The Calcium-Sensing Receptor and the Reproductive System.
- Journal Article
- Review
Summary
This research review focuses on understanding the unique role of the Calcium-Sensing Receptor (CaSR) in various aspects of mammalian reproduction. It concludes that the CaSR plays an essential role in a multitude of reproductive processes but calls for more research to unravel the complex workings of this receptor and its relationship with the reproductive system.
Role of Calcium-Sensing Receptor in Mammalian Reproduction
The Calcium-Sensing Receptor (CaSR) is responsible for regulating extracellular calcium levels and translating changes in these levels into cellular reactions. This study reviews the research data on how this receptor functions in different reproductive organs. Several notable findings were:
- CaSR is present in placental cells that mediate the transport of calcium (Ca(2+)) from the mother to the fetus, enabling proper fetal development. This presence was identified in both mice and humans.
- Experiments on mice lacking the CaSR gene (casr knock-out mice) showed a downregulation of the maternal-fetal calcium transport.
- CaSR can stimulate cell proliferation, as evidenced by its activation in human and rat ovarian surface epithelial cells.
- In various species, the activation of the CaSR plays a role in oocyte (female germ cell) maturation.
- CaSR in rat and horse sperms was associated with improving sperm motility and capacitation (the ability of sperm to fertilize an egg).
CaSR Involvement in Implantation and Decidualization
The study also reviewed the role of CaSR in the implantation of the blastocyst (a group of cells formed five days after fertilization) and how it functions in the uterus during early pregnancy:
- CaSR expression at the implantation site and in decidual cells (cells that line the uterus during early pregnancy) suggests that this receptor plays a significant role in blastocyst implantation and decidualization in the rat uterus.
- Presence of CaSR in human extravillous cytotrophoblasts (cells that help in placental development) implies that it might have a role in human placental formation.
Implication of CaSR in Pathological Conditions
The study concludes by acknowledging an association between abnormal CaSR expression and reproductive tissue pathologies. However, more research and understanding are needed to know the physiological stimuli that trigger CaSR, the G-proteins linked to CaSR, the activated intracellular signaling pathway, and the functional relevance of CaSR activation in each organ. This is deemed important to better grasp the physiologic and pathophysiologic effects of CaSR on the mammalian reproductive system.
Cite This Article
Publication
Researcher Affiliations
- Pathophysiology of the Placenta, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University Vienna Vienna, Austria.
References
- Adebanjo OA, Igietseme J, Huang CL, Zaidi M. The effect of extracellularly applied divalent cations on cytosolic Ca2+ in murine leydig cells: evidence for a Ca2+-sensing receptor.. J Physiol 1998 Dec 1;513 ( Pt 2)(Pt 2):399-410.
- Aguilar HN, Mitchell BF. Physiological pathways and molecular mechanisms regulating uterine contractility.. Hum Reprod Update 2010 Nov-Dec;16(6):725-44.
- Ahearn TU, Tchrakian N, Wilson KM, Lis R, Nuttall E, Sesso HD, Loda M, Giovannucci E, Mucci LA, Finn S, Shui IM. Calcium-Sensing Receptor Tumor Expression and Lethal Prostate Cancer Progression.. J Clin Endocrinol Metab 2016 Jun;101(6):2520-7.
- Alavi-Shoushtari SM, Asri-Rezaie S, Abedizadeh R, Khaki A, Pak M, Alizadeh S. Calcium and magnesium concentrations in uterine fluid and blood serum during the estrous cycle in the bovine.. Vet Res Forum 2012 Spring;3(2):137-41.
- Alavi Shoushtari SM, Asri Rezaie S, Khaki A, Belbasi A, Tahmasebian H. Calcium and magnesium content of the uterine fluid and blood serum during the estrous cycle and pre-pubertal phase in water buffaloes.. Vet Res Forum 2014 Fall;5(4):301-5.
- Alfadda TI, Saleh AM, Houillier P, Geibel JP. Calcium-sensing receptor 20 years later.. Am J Physiol Cell Physiol 2014 Aug 1;307(3):C221-31.
- Almog T, Naor Z. The role of Mitogen activated protein kinase (MAPK) in sperm functions.. Mol Cell Endocrinol 2010 Jan 27;314(2):239-43.
- Armant DR. Intracellular Ca2+ signaling and preimplantation development.. Adv Exp Med Biol 2015;843:151-71.
- Baczyk D, Kingdom JC, Uhlén P. Calcium signaling in placenta.. Cell Calcium 2011 May;49(5):350-6.
- Baker MA, Hetherington L, Ecroyd H, Roman SD, Aitken RJ. Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation.. J Cell Sci 2004 Jan 15;117(Pt 2):211-22.
- Benirschke K, Burton GJ, Baergen RN. Pathology of the Human Placenta. .
- Bernadotte F, Holmdahl R, Juhlin C, Mattsson R. Expression of a cell surface antigen with potential Ca2+-sensor/receptor function in rat placenta and uterus.. J Reprod Immunol 1989 Nov;16(2):199-205.
- Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling.. Nat Rev Mol Cell Biol 2000 Oct;1(1):11-21.
- Bilderback TR, Lee F, Auersperg N, Rodland KD. Phosphatidylinositol 3-kinase-dependent, MEK- independent proliferation in response to CaR activation.. Am J Physiol Cell Physiol 2002 Jul;283(1):C282-8.
- Bjerneroth G, Juhlin C, Akerström G, Rastad J. Immunoelectron microscopical evidence of a calcium receptor function in parathyroid, placenta and kidney.. J Submicrosc Cytol Pathol 1992 Apr;24(2):179-86.
- Bond H, Dilworth MR, Baker B, Cowley E, Requena Jimenez A, Boyd RD, Husain SM, Ward BS, Sibley CP, Glazier JD. Increased maternofetal calcium flux in parathyroid hormone-related protein-null mice.. J Physiol 2008 Apr 1;586(7):2015-25.
- Bradbury RA, Cropley J, Kifor O, Lovicu FJ, de Iongh RU, Kable E, Brown EM, Seely EW, Peat BB, Conigrave AD. Localization of the extracellular Ca(2+)-sensing receptor in the human placenta.. Placenta 2002 Feb-Mar;23(2-3):192-200.
- Bradbury RA, Sunn KL, Crossley M, Bai M, Brown EM, Delbridge L, Conigrave AD. Expression of the parathyroid Ca(2+)-sensing receptor in cytotrophoblasts from human term placenta.. J Endocrinol 1998 Mar;156(3):425-30.
- Breitbart H. Intracellular calcium regulation in sperm capacitation and acrosomal reaction.. Mol Cell Endocrinol 2002 Feb 22;187(1-2):139-44.
- Brennan SC, Thiem U, Roth S, Aggarwal A, Fetahu ISh, Tennakoon S, Gomes AR, Brandi ML, Bruggeman F, Mentaverri R, Riccardi D, Kallay E. Calcium sensing receptor signalling in physiology and cancer.. Biochim Biophys Acta 2013 Jul;1833(7):1732-44.
- Brennan SC, Wilkinson WJ, Tseng HE, Finney B, Monk B, Dibble H, Quilliam S, Warburton D, Galietta LJ, Kemp PJ, Riccardi D. The extracellular calcium-sensing receptor regulates human fetal lung development via CFTR.. Sci Rep 2016 Feb 25;6:21975.
- Brown EM. Clinical utility of calcimimetics targeting the extracellular calcium-sensing receptor (CaSR).. Biochem Pharmacol 2010 Aug 1;80(3):297-307.
- Brown EM. Role of the calcium-sensing receptor in extracellular calcium homeostasis.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):333-43.
- Casslén B, Nilsson B. Human uterine fluid, examined in undiluted samples for osmolarity and the concentrations of inorganic ions, albumin, glucose, and urea.. Am J Obstet Gynecol 1984 Dec 1;150(7):877-81.
- Celik O, Celik N, Gungor S, Haberal ET, Aydin S. Selective Regulation of Oocyte Meiotic Events Enhances Progress in Fertility Preservation Methods.. Biochem Insights 2015;8:11-21.
- Chakravarti B, Dwivedi SK, Mithal A, Chattopadhyay N. Calcium-sensing receptor in cancer: good cop or bad cop?. Endocrine 2009 Jun;35(3):271-84.
- Chen H, Kui C, Chan HC. Ca(2+) mobilization in cumulus cells: role in oocyte maturation and acrosome reaction.. Cell Calcium 2013 Jan;53(1):68-75.
- Colloton M, Shatzen E, Wiemann B, Starnes C, Scully S, Henley C, Martin D. Cinacalcet attenuates hypercalcemia observed in mice bearing either Rice H-500 Leydig cell or C26-DCT colon tumors.. Eur J Pharmacol 2013 Jul 15;712(1-3):8-15.
- Conigrave AD, Quinn SJ, Brown EM. L-amino acid sensing by the extracellular Ca2+-sensing receptor.. Proc Natl Acad Sci U S A 2000 Apr 25;97(9):4814-9.
- Conigrave AD, Ward DT. Calcium-sensing receptor (CaSR): pharmacological properties and signaling pathways.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):315-31.
- Conti M, Hsieh M, Park JY, Su YQ. Role of the epidermal growth factor network in ovarian follicles.. Mol Endocrinol 2006 Apr;20(4):715-23.
- Correia J, Michelangeli F, Publicover S. Regulation and roles of Ca2+ stores in human sperm.. Reproduction 2015 Aug;150(2):R65-76.
- Crankshaw DJ, Pistilli MJ, O'Brien YM, Sweeney EM, Dockery P, Holloway AC, Morrison JJ. The effects of extracellular calcium-sensing receptor ligands on the contractility of pregnant human myometrium in vitro.. Reprod Sci 2013 Aug;20(8):882-90.
- de Kretser D. Molecular Biology of the Male Reproductive System. .
- De Santis T, Casavola V, Reshkin SJ, Guerra L, Ambruosi B, Fiandanese N, Dalbies-Tran R, Goudet G, Dell'Aquila ME. The extracellular calcium-sensing receptor is expressed in the cumulus-oocyte complex in mammals and modulates oocyte meiotic maturation.. Reproduction 2009 Sep;138(3):439-52.
- Dell'Aquila ME, De Santis T, Cho YS, Reshkin SJ, Caroli AM, Maritato F, Minoia P, Casavola V. Localization and quantitative expression of the calcium-sensing receptor protein in human oocytes.. Fertil Steril 2006 Apr;85 Suppl 1:1240-7.
- Diez-Fraile A, Mussche S, Vanden Berghe T, Espeel M, Vandenabeele P, D'Herde KG. Expression of calcium-sensing receptor in quail granulosa explants: a key to survival during folliculogenesis.. Anat Rec (Hoboken) 2010 May;293(5):890-9.
- Fan HY, Liu Z, Mullany LK, Richards JS. Consequences of RAS and MAPK activation in the ovary: the good, the bad and the ugly.. Mol Cell Endocrinol 2012 Jun 5;356(1-2):74-9.
- Fan HY, Sun QY. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals.. Biol Reprod 2004 Mar;70(3):535-47.
- Fazleabas AT, Strakova Z. Endometrial function: cell specific changes in the uterine environment.. Mol Cell Endocrinol 2002 Jan 25;186(2):143-7.
- Feng J, Xu X, Li B, Brown E, Farris AB, Sun SY, Yang JJ. Prostate cancer metastatic to bone has higher expression of the calcium-sensing receptor (CaSR) than primary prostate cancer.. Receptors Clin Investig 2014;1(6).
- Findlay JK. Molecular Biology of the Female Reproductive System. .
- Gellersen B, Brosens IA, Brosens JJ. Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives.. Semin Reprod Med 2007 Nov;25(6):445-53.
- Gilbert T, Leclerc C, Moreau M. Control of kidney development by calcium ions.. Biochimie 2011 Dec;93(12):2126-31.
- González-Fernández L, Macías-García B, Loux SC, Varner DD, Hinrichs K. Focal adhesion kinases and calcium/calmodulin-dependent protein kinases regulate protein tyrosine phosphorylation in stallion sperm.. Biol Reprod 2013 Jun;88(6):138.
- Graca JA, Schepelmann M, Brennan SC, Reens J, Chang W, Yan P, Toka H, Riccardi D, Price SA. Comparative expression of the extracellular calcium-sensing receptor in the mouse, rat, and human kidney.. Am J Physiol Renal Physiol 2016 Mar 15;310(6):F518-33.
- Hellman P, Ridefelt P, Juhlin C, Akerström G, Rastad J, Gylfe E. Parathyroid-like regulation of parathyroid-hormone-related protein release and cytoplasmic calcium in cytotrophoblast cells of human placenta.. Arch Biochem Biophys 1992 Feb 14;293(1):174-80.
- Hjälm G, Murray E, Crumley G, Harazim W, Lundgren S, Onyango I, Ek B, Larsson M, Juhlin C, Hellman P, Davis H, Akerström G, Rask L, Morse B. Cloning and sequencing of human gp330, a Ca(2+)-binding receptor with potential intracellular signaling properties.. Eur J Biochem 1996 Jul 1;239(1):132-7.
- Hobson SA, McNeil SE, Lee F, Rodland KD. Signal transduction mechanisms linking increased extracellular calcium to proliferation in ovarian surface epithelial cells.. Exp Cell Res 2000 Jul 10;258(1):1-11.
- Hough TA, Bogani D, Cheeseman MT, Favor J, Nesbit MA, Thakker RV, Lyon MF. Activating calcium-sensing receptor mutation in the mouse is associated with cataracts and ectopic calcification.. Proc Natl Acad Sci U S A 2004 Sep 14;101(37):13566-71.
- Jones BL, Smith SM. Calcium-Sensing Receptor: A Key Target for Extracellular Calcium Signaling in Neurons.. Front Physiol 2016;7:116.
- Juhlin C, Holmdahl R, Johansson H, Rastad J, Akerström G, Klareskog L. Monoclonal antibodies with exclusive reactivity against parathyroid cells and tubule cells of the kidney.. Proc Natl Acad Sci U S A 1987 May;84(9):2990-4.
- Juhlin C, Lundgren S, Johansson H, Lorentzen J, Rask L, Larsson E, Rastad J, Akerström G, Klareskog L. 500-Kilodalton calcium sensor regulating cytoplasmic Ca2+ in cytotrophoblast cells of human placenta.. J Biol Chem 1990 May 15;265(14):8275-9.
- Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C. European Association of Urology guidelines on Male Infertility: the 2012 update.. Eur Urol 2012 Aug;62(2):324-32.
- Kashir J, Deguchi R, Jones C, Coward K, Stricker SA. Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom.. Mol Reprod Dev 2013 Oct;80(10):787-815.
- Kong WY, Tong LQ, Zhang HJ, Cao YG, Wang GC, Zhu JZ, Zhang F, Sun XY, Zhang TH, Zhang LL. The calcium-sensing receptor participates in testicular damage in streptozotocin-induced diabetic rats.. Asian J Androl 2016 Sep-Oct;18(5):803-8.
- Kornbluth S, Fissore R. Vertebrate Reproduction.. Cold Spring Harb Perspect Biol 2015 Oct 1;7(10):a006064.
- Kovacs CS. Bone development and mineral homeostasis in the fetus and neonate: roles of the calciotropic and phosphotropic hormones.. Physiol Rev 2014 Oct;94(4):1143-218.
- Kovacs CS. Calcium, phosphorus, and bone metabolism in the fetus and newborn.. Early Hum Dev 2015 Nov;91(11):623-8.
- Kovacs CS. Maternal Mineral and Bone Metabolism During Pregnancy, Lactation, and Post-Weaning Recovery.. Physiol Rev 2016 Apr;96(2):449-547.
- Kovacs CS, Chafe LL, Woodland ML, McDonald KR, Fudge NJ, Wookey PJ. Calcitropic gene expression suggests a role for the intraplacental yolk sac in maternal-fetal calcium exchange.. Am J Physiol Endocrinol Metab 2002 Mar;282(3):E721-32.
- Kovacs CS, Ho-Pao CL, Hunzelman JL, Lanske B, Fox J, Seidman JG, Seidman CE, Kronenberg HM. Regulation of murine fetal-placental calcium metabolism by the calcium-sensing receptor.. J Clin Invest 1998 Jun 15;101(12):2812-20.
- Kovacs CS, Lanske B, Hunzelman JL, Guo J, Karaplis AC, Kronenberg HM. Parathyroid hormone-related peptide (PTHrP) regulates fetal-placental calcium transport through a receptor distinct from the PTH/PTHrP receptor.. Proc Natl Acad Sci U S A 1996 Dec 24;93(26):15233-8.
- Leclerc C, Néant I, Moreau M. Early neural development in vertebrates is also a matter of calcium.. Biochimie 2011 Dec;93(12):2102-11.
- Lee KY, DeMayo FJ. Animal models of implantation.. Reproduction 2004 Dec;128(6):679-95.
- Li MW, Mruk DD, Cheng CY. Mitogen-activated protein kinases in male reproductive function.. Trends Mol Med 2009 Apr;15(4):159-68.
- Liao J, Schneider A, Datta NS, McCauley LK. Extracellular calcium as a candidate mediator of prostate cancer skeletal metastasis.. Cancer Res 2006 Sep 15;66(18):9065-73.
- Liu C, Wu GQ, Fu XW, Mo XH, Zhao LH, Hu HM, Zhu SE, Hou YP. The Extracellular Calcium-Sensing Receptor (CASR) Regulates Gonadotropins-Induced Meiotic Maturation of Porcine Oocytes.. Biol Reprod 2015 Dec;93(6):131.
- Liu XL, Lu YS, Gao JY, Marshall C, Xiao M, Miao DS, Karaplis A, Goltzman D, Ding J. Calcium sensing receptor absence delays postnatal brain development via direct and indirect mechanisms.. Mol Neurobiol 2013 Dec;48(3):590-600.
- Lundgren S, Carling T, Hjälm G, Juhlin C, Rastad J, Pihlgren U, Rask L, Akerström G, Hellman P. Tissue distribution of human gp330/megalin, a putative Ca(2+)-sensing protein.. J Histochem Cytochem 1997 Mar;45(3):383-92.
- Lundgren S, Hjälm G, Hellman P, Ek B, Juhlin C, Rastad J, Klareskog L, Akerström G, Rask L. A protein involved in calcium sensing of the human parathyroid and placental cytotrophoblast cells belongs to the LDL-receptor protein superfamily.. Exp Cell Res 1994 Jun;212(2):344-50.
- Macías-García B, Rocha A, González-Fernández L. Extracellular calcium regulates protein tyrosine phosphorylation through calcium-sensing receptor (CaSR) in stallion sperm.. Mol Reprod Dev 2016 Mar;83(3):236-45.
- Macleod RJ. CaSR function in the intestine: Hormone secretion, electrolyte absorption and secretion, paracrine non-canonical Wnt signaling and colonic crypt cell proliferation.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):385-402.
- Magoffin DA. Ovarian theca cell.. Int J Biochem Cell Biol 2005 Jul;37(7):1344-9.
- Mamillapalli R, VanHouten J, Zawalich W, Wysolmerski J. Switching of G-protein usage by the calcium-sensing receptor reverses its effect on parathyroid hormone-related protein secretion in normal versus malignant breast cells.. J Biol Chem 2008 Sep 5;283(36):24435-47.
- Mateo-Lozano S, García M, Rodríguez-Hernández CJ, de Torres C. Regulation of Differentiation by Calcium-Sensing Receptor in Normal and Tumoral Developing Nervous System.. Front Physiol 2016;7:169.
- McNeil L, Hobson S, Nipper V, Rodland KD. Functional calcium-sensing receptor expression in ovarian surface epithelial cells.. Am J Obstet Gynecol 1998 Feb;178(2):305-13.
- Meikle AW, Liu XH, Stringham JD. Extracellular calcium and luteinizing hormone effects on 22-hydroxycholesterol used for testosterone production in mouse Leydig cells.. J Androl 1991 Mar-Apr;12(2):148-51.
- Mendoza FJ, Perez-Marin CC, Garcia-Marin L, Madueño JA, Henley C, Aguilera-Tejero E, Rodriguez M. Localization, distribution, and function of the calcium-sensing receptor in sperm.. J Androl 2012 Jan-Feb;33(1):96-104.
- Metz J, Heinrich D, Forssmann WG. Ultrastructure of the labyrinth in the rat full-term placenta.. Anat Embryol (Berl) 1976 Jun 24;149(2):123-48.
- Mussche S, Leybaert L, D'Herde K. First and second messenger role of calcium. Survival versus apoptosis in serum-free cultured granulosa explants.. Ann N Y Acad Sci 2000;926:101-15.
- Nilsson BO, Ljung L. X-ray micro analyses of cations (Na, K, Ca) and anions (S, P, Cl) in uterine secretions during blastocyst implantation in the rat.. J Exp Zool 1985 Jun;234(3):415-21.
- Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy.. N Engl J Med 2001 Nov 8;345(19):1400-8.
- Nunes C, Silva JV, Silva V, Torgal I, Fardilha M. Signalling pathways involved in oocyte growth, acquisition of competence and activation.. Hum Fertil (Camb) 2015 Jun;18(2):149-55.
- Olausson H, Goldberg GR, Laskey MA, Schoenmakers I, Jarjou LM, Prentice A. Calcium economy in human pregnancy and lactation.. Nutr Res Rev 2012 Jun;25(1):40-67.
- Papadopoulou A, Gole E, Moutafi A, Sfikas C, Oehrl W, Samiotaki M, Papadimitriou A, Papaevagelou V, Nicolaidou P. Calcium sensing receptor in pregnancies complicated by gestational diabetes mellitus.. Placenta 2014 Aug;35(8):632-8.
- Peterlik M, Kállay E, Cross HS. Calcium nutrition and extracellular calcium sensing: relevance for the pathogenesis of osteoporosis, cancer and cardiovascular diseases.. Nutrients 2013 Jan 22;5(1):302-27.
- Pidasheva S, Grant M, Canaff L, Ercan O, Kumar U, Hendy GN. Calcium-sensing receptor dimerizes in the endoplasmic reticulum: biochemical and biophysical characterization of CASR mutants retained intracellularly.. Hum Mol Genet 2006 Jul 15;15(14):2200-9.
- Pistilli MJ, Petrik JJ, Holloway AC, Crankshaw DJ. Immunohistochemical and functional studies on calcium-sensing receptors in rat uterine smooth muscle.. Clin Exp Pharmacol Physiol 2012 Jan;39(1):37-42.
- Ranjzad F, Mahban A, Shemirani AI, Mahmoudi T, Vahedi M, Nikzamir A, Zali MR. Influence of gene variants related to calcium homeostasis on biochemical parameters of women with polycystic ovary syndrome.. J Assist Reprod Genet 2011 Mar;28(3):225-32.
- Riccardi D, Brennan SC, Chang W. The extracellular calcium-sensing receptor, CaSR, in fetal development.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):443-53.
- Ruan YC, Chen H, Chan HC. Ion channels in the endometrium: regulation of endometrial receptivity and embryo implantation.. Hum Reprod Update 2014 Jul-Aug;20(4):517-29.
- Ruat M, Traiffort E. Roles of the calcium sensing receptor in the central nervous system.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):429-42.
- Saidak Z, Boudot C, Abdoune R, Petit L, Brazier M, Mentaverri R, Kamel S. Extracellular calcium promotes the migration of breast cancer cells through the activation of the calcium sensing receptor.. Exp Cell Res 2009 Jul 15;315(12):2072-80.
- Sanders JL, Chattopadhyay N, Kifor O, Yamaguchi T, Brown EM. Extracellular calcium-sensing receptor (CaR) expression and its potential role in parathyroid hormone-related peptide (PTHrP) secretion in the H-500 rat Leydig cell model of humoral hypercalcemia of malignancy.. Biochem Biophys Res Commun 2000 Mar 16;269(2):427-32.
- Schepelmann M, Yarova PL, Lopez-Fernandez I, Davies TS, Brennan SC, Edwards PJ, Aggarwal A, Graça J, Rietdorf K, Matchkov V, Fenton RA, Chang W, Krssak M, Stewart A, Broadley KJ, Ward DT, Price SA, Edwards DH, Kemp PJ, Riccardi D. The vascular Ca2+-sensing receptor regulates blood vessel tone and blood pressure.. Am J Physiol Cell Physiol 2016 Feb 1;310(3):C193-204.
- Schuetz AW, Anisowicz A. Cation and protein composition of ovarian follicular fluid of the pig: relation to follicle size.. Biol Reprod 1974 Aug;11(1):64-72.
- Schultz RM, Kopf GS. Molecular basis of mammalian egg activation.. Curr Top Dev Biol 1995;30:21-62.
- Schwartz GG, John EM, Rowland G, Ingles SA. Prostate cancer in African-American men and polymorphism in the calcium-sensing receptor.. Cancer Biol Ther 2010 Jun 15;9(12):994-9.
- Shui IM, Mucci LA, Wilson KM, Kraft P, Penney KL, Stampfer MJ, Giovannucci E. Common genetic variation of the calcium-sensing receptor and lethal prostate cancer risk.. Cancer Epidemiol Biomarkers Prev 2013 Jan;22(1):118-26.
- Silvestre F, Boni R, Fissore RA, Tosti E. Ca2+ signaling during maturation of cumulus-oocyte complex in mammals.. Mol Reprod Dev 2011 Oct-Nov;78(10-11):744-56.
- Silvestre F, Fissore RA, Tosti E, Boni R. [Ca2+]i rise at in vitro maturation in bovine cumulus-oocyte complexes.. Mol Reprod Dev 2012 Jun;79(6):369-79.
- Singh N, Promkan M, Liu G, Varani J, Chakrabarty S. Role of calcium sensing receptor (CaSR) in tumorigenesis.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):455-63.
- Smajilovic S, Yano S, Jabbari R, Tfelt-Hansen J. The calcium-sensing receptor and calcimimetics in blood pressure modulation.. Br J Pharmacol 2011 Oct;164(3):884-93.
- Spencer TE, Dunlap KA, Filant J. Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption.. Mol Cell Endocrinol 2012 May 6;354(1-2):34-53.
- Squires PE, Jones PM, Younis MY, Hills CE. The calcium-sensing receptor and β-cell function.. Vitam Horm 2014;95:249-67.
- Strid H, Care A, Jansson T, Powell T. Parathyroid hormone-related peptide (38-94) amide stimulates ATP-dependent calcium transport in the Basal plasma membrane of the human syncytiotrophoblast.. J Endocrinol 2002 Nov;175(2):517-24.
- Swann K, Lai FA. Egg Activation at Fertilization by a Soluble Sperm Protein.. Physiol Rev 2016 Jan;96(1):127-49.
- Tennakoon S, Aggarwal A, Kállay E. The calcium-sensing receptor and the hallmarks of cancer.. Biochim Biophys Acta 2016 Jun;1863(6 Pt B):1398-407.
- Tfelt-Hansen J, Chattopadhyay N, Yano S, Kanuparthi D, Rooney P, Schwarz P, Brown EM. Calcium-sensing receptor induces proliferation through p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase but not extracellularly regulated kinase in a model of humoral hypercalcemia of malignancy.. Endocrinology 2004 Mar;145(3):1211-7.
- Tfelt-Hansen J, MacLeod RJ, Chattopadhyay N, Yano S, Quinn S, Ren X, Terwilliger EF, Schwarz P, Brown EM. Calcium-sensing receptor stimulates PTHrP release by pathways dependent on PKC, p38 MAPK, JNK, and ERK1/2 in H-500 cells.. Am J Physiol Endocrinol Metab 2003 Aug;285(2):E329-37.
- Tfelt-Hansen J, Schwarz P, Terwilliger EF, Brown EM, Chattopadhyay N. Calcium-sensing receptor induces messenger ribonucleic acid of human securin, pituitary tumor transforming gene, in rat testicular cancer.. Endocrinology 2003 Dec;144(12):5188-93.
- Tfelt-Hansen J, Yano S, John Macleod R, Smajilovic S, Chattopadhyay N, Brown EM. High calcium activates the EGF receptor potentially through the calcium-sensing receptor in Leydig cancer cells.. Growth Factors 2005 Jun;23(2):117-23.
- Thie M, Denker HW. In vitro studies on endometrial adhesiveness for trophoblast: cellular dynamics in uterine epithelial cells.. Cells Tissues Organs 2002;172(3):237-52.
- Tosti E. Calcium ion currents mediating oocyte maturation events.. Reprod Biol Endocrinol 2006 May 9;4:26.
- Tu CL, Bikle DD. Role of the calcium-sensing receptor in calcium regulation of epidermal differentiation and function.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):415-27.
- Tyler Miller R. Control of renal calcium, phosphate, electrolyte, and water excretion by the calcium-sensing receptor.. Best Pract Res Clin Endocrinol Metab 2013 Jun;27(3):345-58.
- Uhm SJ, Gupta MK, Yang JH, Chung HJ, Min TS, Lee HT. Epidermal growth factor can be used in lieu of follicle-stimulating hormone for nuclear maturation of porcine oocytes in vitro.. Theriogenology 2010 May;73(8):1024-36.
- Wang C, Machaty Z. Calcium influx in mammalian eggs.. Reproduction 2013 Apr;145(4):R97-R105.
- Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo-endometrium interactions.. Reprod Biomed Online 2013 Nov;27(5):461-76.
- Westwood FR. The female rat reproductive cycle: a practical histological guide to staging.. Toxicol Pathol 2008 Apr;36(3):375-84.
- Xiao LJ, Yuan JX, Li YC, Wang R, Hu ZY, Liu YX. Extracellular Ca2+-sensing receptor expression and hormonal regulation in rat uterus during the peri-implantation period.. Reproduction 2005 Jun;129(6):779-88.
- Yan S, Yuan C, Yang Q, Li X, Yang N, Liu X, Dong R, Zhang X, Yuan Z, Zhang N, Kong B. A genetic polymorphism (rs17251221) in the calcium-sensing receptor is associated with ovarian cancer susceptibility.. Oncol Rep 2015 Oct;34(4):2151-5.
- Yoshida M, Yoshida K. Sperm chemotaxis and regulation of flagellar movement by Ca2+.. Mol Hum Reprod 2011 Aug;17(8):457-65.
- Zhang C, Miller CL, Brown EM, Yang JJ. The calcium sensing receptor: from calcium sensing to signaling.. Sci China Life Sci 2015 Jan;58(1):14-27.
Citations
This article has been cited 11 times.- Anas M, Diniz WJS, Menezes ACB, Reynolds LP, Caton JS, Dahlen CR, Ward AK. Maternal Mineral Nutrition Regulates Fetal Genomic Programming in Cattle: A Review. Metabolites 2023 Apr 26;13(5).
- Lazrak A, Song W, Yu Z, Zhang S, Nellore A, Hoopes CW, Woodworth BA, Matalon S. Low molecular weight hyaluronan inhibits lung epithelial ion channels by activating the calcium-sensing receptor. Matrix Biol 2023 Feb;116:67-84.
- Chang C, He X, Di R, Wang X, Han M, Liang C, Chu M. Thyroid Transcriptomic Profiling Reveals the Follicular Phase Differential Regulation of lncRNA and mRNA Related to Prolificacy in Small Tail Han Sheep with Two FecB Genotypes. Genes (Basel) 2022 May 10;13(5).
- Liu H, Zhou D, Liu C, Zhuan Q, Luo Y, Mo X, Fu X, Hou Y. The Calcium-Sensing Receptor Is Involved in Follicle-Stimulating Hormone-Induced Cumulus Expansion in in vitro Cultured Porcine Cumulus-Oocyte Complexes. Front Cell Dev Biol 2021;9:625036.
- Wu J, Xia X, Hu Y, Fang X, Orsulic S. Identification of Infertility-Associated Topologically Important Genes Using Weighted Co-expression Network Analysis. Front Genet 2021;12:580190.
- Galliou JM, Kiser JN, Oliver KF, Seabury CM, Moraes JGN, Burns GW, Spencer TE, Dalton J, Neibergs HL. Identification of Loci and Pathways Associated with Heifer Conception Rate in U.S. Holsteins. Genes (Basel) 2020 Jul 8;11(7).
- Shirak A, Zak T, Dor L, Benet-Perlberg A, Weller JI, Ron M, Seroussi E. Quantitative trait loci on LGs 9 and 14 affect the reproductive interaction between two Oreochromis species, O. niloticus and O. aureus. Heredity (Edinb) 2019 Mar;122(3):341-353.
- Mishra AK, Kumar A, Swain DK, Yadav S, Nigam R. Insights into pH regulatory mechanisms in mediating spermatozoa functions. Vet World 2018 Jun;11(6):852-858.
- Liu H, Li W, Zhang Y, Zhang Z, Shang X, Zhang L, Zhang S, Li Y, Somoza AV, Delpi B, Gerton GL, Foster JA, Hess RA, Pazour GJ, Zhang Z. IFT25, an intraflagellar transporter protein dispensable for ciliogenesis in somatic cells, is essential for sperm flagella formation. Biol Reprod 2017 May 1;96(5):993-1006.
- Wang M, Yang L, Sun G, Shao Y, Liu Y, Yang H, Wang Y, Zhang M, Shang Y, Gu X. Assessment of the Effect of Leonurine Hydrochloride in a Mouse Model of PCOS by Gene Expression Profiling. Genes (Basel) 2024 Apr 18;15(4).
- Ahmed A, Saleem MA, Saeed F, Afzaal M, Imran A, Akram S, Hussain M, Khan A, Al Jbawi E. A comprehensive review on the impact of calcium and vitamin D insufficiency and allied metabolic disorders in females. Food Sci Nutr 2023 Sep;11(9):5004-5027.