Effect of lysophosphatidic acid on the follicular development and the ‎expression of lysophosphatidic acid receptor genes during in vitro culture of ‎mouse ovary

Document Type: Original Article

Authors

1 Department of Anatomy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

2 Department of Biotechnology, Faculty of Biological Sciences, Alzahra University, Tehran, Iran

Abstract

Lysophosphatidic acid (LPA) known as a serum-derived growth factor, is involved in several cell physiological functions in the female reproductive system including: oocyte maturation, in vitro fertilization and embryo implantation by its transmembrane G protein-coupled receptors. The aim of the present study was to examine the effect of LPA on in vitro follicular development of mouse ovarian tissue. Neonatal mouse ovarian tissues were cultured in five different concentrations of LPA (0, 5, 10, 20 and 40 µM). The developmental competence and the function of cultured ovarian tissue were assessed by morphological study using hematoxylin and eosin staining and hormonal analysis. The expression of LPA receptor (LPAR 1-4) genes were analyzed by real-time RT-PCR. The proportion of preantral follicles and the level of E2 hormone were significantly higher in the 20 µM LPA-treated group than those in the other treatment groups. There was a significant difference in the expression of LPAR 1-4 genes in 20 µM LPA treated group in comparison with 0 µM LPA (control group) treated and non-cultured groups. In addition, the expression of LPAR1 gene was higher than other receptor genes in all studied groups. In conclusion supplementation of the media with 20 µM LPA, could improve the survival and developmental potential of follicles and it had positive effects on cell function and stimulation of E2 synthesis in mouse whole ovarian tissues.

Keywords

Main Subjects


 

  1. Adhikari D. In vitro activation of dormant follicles for fertility preservation. Adv Exp Med Biol 2013; 761: 29-42.
  2. Jin SY, Lei L, Shikanov A, et al. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril. 2010; 93(8): 2633-2639.
  3. Hirao Y. Isolation of ovarian components essential for growth and development of mammalian oocytes in vitro. J Reprod Dev 2012; 58(2): 167-174.
  4. Filatov MA, Khramova YV, Kiseleva MV, et al. Female fertility preservation strategies: cryopreservation and ovarian tissue in vitro culture, current state of the art and future perspectives. Zygote 2016; 24(5): 635-653.
  5. Silva JR, van den Hurk R, Figueiredo JR. Ovarian follicle development in vitro and oocyte competence: Advances and challenges for farm animals. Domest Anim Endocrinol 2016; 55: 123-135.
  6. Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 1996; 54(1): 197-207.
  7. Devine PJ, Rajapaksa KS, Hoyer PB. In vitro ovarian tissue and organ culture: A review. Front Biosci 2002; 7: 1979-1989.
  8. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006; 132(2): 191-206.
  9. Fortune JE, Yang MY, Muruvi W. In vitro and in vivo regulation of follicular formation and activation in cattle. Reprod Fertil Dev 2011; 23(1): 15-22.
  10. Gupta PS, Nandi S. Isolation and culture of preantral follicles for retrieving oocytes for the embryo production: Present status in domestic animals. Reprod Domest Anim 2012; 47(3): 513-519.
  11. Yutong Z, Viswanathan N. Lysophosphatidic acid (LPA) and its receptors: Role in airway inflammation and remodeling. Biochim Biophys Acta 2013; 831(1): 86-92.
  12. Boruszewska D, Sinderewicz E, Kowalczyk-Zieba I, et al. The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus–oocyte complexes: Cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence. Reprod Biol Endocrinol 2015; 13: 44.
  13. McIntyre TM, Pontsler AV, Silva AR, et al. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPAR gamma agonist. Proc Natl Acad Sci USA 2003; 100(1): 131-136.
  14. Waters CM, Saatian B, Moughal NA, et al. Integrin signaling regulates the nuclear localization and function of the lysophosphatidic acid receptor-1 (LPA1) in mammalian cells. Biochem J 2006; 398: 55-62.
  15. Murch O, Collin M, Thiemermann C. Lysophosphatidic acid reduces the organ injury caused by endotoxemia-a role for G-protein-coupled receptors and peroxisome proliferator activated receptor-gamma. Shock 2007; 27(1): 48-54.
  16. Boruszewska D, Kowalczyk-Zieba I, Sinderewicz E, et al. The effect of lysophosphatidic acid together with interferon tau on the global transcriptomic profile in bovine endometrial cells. Theriogenology 2017; 92: 111-120.
  17. Hinokio K, Yamano S, Nakagawa K, et al. Lysophosphatidic acid stimulates nuclear and cytoplasmic maturation of golden hamster immature oocytes in vitro via cumulus cells. Life Sci 2002; 70(7): 759-767.
  18. Wocławek-Potocka I, Rawińska P, Kowalczyk-Zieba I, et al. Lysophosphatidic acid (LPA) signaling in human and ruminant reproductive tract. Mediators Inflamm 2014; 2014: http://dx.doi.org/10.1155/2014/649702.
  19. Jo JW, Jee BC, Suh CS, et al. Addition of lysophosphatidic acid to mouse oocyte maturation media can enhance fertilization and developmental competence. Hum Reprod 2014; 29(2): 234-241.
  20. Sheng X, Yung YC, Chen A, Chun J. Lysophosphatidic acid signaling in development. Development 2015; 142(8): 1390-1395.
  21. Contos JJ, Fukushima N, Weiner JA, et al. Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 2000; 97(24): 13384-13389.
  22. Onno K, Wouter HM. Ras-MAP kinase signaling by lysophosphatidic acid and other G protein coupled receptor agonists. Oncogene 2001; 20: 1540-1546.
  23. Reddy VS, Singh AK, Rajasekharan R. The Saccharomyces cerevisiae PHM8 gene encodes a soluble magnesium-dependent lysophosphatidic acid phosphatase. J Biol Chem 2008; 283(14): 8846-8854.
  24. Koh JS, Lieberthal W, Heydrick S, et al. Lyso-phosphatidic acid is a major serum noncytokine survival factor for murine macrophages which acts via the phosphatidylinositol 3-kinase signaling pathway. J Clin Invest 1998; 102(4): 716-727.
  25. Anliker B, Choi JW, Lin ME, et al. Lysophosphatidic acid (LPA) and its receptor, LPA1, influence embryonic Schwann cell migration, myelination, and cell-to-axon segregation. Glia 2013; 61(12): 2009-2022.
  26. Mori K, Kitayama J, Aoki J, et al. Submucosal connective tissue-type mast cells contribute to the production of lysophosphatidic acid (LPA) in the gastrointestinal tract through the secretion of autotaxin (ATX)/lysophospholipase D (lysoPLD). Virchows Arch 2007; 451(1): 47-56.
  27. Ye X. Lysophospholipid signaling in the function and pathology of the reproductive system. Hum Reprod Update 2008; 14(5): 519-536.
  28. Woclawek-Potocka I, Kondraciuk K, Skarzynski DJ. Lysophosphatidic acid stimulates prostaglandin E2 production in cultured stromal endometrial cells through LPA1 receptor. Exp Biol Med (Maywood) 2009; 234(8): 986-993.
  29. Kowalczyk-Zieba I, Boruszewska D, Saulnier-Blache JS, et al. Lysophosphatidic acid action in the bovine corpus luteum: An in vitro study. J Reprod Dev 2012; 58(6): 661-671.
  30. Lee Z, Cheng CT, Zhang H, et al. Role of LPA4/p2y9/ GPR23 in negative regulation of cell motility. Mol Biol Cell 2008; 19(12): 5435-5445.
  31. Ye X, Chun J. Lysophosphatidic acid (LPA) signaling in vertebrate reproduction. Trends Endocrinol Metab 2010; 21(1): 17-24.
  32. Ye X, Hama K, Contos JJ, et al. LPA3-mediated lyso-phosphatidic acid signaling in embryo implantation and spacing. Nature 2005; 435(7038): 104-108.
  33. Zhao Y, Natarajan V. Lysophosphatidic acid (LPA) and its receptors: Role in airway inflammation and remodeling. Biochim Biophys Acta 2013; 1831(1): 86-92.
  34. Noguchi K, Ishii S, Shimizu T. Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J Biol Chem 2003; 278(28): 25600-25606.
  35. Kitayama J, Shida D, Sako A, et al. Over-expression of lysophosphatidic acid receptor-2 in human invasive ductal carcinoma. Breast Cancer Res 2004; 6(6):
    R640-646.
  36. Liu Z, Armant DR. Lysophosphatidic acid regulates murine blastocyst development by transactivation of receptors for heparin-binding EGF-like growth factor. Exp Cell Res 2004; 296(2): 317-326.
  37. Hinckley M, Vaccari S, Horner K, et al. The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol 2005; 287(2): 249-261.
  38. Nakamoto T, Yasuda K, Yasuhara M, et al. Expression of the endothelial cell differentiation gene 7 (EDG-7), a lysophosphatidic acid receptor, in ovarian tumor. J Obstet Gynaecol Res 2005; 31(4): 344-351.
  39. Kotarsky K, Boketoft A, Bristulf J, et al. Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes. J Pharmacol Exp Ther 2006; 318(2): 619-628.
  40. Kamińska K, Wasielak M, Bogacka I, et al. Quantitative expression of lysophosphatidic acid receptor 3 gene in porcine endometrium during the periimplantation period and estrous cycle. Prostaglandins Other Lipid Mediat 2008; 85(1-2): 26-32.
  41. Lee J, Lee JR, Youm HW, et al. Effect of preoperative simvastatin treatment on transplantation of cryopreserved-warmed mouse ovarian tissue quality. Theriogenology 2015; 83: 285- 293.
  42. OligoAnalyzer 3.1. Available at: https://eu.idtdna.com/ calc/analyzer. Accessed. May 13, 2017.
  43. Amoushahi M, Salehnia M, Mowla SJ, Ghorbanmehr N. Morphological and molecular aspects of in vitro culture of preantral follicles derived from vitrified ovarian. Cell J 2017; 19(3): 332-342.
  44. Abdi S, Salehnia M, Hosseinkhani S. Kit ligand decreases the incidence of apoptosis in cultured vitrified whole mouse ovaries. Reproduction Biomed Online 2015; 30(5): 493-503.
  45. Makker A, Goel MM, Mahdi AA. PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: An update. J Mol Endocrinol 2014; 53(3): 103-118.
  46. Boruszewska D, Torres AC, Kowalczyk-Zieba I, et al. The effect of lysophosphatidic acid during in vitro maturation of bovine oocytes: embryonic development and mRNA abundances of genes involved in apoptosis and oocyte competence. Mediators Inflamm 2014; doi: 10.1155/2014/670670.
  47. Huang MC, Lee HY, Yeh CC, Kong Y, et al. Induction of protein growth factor systems in the ovaries of transgenic mice overexpressing human type 2 lysophosphatidic acid G protein-coupled receptor (LPA2). Oncogene 2004; 23(1): 122-129.
  48. Budnik LT, Brunswig-Spickenheier B, Mukhopadhyay AK. Lysophosphatidic acid signals through mitogen-activated protein kinase-extracellular signal regulated kinase in ovarian theca cells expressing the LPA1/edg2-receptor: Involvement of a nonclassical pathway? Mol Endocrinol 2003; 17 (8): 1593-1606.
  49. Zhao Y, Zhang Y, Li J, et al. MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling. J Cell Physiol 2018; 233(1):226-237.
  50. Boruszewska D, Sinderewicz E, Kowalczyk-Zieba I, et al. Influence of lysophosphatidic acid on estradiol production and follicle stimulating hormone action in bovine granulosa cells. Reprod Biol 2013; 13(4): 344-347.