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Cell-secreted vesicles containing miRNAs modulate epigenetic changes during in vitro culture of bovine gametes and embryos

Grant number: 14/22887-0
Support type:Research Grants - Young Investigators Grants
Duration: September 01, 2015 - May 31, 2021
Field of knowledge:Agronomical Sciences - Veterinary Medicine - Animal Reproduction
Principal researcher:Juliano Coelho da Silveira
Grantee:Juliano Coelho da Silveira
Home Institution: Faculdade de Zootecnia e Engenharia de Alimentos (FZEA). Universidade de São Paulo (USP). Pirassununga , SP, Brazil
Assoc. researchers:Felipe Perecin ; Flávio Vieira Meirelles ; Luciano Andrade Silva
Associated grant(s):21/06645-0 - Extracellular vesicles as a platform for diagnostic and manipulation of the in vitro embryo production system: the next generation in animal reproduction, AP.JP2
19/26496-9 - The use of CRISPR/Cas9 technology to study genes involved in livestock trophoblast development, AV.EXT
19/06696-3 - International consortium for the study of serum extracellular vesicles during early embryonic development of livestock animals, AP.R SPRINT
18/04731-3 - Validation of miRNAs targets through luciferase assay in bovine granulosa cells, AV.EXT
15/21829-9 - Multi-user equipment approved in grant 2014/22887-0: Nanosight LM10, AP.EMU
Associated scholarship(s):20/13075-2 - Dairy cows metabolic status effects on epigenetic changes in the embryo and endometrium: the role of extracellular vesicles, BP.PD
19/25675-7 - In vitro production of bovine embryos in different 3D culture systems: effects on nuclear morphology, methylation pattern, gene transcription and extracellular vesicles, BP.MS
19/21028-7 - Analysis of LH receiver acquisition by granulosa cells mediated by extracellular vesicules present in the follicular fluid, BP.IC
+ associated scholarships 18/26547-0 - Canine obesity and inflammation: a study of microRNAs involved in the expression of macrophages in adipose tissue, BP.MS
19/04981-2 - Effects of extracellular vesicle supplementation during bovine embryo cleavage, BP.MS
17/19681-9 - Extracellular vesicles secreted by in vivo and in vitro produced bovine embryos: miRNA content and molecular effects on endometrium and corpus luteum, BP.DR
17/24326-3 - New method to evaluate intercellular communication mediated by extracellular vesicles within the bovine ovarian follicle, BP.IC
18/01431-9 - PI3K-Akt signaling pathway effect in oocyte maturation and early embryo development in cattle, BP.PD
17/02037-0 - Description of a new mechanism involved in cellular communication between female reproductive system cells and oocyte mediated by extracellular vesicles and their impacts on oocyte maturation, fertilization and bovine embryo cleavage, BP.MS
15/17897-9 - Exosomal communication in the stem cells transdifferentiation in co-culture with neuronal cells, BP.DD
15/21674-5 - Dynamics of RNA expression and epigenetic changes during bovine oocyte maturation and embryonic development: comparing in vivo and in vitro systems, BP.IC
15/16985-1 - Cell-secreted vesicles containing miRNAs modulate epigenetic changes during in vitro culture of bovine gametes and embryos, BP.JP - associated scholarships

Abstract

The use of assisted reproduction techniques presents an alternative to solve reproductive problems in domestic species and humans. However, there is concern that epigenetic changes occurring during in vitro culture adversely affect tissue programing during fetal development and could lead to a higher pre-disposition to develop heart diseases, reproductive problems, and development of tumors, in adulthood. Epigenetic changes are regulated by DNA methylation, posttranscriptional histone modifications or microRNAs. MicroRNAs are non-coding RNA molecules that regulates gene expression during different tissue developing processes. Recently, cell-secreted vesicles called exosomes and microvesicles carrying bioactive materials including miRNAs were identified in different body fluids. Cell-secreted vesicles are considered a new class of intercellular communication with possible implications in different physiological processes. However, its role during oocyte maturation and embryo development is not well understood. Our main hypothesis that will be tested is that cell-secreted vesicles containing miRNAs originating from the reproductive tract modulate epigenetic changes during in vitro culture of gametes and embryos. In order to test this hypothesis cell-secreted vesicles will be isolated from follicular fluid and oviductual cells culture media and added to the oocyte maturation and embryo culture media. The first aim of this project is to determine the relationship between miRNAs and epigenetic changes during oocyte maturation and embryo development in vitro. The second aim of this project is to determine the effects exerted by vesicles secreted by reproductive tract cells on oocyte maturation rates, fertilization and embryo cleavage. The third aim of this proposal is to determine the role of cell-secreted vesicles and miRNAs in oocyte maturation and production of bovine embryos in high and low oxygen tension. Results obtained in this research will establish the role of cell-secreted vesicles by the reproductive tract in regulating epigenetic changes acquired during in vitro culture of oocytes and embryos, generating new therapeutic tools for domestic agriculture species and humans. (AU)

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Scientific publications (29)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
MAZZARELLA, ROSANE; BASTOS, NATALIA MARINS; BRIDI, ALESSANDRA; DEL COLLADO, MAITE; ANDRADE, GABRIELLA MAMEDE; PINZON, JORGE; PRADO, CIBELE MARIA; SILVA, LUCIANO ANDRADE; MEIRELLES, FLAVIO VIEIRA; PUGLIESI, GUILHERME; et al. Changes in Oviductal Cells and Small Extracellular Vesicles miRNAs in Pregnant Cows. FRONTIERS IN VETERINARY SCIENCE, v. 8, . (15/21829-9, 14/22887-0, 19/04981-2)
SAMPAIO, RAFAEL VILAR; SANGALLI, JULIANO RODRIGUES; CAMARA DE BEM, TIAGO HENRIQUE; AMBRIZI, DEWISON RICARDO; DEL COLLADO, MAITE; BRIDI, ALESSANDRA; CAVALCANTE MENDES DE AVILA, ANA CLARA FAQUINELI; MACABELLI, CAROLINA HABERMANN; OLIVEIRA, LILIAN DE JESUS; DA SILVEIRA, JULIANO COELHO; et al. Catalytic inhibition of H3K9me2 writers disturbs epigenetic marks during bovine nuclear reprogramming. SCIENTIFIC REPORTS, v. 10, n. 1, . (15/08807-6, 14/22887-0, 13/08135-2, 14/50947-7, 14/21034-3, 15/25111-5, 12/50533-2, 13/07160-3)
NATÁLIA MARINS BASTOS; JULIANA GERMANO FERST; RODRIGO SILVA GOULART; JULIANO COELHO DA SILVEIRA. The role of the oviduct and extracellular vesicles during early embryo development in bovine. Animal Reproduction, v. 19, n. 1, . (15/21829-9, 14/22887-0, 20/08478-0, 20/13075-2)
DEL COLLADO, MAITE; ANDRADE, GABRIELLA MAMEDE; MEIRELLES, FLAVIO VIEIRA; DA SILVEIRA, JULIANO COELHO; PERECIN, FELIPE. Contributions from the ovarian follicular environment to oocyte function. ANIMAL REPRODUCTION, v. 15, n. 3, p. 261-270, . (14/22887-0, 14/21034-3, 17/19825-0, 18/01431-9, 13/08135-2)
BOMFIM, MONALISA M.; ANDRADE, GABRIELLA M.; DEL COLLADO, MAITE; SANGALLI, JULIANO R.; FONTES, PATRICIA K.; NOGUEIRA, MARCELO F. G.; MEIRELLES, FLAVIO V.; DA SILVEIRA, JULIANO C.; PERECIN, FELIPE. Antioxidant responses and deregulation of epigenetic writers and erasers link oxidative stress and DNA methylation in bovine blastocysts. Molecular Reproduction and Development, v. 84, n. 12, p. 1296-1305, . (14/22887-0, 14/21034-3, 13/08135-2, 14/21042-6, 12/50533-2)
DEL COLLADO, MAITE; DA SILVEIRA, JULIANO COELHO; SANGALLI, JULIANO RODRIGUES; ANDRADE, GABRIELLA MAMEDE; DA SILVA SOUSA, LETICIA RABELLO; SILVA, LUCIANO ANDRADE; MEIRELLES, FLAVIO VIEIRA; PERECIN, FELIPE. Fatty Acid Binding Protein 3 And Transzonal Projections Are Involved In Lipid Accumulation During In Vitro Maturation Of Bovine Oocytes. SCIENTIFIC REPORTS, v. 7, . (14/22887-0, 15/26056-8, 14/21034-3, 14/03281-3, 13/08135-2)
DE BEM, T. H. C.; DA SILVEIRA, J. C.; SAMPAIO, R. V.; SANGALLI, J. R.; OLIVEIRA, M. L. F.; FERREIRA, R. M.; SILVA, L. A.; PERECIN, F.; KING, W. A.; MEIRELLES, F. V.; et al. Low levels of exosomal-miRNAs in maternal blood are associated with early pregnancy loss in cloned cattle. SCIENTIFIC REPORTS, v. 7, . (14/22887-0, 12/50533-2, 13/08135-2)
DEL COLLADO, MAITE; DA SILVEIRA, JULIANO C.; OLIVEIRA, MARCELO L. F.; ALVES, BARBARA M. S. M.; SIMAS, ROSINEIDE C.; GODOY, ADRIANA T.; COELHO, MIRELA B.; MARQUES, LYGIA A.; CARRIERO, MATEUS M.; NOGUEIRA, MARCELO F. G.; et al. In vitro maturation impacts cumulus-oocyte complex metabolism and stress in cattle. Reproduction, v. 154, n. 6, p. 881-893, . (14/22887-0, 14/21034-3, 14/03281-3, 12/50533-2, 13/08135-2)
DE FIGUEIREDO PESSOA, LAIS VICARI; LISBOA PIRES, PEDRO RATTO; DEL COLLADO, MAITE; GODOY PIERI, NAIRA CAROLINE; RECCHIA, KAIANA; SOUZA, ALINE FERNANDA; PERECIN, FELIPE; DA SILVEIRA, JULIANO COELHO; CESAR DE ANDRADE, ANDRE FURUGEN; AMBROSIO, CARLOS EDUARDO; et al. Generation and miRNA Characterization of Equine Induced Pluripotent Stem Cells Derived from Fetal and Adult Multipotent Tissues. STEM CELLS INTERNATIONAL, . (08/57877-3, 14/22887-0, 13/17955-3, 12/50533-2, 15/26818-5, 13/08135-2)
SANTOS ROBALLO, KELLY CRISTINE; DA SILVEIRA, JULIANO COELHO; BRESSAN, FABIANA FERNANDES; DE SOUZA, ALINE FERNANDA; PEREIRA, VITORIA MATTOS; PINZON PORRAS, JORGE ELIECER; ROS, FELIPE AUGUSTO; PULZ, LIDIA HILDEBRAND; STREFEZZI, RICARDO DE FRANCISCO; MARTINS, DANIELE DOS SANTOS; et al. Neurons-derived extracellular vesicles promote neural differentiation of ADSCs: a model to prevent peripheral nerve degeneration. SCIENTIFIC REPORTS, v. 9, . (15/17897-9, 14/22887-0, 15/21829-9, 13/08135-2)
BRIDI, ALESSANDRA; ANDRADE, GABRIELLA M.; DEL COLLADO, MAITE; SANGALLI, JULIANO R.; DE AVILA, ANA C. F. C. M.; MOTTA, IGOR G.; DA SILVA, JULIO C. B.; PUGLIESI, GUILHERME; SILVA, LUCIANO A.; MEIRELLES, FLAVIO V.; et al. mall extracellular vesicles derived from in vivo- or in vitro-produced bovine blastocysts have different miRNAs profiles-Implications for embryo-maternal recognitio. Molecular Reproduction and Development, v. 88, n. 9, . (15/21829-9, 14/22887-0, 17/19681-9, 18/13155-6)
ANDRADE, GABRIELLA MAMEDE; BOMFIM, MONALISA MEDRADO; DEL COLLADO, MAITE; MEIRELLES, FLAVIO VIEIRA; PERECIN, FELIPE; DA SILVEIRA, JULIANO COELHO. Oxygen tension modulates extracellular vesicles and its miRNA contents in bovine embryo culture medium. Molecular Reproduction and Development, v. 86, n. 8, p. 1067-1080, . (12/50533-2, 14/21034-3, 15/21829-9, 14/22887-0, 14/21042-6, 13/08135-2)
BRIDI, ALESSANDRA; PERECIN, FELIPE; DA SILVEIRA, JULIANO COELHO. Extracellular Vesicles Mediated Early Embryo-Maternal Interactions. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, v. 21, n. 3, . (17/19681-9, 18/13155-6, 14/22887-0)
CAVALCANTE MENDES DE AVILA, ANA CLARA FAQUINELI; ANDRADE, GABRIELLA MAMEDE; BRIDI, ALESSANDRA; GIMENES, LINDSAY UNNO; MEIRELLES, FLAVIO VIEIRA; PERECIN, FELIPE; DA SILVEIRA, JULIANO COELHO. Extracellular vesicles and its advances in female reproduction. ANIMAL REPRODUCTION, v. 16, n. 1, p. 31-38, . (18/01431-9, 14/22887-0, 17/02037-0)
HAMDI, MERIEM; CANON-BELTRAN, KARINA; MAZZARELLA, ROSANE; CAJAS, YULIA N.; LEAL, CLAUDIA L. V.; GUTIERREZ-ADAN, ALFONSO; GONZALEZ, ENCINA M.; DA SILVEIRA, JULIANO C.; RIZOS, DIMITRIOS. Characterization and profiling analysis of bovine oviduct and uterine extracellular vesicles and their miRNA cargo through the estrous cycle. FASEB JOURNAL, v. 35, n. 12, . (17/20339-3, 19/04981-2, 15/21829-9, 14/22887-0)
DE LIMA, MARINA AMARO; MOROTTI, FABIO; BAYEUX, BERNARDO MARCOZZI; DE REZENDE, ROMULO GERMANO; BOTIGELLI, RAMON CESAR; CAMARA DE BEM, TIAGO HENRIQUE; FONTES, PATRICIA KUBO; GOUVEIA NOGUEIRA, MARCELO FABIO; MEIRELLES, FLAVIO VIEIRA; BARUSELLI, PIETRO SAMPAIO; et al. Ovarian follicular dynamics, progesterone concentrations, pregnancy rates and transcriptional patterns in Bos indicus females with a high or low antral follicle count. SCIENTIFIC REPORTS, v. 10, n. 1, . (18/13155-6, 14/22887-0, 12/50533-2)
GARNICA, TAISMARA K.; LESBON, JESSIKA C. C.; AVILA, ANA C. F. C. M.; ROCHETTI, ARINA L.; MATIZ, OSCAR R. S.; RIBEIRO, ROANA C. S.; ZOPPA, ALINE; NISHIYA, ADRIANA T.; COSTA, MIRELA T.; DE NARDI, ANDRIGO B.; et al. Liquid biopsy based on small extracellular vesicles predicts chemotherapy response of canine multicentric lymphomas. SCIENTIFIC REPORTS, v. 10, n. 1, . (17/15406-3, 14/22887-0, 14/02493-7, 15/21829-9)
DA SILVEIRA, JULIANO C.; DE AVILA, ANA CLARA F. C. M.; GARRETT, HANNAH L.; BRUEMMER, JASON E.; WINGER, QUINTON A.; BOUMA, GERRIT J.. Cell-secreted vesicles containing microRNAs as regulators of gamete maturation. Journal of Endocrinology, v. 236, n. 1, p. R15-R27, . (14/22887-0, 13/10473-3, 17/02037-0, 15/16985-1, 12/50533-2)
SANTOS, G.; BOTTINO, M. P.; SANTOS, A. P. C.; SIMOES, L. M. S.; SOUZA, J. C.; FERREIRA, M. B. D.; DA SILVEIRA, J. C.; AVILA, A. C. F. C. M.; BRIDE, A.; SALES, J. N. S.. Subclinical mastitis interferes with ovulation, oocyte and granulosa cell quality in dairy cows. Theriogenology, v. 119, p. 214-219, . (14/22887-0, 15/21829-9)
SANGALLI, JULIANO RODRIGUES; SAMPAIO, RAFAEL VILAR; DEL COLLADO, MAITE; DA SILVEIRA, JULIANO COELHO; CAMARA DE BEM, TIAGO HENRIQUE; PERECIN, FELIPE; SMITH, LAWRENCE CHARLES; MEIRELLES, FLAVIO VIEIRA. Metabolic gene expression and epigenetic effects of the ketone body beta-hydroxybutyrate. SCIENTIFIC REPORTS, v. 8, . (13/08135-2, 14/22887-0, 16/13416-9, 14/21097-5, 14/21034-3, 13/06673-7, 12/50533-2)
ANDRADE, GABRIELLA MAMEDE; DA SILVEIRA, JULIANO COELHO; PERRINI, CLAUDIA; DEL COLLADO, MAITE; GEBREMEDHN, SAMUEL; TESFAYE, DAWIT; MEIRELLES, FLAVIO VIEIRA; PERECIN, FELIPE. The role of the PI3K-Akt signaling pathway in the developmental competence of bovine oocytes. PLoS One, v. 12, n. 9, . (14/21034-3, 13/08135-2, 14/22887-0, 12/50533-2)
OTAGUIRI, KATIA KAORI; DOS SANTOS, DAIANE FERNANDA; SLAVOV, SVETOSLAV NANEV; DEPIERI, LIVIA VIEIRA; BONINI PALMA, PATRICIA VIANNA; MEIRELLES, FLAVIO VIEIRA; COVAS, DIMAS TADEU; DA SILVEIRA, JULIANO COELHO; KASHIMA, SIMONE. TAX-mRNA-Carrying Exosomes from Human T Cell Lymphotropic Virus Type 1-Infected Cells Can Induce Interferon-Gamma Production In Vitro. AIDS Research and Human Retroviruses, v. 34, n. 12, . (14/22887-0, 15/16985-1)
DE AVILA, A. C. F. C. M.; DA SILVEIRA, J. C.. Role of extracellular vesicles during oocyte maturation and early embryo development. REPRODUCTION FERTILITY AND DEVELOPMENT, v. 32, n. 1-2, p. 56-64, . (15/21829-9, 14/22887-0, 17/02037-0)
CAVALCANTE MENDES DE AVILA, ANA CLARA FAQUINELI; BRIDI, ALESSANDRA; ANDRADE, GABRIELLA MAMEDE; DEL COLLADO, MAITE; SANGALLI, JULIANO RODRIGUES; NOCITI, RICARDO PERECIN; DA SILVA JUNIOR, WILSON ARAUJO; BASTIEN, ALEXANDRE; ROBERT, CLAUDE; MEIRELLES, FLAVIO VIEIRA; et al. Estrous cycle impacts microRNA content in extracellular vesicles that modulate bovine cumulus cell transcripts during in vitro maturation. BIOLOGY OF REPRODUCTION, v. 102, n. 2, p. 362-375, . (18/14869-2, 15/21829-9, 14/22887-0, 17/02037-0)
ANDRADE, GABRIELLA MAMEDE; DEL COLLADO, MAITE; MEIRELLES, FLAVIO VIEIRA; DA SILVEIRA, JULIANO COELHO; PERECIN, FELIPE. Intrafollicular barriers and cellular interactions during ovarian follicle development. ANIMAL REPRODUCTION, v. 16, n. 3, p. 485-496, . (18/01431-9, 18/13155-6, 17/19825-0, 14/22887-0, 13/08135-2)
ANDRADE, G. M.; MEIRELLES, F. V.; PERECIN, F.; DA SILVEIRA, J. C.. Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle. REPRODUCTION IN DOMESTIC ANIMALS, v. 52, n. 6, p. 1036-1045, . (14/22887-0, 14/21034-3, 12/50533-2, 13/10473-3, 13/08135-2)
DA SILVEIRA, JULIANO C.; ANDRADE, GABRIELLA M.; DEL COLLADO, MAITE; SAMPAIO, RAFAEL V.; SANGALLI, JULIANO R.; SILVA, LUCIANO A.; PINAFFI, FABIO V. L.; JARDIM, IZABELLE B.; CESAR, MARCELO C.; NOGUEIRA, MARCELO F. G.; et al. Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development. PLoS One, v. 12, n. 6, . (14/22887-0, 14/21034-3, 12/50533-2, 13/10473-3, 13/08135-2)
DA SILVEIRA, JULIANO COELHO; ANDRADE, GABRIELLA MAMEDE; SIMAS, ROSINEIDE COSTA; MARTINS-JUNIOR, HELIO ALVES; EBERLIN, MARCOS NOGUEIRA; SMITH, LAWRENCE CHARLES; PERECIN, FELIPE; MEIRELLES, FLAVIO VIEIRA. Lipid profile of extracellular vesicles and their relationship with bovine oocyte developmental competence: New players in intra follicular cell communication. Theriogenology, v. 174, p. 1-8, . (11/15416-2, 19/15491-6, 15/21829-9, 12/50533-2, 13/08135-2, 14/22887-0, 14/21034-3)
PEDROSA, ANA CAROLINA; TORRES, MARIANA ANDRADE; ALKMIN, DIEGO VILELA; PINZON, JORGE E. P.; MASSAMI KITAMURA MARTINS, SIMONE MARIA; DA SILVEIRA, JULIANO COELHO; CESAR DE ANDRADE, ANDRE FURUGEN. Spermatozoa and seminal plasma small extracellular vesicles miRNAs as biomarkers of boar semen cryotolerance. Theriogenology, v. 174, p. 60-72, . (16/24690-4, 18/12500-1, 15/21829-9, 14/22887-0)

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