Effects of Assisted Reproductive Technologies on Social Behavior of BTBR Mice – A Model of Autism Spectrum Disorder

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The present work is the first attempt to study the effect of such assisted reproductive technologies (ARTs), as in vitro culture of preimplantation embryos on the social behavior of offspring, using BTBR mice (BTBR T+Itpr3tf/J) as an idiopathic model of a-utism. The C57BL/6J mice were used as controls. Social behavior was studied in adult offspring mice obtained after in vitro culture and embryo transfer (ET) (groups ET-C57BL/6J and ET-BTBR). The BTBR mice demonstrated the reduced levels of social recognition and affiliation compared to C57BL/6J mice. The social affiliation and recognition test revealed that ET-C57BL/6J males had a high level of social interaction, which was of similar magnitude as in naturally conceived C57BL/6J males. However, ET-C57BL/6J and ET-BTBR females demonstrated a decrease in interest to a new stranger compared to naturally conceived controls of the same sex, which was revealed in a social recognition session of this test. Thus, the in vitro culture affected the social recognition in the offspring of C57BL/6J and BTBR mice, but only in females.

作者简介

I. Rozhkova

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

S. Okotrub

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

E. Brusentsev

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

T. Igonina

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

T. Rakhmanova

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: amstis@yandex.ru
Russia, Novosibirsk; Russia, Novosibirsk

D. Lebedeva

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: amstis@yandex.ru
Russia, Novosibirsk; Russia, Novosibirsk

T. Yatsuk

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

V. Kozeneva

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: amstis@yandex.ru
Russia, Novosibirsk; Russia, Novosibirsk

V. Naprimerov

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

Email: amstis@yandex.ru
Russia, Novosibirsk

S. Amstislavsky

Institute of Cytology and Genetics Siberian Branch of the Russian Academy of Sciences

编辑信件的主要联系方式.
Email: amstis@yandex.ru
Russia, Novosibirsk

参考

  1. American Psychiatric Association (APA) (2013) Autism spectrum disorder, diagnostic and statistical manual of mental disorders. Fifth ed. Am Psychiatric Publ. Arlington. VA. 50–59.
  2. Kodak T, Bergmann S (2020) Autism spectrum disorder: characteristics, associated behaviors, and early intervention. Pediatr Clin North Am 67: 525–535. https://doi.org/10.1016/j.pcl.2020.02.007
  3. Ivanov HY, Stoyanova VK, Popov NT, Vachev TI (2015) Autism spectrum disorder – a complex genetic disorder. Folia Med (Plovdiv) 57: 19–28. https://doi.org/10.1515/folmed-2015-0015
  4. Waye MMY, Cheng HY (2017) Genetics and epigenetics of autism: a review. Psychiatry Clin Neurosci 72: 228–244. https://doi.org/10.1111/pcn.12606
  5. Yang G, Shcheglovitov A (2020) Probing disrupted neurodevelopment in autism using human stem cell-derived neurons and organoids: An outlook into future diagnostics and drug development. Dev Dyn 249: 6–33. https://doi.org/10.1002/dvdy.100
  6. Girault JB, Piven J (2020) The Neurodevelopment of autism from infancy through toddlerhood. Neuroimaging Clin N Am 30: 97–114. https://doi.org/10.1016/j.nic.2019.09.009
  7. Ramos-Ibeas P, Heras S, Gomez-Redondo I, Planells B, Fernandez-Gonzalez R, Pericuesta E, Laguna-Barraza R, Perez-Cerezales S, Gutierrez-Adan A (2019) Embryo responses to stress induced by assisted reproductive technologies. Mol Reprod Dev 86: 1292–1306. https://doi.org/10.1002/mrd.23119
  8. Berntsen S, Soderstrom-Anttila V, Wennerholm U-B, Laivuori H, Loft A, Oldereid NB, Romundstad LB, Bergh C, Pinborg A (2019) The health of children conceived by ART: “the chicken or the egg?” Hum Reprod Update 25: 137–158.
  9. Sandin S, Nygren KG, Iliadou A, Hultman CM, Reichenberg A (2013) Autism and mental retardation among offspring born after in vitro fertilization. JAMA 310: 75–84. https://doi.org/10.1001/jama.2013.7222
  10. Kissin DM, Zhang Y, Boulet SL, Fountain C, Bearman P, Schieve L, Yeargin-Allsopp M, Jamieson DJ (2015) Association of assisted reproductive technology (ART) treatment and parental infertility diagnosis with autism in ART-conceived children. Hum Reprod 30: 454–465. https://doi.org/10.1093/humrep/deu338
  11. Liu L, Gao J, He X, Cai Y, Wang L, Fan X (2017) Association between assisted reproductive technology and the risk of autism spectrum disorders in the offspring: a meta-analysis. Sci Rep 7: 46207. https://doi.org/10.1038/srep46207
  12. Andreadou MT, Katsaras GN, Talimtzi P, Doxani C, Zintzaras E, Stefanidis I (2021) Association of assisted reproductive technology with autism spectrum disorder in the offspring: an updated systematic review and meta-analysis. Eur J Pediatr 180: 2741–2755. https://doi.org/10.1007/s00431-021-04187-9
  13. Rumbold AR, Moore VM, Whitrow MJ, Oswald TK, Moran LJ, Fernandez RC, Barnhart KT, Davies MJ (2017) The impact of specific fertility treatments on cognitive development in childhood and adolescence: a systematic review. Hum Reprod 32: 1489–1507. https://doi.org/10.1093/humrep/dex085
  14. La Rovere M, Franzago M, Stuppia L (2019) Epigenetics and neurological disorders in ART. Int J Mol Sci 20: 4169. https://doi.org/10.3390/ijms20174169
  15. Sunde A (2019) Embryo culture and phenotype of the offspring. In Vitro Fertilization: 877–889.
  16. Gleicher N, Kushnir VA, Barad DH (2014) Preimplantation genetic screening (PGS) still in search of a clinical application: a systematic review. Reprod Biol Endocrinol 12: 22. https://doi.org/10.1186/1477-7827-12-22
  17. Pontesilli M, Painter RC, Grooten IJ, van der Post JA, Mol BW, Vrijkotte TG, Repping S, Roseboom TJ (2015) Subfertility and assisted reproduction techniques are associated with poorer cardiometabolic profiles in childhood. Reprod Biomed Online 30: 258–267. https://doi.org/10.1016/j.rbmo.2014.11.006
  18. Dayan N, Lanes A, Walker MC, Spitzer KA, Laskin CA (2016) Effect of chronic hypertension on assisted pregnancy outcomes: a population-based study in Ontario, Canada. Fertil Steril 105: 1003–1009. https://doi.org/10.1016/j.fertnstert.2015.11.039
  19. Bergh C, Wennerholm UB (2020) Long-term health of children conceived after assisted reproductive technology. Ups J Med Sci 125: 152–157. https://doi.org/10.1080/03009734.2020.1729904
  20. Banerjee S, Riordan M, Bhat MA (2014) Genetic aspects of autism spectrum disorders: insights from animal models. Front Cell Neurosci 8: 58. https://doi.org/10.3389/fncel.2014.00058
  21. Kazdoba TM, Leach PT, Crawley JN (2016) Behavioral phenotypes of genetic mouse models of autism. Genes Brain Behav 15: 7–26. https://doi.org/10.1111/gbb.12256
  22. Varghese M, Keshav N, Jacot-Descombes S, Warda T, Wicinski B, Dickstein DL, Harony-Nicolas H, De Rubeis S, Drapeau E, Buxbaum JD, Hof PR (2017) Autism spectrum disorder: neuropathology and animal models. Acta Neuropathol 134: 537–566. https://doi.org/10.1007/s00401-017-1736-4
  23. Pobbe RL, Defensor EB, Pearson BL, Bolivar VJ, Blanchard DC, Blanchard RJ (2011) General and social anxiety I the BTBR T+ tf/J mouse strain. Behav Brain Res 216: 446–451. https://doi.org/10.1016/j.bbr.2010.08.039
  24. Langley EA, Krykbaeva M, Blusztajn JK, Mellott TJ (2015) High maternal choline consumption during pregnancy and nursing alleviates deficits in social interaction and improves anxiety-like behaviors in the BTBR T+Itpr3tf/J mouse model of autism. Behav Brain Res 278: 210–220. https://doi.org/10.1016/j.bbr.2014.09.043
  25. Amodeo DA, Pahua AE, Zarate M, Taylor JA, Peterson S, Posadas R, Oliver BL, Amodeo LR (2019) Differences in the expression of restricted repetitive behaviors in female and male BTBR T + tf/J mice. Behav Brain Res 372: 112028. https://doi.org/10.1016/j.bbr.2019.112028
  26. Ahmad SF, Ansari MA, Nadeem A, Bakheet SA, Alqahtani F, Alhoshani AR, Alasmari F, Alsaleh NB, Attia SM (2020) 5-aminoisoquinolinone attenuates social behavior deficits and immune abnormalities in the BTBR T+ Itpr3tf/J mouse model for autism. Pharmacol Biochem Behav 189: 172859. https://doi.org/10.1016/j.pbb.2020.172859
  27. Reshetnikov VV, Ayriyants KA, Ryabushkina YA, Sozonov NG, Bondar NP (2021) Sex-specific behavioral and structural alterations caused by early-life stress in C57BL/6 and BTBR mice. Behav Brain Res 414: 113489. https://doi.org/10.1016/j.bbr.2021.113489
  28. Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, Abel T, Schultz RM (2004) Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci U S A 101: 1595–1600. https://doi.org/10.1073/pnas.0306846101
  29. Rose C, Schwegler H, Hanke J, Rohl FW, Yilmazer-Hanke DM (2006) Differential effects of embryo transfer and maternal factors on anxiety-related behavior and numbers of neuropeptide Y (NPY) and parvalbumin (PARV) containing neurons in the amygdala of inbred C3H/HeN and DBA/2J mice. Behav Brain Res 173: 163–168.
  30. Lopez-Cardona AP, Fernandez-Gonzalez R, Perez-Crespo M, Alen F, de Fonseca FR, Orio L, Gutierrez-Adan A (2015) Effects of synchronous and asynchronous embryo transfer on postnatal development, adult health, and behavior in mice. Biol Reprod 93: 85. https://doi.org/10.1095/biolreprod.115.130385
  31. Lerch S, Tolksdorf G, Schutz P, Brandwein C, Dormann C, Gass P, Chourbaji S (2016) Effects of embryo transfer on emotional behaviors in C57BL/6 mice. J Am Assoc Lab Anim Sci 55: 510–519.
  32. Baan M, Krentz KJ, Fontaine DA, Davis DB (2016) Successful in vitro fertilization and generation of transgenics in Black and Tan Brachyury (BTBR) mice. Transgenic Res 25: 847–854. https://doi.org/10.1007/s11248-016-9974-0
  33. Emiliani S, Van den Bergh M, Vannin AS, Biramanel J, Englert Y (2000) Comparison of ethylene glycol, 1,2-propanediol and glycerol for cryopreservation of slow-cooled mouse zygotes, 4-cell embryos and blastocysts. Hum Reprod 4: 905–910. https://doi.org/10.1093/humrep/15.4.905
  34. Hogan B, Constantiny F, Lacy E (1986) Manipulating the mouse embryo. A laboratory manual. N.Y. Spring Harbor Lab.
  35. Амстиславский СЯ, Игонина ТН, Рожкова ИН, Брусенцев ЕЮ, Роговая АА, Рагаева ДС, Напримеров ВА, Литвинова ЕА, Плюснина ИЗ, Маркель АЛ (2013) Редеривация путем трансплантации эмбрионов линий лабораторных мышей и крыс. Вавиловск журн генетики и селекции 17: 147–161. [Amstislavsky SIA, Igonina TN, Rozhkova IN, Brusentsev IM, Rogovaya AA, Ragaeva DS, Naprimerov VA, Litvinova EA, Plusnina IZ, Markel AL (2013) Rederivation by transplantation of embryo lines of laboratory mice and rats. Vavilov J Genetics and Breeding 17: 147–161. (In Russ)].
  36. Ranneva S, Pavlov K, Gromova A, Amstislavskaya T, Lipina T (2017) Features of emotional and social behavioral phenotypes of calsyntenin2 knockout mice. Behav Brain Res 332: 343–354. https://doi.org/10.1016/j.bbr.2017.06.029
  37. Lee B, Sur B, Cho SG, Yeom M, Shim I, Lee H, Hahm DH (2016) Ginsenoside Rb1 rescues anxiety-like responses in a rat model of post-traumatic stress disorder. J Nat Med 70: 133–144. https://doi.org/10.1007/s11418-015-0943-3
  38. Kaidanovich-Beilin O, Lipina T, Vukobradovic I, Roder J, Woodgett JR (2011) Assessment of social interaction behaviors. J Vis Exp: 2473. https://doi.org/10.3791/2473
  39. Carter MD, Shah CR, Muller CL, Crawley JN, Carneiro AM, Veenstra-VanderWeele J (2011) Absence of preference for social novelty and increased grooming in integrin β3 knockout mice: initial studies and future directions. Autism Res 4: 57–67. https://doi.org/10.1002/aur.180
  40. Meyza KZ, Blanchard DC (2017) The BTBR mouse model of idiopathic autism - Current view on mechanisms. Neurosci Biobehav Rev 76: 99–110. https://doi.org/10.1016/j.neubiorev.2016.12.037
  41. Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE, Solter D, Knowles BB (2004) Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597–606. https://doi.org/10.1016/j.devcel.2004.09.004
  42. Fernandez-Gonzalez R, Ramirez MA, Pericuesta E, Calle A, Gutierrez-Adan A (2010) Histone modifications at the blastocyst Axin1(Fu) locus mark the heritability of in vitro culture-induced epigenetic alterations in mice. Biol Reprod 83: 720–727. https://doi.org/10.1095/biolreprod.110.084715
  43. Peippo J, Bredbacka P (1995) Sex-related growth rate differences in mouse preimplantation embryos in vivo and in vitro. Mol Reprod Dev 40: 56–61. https://doi.org/10.1002/mrd.1080400108
  44. Perez-Crespo M, Ramirez MA, Fernandez-Gonzalez R, Rizos D, Lonergan P, Pintado B, Gutierrez-Adan A (2005) Differential sensitivity of male and female mouse embryos to oxidative induced heat-stress is mediated by glucose-6-phosphate dehydrogenase gene expression. Mol Reprod Dev 72: 502–510. https://doi.org/10.1002/mrd.20366
  45. Gutierrez-Adan A, Perez-Crespo M, Fernandez-Gonzalez R, Ramirez MA, Moreira P, Pintado B, Lonergan P, Rizos D (2006) Developmental consequences of sexual dimorphism during pre-implantation embryonic development. Reprod Domest Anim 41(2): 54–62. https://doi.org/10.1111/j.1439-0531.2006.00769.x
  46. Bermejo-Alvarez P, Rizos D, Lonergan P, Gutierrez-Adan A (2011) Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction 141: 563–570. https://doi.org/10.1530/REP-10-0482
  47. de Waal E, Mak W, Calhoun S, Stein P, Ord T, Krapp C, Coutifaris C, Schultz RM, Bartolomei MS (2014) In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod 90: 22. https://doi.org/10.1095/biolreprod.113.114785
  48. Zhu W, Zheng J, Wen Y, Li Y, Zhou C, Wang Z (2020) Effect of embryo vitrification on the expression of brain tissue proteins in mouse offspring. Gynecol Endocrinol 36: 973–977. https://doi.org/10.1080/09513590.2020.1734785
  49. Qin NX, Zhao YR, Shi WH, Zhou ZY, Zou KX, Yu CJ, Liu X, Dong ZH, Mao YT, Zhou CL, Yu JL, Liu XM, Sheng JZ, Ding GL, Zhao WL, Wu YT, Huang HF (2021) Anxiety and depression-like behaviours are more frequent in aged male mice conceived by ART compared with natural conception. Reproduction 162: 437–448. https://doi.org/10.1530/REP-21-0175
  50. Hvidtjorn D, Grove J, Schendel D, Schieve LA, Svarke C, Ernst E, Thorsen P (2011) Risk of autism spectrum disorders in children born after assisted conception: a population-based follow-up study. J Epidemiol Community Health 65: 497–502. https://doi.org/10.1136/jech.2009.093823
  51. Davidovitch M, Chodick G, Shalev V, Eisenberg VH, Dan U, Reichenberg A, Sandin S, Levine SZ (2018) Infertility treatments during pregnancy and the risk of autism spectrum disorder in the offspring. Prog Neuropsychopharmacol Biol Psychiatry 86: 175–179. https://doi.org/10.1016/j.pnpbp.2018.05.022

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版权所有 © И.Н. Рожкова, С.В. Окотруб, Е.Ю. Брусенцев, Т.Н. Игонина, Т.А. Рахманова, Д.А. Лебедева, Т.А. Яцук, В.С. Козенева, В.А. Напримеров, С.Я. Амстиславский, 2023

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