Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes

Ilustraciones

Autores:: Londoño Vásquez, Daniela

Tipo de recurso:: Doctoral thesis

Fecha de publicación:: 2023

Institución:: Universidad Nacional de Colombia

Repositorio:: Universidad Nacional de Colombia

Idioma:: eng

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dc.title.eng.fl_str_mv	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
dc.title.translated.spa.fl_str_mv	Rol de las proteínas motoras de los microtúbulos en el anclaje y el posicionamiento del huso meiótico durante la meiosis I en oocitos de ratón
title	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
spellingShingle	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes 630 - Agricultura y tecnologías relacionadas::636 - Producción animal mcMTOCs Microtubules F-actin Dynein Eg5 kinesin Microtúbulos Proteína motora Microtúbulo Oocito
title_short	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
title_full	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
title_fullStr	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
title_full_unstemmed	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
title_sort	Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes
dc.creator.fl_str_mv	Londoño Vásquez, Daniela
dc.contributor.advisor.none.fl_str_mv	Balboula, Ahmed Z. Camargo Rodriguez, Omar
dc.contributor.author.none.fl_str_mv	Londoño Vásquez, Daniela
dc.subject.ddc.spa.fl_str_mv	630 - Agricultura y tecnologías relacionadas::636 - Producción animal
topic	630 - Agricultura y tecnologías relacionadas::636 - Producción animal mcMTOCs Microtubules F-actin Dynein Eg5 kinesin Microtúbulos Proteína motora Microtúbulo Oocito
dc.subject.proposal.eng.fl_str_mv	mcMTOCs Microtubules F-actin Dynein Eg5 kinesin
dc.subject.proposal.spa.fl_str_mv	Microtúbulos
dc.subject.wikidata.none.fl_str_mv	Proteína motora Microtúbulo Oocito
description	Ilustraciones
publishDate	2023
dc.date.issued.none.fl_str_mv	2023-01
dc.date.accessioned.none.fl_str_mv	2024-02-07T13:35:26Z
dc.date.available.none.fl_str_mv	2024-02-07T13:35:26Z
dc.type.spa.fl_str_mv	Trabajo de grado - Doctorado
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dc.identifier.instname.spa.fl_str_mv	Universidad Nacional de Colombia
dc.identifier.reponame.spa.fl_str_mv	Repositorio Institucional Universidad Nacional de Colombia
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url	https://repositorio.unal.edu.co/handle/unal/85641 https://repositorio.unal.edu.co/
identifier_str_mv	Universidad Nacional de Colombia Repositorio Institucional Universidad Nacional de Colombia
dc.language.iso.spa.fl_str_mv	eng
language	eng
dc.relation.indexed.spa.fl_str_mv	LaReferencia
dc.relation.references.spa.fl_str_mv	Azzu, V., & Valencak, T. G. (2017). Energy Metabolism and Ageing in the Mouse: A MiniReview. Gerontology, 63(4), 327–336. https://doi.org/10.1159/000454924 Bazer, F. W., Thatcher, W. W., Hansen, P. J., Mirando, M. A., Ott, T. L., & Plante, C. (1991). Physiological mechanisms of pregnancy recognition in ruminants. Journal of Reproduction and Fertility. Supplement, 43, 39–47. https://doi.org/10.1530/biosciprocs.2.004 Goodson, H. V, & Jonasson, E. M. (2018). Microtubules and Microtubule-Associated Proteins. Cold Spring Harbor Perspectives in Biology Hall, H., Surti, U., Hoffner, L., Shirley, S., Feingold, E., & Hassold, T. (2006). The origin of trisomy 22: Evidence for acrocentric chromosome-specific patterns of nondisjunction. American Journal of Human Genetics, 221(3), 212–221. https://doi.org/10.1002/ajmg.a Hassold, T., & Hunt, P. (2001). To err (meiotically) is human: The genesis of human https://doi.org/10.1038/35066065 Mogessie, B., Scheffler, K., & Schuh, M. (2018). Assembly and Positioning of the Oocyte Meiotic Spindle. Annual Review of Cell and Developmental Biology, 34, 381–403. https://doi.org/10.1146/annurev-cellbio-100616-060553 Szollosi, D., Calarco, P., & Donahue, R. P. (1972). Absence of centrioles in the first and second meiotic spindles of mouse oocytes. Journal of Cell Science, 11(2), 521–541. https://doi.org/10.1242/jcs.11.2.521 Abrieu, A., Magnaghi-Jaulin, L., Kahana, J. A., Peter, M., Castro, A., Vigneron, S., Lorca, T., Cleveland, D. W., & Labbé, J. C. (2001). Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell, 106(1), 83–93. https://doi.org/10.1016/S0092-8674(01)00410-X Basu, J., Logarinho, E., Herrmann, S., Bousbaa, H., Li, Z., Chan, G. K. T., Yen, T. J., Sunkel, C. E., & Goldberg, M. L. (1998). Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma, 107(6–7), 376–385. https://doi.org/10.1007/s004120050321 Bloom, G. S. (1992). Motor proteins for cytoplasmic microtubules. Current Opinion in Cell Biology, 4(1), 66–73. https://doi.org/10.1016/0955-0674(92)90060-P Camlin, N. J., McLaughlin, E. A., & Holt, J. E. (2017). Motoring through: The role of kinesin superfamily proteins in female meiosis. Human Reproduction Update, 23(4), 409–420. https://doi.org/10.1093/humupd/dmx010 Cianfrocco, M. A., DeSantis, M. E., Leschziner, A. E., & Samara L. Reck-Peterson. (2016). Mechanism and Regulation of Cytoplasmic Dynein Michael. Physiology & Behavior, 176(1), 139–148. https://doi.org/10.1146/annurev-cellbio-100814-125438.Mechanism Desai, A., & Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annual Review of Cell and Developmental Biology, 13, 83–117. https://doi.org/10.1146/annurev.cellbio.13.1.83 Garcia-Cruz, R., Brieño, M. A., Roig, I., Grossmann, M., Velilla, E., Pujol, A., Cabero, L., Pessarrodon , A., Barbero, J. L., & Garcia Caldés, M. (2010). Dynamics of cohesin proteins REC8, STAG3, SMC1β and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Human Reproduction, 25(9), 2316–2327. https://doi.org/10.1093/humrep/deq180 Gueth-Hallonet, C., Antony, C., Aghion, J., Santa-Maria, A., Lajoie-Mazenc, I., Wright, M., & Maro, B. (1993). γ-Tubulin is present in acentriolar MTOCs during early mouse development. Journal of Cell Science, 105(1), 157–166. https://doi.org/10.1242/jcs.105.1.157 Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A., & Karsenti, E. (1996). Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature, 382(6590), 420–425. https://doi.org/10.1038/382420a0 Höing, S., Yeh, T. Y., Baumann, M., Martinez, N. E., Habenberger, P., Kremer, L., Drexler, H. C. A., Küchler, P., Reinhardt, P., Choidas, A., Zischinsky, M. L., Zischinsky, G., Nandini, S., Ledray, A. P., Ketcham, S. A., Reinhardt, L., Abo-Rady, M., Glatza, M., King, S. J., … Sterneckert, J. (2018). Dynarrestin, a Novel Inhibitor of Cytoplasmic Dynein. Cell Chemical Biology, 25(4), 357-369.e6. https://doi.org/10.1016/j.chembiol.2017.12.014 Kapoor, T. M., Mayer, T. U., Coughlin, M. L., & Mitchison, T. J. (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. Journal of Cell Biology, 150(5), 975–988. https://doi.org/10.1083/jcb.150.5.975 Kim, J., Ishiguro, K. I., Nambu, A., Akiyoshi, B., Yokobayashi, S., Kagami, A., Ishiguro, T., Pendas, A. M., Takeda, N., Sakakibara, Y., Kitajima, T. S., Tanno, Y., Sakuno, T., & Watanabe, Y. (2015). Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature, 517(7535), 466–471. https://doi.org/10.1038/nature14097 Kull, F. J., Vale, R. D., & Fletterick, R. J. (1998). Kinesin Myosin common ancestor:kinesin and myosin motor proteins and G proteins. Journal of Muscle Research and Cell Motility, 19(877–886), 1–10. papers2://publication/uuid/F36A5F3D-2227-42AE-A03CAF2E46DCB611 Li, H., Guo, F., Rubinstein, B., & Li, R. (2008). Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nature Cell Biology, 10(11), 1301– 1308. https://doi.org/10.1038/ncb1788 Londoño-Vásquez, D., Rodriguez-Lukey, K., Behura, S. K., & Balboula, A. Z. (2022). Microtubule organizing centers regulate spindle positioning in mouse oocytes. Developmental Cell, 57(2), 197-211.e3. https://doi.org/10.1016/j.devcel.2021.12.011 McClellan, K. A., Gosden, R., & Taketo, T. (2003). Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Developmental Biology, 258(2), 334– 348. https://doi.org/10.1016/S0012-1606(03)00132-5
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dc.format.extent.spa.fl_str_mv	122 páginas
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dc.publisher.spa.fl_str_mv	Universidad Nacional de Colombia
dc.publisher.program.spa.fl_str_mv	Medellín - Ciencias Agrarias - Doctorado en Ciencias Agrarias
dc.publisher.faculty.spa.fl_str_mv	Facultad de Ciencias Agrarias
dc.publisher.place.spa.fl_str_mv	Medellín, Colombia
dc.publisher.branch.spa.fl_str_mv	Universidad Nacional de Colombia - Sede Medellín
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spelling	Atribución-SinDerivadas 4.0 Internacionalhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/closedAccesshttp://purl.org/coar/access_right/c_14cbBalboula, Ahmed Z.df0c47894cc7e059a65fff25ec860a54Camargo Rodriguez, Omar1e6ec0b05ff3ed235c48699c90259626Londoño Vásquez, Daniela321180aa3358331c9cb06108a9477ef52024-02-07T13:35:26Z2024-02-07T13:35:26Z2023-01https://repositorio.unal.edu.co/handle/unal/85641Universidad Nacional de ColombiaRepositorio Institucional Universidad Nacional de Colombiahttps://repositorio.unal.edu.co/IlustracionesChromosome segregation errors frequently occur during oocyte meiosis I (MI) leading to aneuploidy, the major cause of miscarriage and congenital abnormalities. Post nuclear envelope break down, the meiotic spindle is assembled at the center of the oocyte. This initial position prevents the occurrence of aneuploidy. During metaphase I (Met I), the spindle migrates toward the cortex to allow a highly asymmetric division. In mouse oocytes, spindle positioning and migration is regulated by two opposing forces, F-actin and metaphase cytoplasmic microtubule organizing centers (mcMTOCs), whereby mcMTOCnucleated microtubules (MTs) anchor the spindle to the cortex exerting an opposing pulling force on the spindle against that of F-actin-mediated force which builds to move the spindle to the cortex for PB extrusion. However, the molecular mechanism of how MTs regulate spindle positioning remains unknown. First, oocyte MT dynamics have been investigated during MI. Interestingly, mcMTOCnucleated MTs depend on the maturation time, whereby, at Met I when the spindle is still located at the center of the oocyte, the MTs nucleated by mcMTOCs play an important role in maintaining and regulating this initial central position. However, at late Met I, the mcMTOC-nucleated MTs gradually decrease allowing spindle migration. MT motors are ATPase-associated proteins that convert energy into mechanical force and move along the length of MTs. In somatic cells, MT motor proteins regulate MT dynamics necessary for mitotic spindle positioning. In contrast, their role in mammalian oocytes has not been investigated. Perturbation of dynein protein results in abnormal spindle positioning, accelerated spindle migration towards the cortex, and increased incidence of aneuploidy. In contrast, Eg5 kinesin inhibition results in failed spindle migration. On the other hand, X Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes perturbing F-actin around the mcMTOCs, results in abnormal spindle positioning and migration. These findings suggest that MT dynamics regulate spindle positioning and migration. Dynein and Eg5 kinesin motor proteins drive two antagonistic forces to fine-tune mcMTOC-mediated MT pulling force and provide the first mechanistic insight into mcMTOC-nucleated MT role in directly influencing spindle positioning and timely migration and F-actin ring contribute to regulates mcMTOC dynamics.En la fase de meiosis I del oocito, frecuentemente ocurren errores durante el proceso de segregación cromosómica, resultando en aneuploidías que son la principal causa de aborto espontáneo y mal formaciones congénitas. Después de la ruptura de la envoltura nuclear, en el centro del oocito, inicia la formación del huso meiótico, cuya posición inicial es indispensable para la prevención de aneuploidías. Posteriormente, en la metafase I, el huso meiótico migra hacia la corteza para permitir una marcada división asimétrica. En los oocitos de ratón, el posicionamiento y la migración del huso meiótico está regulado por dos fuerzas opuestas, la F-actina y los centros organizadores de microtúbulos citoplasmáticos en metafase (mcMTOCs, por sus siglas en inglés). Es así como, los microtúbulos (MTs) nucleados por los mcMTOCs anclan el huso a la corteza, ejerciendo una fuerza de tracción opuesta en el huso contra la fuerza mediada por la F-actina que se acumula para movilizar el huso a la corteza para la expulsión del cuerpo polar. Sin embargo, el mecanismo molecular por el cual los MTs regulan el posicionamiento del huso sigue siendo desconocido. En primer lugar, se investigó la dinámica de los MTs durante la meiosis I del oocito. Donde se identificó que los MT nucleados por los mcMTOCs dependen del tiempo de maduración del oocito. Por lo cual, en metafase I, cuando el huso aún se encuentra localizado en el centro del oocito, los MT nucleados por los mcMTOCs juegan un papel indispensable en el mantenimiento y regulación de la posición inicial del huso en el centro del oocito. Sin embargo, en la metafase I tardía, los MTs nucleados por los mcMTOCs disminuyen gradualmente permitiendo la migración del huso. Las proteínas motoras están asociadas a la ATPasa que convierten energía en fuerza mecánica y se mueven a lo largo de los MTs. En las células somáticas, estas juegan un rol indispensable en la regulación de la XII Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes dinámica de los MTs, necesarias para el posicionamiento del huso mitótico, no obstante, el rol de estas proteínas no ha sido investigado en los oocitos de mamíferos. La perturbación de la proteína dineína resulta en un posicionamiento anormal del huso, una migración del huso acelerada hacia la corteza e incrementa la incidencia de aneuploidías. En contraste, la inhibición de la proteína kinesina Eg5 muestra como resultado una migración fallida del huso. Finalmente, la perturbación de la F-actina alrededor de los mcMTOCs resulta en un anormal posicionamiento y migración del huso meiótico. Estos hallazgos sugieren que la dinámica de los MTs regula el posicionamiento y migración del huso. La dineína y la kinesina Eg5 impulsan dos fuerzas antagónicas para afinar la fuerza de tracción de los MTs nucleados por los mcMTOCs. Además, proporcionan la primera visión mecánica del papel de los MTs nucleados por los mcMTOCs, ya que regulan el posicionamiento y migración oportuna del huso meiótico. A su vez, la F-actina, componente del citoesqueleto, regula la dinámica de los mcMTOCs. Palabras clave: (mcMTOCs, microtúbulos, F-actina, dineína, kinesina E (texto tomado de la fuente)DoctoradoDoctor en Ciencias AgrariasDevelopmental biologyÁrea Curricular en Producción Agraria Sostenible122 páginasapplication/pdfengUniversidad Nacional de ColombiaMedellín - Ciencias Agrarias - Doctorado en Ciencias AgrariasFacultad de Ciencias AgrariasMedellín, ColombiaUniversidad Nacional de Colombia - Sede Medellín630 - Agricultura y tecnologías relacionadas::636 - Producción animalmcMTOCsMicrotubulesF-actinDyneinEg5 kinesinMicrotúbulosProteína motoraMicrotúbuloOocitoRole of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytesRol de las proteínas motoras de los microtúbulos en el anclaje y el posicionamiento del huso meiótico durante la meiosis I en oocitos de ratónTrabajo de grado - Doctoradoinfo:eu-repo/semantics/masterThesisinfo:eu-repo/semantics/acceptedVersionhttp://purl.org/coar/resource_type/c_db06Texthttp://purl.org/redcol/resource_type/TDLaReferenciaAzzu, V., & Valencak, T. G. (2017). Energy Metabolism and Ageing in the Mouse: A MiniReview. Gerontology, 63(4), 327–336. https://doi.org/10.1159/000454924Bazer, F. W., Thatcher, W. W., Hansen, P. J., Mirando, M. A., Ott, T. L., & Plante, C. (1991). Physiological mechanisms of pregnancy recognition in ruminants. Journal of Reproduction and Fertility. Supplement, 43, 39–47. https://doi.org/10.1530/biosciprocs.2.004Goodson, H. V, & Jonasson, E. M. (2018). Microtubules and Microtubule-Associated Proteins. Cold Spring Harbor Perspectives in BiologyHall, H., Surti, U., Hoffner, L., Shirley, S., Feingold, E., & Hassold, T. (2006). The origin of trisomy 22: Evidence for acrocentric chromosome-specific patterns of nondisjunction. American Journal of Human Genetics, 221(3), 212–221. https://doi.org/10.1002/ajmg.aHassold, T., & Hunt, P. (2001). To err (meiotically) is human: The genesis of human https://doi.org/10.1038/35066065Mogessie, B., Scheffler, K., & Schuh, M. (2018). Assembly and Positioning of the Oocyte Meiotic Spindle. Annual Review of Cell and Developmental Biology, 34, 381–403. https://doi.org/10.1146/annurev-cellbio-100616-060553Szollosi, D., Calarco, P., & Donahue, R. P. (1972). Absence of centrioles in the first and second meiotic spindles of mouse oocytes. Journal of Cell Science, 11(2), 521–541. https://doi.org/10.1242/jcs.11.2.521Abrieu, A., Magnaghi-Jaulin, L., Kahana, J. A., Peter, M., Castro, A., Vigneron, S., Lorca, T., Cleveland, D. W., & Labbé, J. C. (2001). Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell, 106(1), 83–93. https://doi.org/10.1016/S0092-8674(01)00410-XBasu, J., Logarinho, E., Herrmann, S., Bousbaa, H., Li, Z., Chan, G. K. T., Yen, T. J., Sunkel, C. E., & Goldberg, M. L. (1998). Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma, 107(6–7), 376–385. https://doi.org/10.1007/s004120050321Bloom, G. S. (1992). Motor proteins for cytoplasmic microtubules. Current Opinion in Cell Biology, 4(1), 66–73. https://doi.org/10.1016/0955-0674(92)90060-PCamlin, N. J., McLaughlin, E. A., & Holt, J. E. (2017). Motoring through: The role of kinesin superfamily proteins in female meiosis. Human Reproduction Update, 23(4), 409–420. https://doi.org/10.1093/humupd/dmx010Cianfrocco, M. A., DeSantis, M. E., Leschziner, A. E., & Samara L. Reck-Peterson. (2016). Mechanism and Regulation of Cytoplasmic Dynein Michael. Physiology & Behavior, 176(1), 139–148. https://doi.org/10.1146/annurev-cellbio-100814-125438.MechanismDesai, A., & Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annual Review of Cell and Developmental Biology, 13, 83–117. https://doi.org/10.1146/annurev.cellbio.13.1.83Garcia-Cruz, R., Brieño, M. A., Roig, I., Grossmann, M., Velilla, E., Pujol, A., Cabero, L., Pessarrodon , A., Barbero, J. L., & Garcia Caldés, M. (2010). Dynamics of cohesin proteins REC8, STAG3, SMC1β and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Human Reproduction, 25(9), 2316–2327. https://doi.org/10.1093/humrep/deq180Gueth-Hallonet, C., Antony, C., Aghion, J., Santa-Maria, A., Lajoie-Mazenc, I., Wright, M., & Maro, B. (1993). γ-Tubulin is present in acentriolar MTOCs during early mouse development. Journal of Cell Science, 105(1), 157–166. https://doi.org/10.1242/jcs.105.1.157Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A., & Karsenti, E. (1996). Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature, 382(6590), 420–425. https://doi.org/10.1038/382420a0Höing, S., Yeh, T. Y., Baumann, M., Martinez, N. E., Habenberger, P., Kremer, L., Drexler, H. C. A., Küchler, P., Reinhardt, P., Choidas, A., Zischinsky, M. L., Zischinsky, G., Nandini, S., Ledray, A. P., Ketcham, S. A., Reinhardt, L., Abo-Rady, M., Glatza, M., King, S. J., … Sterneckert, J. (2018). Dynarrestin, a Novel Inhibitor of Cytoplasmic Dynein. Cell Chemical Biology, 25(4), 357-369.e6. https://doi.org/10.1016/j.chembiol.2017.12.014Kapoor, T. M., Mayer, T. U., Coughlin, M. L., & Mitchison, T. J. (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. Journal of Cell Biology, 150(5), 975–988. https://doi.org/10.1083/jcb.150.5.975Kim, J., Ishiguro, K. I., Nambu, A., Akiyoshi, B., Yokobayashi, S., Kagami, A., Ishiguro, T., Pendas, A. M., Takeda, N., Sakakibara, Y., Kitajima, T. S., Tanno, Y., Sakuno, T., & Watanabe, Y. (2015). Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature, 517(7535), 466–471. https://doi.org/10.1038/nature14097Kull, F. J., Vale, R. D., & Fletterick, R. J. (1998). Kinesin Myosin common ancestor:kinesin and myosin motor proteins and G proteins. Journal of Muscle Research and Cell Motility, 19(877–886), 1–10. papers2://publication/uuid/F36A5F3D-2227-42AE-A03CAF2E46DCB611Li, H., Guo, F., Rubinstein, B., & Li, R. (2008). Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nature Cell Biology, 10(11), 1301– 1308. https://doi.org/10.1038/ncb1788Londoño-Vásquez, D., Rodriguez-Lukey, K., Behura, S. K., & Balboula, A. Z. (2022). Microtubule organizing centers regulate spindle positioning in mouse oocytes. Developmental Cell, 57(2), 197-211.e3. https://doi.org/10.1016/j.devcel.2021.12.011McClellan, K. A., Gosden, R., & Taketo, T. (2003). Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Developmental Biology, 258(2), 334– 348. https://doi.org/10.1016/S0012-1606(03)00132-5InvestigadoresLICENSElicense.txtlicense.txttext/plain; charset=utf-85879https://repositorio.unal.edu.co/bitstream/unal/85641/1/license.txteb34b1cf90b7e1103fc9dfd26be24b4aMD51ORIGINALDaniela Londono Vasquez_tesis_embargo.pdfDaniela Londono Vasquez_tesis_embargo.pdfTesis de Doctorado en Ciencias Agrariasapplication/pdf3314505https://repositorio.unal.edu.co/bitstream/unal/85641/4/Daniela%20Londono%20Vasquez_tesis_embargo.pdfb2fde39e33ba49978ccf21e7c2ea0384MD54CC-LICENSEDaniela Londono Vasquez_licencia_embargo.pdfDaniela Londono Vasquez_licencia_embargo.pdfapplication/pdf220664https://repositorio.unal.edu.co/bitstream/unal/85641/3/Daniela%20Londono%20Vasquez_licencia_embargo.pdfc8c787ea5b0e2e1125554fc5bc0442a5MD53THUMBNAILDaniela Londono Vasquez_tesis_embargo.pdf.jpgDaniela Londono Vasquez_tesis_embargo.pdf.jpgGenerated 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Role of microtubule motor proteins in the spindle anchoring and positioning during meiosis I in mouse oocytes

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