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Inhibition of Hsp90 during in vitro maturation under thermoneutral or heat shock conditions compromises the developmental competence of bovine oocytes

Published online by Cambridge University Press:  15 September 2022

Eliza Diniz de Souza ,
Jessica Fernanda da Silva e Souza ,
Pedro Manoel de Oliveira Netto ,
Luciano de Rezende Carvalheira ,
Ribrio Ivan Tavares Pereira Batista Open the ORCID record for Ribrio Ivan Tavares Pereira Batista [Opens in a new window] ,
Carolina Capobiango Romano Quintão ,
Iuri Drumond Louro  and
Luiz Sergio Almeida Camargo Open the ORCID record for Luiz Sergio Almeida Camargo [Opens in a new window]
Eliza Diniz de Souza
Affiliation:
Universidade Federal do Espírito Santo, Av. Mal. Campos, 1468 – Maruipe, Vitória, ES, Brazil. 29047-105
Jessica Fernanda da Silva e Souza
Affiliation:
Universidade Federal de Juiz de Fora, Rua José Lourenço Kelmer, s/n, Campus Universitário, Juiz de Fora, MG, Brazil. 36036-900
Pedro Manoel de Oliveira Netto
Affiliation:
Embrapa Dairy Cattle, Rua Eugênio do Nascimento, 610, Juiz de Fora, MG, Brazil. 36038-330
Luciano de Rezende Carvalheira
Affiliation:
Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Caixa postal 567, Belo Horizonte, MG, Brazil. 31270-901
Ribrio Ivan Tavares Pereira Batista
Affiliation:
Universidade Federal Fluminense, Av. Vital Brasil Filho, 64, Niteroi, RJ, Brazil. 24230-340
Carolina Capobiango Romano Quintão
Affiliation:
Embrapa Dairy Cattle, Rua Eugênio do Nascimento, 610, Juiz de Fora, MG, Brazil. 36038-330
Iuri Drumond Louro
Affiliation:
Universidade Federal do Espírito Santo, Av. Mal. Campos, 1468 – Maruipe, Vitória, ES, Brazil. 29047-105
Luiz Sergio Almeida Camargo*
Affiliation:
Embrapa Dairy Cattle, Rua Eugênio do Nascimento, 610, Juiz de Fora, MG, Brazil. 36038-330
*
Author for correspondence: Luiz Sergio Almeida Camargo. Embrapa Dairy Cattle, Rua Eugênio do Nascimento, 610, Dom Bosco CEP: 36038-330, Juiz de Fora, MG, Brasil. E-mails: luiz.camargo@embrapa.br or camargo3112@gmail.com
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Summary

Heat shock protein 90 (Hsp90) is critical for cell homeostasis but its role on bovine oocyte maturation is not well known. We investigated the importance of Hsp90 for competence of bovine oocyte using 17-(allylamino)-17-demethoxygeldanamycin (17AAG), an inhibitor of Hsp90, during in vitro maturation (IVM). Three experiments evaluated the effect of 17AAG on developmental competence of oocytes matured in vitro under thermoneutral (38.5ºC) or heat shock (HS; 41.5ºC) temperatures. The first experiment found that the blastocyst rates were lower (P < 0.05) with 2 µM 17AAG compared with the untreated control (0 µM). The abundance of HSF1 transcripts was higher in oocytes matured with 2 µM than with 0 and 1 µM 17AAG, whereas the abundance of HSP90AA1 and HSPA1A transcripts was lower (P < 0.05) with 1 and 2 µM than with 0 µM. The second experiment found that 2 µM 17AAG for 12 or 24 h during IVM decreased (P < 0.05) the blastocysts rates. In the third experiment, the association of 2 μM 17AAG with HS for 12 h during IVM resulted in lower (P < 0.05) blastocysts rates than 17AAG, HS or untreated control. In conclusion, inhibition of Hsp90 during in vitro maturation compromises further embryo development; the association of Hsp90 inhibition with HS aggravates the deleterious effect of both on oocyte developmental competence.

Keywords

CattleGeldanamycinGene expressionHeat shock proteinHeat stress
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 854 - 862
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Ascari, I. J., Alves, N. G., Jasmin, J., Lima, R. R., Quintão, C. C. R., Oberlender, G., Moraes, E. A. and Camargo, L. S. A. (2017). Addition of insulin-like growth factor I to the maturation medium of bovine oocytes subjected to heat shock: Effects on the production of reactive oxygen species, mitochondrial activity and oocyte competence. Domestic Animal Endocrinology, 60, 50–60. doi: 10.1016/j.domaniend.2017.03.003 CrossRefGoogle Scholar
Barnier, J. V., Bensaude, O., Morange, M. and Babinet, C. (1987). Mouse 89 kD heat shock protein. Two polypeptides with distinct developmental regulation. Experimental Cell Research, 170(1), 186–194. doi: 10.1016/0014-4827(87)90128-5 CrossRefGoogle ScholarPubMed
Bettegowda, A. and Smith, G. W. (2007). Mechanisms of maternal mRNA regulation: Implications for mammalian early embryonic development. Frontiers in Bioscience: a Journal and Virtual Library, 12, 3713–3726. doi: 10.2741/2346 CrossRefGoogle ScholarPubMed
Camargo, L. S. A., Viana, J. H. M., Ramos, A. A., Serapião, R. V., de Sá, W. F., Ferreira, A. M., Guimarães, M. F. M. and do Vale Filho, V. R. (2007). Developmental competence and expression of the Hsp 70.1 gene in oocytes obtained from Bos indicus and Bos taurus dairy cows in a tropical environment. Theriogenology, 68(4), 626–632. doi: 10.1016/j.theriogenology.2007.03.029 CrossRefGoogle Scholar
Camargo, L. S. A., Aguirre-Lavin, T., Adenot, P., Araujo, T. D., Mendes, V. R. A., Louro, I. D., Beaujean, N. and Souza, E. D. (2019). Heat shock during in vitro maturation induces chromatin modifications in the bovine embryo. Reproduction, 158(4), 313–322. doi: 10.1530/REP-19-0245 CrossRefGoogle ScholarPubMed
Conde, R., Belak, Z. R., Nair, M., O’Carroll, R. F. and Ovsenek, N. (2009). Modulation of Hsf1 activity by novobiocin and geldanamycin. Biochemistry and Cell Biology, 87(6), 845–851. doi: 10.1139/o09-049 CrossRefGoogle ScholarPubMed
de Cárcer, G. (2004). Heat shock protein 90 regulates the metaphase-anaphase transition in a polo-like kinase-dependent manner. Cancer Research, 64(15), 5106–5112. doi: 10.1158/0008-5472.CAN-03-2214 CrossRefGoogle Scholar
Edwards, J. L. and Hansen, P. J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Molecular Reproduction and Development, 46(2), 138–145. doi: 10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R 3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Fair, T., Carter, F., Park, S., Evans, A. C. O. and Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology, 68, Suppl. 1, S91–S97. doi: 10.1016/j.theriogenology.2007.04.018 CrossRefGoogle ScholarPubMed
Fisher, D. L., Brassac, T., Galas, S. and Dorée, M. (1999). Dissociation of MAP kinase activation and MPF activation in hormone-stimulated maturation of Xenopus oocytes. Development, 126(20), 4537–4546. doi: 10.1242/dev.126.20.4537, PubMed: 10498688CrossRefGoogle ScholarPubMed
Fisher, D. L., Mandart, E. and Dorée, M. (2000). Hsp90 is required for c-Mos activation and biphasic MAP kinase activation in Xenopus oocytes. EMBO Journal, 19(7), 1516–1524. doi: 10.1093/emboj/19.7.1516 CrossRefGoogle ScholarPubMed
Gautier, J., Minshull, J., Lohka, M., Glotzer, M., Hunt, T. and Maller, J. L. (1990). Cyclin is a component of maturation-promoting factor from Xenopus. Cell, 60(3), 487–494. doi: 10.1016/0092-8674(90)90599-a CrossRefGoogle ScholarPubMed
Gendelman, M. and Roth, Z. (2012). Seasonal effect on germinal vesicle-stage bovine oocytes is further expressed by alterations in transcript levels in the developing embryos associated with reduced developmental competence. Biology of Reproduction, 86(1), 1–9. doi: 10.1095/biolreprod.111.092882 CrossRefGoogle ScholarPubMed
Grøndahl, C., Greve, T., Schmidt, M. and Hunter, R. H. F. (1996). Bovine pre-ovulatory follicles are cooler than ovarian stroma and deep rectal temperature. Theriogenology, 45(1), 289. doi: 10.1016/0093-691X(96)84762-5 CrossRefGoogle Scholar
Haupt, A., Joberty, G., Bantscheff, M., Fröhlich, H., Stehr, H., Schweiger, M. R., Fischer, A., Kerick, M., Boerno, S. T., Dahl, A., Lappe, M., Lehrach, H., Gonzalez, C., Drewes, G. and Lange, B. M. (2012). Hsp90 inhibition differentially destabilises MAP kinase and TGF-beta signalling components in cancer cells revealed by kinase-targeted chemoproteomics. BMC Cancer, 12, 38. doi: 10.1186/1471-2407-12-38 CrossRefGoogle ScholarPubMed
Hoter, A., El-Sabban, M. E. and Naim, H. Y. (2018). The HSP90 family: Structure, regulation, function, and implications in health and disease. International Journal of Molecular Sciences, 19(9), 2560. doi: 10.3390/ijms19092560 CrossRefGoogle ScholarPubMed
Hunter, R. H. F. and Einer-Jensen, N. (2005). Pre-ovulatory temperature gradients within mammalian ovaries: A review. Journal of Animal Physiology and Animal Nutrition, 89(7–8), 240–243. doi: 10.1111/j.1439-0396.2005.00509.x CrossRefGoogle ScholarPubMed
Johnson, V. A., Singh, E. K., Nazarova, L. A., Alexander, L. D. and McAlpine, S. R. (2010). Macrocyclic inhibitors of hsp90. Current Topics in Medicinal Chemistry, 10(14), 1380–1402. doi: 10.2174/156802610792232088 CrossRefGoogle ScholarPubMed
Key, N., Sneeringer, S. and Marquardt, D. (2014). Climate change, heat stress, and U.S. dairy production. http://www.ers.usda.gov/publications/err-economic-research-report/err175. SSRN Electronic Journal. doi: 10.2139/ssrn.2506668 CrossRefGoogle Scholar
Kim, H. R., Kang, H. S. and Kim, H. D. (1999). Geldanamycin induces heat shock protein expression through activation of HSF1 in K562 erythroleukemic cells. IUBMB Life, 48(4), 429–433. doi:10.1 doi: 10.1093/af/vfy027080/713803536 CrossRefGoogle ScholarPubMed
Kregel, K. C. (2002). Heat shock proteins: Modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology, 92(5), 2177–2186. doi: 10.1152/japplphysiol.01267.2001 CrossRefGoogle ScholarPubMed
Lang, B. J., Guerrero, M. E., Prince, T. L., Okusha, Y., Bonorino, C. and Calderwood, S. K. (2021). The functions and regulation of heat shock proteins; key orchestrators of proteostasis and the heat shock response. Archives of Toxicology, 95(6), 1943–1970. doi: 10.1007/s00204-021-03070-8 CrossRefGoogle ScholarPubMed
Lang, B. J., Prince, T. L., Okusha, Y., Bunch, H. and Calderwood, S. K. (2022). Heat shock proteins in cell signaling and cancer. Biochimica et Biophysica Acta. Molecular Cell Research, 1869(3), 119187. doi: 10.1016/j.bbamcr.2021.119187 CrossRefGoogle ScholarPubMed
Lanneau, D., Brunet, M., Frisan, E., Solary, E., Fontenay, M. and Garrido, C. (2008). Heat shock proteins: Essential proteins for apoptosis regulation. Journal of Cellular and Molecular Medicine, 12(3), 743–761. doi: 10.1111/j.1582-4934.2008.00273.x CrossRefGoogle ScholarPubMed
Liu, Y. H., Liu, X. M., Wang, P. C., Yu, X. X., Miao, J. K., Liu, S., Wang, Y. K., Du, Z. Q. and Yang, C. X. (2018). Heat shock protein 90α couples with the MAPK-signaling pathway to determine meiotic maturation of porcine oocytes1. Journal of Animal Science, 96(8), 3358–3369. doi: 10.1093/jas/sky213 CrossRefGoogle Scholar
López-Gatius, F. and Hunter, R. (2017). Clinical relevance of pre-ovulatory follicular temperature in heat-stressed lactating dairy cows. Reproduction in Domestic Animals, 52(3), 366–370. doi: 10.1111/rda.12916 CrossRefGoogle ScholarPubMed
Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M. A., Clarke, H. J., Khandjian, É. W., Richard, F. J., Hyttel, P. and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biology of Reproduction, 91(4), 90. doi: 10.1095/biolreprod.114.119867 CrossRefGoogle Scholar
Marchais, M., Gilbert, I., Bastien, A., Macaulay, A. and Robert, C. (2022). Mammalian cumulus–oocyte complex communication: A dialog through long and short distance messaging. Journal of Assisted Reproduction and Genetics, 39(5), 1011–1025. doi: 10.1007/s10815-022-02438-8 CrossRefGoogle ScholarPubMed
Massimini, M., Palmieri, C., De Maria, R., Romanucci, M., Malatesta, D., De Martinis, M., Maniscalco, L., Ciccarelli, A., Ginaldi, L., Buracco, P., Bongiovanni, L. and Della Salda, L. (2017). 17-AAG and apoptosis, autophagy, and mitophagy in canine osteosarcoma cell lines. Veterinary Pathology, 54(3), 405–412. doi: 10.1177/0300985816681409 CrossRefGoogle ScholarPubMed
Metchat, A., Åkerfelt, M., Bierkamp, C., Delsinne, V., Sistonen, L., Alexandre, H. and Christians, E. S. (2009). Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90α expression. Journal of Biological Chemistry, 284(14), 9521–9528. doi: 10.1074/jbc.M808819200 CrossRefGoogle ScholarPubMed
Morán Luengo, T., Mayer, M. P. and Rüdiger, S. G. D. (2019). The Hsp70–Hsp90 chaperone cascade in protein folding. Trends in Cell Biology, 29(2), 164–177. doi: 10.1016/j.tcb.2018.10.004 CrossRefGoogle ScholarPubMed
Mori, M., Hitora, T., Nakamura, O., Yamagami, Y., Horie, R., Nishimura, H. and Yamamoto, T. (2015). Hsp90 inhibitor induces autophagy and apoptosis in osteosarcoma cells. International Journal of Oncology, 46(1), 47–54. doi: 10.3892/ijo.2014.2727 CrossRefGoogle ScholarPubMed
Morimoto, R. I. (1993). Cells in stress: Transcriptional activation of heat shock genes. Science, 259(5100), 1409–1410. doi: 10.1126/science.8451637 CrossRefGoogle ScholarPubMed
Payton, R. R., Romar, R., Coy, P., Saxton, A. M., Lawrence, J. L. and Edwards, J. L. (2004). Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro . Biology of Reproduction, 71(4), 1303–1308. doi: 10.1095/biolreprod.104.029892 CrossRefGoogle ScholarPubMed
Pöhland, R., Souza-Cácares, M. B., Datta, T. K., Vanselow, J., Martins, M. I. M., da Silva, W. A. L., Cardoso, C. J. T. and Melo-Sterza, F. A. (2020). Influence of long-term thermal stress on the in vitro maturation on embryo development and heat shock protein abundance in zebu cattle. Animal Reproduction, 17(3), e20190085. doi: 10.1590/1984-3143-AR2019-0085 CrossRefGoogle ScholarPubMed
Prodromou, C. (2016). Mechanisms of Hsp90 regulation. Biochemical Journal, 473(16), 2439–2452. doi: 10.1042/BCJ20160005 CrossRefGoogle ScholarPubMed
Ramakers, C., Ruijter, J. M., Deprez, R. H. and Moorman, A. F. M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters, 339(1), 62–66. doi: 10.1016/s0304-3940(02)01423-4 CrossRefGoogle ScholarPubMed
Reyes, J. M., Chitwood, J. L. and Ross, P. J. (2015). RNA-seq profiling of single bovine oocyte transcript abundance and its modulation by cytoplasmic polyadenylation. Molecular Reproduction and Development, 82(2), 103–114. doi: 10.1002/mrd.22445 CrossRefGoogle ScholarPubMed
Rispoli, L. A., Edwards, J. L., Pohler, K. G., Russell, S., Somiari, R. I., Payton, R. R. and Schrick, F. N. (2019). Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows. PLoS One 14(12), e0227095. doi: 10.1371/journal.pone.0227095 CrossRefGoogle ScholarPubMed
Rodrigues, T. A., Ispada, J., Risolia, P. H. B., Rodrigues, M. T., Lima, R. S., Assumpção, M. E. O. A., Visintin, J. A. and Paula-Lopes, F. F. (2016). Thermoprotective effect of insulin-like growth factor 1 on in vitro matured bovine oocyte exposed to heat shock. Theriogenology, 86(8), 2028–2039. doi: 10.1016/j.theriogenology.2016.06.023 CrossRefGoogle ScholarPubMed
Roth, Z. (2015). Physiology and Endocrinology Symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function1. Journal of Animal Science, 93(5), 2034–2044. doi: 10.2527/jas.2014-8625 CrossRefGoogle Scholar
Roth, Z. and Hansen, P. J. (2004). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biology of Reproduction, 71(6), 1898–1906. doi: 10.1095/biolreprod.104.031690 CrossRefGoogle ScholarPubMed
Roth, Z. and Hansen, P. J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction, 129(2), 235–244. doi: 10.1530/rep.1.00394 CrossRefGoogle ScholarPubMed
Schmittgen, T. D. and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108. doi: 10.1038/nprot.2008.73 CrossRefGoogle Scholar
Schopf, F. H., Biebl, M. M. and Buchner, J. (2017). The HSP90 chaperone machinery. Nature Reviews. Molecular Cell Biology, 18(6), 345–360. doi: 10.1038/nrm.2017.20 CrossRefGoogle ScholarPubMed
Schulte, T. W. and Neckers, L. M. (1998). The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemotherapy and Pharmacology, 42(4), 273–279. doi: 10.1007/s002800050817 CrossRefGoogle ScholarPubMed
Silva, C. F., Sartorelli, E. S., Castilho, A. C. S., Satrapa, R. A., Puelker, R. Z., Razza, E. M., Ticianelli, J. S., Eduardo, H. P., Loureiro, B. and Barros, C. M. (2013). Effects of heat stress on development, quality and survival of Bos indicus and Bos taurus embryos produced in vitro . Theriogenology, 79(2), 351–357. doi: 10.1016/j.theriogenology.2012.10.003 CrossRefGoogle ScholarPubMed
Son, M.-J., Park, J.-M., Min, S.-H., Hong, J.-H., Park, H. and Koo, D.-B. (2010). HSP90 inhibitor, 17-AAG, affects meiotic maturation and preimplantation embryos development in pigs. Biology of Reproduction, 83(Suppl 1), 256–256. doi: 10.1093/biolreprod/83.s1.256 CrossRefGoogle Scholar
Son, M.-J., Park, J.-M., Min, S.-H., Hong, J.-H., Park, H. and Koo, D.-B. (2011). Hsp90 inhibitor induces cell cycle arrest and apoptosis of early embryos and primary cells in pigs. Reproductive and Developmental Biologi, 35, 33–45.Google Scholar
Torres-Júnior, J. R. d. S., Pires, M. d. F. A., de Sá, W. F., Ferreira, A. d. M., Viana, J. H. M., Camargo, L. S. A., Ramos, A. A., Folhadella, I. M., Polisseni, J., de Freitas, C., Clemente, C. A. A., de Sá Filho, M. F., Paula-Lopes, F. F. and Baruselli, P. S. (2008). Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology, 69(2), 155–166. doi: 10.1016/j.theriogenology.2007.06.023 CrossRefGoogle Scholar
Trounson, A., Anderiesz, C. and Jones, G. (2001). Maturation of human oocytes in vitro and their developmental competence. Reproduction, 121(1), 51–75. doi: 10.1530/rep.0.1210051 CrossRefGoogle ScholarPubMed
Vabulas, R. M., Raychaudhuri, S., Hayer-Hartl, M. and Hartl, F. U. (2010). Protein folding in the cytoplasm and the heat shock response. Cold Spring Harbor Perspectives in Biology, 2(12), a004390–a004390. doi: 10.1101/cshperspect.a004390 CrossRefGoogle ScholarPubMed
Verlhac, M. H., Kubiak, J. Z., Weber, M., Géraud, G., Colledge, W. H., Evans, M. J. and Maro, B. (1996). Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development, 122(3), 815–822. doi: 10.1242/dev.122.3.815 CrossRefGoogle ScholarPubMed
Wolfenson, D. and Roth, Z. (2019). Impact of heat stress on cow reproduction and fertility. Animal Frontiers: The Review Magazine of Animal Agriculture, 9(1), 32–38. doi: 10.1093/af/vfy027 CrossRefGoogle ScholarPubMed
Wolfenson, D., Roth, Z. and Meidan, R. (2000). Impaired reproduction in heat-stressed cattle: Basic and applied aspects. Animal Reproduction Science, 60–61, 535–547. doi: 10.1016/S0378-4320(00)00102-0 CrossRefGoogle ScholarPubMed
Wu, Y., Li, M. and Yang, M. (2021). Post-translational modifications in oocyte maturation and embryo development. Frontiers in Cell and Developmental Biology, 9, 645318. doi: 10.3389/fcell.2021.645318 CrossRefGoogle ScholarPubMed
Yahara, I. (2019). A role for epigenetic adaption in evolution. Genes to Cells: Devoted to Molecular and Cellular Mechanisms, 24(8), 524–533. doi: 10.1111/gtc.12709 CrossRefGoogle Scholar
Zhao, R. and Houry, W. A. (2005). Hsp90: A chaperone for protein folding and gene regulation. Biochemistry and Cell Biology, 83(6), 703–710. doi: 10.1139/o05-158 CrossRefGoogle ScholarPubMed
Zou, J., Guo, Y., Guettouche, T., Smith, D. F. and Voellmy, R. (1998). Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell, 94(4), 471–480. doi: 10.1016/s0092-8674(00)81588-3 CrossRefGoogle ScholarPubMed