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Research Article

Exosomes Derived From HEK293T Cells Interact in An Efficient and Noninvasive Manner with Mammalian Sperm In Vitro

, , , , ORCID Icon, & show all
Pages 1965-1980 | Received 10 Feb 2020, Accepted 02 Jun 2020, Published online: 14 Aug 2020

References

  • Ombelet W , CookeI, DyerS, SerourG, DevroeyP. Infertility and the provision of infertility medical services in developing countries. Hum. Reprod. Update.14(6), 605–621 (2008).
  • Agarwal A , MulgundA, HamadaA, ChyatteMR. A unique view on male infertility around the globe. Reprod. Biol. Endrocinol.13, 37 (2015).
  • Winters BR , WalshTJ. The epidemiology of male infertility. Urol. Clin. N. Am.41(1), 195–204 (2014).
  • de Kretser DM . Endocrinology of male infertility. Br. Med. Bull.35(2), 187–192 (1979).
  • Kovac JR , LambDJ. Male infertility biomarkers and genomic aberrations in azoospermia. Fertil. Steril.101(5), 31 (2014).
  • Amdani SN , YesteM, JonesC, CowardK. Phospholipase C zeta (PLCzeta) and male infertility: Clinical update and topical developments. Adv. Biol. Regul.61, 58–67 (2016).
  • Lenzi A , GandiniL, PicardoM, TramerE, SandriG, PanfiliE. Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies. Front. Biosci.5, 1–15 (2000).
  • Tapia JA , Macias-GarciaB, Miro-MoranA, Ortega-FerrusolaC, SalidoGM, PeñaFJ, AparicioIM. The membrane of the mammalian spermatozoa: much more than an inert envelope. Reprod. Domest. Anim.47(3), 65–75 (2012).
  • Barkalina N , JonesC, TownleyH, CowardK. Functionalization of mesoporous silica nanoparticles with a cell-penetrating peptide to target mammalian sperm in vitro. Nanomedicine (Lond.)10(10), 1539–1553 (2015).
  • Najafi A , TaheriAT, MehdipourM, Martinez-PastorF, RouhollahiAA, NouraniMR. Improvement of post-thawed sperm quality in broiler breeder roosters by ellagic acid-loaded liposomes. Poult. Sci.98(1), 440–446 (2019).
  • Kunzmann A , AnderssonB, ThurnherrT, KrugH, ScheyniusA, FadeelB. Toxicology of engineered nanomaterials: focus on biocompatibility, biodistribution and biodegradation. Biochim. Biophys. Acta.1810(3), 361–373 (2011).
  • Szebeni J . Complement activation-related pseudoallergy caused by liposomes, micellar carriers of intravenous drugs, and radiocontrast agents. Crit. Rev. Ther. Drug Carrier Syst.18(6), 567–606 (2001).
  • Barkalina N , JonesC, WoodMJA, CowardK. Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: learning from nature. Hum. Reprod. Update.21(5), 627–639 (2015).
  • Raposo G , StoorvogelW. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol.200(4), 373–383 (2013).
  • Colombo M , RaposoG, ThéryC. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Cell Dev. Biol.30, 255–289 (2014).
  • Osorio-Querejeta I , Carregal-RomeroS, Ayerdi-IzquierdoAet al. MiR-219a-5p enriched extracellular vesicles induce OPC differentiation and EAE improvement more efficiently than liposomes and polymeric nanoparticles. Pharmaceutics.12(2), 186 (2020).
  • Batrakova E , KimMS. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J. Control. Release219, 396–405 (2015).
  • Kowal J , TkachM, ThéryC. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol.29, 116–125 (2014).
  • Thery C , WitwerKW, AikawaEet al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles.7(1), 1535750 (2018).
  • Zhu X , BadawiM, PomeroySet al. Comprehensive toxicity and immunogenicity studies reveal minimal effects in mice following sustained dosing of extracellular vesicles derived from HEK293T cells. J. Extracell. Vesicles6(1), 1324730 (2017).
  • Rosas LE , ElgamalOA, MoX, PhelpsMA, SchmittgenTD, PapenfussTL. In vitro immunotoxicity assessment of culture-derived extracellular vesicles in human monocytes. J. Immunotoxicol.13(5), 652–665 (2016).
  • Li J , ChenX, YiJet al. Identification and characterization of 293T cell-derived exosomes by profiling the protein, mRNA and MicroRNA components. PloS One11(9), 0163043 (2016).
  • Watson DC , YungBC, BergamaschiCet al. Scalable, cGMP-compatible purification of extracellular vesicles carrying bioactive human heterodimeric IL-15/lactad-herin complexes. J. Extracell. Vesicles.7(1), 1442088 (2018).
  • Liu Y , LiD, LiuZet al. Targeted exosome-mediated delivery of opioid receptor Mu siRNA for the treatment of morphine relapse. Sci. Rep.5, 17543 (2015).
  • El-Andaloussi S , LeeY, Lakhal-LittletonSet al. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat. Protoc.7(12), 2112–2126 (2012).
  • Ruiss R , JochumS, MocikatR, HammerschmidtW, ZeidlerR. EBV-gp350 confers B-cell tropism to tailored exosomes and is a neo-antigen in normal and malignant B cells – a new option for the treatment of B-CLL. PloS One.6(10), 25294 (2011).
  • Sun D , ZhuangX, XiangXet al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther.18(9), 1606–1614 (2010).
  • Alvarez-Erviti L , SeowY, YinH, BettsC, LakhalS, WoodMJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol.29(4), 341–345 (2011).
  • ELA S , MagerI, BreakefieldXO, WoodMJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov.12(5), 347–357 (2013).
  • You Y , IkezuT. Emerging roles of extracellular vesicles in neurodegenerative disorders. Neurobiol. Dis.130, 104512 (2019).
  • Ju Z , MaJ, WangC, YuJ, QiaoY, HeiF. Exosomes from iPSCs delivering siRNA attenuate intracellular adhesion molecule-1 expression and neutrophils adhesion in pulmonary microvascular endothelial cells. Inflammation40(2), 486–496 (2017).
  • Wahlgren J , KarlsonTDL, BrisslertMet al. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res.40(17), 130 (2012).
  • Ohno S , TakanashiM, SudoKet al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther.21(1), 185–191 (2013).
  • Tian Y , LiS, SongJet al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials.35(7), 2383–2390 (2014).
  • Piehl LL , FischmanML, HellmanU, CisaleH, MirandaPV. Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing. Theriogenology79(7), 1071–1082 (2013).
  • Du J , ShenJ, WangYet al. Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget7(37), 58832–58847 (2016).
  • Zhou W , StangerSJ, AndersonALet al. Mechanisms of tethering and cargo transfer during epididymosome-sperm interactions. BMC Biol.17(1), 35 (2019).
  • Fernández-Gago R , DominguezJC, Martínez-PastorF. Seminal Plasma applied post-thawing affects boar sperm physiology. Theriogenology80(4), 400–410 (2013).
  • Mogielnicka-Brzozowska M , StrzezekR, WsilewskaK, KordanW. Prostasomes of canine seminal plasma – zinc-binding ability and effects on motility characteristics and plasma membrane integrity of spermatozoa. Reprod. Domest. Anim.50(3), 484–491 (2015).
  • Aalberts M , StoutTA, StoorvogelW. Prostasomes: extracellular vesicles from the prostate. Reproduction147(1), 1–14 (2013).
  • Carpi A , SabaneghE, MechanickJ. Controversies in the management of nonobstructive azoospermia. Fertil. Steril.91(4), 963–970 (2009).
  • Shin D , LoKC, LipshultzLI. Treatment Options for the Infertile Male With Cancer. J. Natl. Cancer Inst. Monogr.34, 48–50 (2005).
  • Dragovic RA , CollettGP, HolePet al. Isolation of syncytiotrophoblast microvesicles and exosomes and their characterisation by multicolour flow cytometry and fluorescence Nanoparticle Tracking Analysis. Methods.87, 64–74 (2015).
  • Carnell-Morris P , TannettaD, SiupaA, HoleP, DragovicR. Analysis of extracellular vesicles using fluorescence nanoparticle tracking analysis. In: Extracellular Vesicles: Methods and Protocols, Methods in Molecular Biology (Volume 1660)KuoW, JiaS. ( Eds). Humana Press, New York, NY Chapter 13 (2017).
  • Yeste M , Fernandez-NovellJM, Ramio-LluchLet al. Intracellular calcium movements of boar spermatozoa during ‘in vitro’ capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model. Andrology3(4), 729–747 (2015).
  • Jimenez I , Gonzalez-MarquezH, OrtizRet al. Changes in the distribution of lectin receptors during capacitation and acrosome reaction in boar spermatozoa. Theriogenology59(5–6), 1171–1180 (2003).
  • Ramio L , RiveraMM, RamirezAet al. Dynamics of motile-sperm subpopulation structure in boar ejaculates subjected to “in vitro” capacitation and further “in vitro” acrosome reaction. Theriogenology.69(4), 501–502 (2008).
  • Verstegen J , Iguer-OuadaM, OnclinK. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology57(1), 149–179 (2002).
  • Garner DL , JohnsonLA. Viability Assessment of Mammalian Sperm Using SYBR-14 and Propidium Iodide1. Biol. Reprod.53(2), 276–284 (1995).
  • Harrison RA , AshworthPJ, MillerNG. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol. Reprod. Dev.45(3), 378–391 (1996).
  • Guthrie HG , WelchGR. Determination of intracellular reactive oxygen species and high mitochondrial membrane potential in Percoll-treated viable boar sperm using fluorescence-activated flow cytometry. J. Anim. Sci.84(8), 2089–2100 (2006).
  • Webber J , ClaytonA. How pure are your vesicles?J. Extracell. Vesicles2, 19861 (2013).
  • Hoog JL , LotvallJ. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J. Extracell. Vesicles4, 28680 (2015).
  • Poliakov A , SpilmanM, DoklandT, AmlingCL, MobleyJA. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate69(2), 159–167 (2009).
  • Carpintero-Fernández P , Fafián-LaboraJ, O’LoghlenA. Technical advances to study extracellular vesicles. Front. Mol. Biosci.4, 79 (2017).
  • Arienti G , CarliniE, PalmeriniCA. Fusion of human sperm to prostasomes at acidic pH. J. Membr. Biol.155(1), 89–94 (1997).
  • Schwarz A , WennemuthG, PostH, BrandeburgerT, AumüllerG, WilhelmB. Vesicular transfer of membrane components to bovine epididymal spermatozoa. Cell Tissue Res.353(3), 549–561 (2013).
  • Mulcahy LA , PinkRC, CarterDRF. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles3, 24641 (2014).
  • Garcia Herreros M , AparicioIM, NunezIet al. Boar sperm velocity and motility patterns under capacitating and non-capacitating incubation conditions. Theriogenology63(3), 795–805 (2005).
  • Boryshpolets S , Pérez-CerezalesS, EisenbachM. Behavioral mechanism of human sperm in thermotaxis: a role for hyperactivation. Hum. Reprod.30(4), 884–892 (2015).
  • Carlini E , PalmeriniCA, CosmiEV, ArientiG. Fusion of sperm with prostasomes: effects on membrane fluidity. Arch. Biochem. Biophys.343(1), 6–12 (1997).
  • Caballero J , FrenetteG, D’AmoursOet al. Bovine sperm raft membrane associated Glioma Pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. J. Cell Physiol.227(12), 3876–3886 (2012).
  • Cross NL . Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol. Reprod. Dev.45(2), 212–217 (1996).
  • Palmerini CA , SaccardiC, CarliniE, FabianiR, ArientiG. Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction. Fertil. Steril.80(5), 1181–1184 (2003).
  • Bechoua S , RieuI, SionB, GrizardG. Prostasomes as potential modulators of tyrosine phosphorylation in human spermatozoa. Syst. Biol. Reprod. Med.57(3), 139–148 (2011).
  • Arienti G , CarliniE, SaccardiC, PalmeriniCA. Nitric oxide and fusion with prostasomes increase cytosolic calcium in progesterone-stimulated sperm. Arch. Biochem. Biophys.402(2), 255–258 (2002).
  • Garcia JC , DominguezJC, PenaFJet al. Thawing boar semen in the presence of seminal plasma: effects on sperm quality and fertility. Anim. Reprod. Sci.119(1–2), 160–165 (2010).
  • Fernández-Gago R , DomínguezJC, Martínez-PastorF. Seminal plasma applied post-thawing affects boar sperm physiology: a flow cytometry study. Theriogenology80(4), 400–410 (2013).