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

• Grant number: 14/22887-0
• Support Opportunities: Research Grants - Young Investigators Grants
• Duration: September 01, 2015 - May 31, 2021
• Field of knowledge: Agronomical Sciences - Veterinary Medicine - Animal Reproduction
• Principal Investigator: Juliano Coelho da Silveira
• Grantee: Juliano Coelho da Silveira
• Host Institution: Faculdade de Zootecnia e Engenharia de Alimentos (FZEA). Universidade de São Paulo (USP). Pirassununga , SP, Brazil
• Associated 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): 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; 18/26547-0 - Canine obesity and inflammation: a study of microRNAs involved in the expression of macrophages in adipose tissue, BP.MS; + associated scholarships 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)

Scientific publications

(37)

(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)

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, 2022-04-20. (20/08478-0, 15/21829-9, 20/13075-2, 14/22887-0)

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, 2019. (08/57877-3, 13/17955-3, 15/26818-5, 13/08135-2, 12/50533-2, 14/22887-0)

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, MAR 4 2021. (15/21829-9, 19/04981-2, 14/22887-0)

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, JUL 13 2020. (15/08807-6, 14/22887-0, 13/08135-2, 14/50947-7, 14/21034-3, 15/25111-5, 12/50533-2, 13/07160-3)

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, JUN 1 2017. (14/03281-3, 13/08135-2, 15/26056-8, 14/22887-0, 14/21034-3)

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, JAN-MAR 2019. (18/01431-9, 17/02037-0, 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, NOV 11 2020. (12/50533-2, 18/13155-6, 14/22887-0)

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, NOV 23 2020. (14/02493-7, 15/21829-9, 17/15406-3, 14/22887-0)

BRIDI, ALESSANDRA; PERECIN, FELIPE; DA SILVEIRA, JULIANO COELHO. Extracellular Vesicles Mediated Early Embryo-Maternal Interactions. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, v. 21, n. 3, FEB 2020. (17/19681-9, 18/13155-6, 14/22887-0)

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, AUG 2019. (12/50533-2, 14/21034-3, 15/21829-9, 14/22887-0, 14/21042-6, 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, OCT 30 2017. (13/08135-2, 12/50533-2, 14/22887-0)

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, DEC 2017. (14/22887-0, 14/21034-3, 13/08135-2, 14/21042-6, 12/50533-2)

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, JUL-SEP 2018. (18/01431-9, 13/08135-2, 17/19825-0, 14/22887-0, 14/21034-3)

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, AUG 1 2019. (15/17897-9, 14/22887-0, 15/21829-9, 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, DEC 2017. (14/03281-3, 13/08135-2, 12/50533-2, 14/22887-0, 14/21034-3)

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, DEC 2021. (17/20339-3, 19/04981-2, 15/21829-9, 14/22887-0)

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 on H3K9ac in bovine cells, oocytes and embryos (vol 8, 13766, 2018). SCIENTIFIC REPORTS, v. 8, p. 1-pg., 2018-11-16. (16/13416-9, 14/22887-0, 14/21034-3, 12/50533-2, 14/50947-7, 13/06673-7, 13/08135-2, 14/21097-5)

DA SILVA NUNES, PAOLA CAROLINE; MAZZARELLA, ROSANE; DA SILVEIRA, JULIANO COELHO; DELLOVA, DEISE CARLA ALMEIDA LEITE. Evaluation of circulating extracellular vesicles and miRNA in neutered and obese female dogs. SCIENTIFIC REPORTS, v. 12, n. 1, p. 11-pg., 2022-09-30. (18/26547-0, 15/21829-9, 14/22887-0)

VERDE LEAL, CLAUDIA LIMA; CANON-BELTRAN, KARINA; CAJAS, YULIA N.; HAMDI, MERIEM; YARYES, ARACELLI; MILLAN DE LA BLANCA, MARIA GEMMA; BELTRAN-BRENA, PAULA; MAZZARELLA, ROSANE; DA SILVEIRA, JULIANO COELHO; GUTIERREZ-ADAN, ALFONSO; et al. Extracellular vesicles from oviductal and uterine fluids supplementation in sequential in vitro culture improves bovine embryo quality. JOURNAL OF ANIMAL SCIENCE AND BIOTECHNOLOGY, v. 13, n. 1, p. 20-pg., 2022-10-25. (17/20339-3, 19/04981-2, 15/21829-9, 14/22887-0)

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, AUG 2021. (18/13155-6, 15/21829-9, 17/19681-9, 14/22887-0)

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, FEB 2020. (14/22887-0, 18/14869-2, 17/02037-0, 15/21829-9)

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, 2020. (17/02037-0, 15/21829-9, 14/22887-0)

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, NOV 2018. (14/22887-0, 15/16985-1)

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, JUL-SEP 2019. (18/01431-9, 18/13155-6, 17/19825-0, 14/22887-0, 13/08135-2)

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, OCT 1 2018. (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, SEP 13 2018. (13/08135-2, 16/13416-9, 13/06673-7, 12/50533-2, 14/21097-5, 14/22887-0, 14/21034-3)

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, JAN 2018. (13/10473-3, 15/16985-1, 12/50533-2, 17/02037-0, 14/22887-0)

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, JUN 15 2017. (13/10473-3, 13/08135-2, 12/50533-2, 14/22887-0, 14/21034-3)

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, SEP 18 2017. (12/50533-2, 13/08135-2, 14/22887-0, 14/21034-3)

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, DEC 2017. (13/10473-3, 13/08135-2, 12/50533-2, 14/22887-0, 14/21034-3)

BASTOS, NATALIA MARINS; GOULART, RODRIGO SILVA; BAMBIL, DANILO BRITO; BRIDI, ALESSANDRA; MAZZARELLA, ROSANE; ALVES, LUANA; ROSA, PAOLA MARIA DA SILVA; NETO, ADOMAR LAURINDO; SILVA, SAULO LUZ; SANTANA, MIGUEL HENRIQUE DE ALMEIDA; et al. High body energy reserve influences extracellular vesicles miRNA contents within the ovarian follicle. PLoS One, v. 18, n. 1, p. 22-pg., 2023-01-10. (15/21829-9, 14/22887-0, 20/08478-0)

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, v. 2019, p. 15-pg., 2019-01-01. (14/22887-0, 08/57877-3, 12/50533-2, 15/26818-5, 13/17955-3, 13/08135-2)

FERRONATO, GIULIANA DE AVILA; DOS SANTOS, CAROLINA MONICA; ROSA, PAOLA MARIA DA S.; BRIDI, ALESSANDRA; PERECIN, FELIPE; MEIRELLES, FLAVIO VIEIRA; SANGALLI, JULIANO RODRIGUES; DA SILVEIRA, JULIANO COELHO. Bovine in vitro oocyte maturation and embryo culture in liquid marbles 3D culture system. PLoS One, v. 18, n. 4, p. 17-pg., 2023-04-21. (19/25675-7, 14/22887-0, 21/06645-0)

BASTOS, NATALIA MARINS; FERST, JULIANA GERMANO; GOULART, RODRIGO SILVA; DA SILVEIRA, JULIANO COELHO. The role of the oviduct and extracellular vesicles during early embryo development in bovine. ANIMAL REPRODUCTION, v. 19, n. 1, p. 13-pg., 2022-01-01. (14/22887-0, 20/08478-0, 15/21829-9, 20/13075-2)

P.C.S. NUNES; S.M. SILVA; R. MAZZARELLA; C.G. LIMA; J.C. SILVEIRA; D.C.A. LEITE-DELLOVA. [Vesículas extracelulares pequenas no soro de cães com sobrepeso e obesos, antes e depois da perda de peso: observações preliminares]. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, v. 75, n. 1, p. 147-152, 2023-02-10. (15/21829-9, 18/26547-0, 19/04981-2, 14/22887-0)

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, OCT 15 2021. (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, OCT 15 2021. (16/24690-4, 18/12500-1, 15/21829-9, 14/22887-0)