Expression pattern of olfactory receptor genes in human cumulus cells as an indicator for competent oocyte selection

Expression pattern of olfactory receptor genes in human cumulus cells as an indicator for competent oocyte selection

Odorant or olfactory receptors are mainly localized in the olfactory epithelium for the perception of different odors.Interestingly, many ectopic olfactory receptors with low expression levels have recently been found in nonolfactory tissues to involve inlocal functions. Therefore, we investigated the probable role of the olfactory signaling pathway in the surrounding microenvironmentof oocyte. This study included 22 women in intracytoplasmic sperm injection cycle. The expression of olfactory target molecules incumulus cells surrounding the growing and mature oocytes was evaluated by Western blotting and real-time polymerase chain reaction.Additionally, integrated bioinformatics analyses were carried out and 6 ectopic olfactory receptors were selected for further evaluation.The initiation of olfactory transduction cascade in cumulus cells of competent oocytes was confirmed by analyzing the expression ofadenylyl cyclase type 3 and olfactory market protein. Moreover, the expression pattern of the selected olfactory receptors was evaluatedand OR10H2 was selected due to a high level of expression in mature fertile oocytes. We suggested that OR10H2 could be consideredas a reliable biomarker for oocyte selection in assisted reproduction technique programs. However, further studies are required toelucidate the role of olfactory transduction cascade in embryo quality and implantation.

___

  • Albeanu DF, Provost AC, Agarwal P, Soucy ER, Zak JD et al. (2018). Olfactory marker protein (OMP) regulates formation and refinement of the olfactory glomerular map. Nature Communication 9 (1): 5073. doi: 10.1038/s41467-018-07544- 9.
  • Amireault P, Dube F (2005). Intracellular cAMP and calcium signaling by serotonin in mouse cumulus-oocyte complexes. Molcular Pharmacology 68 (6): 1678-1687. doi: 10.1124/ mol.104.010124.
  • Antal MC, Bénardais K, Samama B, Auger C, Schini-Kerth V et al. (2017). Adenylate cyclase type III is not a ubiquitous marker for all primary cilia during development. PLoS One 12 (1): e0170756. doi: 10.1371/journal.pone.0170756.
  • Bhattarai JP, RoaJ, HerbisonAE, and HanSK(2014). Serotonin acts through 5-HT1 and 5-HT2 receptors to exert biphasic actions on GnRH neuron excitability in the mouse. Endocrinology 155 (2): 513-524. doi: 10.1210/en.2013-1692.
  • Carvacho I, Maier TJ, Machaca K (2018). Ion channel function during oocyte maturation and fertilization. Frontiers in Cell and Developmental Biology 6: 63. doi: 10.3389/fcell.2018.00063.
  • Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N et al. (2007). Integration of biological networks and gene expression data using Cytoscape. Nature protocol 2 (10): 2366. doi: 10.1038/ nprot.2007.324.
  • Giacomo Di, Camaioni MA, Klinger FG, Bonfiglio R, Salustri A (2016). Cyclic AMP-elevating agents promote cumulus cell survival and hyaluronan matrix stability, thereby prolonging the time of mouse oocyte fertilizability. Journal of Biological Chemistry 291 (8): 3821-3836. doi: 10.1074/jbc.M115.680983.
  • Dibattista M, Reisert J (2016). The odorant receptor-dependent role of olfactory marker protein in olfactory receptor neurons. Journal of Neuroscience 36 (10): 2995-3006. doi: 10.1523/ JNEUROSCI.4209-15.2016.
  • Doty RL, Kamath V (2014). The influences of age on olfaction: a review. Frontiers in Psychology 5: 20. doi: 10.3389/ fpsyg.2014.00020.
  • Ferrer I, Garcia-Esparcia P, Carmona M, Carro E, Aronica E et al. (2016). Olfactory receptors in non-chemosensory organs: the nervous system in health and disease. Frontiers in Aging Neuroscience 8: 163. doi: 10.3389/fnagi.2016.00163.
  • Flegel C, Manteniotis S, Osthold S, Hatt H, Gisselmann G (2013). Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS One 2013; 8 (2): e55368. doi: 10.1371/ journal.pone.0055368.
  • Flegel C, Vogel F, Hofreuter A, Schreiner BS, Osthold S et al. (2016). Characterization of the olfactory receptors expressed in human spermatozoa. Frontiers in Molecular Biosciences 2: 73. doi: 10.3389/fmolb.2015.00073.
  • Frohlich P, Meston C (2000). Evidence that serotonin affects female sexual functioning via peripheral mechanisms. Physiology & Behavior 71 (3-4): 383-393. doi: 10.1016/S0031- 9384(00)00344-9.
  • Guidobaldi HA, Teves ME, Uñates DR, Anastasía A, Giojalas LC (2008). Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PloS one 3 (8). doi: 10.1371/journal.pone.0003040.
  • Horner K, Livera G, Hinckley M, Trinh K, Storm D, et al. (2003). Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Developmental Biology 258 (2): 385-396. doi: 10.1016/S0012-1606(03)00134-9.
  • Hosseini E, Mehraein F, Shahhoseini M, Karimian L, Nikmard F et al. (2016). Epigenetic alterations of CYP19A1 gene in Cumulus cells and its relevance to infertility in endometriosis. Journal of Assisted Reproduction and Genetics 33 (8): 1105-1113. doi: 10.1007/s10815-016-0727-z.
  • Hunter R, Gadea J (2014). Cross-talk between free and bound spermatozoa to modulate initial sperm: egg ratios at the site of fertilization in the mammalian oviduct. Theriogenology 82 (3): 367-372. doi: 10.1016/j.theriogenology.2014.04.015.
  • Kang N, Kim H, Jae Y, Lee N, Ku CR et al. (2015). Olfactory marker protein expression is an indicator of olfactory receptorassociated events in non-olfactory tissues. PLoS One 10 (1): e0116097. doi: 10.1371/journal.pone.0116097.
  • Kang N, Koo J (2012). Olfactory receptors in nonchemosensory tissues. BMB Reports 45: 612. doi: 10.5483/ BMBRep.2012.45.11.232.
  • Kim GH, Lee IK, Fritz L (1996). Cell-cell recognition during fertilization in a red alga, Antithamnion sparsum (Ceramiaceae, Rhodophyta). Plant and Cell Physiology 37: 621-628. doi: 10.1093/oxfordjournals.pcp.a028990.
  • Kim HS, Yumkham S, Choi JH, Son GH, Kim K et al. (2006). Serotonin stimulates GnRH secretion through the c-SrcPLC γ1 pathway in GT1–7 hypothalamic cells. Journal of Endocrinology 190 (3): 581-591. doi: 10.1677/joe.1.06727.
  • Magli MC, Jones GM, Lundin K, Van den Abbeel E (2012). Atlas of human embryology: from oocytes to preimplantation embryos. Human Reproduction 27(Suppl1): i1. doi: 10.1093/ humrep/des229.
  • Menkveld R (2010). Clinical significance of the low normal sperm morphology value as proposed in the fifth edition of the WHO Laboratory Manual for the Examination and Processing of Human Semen. Asian journal of Andrology 12 (1): 47. doi: 10.1038/aja.2009.14.
  • Milardi D, Colussi C, Grande G, Vincenzoni F, Pierconti F et al. (2018). Olfactory receptors in semen and in the male tract: from proteome to proteins. Frontiers in Endocrinology 8: 379. doi: 10.3389/fendo.2017.00379.
  • Ozgur K, Bulut H, Berkkanoglu M, Coetzee K, Ay S (2015). Oocyte maturation-index as measure of oocyte cohort quality; a retrospective analysis of 3135 ICSI cycles. Middle East Fertility Society Journal 20 (1): 37-42. doi: 10.1016/j.mefs.2014.04.005.
  • Salehi E, Aflatoonian R, Moeini A, Yamini N, Asadi E et al. (2017). Apoptotic biomarkers in cumulus cells in relation to embryo quality in polycystic ovary syndrome.Archives of Gynecology and Obstetrics 296 (6): 1219-1227. doi: 10.1007/s00404-017- 4523-5.
  • Sen A, Caiazza F (2013). Oocyte maturation: a story of arrest and release.Frontiers in Bioscience 5: 451-477. doi: 10.2741/S383.
  • Sharma RK, Sabanegh E, Mahfouz R, Gupta S, Thiyagarajan A et al. (2010). TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 76 (6): 1380-1386. doi: 10.1016/j.urology.2010.04.036.
  • Soonthornsumrith B, Saetan J, Kruangkum T, Thongbuakaew T, Senarai T et al. (2018). Three-dimensional organization of the brain and distribution of serotonin in the brain and ovary, and its effects on ovarian steroidogenesis in the giant freshwater prawn, Macrobrachium rosenbergii. Invertebrate Neuroscience 18 (2): 5. doi: 10.1007/s10158-018-0209-3.
  • Sun T, Diaz FJ (2019). Ovulatory signals alter granulosa cell behavior through YAP1 signaling. Reproductive Biology and Endocrinology17 (1): 113. doi: 10.1186/s12958-019-0552-1.
  • Teves ME, Guidobaldi HA, Uñates DR, Sanchez R, Miska W et al. (2009). Molecular mechanism for human sperm chemotaxis mediated by progesterone. PloS one 4 (12): e8211. doi: 10.1371/ journal.pone.0008211.
  • UphouseL (2014). Pharmacology of serotonin and female sexual behavior. Pharmacology Biochemistry and Behavior 121: 31- 42. doi: 10.1016/j.pbb.2013.11.008.
  • YangC-K, Wu RS-C, Wu C-H, LinTR-Y, Tsai H-D (2015). Sleep deprivation enhances peripheral serotonin secretion to regulate the large follicle steroidogenesis of rats. Taiwanese Journal of Obstetrics and Gynecology 54 (3): 260-265. doi: 10.1016/j.tjog.2014.10.007.
  • Yoshida M, Yoshida K (2011). Sperm chemotaxis and regulation of flagellar movement by Ca2+. Molecular Human Reproduction 17 (8): 457-465. doi: 10.1093/molehr/gar041.
  • Zhang Y, Wu LL, Wan X, Wang HH, Li XH et al. (2019). Loss of PKC mu function induces cytoskeletal defects in mouse oocyte meiosis. Journal of Cellular Physiology 234 (10): 18513-18523. doi:10.1002/jcp.28487.
Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

The inhibitory effect of melatonin on osteoclastogenesis of RAW 264.7 cells in low concentrations of RANKL and MCSF

Menemşe GÜMÜŞDERELİOĞLU, Hala JARRAR, Damla ÇETİN ALTINDAL

Wai Feng LİM, Suriati Mohd NASİR, Lay Kek TEH, Richard Johari JAMES, Mohd Hafidz Mohd IZHAR, Mohd Zaki SALLEH

Neda DAEİ-FARSHBAF, Reza AFLATOONİAN, Fatemeh-sadat AMJADİ, Sara TALEAHMAD, Mahnaz ASHRAFİ, Mehrdad BAKHTİYARİ

Expression of soluble, active, fluorescently tagged hephaestin in COS and CHO cell lines

Kaila S. SRAI, Basharut A. SYED, Elif Sibel ASLAN, Kenneth N. WHITE, Robert W. EVANS

Gokhan KARAKULAH, Cihangir YANDİM

Expression pattern of olfactory receptor genes in human cumulus cells as an indicator for competent oocyte selection

Sara TALEAHMAD, Neda DAEI FARSHBAF, Fatemeh Sadat AMJADI, Mehrdad BAKHTIYARI, Reza AFLATOONIAN, Mahnaz ASHRAFI

Genome-wide identification of Chiari malformation type I associated candidate genes and chromosomal variations

Timuçin AVŞAR, Şeyma ÇALIŞ, Türker KILIÇ, Baran YILMAZ, Gülden DEMİRCİ OTLUOĞLU, Can HOLYAVKİN

Kaan ADACAN, Pinar OBAKAN YERLİKAYA

The methanolic extract of Garcinia atroviridis (MeGa) reduces body weight and food intake, and improves lipid profiles by altering the lipid metabolism: a rat model

Wai Feng LIM, Suriati Mohd NASIR, Lay Kek TEH, Richard Johari JAMES, Mohd Zaki SALLEH, Mohd Hafidz Mohd IZHAR

PtdIns(4,5)P2 and PtdIns(3,4,5)P3 dynamics during focal adhesions assembly and disassembly in a cancer cell line

Dhurgham ALFAHAD, Philip DASH, Salem ALHARETHI, Bandar ALHARBI, Khatab MAWLOOD