In vitro decidualisation of human endometrial stromal cells is enhanced by seminal fluid extracellular vesicles

References

• Authority HFAE. Fertility treatment 2014 - Trends and figures. 2016. p. 1–13 https://www.hfea.gov.uk/about-us/publications/
   Google Scholar
• Gardner DK, Surrey E, Minjarez D, et al. Single blastocyst transfer: a prospective randomized trial. Fertil Steril. 2004;81(3):551–555.
   PubMed Web of Science ®Google Scholar
• Salamonsen LA, Nie G, Hannan NJ, et al. Society for reproductive biology founders’ lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod Fertil Dev. 2009;21(7):923–934.
   PubMed Web of Science ®Google Scholar
• Dunn CL, Kelly RW, Critchley HO. Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed Online. 2003;7(2):151–161.
   Google Scholar
• Ben-Jonathan N, Mershon JL, Allen DL, et al. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr Rev. 1996;17(6):639–669.
   PubMed Web of Science ®Google Scholar
• Bole-Feysot C, Goffin V, Edery M, et al. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998;19(3):225–268.
   PubMed Web of Science ®Google Scholar
• Marano RJ, Ben-Jonathan N. Minireview: extrapituitary prolactin: an update on the distribution, regulation, and functions. Mol Endocrinol. 2014;28(5):622–633.
   PubMedGoogle Scholar
• Fowler DJ, Nicolaides KH, Miell JP. Insulin-like growth factor binding protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum Reprod Update. 2000;6(5):495–504.
   PubMed Web of Science ®Google Scholar
• Doyle U, Sampson N, Zenzmaier C, et al. Seminal plasma enhances and accelerates progesterone-induced decidualisation of human endometrial stromal cells. Reprod Fertil Dev. 2012;24(3):517–522.
   Web of Science ®Google Scholar
• Narukawa S, Kanzaki H, Inoue T, et al. Androgens induce prolactin production by human endometrial stromal cells in vitro. J Clin Endocrinol Metab. 1994;78(1):165–168.
   Web of Science ®Google Scholar
• Crawford G, Ray A, Gudi A, et al. The role of seminal plasma for improved outcomes during in vitro fertilization treatment: review of the literature and meta-analysis. Hum Reprod Update. 2015;21(2):275–284.
   Web of Science ®Google Scholar
• Bromfield JJ. Seminal fluid and reproduction: much more than previously thought. J Assist Reprod Genet. 2014;31(6):627–636.
   PubMed Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383.
   PubMed Web of Science ®Google Scholar
• Minciacchi VR, Spinelli C, Reis-Sobreiro M, et al. MYC mediates large oncosome-induced fibroblast reprogramming in prostate cancer. Cancer Res. 2017;77(9):2306–2317.
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113(8):E968–77.
   PubMed Web of Science ®Google Scholar
• Tannetta D, Dragovic R, Alyahyaei Z, et al. Extracellular vesicles and reproduction-promotion of successful pregnancy. Cell Mol Immunol. 2014;11(6):548–563.
   Web of Science ®Google Scholar
• Aalberts M, Stout TA, Stoorvogel W. Prostasomes: extracellular vesicles from the prostate. Reproduction. 2014;147(1):R1–14.
   PubMed Web of Science ®Google Scholar
• Sullivan R. Epididymosomes: role of extracellular microvesicles in sperm maturation. Front Biosci (Schol Ed). 2016;8:106–114.
   Google Scholar
• Brody I, Ronquist G, Gottfries A. Ultrastructural localization of the prostasome - an organelle in human seminal plasma. Ups J Med Sci. 1983;88(2):63–80.
   Web of Science ®Google Scholar
• Hoog JL, Lotvall J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J Extracell Vesicles. 2015;4:28680.
   PubMed Web of Science ®Google Scholar
• Park KH, Kim B-J, Kang J, et al. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 2011;4(173):ra31.
   Web of Science ®Google Scholar
• Nishida M. The Ishikawa cells from birth to the present. Hum Cell. 2002;15(3):104–117.
   Google Scholar
• Samalecos A, Reimann K, Wittmann S, et al. Characterization of a novel telomerase-immortalized human endometrial stromal cell line, St-T1b. Reprod Biol Endocrinol. 2009;7:76.
   Web of Science ®Google Scholar
• Bode CJ, Jin H, Rytting E, et al. In vitro models for studying trophoblast transcellular transport. Methods Mol Med. 2006;122:225–239.
   PubMedGoogle Scholar
• Welton JL, Webber JP, Botos L-A, et al. Ready-made chromatography columns for extracellular vesicle isolation from plasma. J Extracell Vesicles. 2015;4:27269.
   PubMed Web of Science ®Google Scholar
• Pinheiro J, Bates DM. Mixed-effects models in S and S-PLUS. New York, Springer; 2000.
   Google Scholar
• Dragovic RA, Jha RK, Kumar V, et al. Multicolor flow cytometry and nanoparticle tracking analysis of extracellular vesicles in the plasma of normal pregnant and pre-eclamptic women. Biol Reprod. 2013;89(6):151.
   PubMed Web of Science ®Google Scholar
• Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018; 75(2): 193–208.
   Web of Science ®Google Scholar
• Szabó-Taylor, KE, Toth EA, Balogh AM, et al. Monocyte activation drives preservation of membrane thiols by promoting release of oxidised membrane moieties via extracellular vesicles. Free Radic Biol Med. 2017;108:56–65.
   Web of Science ®Google Scholar
• Ronquist GK, Larsson A, Stavreus-Evers A, et al. Prostasomes are heterogeneous regarding size and appearance but affiliated to one DNA-containing exosome family. Prostate. 2012;72(16):1736–1745.
   Web of Science ®Google Scholar
• Daniel JC Jr., Jetton AE, Chilton BS. Prolactin as a factor in the uterine response to progesterone in rabbits. J Reprod Fertil. 1984;72(2):443–452.
   Google Scholar
• Chilton BS, Daniel JC Jr. Differences in the rabbit uterine response to progesterone as influenced by growth hormone or prolactin. J Reprod Fertil. 1987;79(2):581–587.
   Google Scholar
• Mati JK, Mugambi M, Muriuki PB, et al. Effect of prolactin on isolated rabbit myometrium. J Endocrinol. 1974;60(2):379–380.
   Web of Science ®Google Scholar
• Franchi A, Bocca S, Anderson S, et al. Expression of milk fat globule EGF-factor 8 (MFG-E8) mRNA and protein in the human endometrium and its regulation by prolactin. Mol Hum Reprod. 2011;17(6):360–371.
   Web of Science ®Google Scholar
• Ain R, Dai G, Dunmore JH, et al. A prolactin family paralog regulates reproductive adaptations to a physiological stressor. Proc Natl Acad Sci USA. 2004;101(47):16543–16548.
   PubMed Web of Science ®Google Scholar
• Stefanoska I, Jovanović Krivokuća M, Vasilijić S, et al. Prolactin stimulates cell migration and invasion by human trophoblast in vitro. Placenta. 2013;34(9):775–783.
   Web of Science ®Google Scholar
• Luciano AA, Maslar IA, Kusmik WF, et al. Stimulatory activity of serum on prolactin production by human decidua. Am J Obstet Gynecol. 1980;138(6):665–669.
   Web of Science ®Google Scholar
• Matsui N, Kawano Y, Nakamura S, et al. Changes in vascular endothelial growth factor production associated with decidualization by human endometrial stromal cells in vitro. Acta Obstet Gynecol Scand. 2004;83(2):138–143.
   Web of Science ®Google Scholar
• Robertson SA, Sharkey DJ. Seminal fluid and fertility in women. Fertil Steril. 2016;106(3):511–519.
   PubMed Web of Science ®Google Scholar
• Robertson SA, Guerin LR, Bromfield JJ, et al. Seminal fluid drives expansion of the CD4+CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod. 2009;80(5):1036–1045.
   Web of Science ®Google Scholar
• McGuane JT, Watson KM, Zhang J, et al. Seminal plasma promotes lesion development in a xenograft model of endometriosis. Am J Pathol. 2015;185(5):1409–1422.
   Web of Science ®Google Scholar
• Pereira Suarez AL, López-Rincón G, Martínez Neri PA, et al. Prolactin in inflammatory response. Adv Exp Med Biol. 2015;846:243–264.
   PubMed Web of Science ®Google Scholar
• Costanza M, Binart N, Steinman L, et al. Prolactin: a versatile regulator of inflammation and autoimmune pathology. Autoimmun Rev. 2015;14(3):223–230.
   Web of Science ®Google Scholar
• Matera L, Cesano A, Bellone G, et al. Modulatory effect of prolactin on the resting and mitogen-induced activity of T, B, and NK lymphocytes. Brain Behav Immun. 1992;6(4):409–417.
   Web of Science ®Google Scholar
• Gerli R, Rambotti P, Nicoletti I, et al. Reduced number of natural killer cells in patients with pathological hyperprolactinemia. Clin Exp Immunol. 1986;64(2):399–406.
   Web of Science ®Google Scholar
• Chang HJ, Lee JH, Hwang KJ, et al. Transforming growth factor (TGF)-beta1-induced human endometrial stromal cell decidualization through extracellular signal-regulated kinase and Smad activation in vitro: peroxisome proliferator-activated receptor gamma acts as a negative regulator of TGF-beta1. Fertil Steril. 2008;90(4 Suppl):1357–1365.
   Google Scholar
• Lane B, Oxberry W, Mazella J, et al. Decidualization of human endometrial stromal cells in-Vitro - Effects of progestin and relaxin on the ultrastructure and production of decidual secretory proteins. Hum Reprod. 1994;9(2):259–266.
   Web of Science ®Google Scholar
• Moy E, Kimzey LM, Nelson LM, et al. Glycoprotein hormone alpha-subunit functions synergistically with progesterone to stimulate differentiation of cultured human endometrial stromal cells to decidualized cells: a novel role for free alpha-subunit in reproduction. Endocrinology. 1996;137(4):1332–1339.
   Web of Science ®Google Scholar
• Frank GR, Brar AK, Cedars MI, et al. Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology. 1994;134(1):258–263.
   Web of Science ®Google Scholar
• Oliw EH, Fabiani R, Johansson L, et al. Arachidonic acid 15-lipoxygenase and traces of E prostaglandins in purified human prostasomes. J Reprod Fertil. 1993;99(1):195–199.
   Google Scholar
• Inder KL, Zheng YZ, Davis MJ, et al. Expression of PTRF in PC-3 Cells modulates cholesterol dynamics and the actin cytoskeleton impacting secretion pathways. Mol Cell Proteomics. 2012;11(2):M111.012245.
   Web of Science ®Google Scholar
• Zervomanolakis I, Ott HW, Hadziomerovic D, et al. Physiology of upward transport in the human female genital tract. Ann N Y Acad Sci. 2007;1101:1–20.
   PubMed Web of Science ®Google Scholar
• Vashisht M, Rani P, Onteru SK, et al. Curcumin encapsulated in milk exosomes resists human digestion and possesses enhanced intestinal permeability in vitro. Appl Biochem Biotechnol. 2017;183:993–1007.
   Web of Science ®Google Scholar
• Chen CC, Liu L, Ma F, et al. Elucidation of exosome migration across the blood-brain barrier model In Vitro. Cell Mol Bioeng. 2016;9(4):509–529.
   PubMed Web of Science ®Google Scholar