ERbeta and ERalpha. Proc. Natl. Acad. Sci. USA, 2006, 103(5), 1605-1608.
[] [PMID: 16423895]
Cai, J-J.; Wen, J.; Jiang, W-H.; Lin, J.; Hong, Y.; Zhu, Y.S. Androgen actions on endothelium functions and cardiovascular diseases. J. Geriatr. Cardiol., 2016, 13(2), 183-196.
[PMID: 27168746]
Takov, K.; Wu, J.; Denvir, M.A.; Smith, L.B.; Hadoke, P.W.F. The role of androgen receptors in atherosclerosis. Mol. Cell. Endocrinol., 2018, 465, 82-91.
[] [PMID: 29024781]
Lu, Q.; Schnitzler, G.R.; Vallaster, C.S.; Ueda, K.; Erdkamp, S.; Briggs, C.E.; Iyer, L.K.; Jaffe, I.Z.; Karas, R.H. Unliganded estrogen receptor alpha regulates vascular cell function and gene expression. Mol. Cell. Endocrinol., 2017, 442, 12-23.
[] [PMID: 27888004]
Minshall, R.D.; Pavcnik, D.; Browne, D.L.; Hermsmeyer, K. Nongenomic vasodilator action of progesterone on primate coronary arteries. J. Appl. Physiol., 2002, 92(2), 701-708.
[] [PMID: 11796684]
Ohura, N.; Yamamoto, K.; Ichioka, S.; Sokabe, T.; Nakatsuka, H.; Baba, A.; Shibata, M.; Nakatsuka, T.; Harii, K.; Wada, Y.; Kohro, T.; Kodama, T.; Ando, J. Global analysis of shear stress-responsive genes in vascular endothelial cells. J. Atheroscler. Thromb., 2003, 10(5), 304-313.
[] [PMID: 14718748]
Pang, Y.; Thomas, P. Progesterone induces relaxation of human umbilical cord vascular smooth muscle cells through mPRα (PAQR7). Mol. Cell. Endocrinol., 2018, 474, 20-34.
[] [PMID: 29428395]
Pang, Y.; Dong, J.; Thomas, P. Progesterone increases nitric oxide synthesis in human vascular endothelial cells through activation of membrane progesterone receptor-α. Am. J. Physiol. Endocrinol. Metab., 2015, 308(10), E899-E911.
[] [PMID: 25805192]
Perusquía, M.; Stallone, J.N. Do androgens play a beneficial role in the regulation of vascular tone? Nongenomic vascular effects of testosterone metabolites. Am. J. Physiol. Heart Circ. Physiol., 2010, 298(5), H1301-H1307.
[] [PMID: 20228257]
Isidoro, L.; Ferrer, M.; Perusquía, M. Vasoactive androgens: Vasorelaxing effects and their potential regulation of blood pressure. Endocr. Res., 2018, 43(3), 166-175.
[] [PMID: 29528756]
Perusquía, M.; Contreras, D.; Herrera, N. Hypotestosteronemia is an important factor for the development of hypertension: elevated blood pressure in orchidectomized conscious rats is reversed by different androgens. Endocrine, 2019, 65(2), 416-425.
[] [PMID: 31203561]
Boese, A.C.; Kim, S.C.; Yin, K-J.; Lee, J.P.; Hamblin, M.H. Sex differences in vascular physiology and pathophysiology: estrogen and androgen signaling in health and disease. Am. J. Physiol. Heart Circ. Physiol., 2017, 313(3), H524-H545.
[] [PMID: 28626075]
Hannan, J.L.; Cheung, G.L.; Blaser, M.C.; Pang, J.J.; Pang, S.C.; Webb, R.C.; Adams, M.A. Characterization of the vasculature supplying the genital tissues in female rats. J. Sex. Med., 2012, 9(1), 136-147.
[] [PMID: 22023507]
Mercier, J.; Tang, A.; Morin, M.; Lemieux, M.C.; Khalifé, S.; Reichetzer, B.; Dumoulin, C. Test-retest reliability of internal pudendal artery blood flow using color Doppler ultrasound in healthy women. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2018, 29(12), 1817-1824.
[] [PMID: 29552737]
Mangır, N.; Hillary, C.J.; Chapple, C.R.; MacNeil, S. Oestradiol-releasing Biodegradable Mesh Stimulates Collagen Production and Angiogenesis: An Approach to Improving Biomaterial Integration in Pelvic Floor Repair. Eur. Urol. Focus, 2019, 5(2), 280-289.
[] [PMID: 28753895]
Keast, J.R. Plasticity of pelvic autonomic ganglia and urogenital innervation. Int. Rev. Cytol., 2006, 248, 141-208.
[] [PMID: 16487791]
Nguyen, T-V.; Ducharme, S.; Karama, S. Effects of Sex Steroids in the Human Brain. Mol. Neurobiol., 2017, 54(9), 7507-7519.
[] [PMID: 27822715]
Sengelaub, D.R.; Xu, X-M. Protective effects of gonadal hormones on spinal motoneurons following spinal cord injury. Neural Regen. Res., 2018, 13(6), 971-976.
[] [PMID: 29926818]
Garcia-Ovejero, D.; Azcoitia, I.; Doncarlos, L.L.; Melcangi, R.C.; Garcia-Segura, L.M. Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res. Brain Res. Rev., 2005, 48(2), 273-286.
[] [PMID: 15850667]
Hernández-Aragón, L.G.; García-Villamar, V.; Carrasco-Ruiz, M.L.; Nicolás-Toledo, L.; Ortega, A.; Cuevas-Romero, E.; Martínez-Gómez, M.; Castelán, F. Role of Estrogens in the Size of Neuronal Somata of Paravaginal Ganglia in Ovariectomized Rabbits. BioMed Res. Int., 2017, 20172089645
[] [PMID: 28316975]
García-Villamar, V.; Hernández-Aragón, L.G.; Chávez-Ríos, J.R.; Ortega, A.; Martínez-Gómez, M.; Castelán, F. Expression of Glial Cell Line-Derived Neurotrophic Factor (GDNF) and the GDNF Family Receptor Alpha Subunit 1 in the Paravaginal Ganglia of Nulliparous and Primiparous Rabbits. Int. Neurourol. J., 2018, 22(Suppl. 1), S23-S33.
[] [PMID: 29385786]
Castelán, F.; Xelhuantzi, N.; Hernández-Aragón, L.G.; Rodríguez-Antolín, J.; Cuevas, E.; Martínez-Gómez, M. Morphometry of paravaginal ganglia from the pelvic plexus: impact of multiparity, primiparity, and pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol., 2013, 170(1), 286-292.
[] [PMID: 23932302]
Grigoriadis, C.; Hassiakos, D.; Bakas, P.; Tympa, A.; Panoulis, C.; Creatsas, G.; Kondi-Pafiti, A.; Liapis, A. Effect of gonadal steroid receptors alterations on the pathophysiology of pelvic organ prolapse and urinary incontinence. Minerva Ginecol., 2016, 68(1), 37-42.
[PMID: 25714872]
Copas, P.; Bukovsky, A.; Asbury, B.; Elder, R.F.; Caudle, M.R. Estrogen, progesterone, and androgen receptor expression in levator ani muscle and fascia. J. Womens Health Gend. Based Med., 2001, 10(8), 785-795.
[] [PMID: 11703891]
Traish, A.M.; Vignozzi, L.; Simon, J.A.; Goldstein, I.; Kim, N.N. Role of Androgens in Female Genitourinary Tissue Structure and Function: Implications in the Genitourinary Syndrome of Menopause. Sex. Med. Rev., 2018, 6(4), 558-571.
[] [PMID: 29631981]
Davis, S.R.; Wahlin-Jacobsen, S. Testosterone in women--the clinical significance. Lancet Diabetes Endocrinol., 2015, 3(12), 980-992.
[] [PMID: 26358173]
Burger, H.G. Androgen production in women. Fertil. Steril., 2002, 77(Suppl. 4), S3-S5.
[] [PMID: 12007895]
Ho, M.H.; Bhatia, N.N.; Bhasin, S. Anabolic effects of androgens on muscles of female pelvic floor and lower urinary tract. Curr. Opin. Obstet. Gynecol., 2004, 16(5), 405-409.
[] [PMID: 15353950]
Kim, M.M.; Kreydin, E.I. The Association of Serum Testosterone Levels and Urinary Incontinence in Women. J. Urol., 2018, 199(2), 522-527.
[] [PMID: 28847480]
Wasenda, E.J.; Kamisan Atan, I.; Subramaniam, N.; Dietz, H.P. Pelvic organ prolapse: does hormone therapy use matter? Menopause, 2017, 24(10), 1185-1189.
[] [PMID: 28538602]
Pöllänen, E.; Kangas, R.; Horttanainen, M.; Niskala, P.; Kaprio, J.; Butler-Browne, G.; Mouly, V.; Sipilä, S.; Kovanen, V. Intramuscular sex steroid hormones are associated with skeletal muscle strength and power in women with different hormonal status. Aging Cell, 2015, 14(2), 236-248.
[] [PMID: 25645687]
Karahan, N.; Arslan, H.; Çam, Ç. The behaviour of pelvic floor muscles during uterine contractions in spontaneous and oxytocin-induced labour. J. Obstet. Gynaecol., 2018, 38(5), 629-634.
[] [PMID: 29430972]
Fitzgerald, C.M.; Mallinson, T. The association between pelvic girdle pain and pelvic floor muscle function in pregnancy. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2012, 23(7), 893-898.
[] [PMID: 22290191]
Pérez-López, F.R. Iodine and thyroid hormones during pregnancy and postpartum. Gynecol. Endocrinol., 2007, 23(7), 414-428.
[] [PMID: 17701774]
Parker-Autry, C.Y.; Burgio, K.L.; Richter, H.E. Vitamin D status: a review with implications for the pelvic floor. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2012, 23(11), 1517-1526.
[] [PMID: 22415704]
Aydogmus, S.; Kelekci, S.; Aydogmus, H.; Demir, M.; Yilmaz, B.; Sutcu, R. Association of antepartum vitamin D levels with postpartum pelvic floor muscle strength and symptoms. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2015, 26(8), 1179-1184.
[] [PMID: 25792352]
Cuevas-Romero, E.; Sánchez-Cardiel, A.; Zamora-Gallegos, A.M.; Cruz-Lumbreras, R.; Corona-Quintanilla, D.L.; Castelán, F.; Martínez-Gómez, M. Moderate-to-high normal levels of thyrotropin is a risk factor for urinary incontinence and an unsuitable quality of life in women over 65 years. Clin. Exp. Pharmacol. Physiol., 2017, 44(Suppl. 1), 86-92.
[] [PMID: 28556290]
Minassian, V.A.; Stewart, W.F.; Wood, G.C. Urinary incontinence in women: variation in prevalence estimates and risk factors. Obstet. Gynecol., 2008, 111(2 Pt 1), 324-331.
[] [PMID: 18238969]
Andersen, L.F.; Agner, T.; Walter, S.; Hansen, J.M. Micturition pattern in hyperthyroidism and hypothyroidism. Urology, 1987, 29(2), 223-224.
[] [PMID: 3811104]
Justo, D.; Schwartz, N.; Dvorkin, E.; Gringauz, I.; Groutz, A. Asymptomatic urinary retention in elderly women upon admission to the Internal Medicine department: A prospective study. Neurourol. Urodyn., 2017, 36(3), 794-797.
[] [PMID: 27176656]
Mayerl, S.; Schmidt, M.; Doycheva, D.; Darras, V.M.; Hüttner, S.S.; Boelen, A.; Visser, T.J.; Kaether, C.; Heuer, H.; von Maltzahn, J. Thyroid Hormone Transporters MCT8 and OATP1C1 Control Skeletal Muscle Regeneration. Stem Cell Reports, 2018, 10(6), 1959-1974.
[] [PMID: 29706500]
Flamant, F.; Cheng, S-Y.; Hollenberg, A.N.; Moeller, L.C.; Samarut, J.; Wondisford, F.E.; Yen, P.M.; Refetoff, S. Thyroid Hormone Signaling Pathways: Time for a More Precise Nomenclature. Endocrinology, 2017, 158(7), 2052-2057.
[] [PMID: 28472304]
Luongo, C.; Dentice, M.; Salvatore, D. Deiodinases and their intricate role in thyroid hormone homeostasis. Nat. Rev. Endocrinol., 2019, 15(8), 479-488.
[] [PMID: 31160732]
Pradidarcheep, W.; Wallner, C.; Dabhoiwala, N.F.; Lamers, W.H. Anatomy and histology of the lower urinary tract. Handb. Exp. Pharmacol., 2011, 202, 117-148.
[] [PMID: 21290225]
Poortmans, A.; Wyndaele, J.J.M. levator ani in the rat: does it really lift the anus? Anat. Rec., 1998, 251(1), 20-27.
[<20:AID-AR5>3.0.CO;2-I] [PMID: 9605216]
Rand, M.N.; Breedlove, S.M. Androgen locally regulates rat bulbocavernosus and levator ani size. J. Neurobiol., 1992, 23(1), 17-30.
[] [PMID: 1564453]
Cruz, Y.; Jiang, H-H.; Zaszczurynski, P. Electromyography of Pelvic Floor Muscles in Rats.Advances in Applied Electromyography; Mizrahi, J., Ed.; InTech, 2011.
Cuevas, E.; Alvarado, M.; Pacheco, P. Absence of the tail in female rats disrupts the copulatory pattern of experienced male partners. Anim. Behav., 2008, 75, 1243-1251.
Martinez-Gomez, M.; Chirino, R.; Beyer, C.; Komisaruk, B.R.; Pacheco, P. Visceral and postural reflexes evoked by genital stimulation in urethane-anesthetized female rats. Brain Res., 1992, 575(2), 279-284.
[] [PMID: 1533338]
Pacheco, P.; Martinez-Gomez, M.; Whipple, B.; Beyer, C.; Komisaruk, B.R. Somato-motor components of the pelvic and pudendal nerves of the female rat. Brain Res., 1989, 490(1), 85-94.
[] [PMID: 2758331]
Martínez-Gómez, M.; Corona-Quintanilla, D.L.; Cruz-Gómez, Y. The Role of Pelvic and Perineal Muscles in Reproductive and Excretory Functions.Applications of EMG in Clinical and Sports Medicine; Steele, C., Ed.; InTech, 2012.
Alperin, M.; Tuttle, L.J.; Conner, B.R.; Dixon, D.M.; Mathewson, M.A.; Ward, S.R.; Lieber, R.L. Comparison of pelvic muscle architecture between humans and commonly used laboratory species. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2014, 25(11), 1507-1515.
[] [PMID: 24915840]
Dubé, J.Y.; Lesage, R.; Tremblay, R.R. Androgen and estrogen binding in rat skeletal and perineal muscles. Can. J. Biochem., 1976, 54(1), 50-55.
[] [PMID: 175903]
Carrasco-Ruiz, M.L.Á.; Hernández-Aragón, L.G.; Chávez-Ríos, J.R.; Rodríguez-Antolín, J.; Pacheco, P.; Martínez-Gómez, M.; Cuevas-Romero, E.; Castelán, F. High Estradiol Differentially Affects the Expression of the Glucose Transporter Type 4 in Pelvic Floor Muscles of Rats. Int. Neurourol. J., 2018, 22(3), 161-168.
[] [PMID: 30286578]
Nordeen, E.J.; Nordeen, K.W.; Sengelaub, D.R.; Arnold, A.P. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science, 1985, 229(4714), 671-673.
[] [PMID: 4023706]
Johansen, J.A.; Breedlove, S.M.; Jordan, C.L. Androgen receptor expression in the levator ani muscle of male mice. J. Neuroendocrinol., 2007, 19(10), 823-826.
[] [PMID: 17850465]
Monks, D.A.; O’Bryant, E.L.; Jordan, C.L. Androgen receptor immunoreactivity in skeletal muscle: enrichment at the neuromuscular junction. J. Comp. Neurol., 2004, 473(1), 59-72.
[] [PMID: 15067718]
Rudolph, L.M.; Sengelaub, D.R. Critical period for estrogen-dependent motoneuron dendrite growth is coincident with ERα expression in target musculature. Dev. Neurobiol., 2013, 73(1), 72-84.
[] [PMID: 22678724]
Cuevas, E.; Camacho, M.; Alvarado, M.; Hudson, R.; Pacheco, P. Participation of estradiol and progesterone in the retrograde labeling of pubococcygeus motoneurons of the female rat. Neuroscience, 2006, 140(4), 1435-1442.
[] [PMID: 16650616]
Kane, D.D.; Kerns, J.M.; Lin, D.L.; Damaser, M.S. Early structural effects of oestrogen on pudendal nerve regeneration in the rat. BJU Int., 2004, 93(6), 870-878.
[] [PMID: 15050008]
Max, S.R.; Knudsen, J.F. Effect of sex hormones on glucose-6-phosphate dehydrogenase in rat levator ani muscle. Mol. Cell. Endocrinol., 1980, 17(2), 111-118.
[] [PMID: 7364148]
Max, S.R. Effect of estrogen on denervated muscle. J. Neurochem., 1981, 36(3), 1077-1082.
[] [PMID: 7205258]
Yang, H-C.; Wu, Y-H.; Liu, H-Y.; Stern, A.; Chiu, D.T. What has passed is prolog: new cellular and physiological roles of G6PD. Free Radic. Res., 2016, 50(10), 1047-1064.
[] [PMID: 27684214]
Alvarado, M.; Cuevas, E.; Lara-García, M.; Camacho, M.; Carrillo, P.; Hudson, R.; Pacheco, P. Effect of gonadal hormones on the cross-sectional area of pubococcygeus muscle fibers in male rat. Anat. Rec. (Hoboken), 2008, 291(5), 586-592.
[] [PMID: 18399549]
Lara-García, M.; Alvarado, M.; Cuevas, E.; Cortés-sol, A.; Domínguez, A.; Tovar, A.; Pacheco, P. The effects of castration and hormone replacement on the cross-sectional area of pubococcygeus muscle fibers in the female rat. Anat. Rec. (Hoboken), 2011, 294(7), 1242-1248.
[] [PMID: 21618707]
Ponnusamy, S.; Sullivan, R.D.; Thiyagarajan, T.; Tillmann, H.; Getzenberg, R.H.; Narayanan, R. Tissue Selective Androgen Receptor Modulators (SARMs) Increase Pelvic Floor Muscle Mass in Ovariectomized Mice. J. Cell. Biochem., 2017, 118(3), 640-646.
[] [PMID: 27681158]
Mammadov, R.; Simsir, A.; Tuglu, I.; Evren, V.; Gurer, E.; Özyurt, C. The effect of testosterone treatment on urodynamic findings and histopathomorphology of pelvic floor muscles in female rats with experimentally induced stress urinary incontinence. Int. Urol. Nephrol., 2011, 43(4), 1003-1008.
[] [PMID: 21442470]
Max, S.R. Androgen-estrogen synergy in rat levator ani muscle: glucose-6-phosphate dehydrogenase. Mol. Cell. Endocrinol., 1984, 38(2-3), 103-107.
[] [PMID: 6510548]
Campbell, S.E.; Febbraio, M.A. Effect of the ovarian hormones on GLUT4 expression and contraction-stimulated glucose uptake. Am. J. Physiol. Endocrinol. Metab., 2002, 282(5), E1139-E1146.
[] [PMID: 11934680]
Martínez-Gómez, M.; Lucio, R.A.; Carro, M.; Pacheco, P.; Hudson, R. Striated muscles and scent glands associated with the vaginal tract of the rabbit. Anat. Rec., 1997, 247(4), 486-495.
[<486:AID-AR7>3.0.CO;2-P] [PMID: 9096788]
Spettel, S.; De, E.; Elias, T.; Schuler, C.; Leggett, R.E.; Levin, R.M. Citrate synthase, sarcoplasmic reticular calcium ATPase, and choline acetyltransferase activities of specific pelvic floor muscles of the rabbit. Mol. Cell. Biochem., 2012, 370(1-2), 1-5.
[] [PMID: 22911511]
Rajasekaran, M.R.; Sohn, D.; Salehi, M.; Bhargava, V.; Fritsch, H.; Mittal, R.K. Role of puborectalis muscle in the genesis of urethral pressure. J. Urol., 2012, 188(4), 1382-1388.
[] [PMID: 22906663]
Beyer, C.; Hoffman, K.L.; González-Flores, O. Neuroendocrine regulation of estrous behavior in the rabbit: similarities and differences with the rat. Horm. Behav., 2007, 52(1), 2-11.
[] [PMID: 17490662]
Fry, C.; Jabr, R. The Integrated Physiology of the Lower Urinary Tract. Neurourology; Springer: Dordrecht, 2019, pp. 65-77.
Corona-Quintanilla, D.L.; Castelán, F.; Fajardo, V.; Manzo, J.; Martínez-Gómez, M. Temporal coordination of pelvic and perineal striated muscle activity during micturition in female rabbits. J. Urol., 2009, 181(3), 1452-1458.
[] [PMID: 19157450]
Sánchez-García, O.; Hernández-Aragón, L.G.; López-García, K.; Juárez, M.; Martínez-Gómez, M.; Castelán, F. Signs of damage in pelvic floor muscles at the end of pregnancy in rabbits. Int. Urogynecol. J. Pelvic Floor Dysfunct., 2019, 30(6), 977-984.
[] [PMID: 30706078]
López-García, K.; Cuevas, E.; Sánchez-García, O.; Pacheco, P.; Martínez-Gómez, M.; Castelán, F. Differential damage and repair responses of pubococcygeus and bulbospongiosus muscles in multiparous rabbits. Neurourol. Urodyn., 2016, 35(2), 180-185.
[] [PMID: 25451605]
Martínez-Gómez, M.; Mendoza-Martínez, G.; Corona-Quintanilla, D.L.; Fajardo, V.; Rodríguez-Antolín, J.; Castelán, F. Multiparity causes uncoordinated activity of pelvic- and perineal-striated muscles and urodynamic changes in rabbits. Reprod. Sci., 2011, 18(12), 1246-1252.
[] [PMID: 21701040]
López-García, K.; Cuevas, E. Corona-Quintanilla, D.L.; Jiménez-Estrada, I.; Martínez-Gómez, M.; Castelán, F. Effect of multiparity on morphometry and oestrogen receptor expression of pelvic and perineal striated muscles in rabbits: is serum oestradiol relevant? Eur. J. Obstet. Gynecol. Reprod. Biol., 2013, 169(1), 113-120.
[] [PMID: 23664379]
López-Juárez, R.; Zempoalteca, R.; Corona-Quintanilla, D.L.; Jiménez-Estrada, I.; Castelán, F.; Martínez-Gómez, M. Multiparity modifies contractile properties of pelvic muscles affecting the genesis of vaginal pressure in rabbits. Neurourol. Urodyn., 2018, 37(1), 106-114.
[] [PMID: 28543684]
López-García, K.; Mariscal-Tovar, S.; Serrano-Meneses, M.A.; Castelán, F.; Martínez-Gómez, M.; Jiménez-Estrada, I. Fiber type composition of pubococcygeus and bulbospongiosus striated muscles is modified by multiparity in the rabbit. Neurourol. Urodyn., 2017, 36(6), 1456-1463.
[] [PMID: 27677101]
González-Mariscal, G.; Díaz-Sánchez, V.; Melo, A.I.; Beyer, C.; Rosenblatt, J.S. Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns, and steroid plasma levels. Physiol. Behav., 1994, 55(6), 1081-1089.
[] [PMID: 8047575]
de los Ángeles Carrasco-Ruiz, M.; García-Villamar, V.; López-García, K.; Sánchez-García, O.; Pacheco, P.; Cuevas, E.; Martínez-Gómez, M.; Castelán, F. Aromatase expression is linked to estrogenic sensitivity of periurethral muscles in female rabbits. Cell Biochem. Funct., 2015, 33(4), 188-195.
[] [PMID: 25850953]
Labrie, F. Intracrinology. Mol. Cell. Endocrinol., 1991, 78, C113-C118.
[] [PMID: 1838082]
Labrie, F. All sex steroids are made intracellularly in peripheral tissues by the mechanisms of intracrinology after menopause. J. Steroid Biochem. Mol. Biol., 2015, 145, 133-138.
[] [PMID: 24923731]
Aizawa, K.; Iemitsu, M.; Otsuki, T.; Maeda, S.; Miyauchi, T.; Mesaki, N. Sex differences in steroidogenesis in skeletal muscle following a single bout of exercise in rats. J. Appl. Physiol., 2008, 104(1), 67-74.
[] [PMID: 17975125]
Aizawa, K.; Iemitsu, M.; Maeda, S.; Jesmin, S.; Otsuki, T.; Mowa, C.N.; Miyauchi, T.; Mesaki, N. Expression of steroidogenic enzymes and synthesis of sex steroid hormones from DHEA in skeletal muscle of rats. Am. J. Physiol. Endocrinol. Metab., 2007, 292(2), E577-E584.
[] [PMID: 17018772]
Larionov, A.A.; Vasyliev, D.A.; Mason, J.I.; Howie, A.F.; Berstein, L.M.; Miller, W.R. Aromatase in skeletal muscle. J. Steroid Biochem. Mol. Biol., 2003, 84(4), 485-492.
[] [PMID: 12732294]
Sánchez-García, O.; Rodríguez-Castelán, J.; Martínez-Gómez, M.; Cuevas, E.; Castelán, F. Hypothyroidism modifies morphometry and thyroid-hormone receptor expression in periurethral muscles of female rabbits. Neurourol. Urodyn., 2016, 35(8), 895-901.
[] [PMID: 26250619]
Rodríguez-Castelán, J.; Anaya-Hernández, A.; Méndez-Tepepa, M.; Martínez-Gómez, M.; Castelán, F.; Cuevas-Romero, E. Distribution of thyroid hormone and thyrotropin receptors in reproductive tissues of adult female rabbits. Endocr. Res., 2017, 42(1), 59-70.
[] [PMID: 27268091]
McAninch, E.A.; Bianco, A.C. Thyroid hormone signaling in energy homeostasis and energy metabolism. Ann. N. Y. Acad. Sci., 2014, 1311, 77-87.
[] [PMID: 24697152]
Weinstein, S.P.; Watts, J.; Haber, R.S. Thyroid hormone increases muscle/fat glucose transporter gene expression in rat skeletal muscle. Endocrinology, 1991, 129(1), 455-464.
[] [PMID: 2055200]
Brown, J.G.; Bates, P.C.; Holliday, M.A.; Millward, D.J. Thyroid hormones and muscle protein turnover. The effect of thyroid-hormone deficiency and replacement in thryoidectomized and hypophysectomized rats. Biochem. J., 1981, 194(3), 771-782.
[] [PMID: 6171261]
Kjeldsen, K.; Nørgaard, A.; Gøtzsche, C.O.; Thomassen, A.; Clausen, T. Effect of thyroid function on number of Na-K pumps in human skeletal muscle. Lancet, 1984, 2(8393), 8-10.
[] [PMID: 6145984]
Harrison, A.P.; Tivey, D.R.; Clausen, T.; Duchamp, C.; Dauncey, M.J. Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutrition. Br. J. Nutr., 1996, 76(6), 841-855.
[] [PMID: 9014653]
Leal, A.L.R.C.; Albuquerque, J.P.C.; Matos, M.S.; Fortunato, R.S.; Carvalho, D.P.; Rosenthal, D.; da Costa, V.M. Thyroid hormones regulate skeletal muscle regeneration after acute injury. Endocrine, 2015, 48(1), 233-240.
[] [PMID: 24798447]
Calonne, J.; Isacco, L.; Miles-Chan, J.; Arsenijevic, D.; Montani, J.P.; Guillet, C.; Boirie, Y.; Dulloo, A.G. Reduced Skeletal Muscle Protein Turnover and Thyroid Hormone Metabolism in Adaptive Thermogenesis That Facilitates Body Fat Recovery During Weight Regain. Front. Endocrinol. (Lausanne), 2019, 10, 119.
[] [PMID: 30873123]
Simonides, W.S.; van Hardeveld, C. Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid, 2008, 18(2), 205-216.
[] [PMID: 18279021]
Lanza, I.R.; Sreekumaran Nair, K. Regulation of skeletal muscle mitochondrial function: genes to proteins. Acta Physiol. (Oxf.), 2010, 199(4), 529-547.
[] [PMID: 20345409]
Salvatore, D.; Simonides, W.S.; Dentice, M.; Zavacki, A.M.; Larsen, P.R. Thyroid hormones and skeletal muscle--new insights and potential implications Nat. Rev. Endocrinol, 2014, 10(4), 206-214. [Internet].
[] [PMID: 24322650]
Sánchez-García, O.; López-Juárez, R.; Rodríguez-Castelán, J.; Corona-Quintanilla, D.L.; Martínez-Gómez, M.; Cuevas-Romero, E.; Castelán, F. Hypothyroidism impairs somatovisceral reflexes involved in micturition of female rabbits. Neurourol. Urodyn., 2018, 37(8), 2406-2413.
[] [PMID: 29664178]
Ingelman-Sundberg, A.; Rosén, J.; Gustafsson, S.A.; Carlström, K. Cytosol estrogen receptors in the urogenital tissues in stress-incontinent women. Acta Obstet. Gynecol. Scand., 1981, 60(6), 585-586.
[] [PMID: 6461158]
Smith, P.; Heimer, G.; Norgren, A.; Ulmsten, U. Localization of steroid hormone receptors in the pelvic muscles. Eur. J. Obstet. Gynecol. Reprod. Biol., 1993, 50(1), 83-85.
[] [PMID: 8365541]
Bernstein, I.T. The pelvic floor muscles: muscle thickness in healthy and urinary-incontinent women measured by perineal ultrasonography with reference to the effect of pelvic floor training. Estrogen receptor studies. Neurourol. Urodyn., 1997, 16(4), 237-275.
[<237:AID-NAU2>3.0.CO;2-F] [PMID: 9220475]
Bukovsky, A.; Indrapichate, K.; Fujiwara, H.; Cekanova, M.; Ayala, M.E.; Dominguez, R.; Caudle, M.R.; Wimalsena, J.; Elder, R.F.; Copas, P.; Foster, J.S.; Fernando, R.I.; Henley, D.C.; Upadhyaya, N.B. Multiple luteinizing hormone receptor (LHR) protein variants, interspecies reactivity of anti-LHR mAb clone 3B5, subcellular localization of LHR in human placenta, pelvic floor and brain, and possible role for LHR in the development of abnormal pregnancy, pelvic floor disorders and Alzheimer’s disease. Reprod. Biol. Endocrinol., 2003, 1, 46.
[] [PMID: 12816543]
Lu, Y.; Lang, J-H.; Zhu, L. [Estrogen receptors in pelvic floor for female stress urinary incontinence]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao, 2007, 29(3), 402-406.
[PMID: 17633471]
Söderberg, M.W.; Johansson, B.; Masironi, B.; Byström, B.; Falconer, C.; Sahlin, L.; Ordeberg, G.E. Pelvic floor sex steroid hormone receptors, distribution and expression in pre- and postmenopausal stress urinary incontinent women. Acta Obstet. Gynecol. Scand., 2007, 86(11), 1377-1384.
[] [PMID: 17963065]
Chen, Y-S.; Hua, K-Q. [Expression of androgen receptor in the vaginal wall and cardinal ligament of patients with pelvic organ prolapse]. Zhonghua Yi Xue Za Zhi, 2008, 88(41), 2920-2923.
[PMID: 19080100]
Zbucka-Kretowska, M.; Marcus-Braun, N.; Eboue, C.; Abeguile, G.; Wolczynski, S.; Kottler, M.L.; Von Theobald, P. Expression of estrogen receptors in the pelvic floor of pre- and post-menopausal women presenting pelvic organ prolapse. Folia Histochem. Cytobiol., 2011, 49(3), 521-527.
[] [PMID: 22038234]
Schott, S.; Reisenauer, C.; Busch, C. Presence of relaxin-2, oxytocin and their receptors in uterosacral ligaments of pre-menopausal patients with and without pelvic organ prolapse. Acta Obstet. Gynecol. Scand., 2014, 93(10), 991-996.
[] [PMID: 25053207]
Matthews, S.G.; Gibb, W.; Lye, S.J.; Lye, S.J.; Challis, J.R.G. Endocrine and paracrine regulation of birth at term and preterm. Endocr. Rev., 2000, 21(5), 514-550.
[PMID: 11041447]
Smith, R. Parturition. N. Engl. J. Med., 2007, 356(3), 271-283.
[] [PMID: 17229954]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Page: [305 - 320]
Pages: 16
DOI: 10.2174/1871530319666191009154751
Price: $65

Article Metrics

PDF: 14
PRC: 1