Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress

A Abuelo, 2015, The importance of the oxidative status of dairy cattle in the periparturient period. Revisiting antioxidant supplementation, J Anim Physiol Anim Nutr (Berl), 99, 1003, 10.1111/jpn.12273

F de Rensis, 2003, Heat stress and seasonal effects on reproduction in the dairy cow—a review, Theriogenology, 60, 1139, 10.1016/S0093-691X(03)00126-2

J-Q Zhang, 2016, Critical Role of FoxO1 in Granulosa Cell Apoptosis Caused by Oxidative Stress and Protective Effects of Grape Seed Procyanidin B2, Oxid Med Cell Longev, 2016, 6147345

L Li, 2016, The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells, Cell Stress Chaperones, 21, 467, 10.1007/s12192-016-0673-9

GJ Hickey, 1988, Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis, Endocrinology, 122, 1426, 10.1210/endo-122-4-1426

L Lee, 2013, Changes in histone modification and DNA methylation of the StAR and Cyp19a1 promoter regions in granulosa cells undergoing luteinization during ovulation in rats, Endocrinology, 154, 458, 10.1210/en.2012-1610

Shail K. Chaube, 2016, Clomiphene Citrate Induces ROS-Mediated Apoptosis in Mammalian Oocytes, Cell Stress Chaperones, 3, 467

M Schieber, 2014, ROS function in redox signaling and oxidative stress, Curr Biol, 24, R453, 10.1016/j.cub.2014.03.034

DJ Betteridge, 2000, What is oxidative stress, Metabolism, 49, 3, 10.1016/S0026-0495(00)80077-3

GJ Burton, 2011, Oxidative stress, Best Pract Res Clin Obstet Gynaecol, 25, 287, 10.1016/j.bpobgyn.2010.10.016

JS Aprioku, 2013, Pharmacology of free radicals and the impact of reactive oxygen species on the testis, J Reprod Infertil, 14, 158

AA Szypowska, 2011, Oxidative stress-dependent regulation of Forkhead box O4 activity by nemo-like kinase, Antioxid Redox Signal, 14, 563, 10.1089/ars.2010.3243

GJPL Kops, 2002, Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress, Nature, 419, 316, 10.1038/nature01036

Y Omata, 2008, Induction of adaptive response and enhancement of PC12 cell tolerance by lipopolysaccharide primarily through the upregulation of glutathione S-transferase A3 via Nrf2 activation, Free Radic Biol Med, 45, 1437, 10.1016/j.freeradbiomed.2008.08.018

M Eldh, 2010, Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA, PLoS One, 5, e15353, 10.1371/journal.pone.0015353

JJ Eppig, 2002, The mammalian oocyte orchestrates the rate of ovarian follicular development, Proc Natl Acad Sci U S A, 99, 2890, 10.1073/pnas.052658699

MM Matzuk, 2002, Intercellular communication in the mammalian ovary: oocytes carry the conversation, Science, 296, 2178, 10.1126/science.1071965

BC Vanderhyden, 1990, Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation, Dev Biol, 140, 307, 10.1016/0012-1606(90)90081-S

BC Vanderhyden, 1992, Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro, Biol Reprod, 46, 1196, 10.1095/biolreprod46.6.1196

GM Kidder, 2010, Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence, Can J Physiol Pharmacol, 88, 399, 10.1139/Y10-009

C Di Pietro, 2016, Exosome-mediated communication in the ovarian follicle, Journal of assisted reproduction and genetics, 33, 303, 10.1007/s10815-016-0657-9

MMH Sohel, 2013, Exosomal and Non-Exosomal Transport of Extra-Cellular microRNAs in Follicular Fluid: Implications for Bovine Oocyte Developmental Competence, PLoS One, 8, e78505, 10.1371/journal.pone.0078505

S El Andaloussi, 2013, Exosomes for targeted siRNA delivery across biological barriers, Adv Drug Deliv Rev, 65, 391, 10.1016/j.addr.2012.08.008

C Ciardiello, 2016, Focus on Extracellular Vesicles: New Frontiers of Cell-to-Cell Communication in Cancer, Int J Mol Sci, 17, 175, 10.3390/ijms17020175

JC da Silveira, 2012, Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle, Biol Reprod, 86, 71, 10.1095/biolreprod.111.093252

M Li, 2014, Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers, Philos Trans R Soc Lond B Biol Sci, 369

A Sharma, 2016, Tumor exosomes: cellular postmen of cancer diagnosis and personalized therapy, Nanomedicine (Lond), 11, 421, 10.2217/nnm.15.210

BT Pan, 1985, Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes, J Cell Biol, 101, 942, 10.1083/jcb.101.3.942

Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. England;01.01.2002.

S Keller, 2006, Exosomes: from biogenesis and secretion to biological function, Immunol Lett, 107, 102, 10.1016/j.imlet.2006.09.005

M Frydrychowicz, 2015, Exosomes—structure, biogenesis and biological role in non-small-cell lung cancer, Scand J Immunol, 81, 2, 10.1111/sji.12247

JPG Sluijter, 2014, Microvesicles and exosomes for intracardiac communication, Cardiovasc Res, 102, 302, 10.1093/cvr/cvu022

AV Vlassov, 2012, Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials, Biochim Biophys Acta, 1820, 940, 10.1016/j.bbagen.2012.03.017

M Silva, 2015, Non-coding RNAs in Exosomes: New Players in Cancer Biology, Curr Genomics, 16, 295, 10.2174/1389202916666150707154719

H Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat Cell Biol, 9, 654, 10.1038/ncb1596

H Peinado, 2012, Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET, Nat Med, 18, 883, 10.1038/nm.2753

M-J Yuan, 2016, Exosomes Mediate the Intercellular Communication after Myocardial Infarction, Int J Med Sci, 13, 113, 10.7150/ijms.14112

U Bernabucci, 2002, Oxidative stress in primiparous cows in relation to dietary starch and the progress of lactation, J Dairy Sci, 85, 2173

Y Guo, 2013, Changes in feed intake, nutrient digestion, plasma metabolites, and oxidative stress parameters in dairy cows with subacute ruminal acidosis and its regulation with pelleted beet pulp, J Anim Sci Biotechnol, 4, 31, 10.1186/2049-1891-4-31

C Castillo, 2006, Plasma malonaldehyde (MDA) and total antioxidant status (TAS) during lactation in dairy cows, Res Vet Sci, 80, 133, 10.1016/j.rvsc.2005.06.003

U Bernabucci, 2005, Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows, J Dairy Sci, 88, 2017, 10.3168/jds.S0022-0302(05)72878-2

WP Weiss, 2004, Changes in vitamin C concentrations in plasma and milk from dairy cows after an intramammary infusion of Escherichia coli, J Dairy Sci, 87, 32, 10.3168/jds.S0022-0302(04)73138-0

A Agarwal, 2005, Role of oxidative stress in female reproduction, Reprod Biol Endocrinol, 3, 28, 10.1186/1477-7827-3-28

P Guerin, 2001, Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings, Hum Reprod Update, 7, 175, 10.1093/humupd/7.2.175

M Brannstrom, 1993, Involvement of leukocytes and cytokines in the ovulatory process and corpus luteum function, Hum Reprod, 8, 1762, 10.1093/oxfordjournals.humrep.a137929

H Yang, 2017, Oxidative stress-induced apoptosis in granulosa cells involves JNK, p53 and Puma, Oncotarget, 8, 25310, 10.18632/oncotarget.15813

S Assou, 2010, Human cumulus cells as biomarkers for embryo and pregnancy outcomes, Mol Hum Reprod, 16, 531, 10.1093/molehr/gaq032

M Shiota, 2003, Correlation of mitogen-activated protein kinase activities with cell survival and apoptosis in porcine granulosa cells, Zoolog Sci, 20, 193, 10.2108/zsj.20.193

H Adeldust, 2015, In vitro maturation of ovine oocyte in a modified granulosa cells co-culture system and alpha-tocopherol supplementation: effects on nuclear maturation and cleavage, J Anim Sci Technol, 57, 27, 10.1186/s40781-015-0061-5

A Tripathi, 2013, An increase of granulosa cell apoptosis mediates aqueous neem (Azadirachta indica) leaf extract-induced oocyte apoptosis in rat, Int J Appl Basic Med Res, 3, 27, 10.4103/2229-516X.112238

H Tamura, 2008, Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate, J Pineal Res, 44, 280, 10.1111/j.1600-079X.2007.00524.x

M Tanabe, 2015, Melatonin protects the integrity of granulosa cells by reducing oxidative stress in nuclei, mitochondria, and plasma membranes in mice, J Reprod Dev, 61, 35, 10.1262/jrd.2014-105

PJ Devine, 2012, Roles of reactive oxygen species and antioxidants in ovarian toxicity, Biol Reprod, 86, 27, 10.1095/biolreprod.111.095224

F Qu, 2012, A molecular mechanism underlying ovarian dysfunction of polycystic ovary syndrome: hyperandrogenism induces epigenetic alterations in the granulosa cells, J Mol Med (Berl), 90, 911, 10.1007/s00109-012-0881-4

BV Chernyak, 2006, Production of reactive oxygen species in mitochondria of HeLa cells under oxidative stress, Biochim Biophys Acta, 1757, 525, 10.1016/j.bbabio.2006.02.019

AY Andreyev, 2005, Mitochondrial metabolism of reactive oxygen species, Biochemistry (Mosc), 70, 200, 10.1007/s10541-005-0102-7

JF Turrens, 2003, Mitochondrial formation of reactive oxygen species, J Physiol, 552, 335, 10.1113/jphysiol.2003.049478

KA Rasbach, 2007, Signaling of mitochondrial biogenesis following oxidant injury, J Biol Chem, 282, 2355, 10.1074/jbc.M608009200

J Michael, 2012, Berridge. Cell cycle and proliferation, Cell signaling biology, 16, 1150

M Li, 2009, Hydrogen peroxide induces G2 cell cycle arrest and inhibits cell proliferation in osteoblasts, Anat Rec (Hoboken), 292, 1107, 10.1002/ar.20925

HK Bryan, 2013, The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation, Biochem Pharmacol, 85, 705, 10.1016/j.bcp.2012.11.016

S Singh, 2010, Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases, Free Radic Res, 44, 1267, 10.3109/10715762.2010.507670

A Amin, 2014, Bovine embryo survival under oxidative-stress conditions is associated with activity of the NRF2-mediated oxidative-stress-response pathway, Mol Reprod Dev, 81, 497, 10.1002/mrd.22316

X Jin, 2016, Protection of Bovine Mammary Epithelial Cells from Hydrogen Peroxide-Induced Oxidative Cell Damage by Resveratrol, Oxid Med Cell Longev, 2016, 2572175

GP Bienert, 2006, Membrane transport of hydrogen peroxide, Biochim Biophys Acta, 1758, 994, 10.1016/j.bbamem.2006.02.015

Y Wang, 2017, Protection of oxidative stress induced apoptosis in osteosarcoma cells by dihydromyricetin through down-regulation of caspase activation and up-regulation of BcL-2, Saudi J Biol Sci, 24, 837, 10.1016/j.sjbs.2016.12.004

H Song, 2010, Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex, Stem Cells, 28, 555, 10.1002/stem.302

M Santonocito, 2014, Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation, Fertil Steril, 102, 1751, 10.1016/j.fertnstert.2014.08.005

R Navakanitworakul, 2016, Characterization and Small RNA Content of Extracellular Vesicles in Follicular Fluid of Developing Bovine Antral Follicles, Sci Rep, 6, 25486, 10.1038/srep25486

W-T Hung, 2015, Extracellular Vesicles from Bovine Follicular Fluid Support Cumulus Expansion, Biol Reprod, 93, 117

S Ailawadi, 2015, Pathologic function and therapeutic potential of exosomes in cardiovascular disease, Biochim Biophys Acta, 1852, 1, 10.1016/j.bbadis.2014.10.008

M Harmati, 2017, Stressors alter intercellular communication and exosome profile of nasopharyngeal carcinoma cells, J Oral Pathol Med, 46, 259, 10.1111/jop.12486

OG de Jong, 2012, Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes, J Extracell Vesicles, 1, 10.3402/jev.v1i0.18396

Du Feng, 2010, Cellular internalization of exosomes occurs through phagocytosis, Traffic, 11, 675, 10.1111/j.1600-0854.2010.01041.x

BN Hannafon, 2013, Intercellular communication by exosome-derived microRNAs in cancer, Int J Mol Sci, 14, 14240, 10.3390/ijms140714240

A Clayton, 2004, Adhesion and signaling by B cell-derived exosomes: the role of integrins, FASEB J, 18, 977, 10.1096/fj.03-1094fje

A Montecalvo, 2012, Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes, Blood, 119, 756, 10.1182/blood-2011-02-338004

C Kahlert, 2013, Exosomes in tumor microenvironment influence cancer progression and metastasis, J Mol Med (Berl), 91, 431, 10.1007/s00109-013-1020-6

P Yousefpour, 2014, Co-opting biology to deliver drugs, Biotechnol Bioeng, 111, 1699, 10.1002/bit.25307

L Braccioli, 2014, Exosomes: a new weapon to treat the central nervous system, Mol Neurobiol, 49, 113, 10.1007/s12035-013-8504-9

MJ Haney, 2015, Exosomes as drug delivery vehicles for Parkinson's disease therapy, J Control Release, 207, 18, 10.1016/j.jconrel.2015.03.033