Cited by 370Genetic Syndromes and ImprintingReproductive Biology and FertilityBirth, Development, and Health

The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.

Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior

Open access

Fernández-Gonzalez, Raúl, Moreira, Pedro, Bilbao, Ainhoa, Jiménez, Adela, Pérez-Crespo, Miriam, Ramírez, Miguel Angel, De Fonseca, Fernando Rodríguez, Pintado, Belén, Gutiérrez-Adán, Alfonso·2004·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0308560101PMC PMC395892

Open this paper in CoChat — free account

Abstract

The long-term developmental and behavioral consequences of mammalian embryo culture are unknown. By altering the culture medium with the addition of FCS, we wanted to determine whether mouse embryos cultured under suboptimal conditions develop aberrant mRNA expression of imprinting genes at the blastocyst stage and whether fetal development, growth, and behavior of adult mice are affected. One-cell embryos obtained from superovulated female B6CBAF 1 mice were cultured for 4 days in K + -modified simplex optimized medium in the presence of either 10% FCS or 1 g/liter BSA. After embryo transfer, born animals were submitted to several developmental and behavior tests. The mRNA expression of some imprinting genes was significantly affected in blastocysts cultured in the presence of FCS. Two of the eight measures of preweaning development and some specific measures of neuromotor development, such as the walking activity, were delayed in the group originated with FCS. After 34 weeks, the weight of female mice cultured in vitro in the presence of FCS was significantly higher than controls. In addition, the locomotion activity of mice was altered at 5 and 15 months. Anatomopathological and histological analysis of animals at 20 months of age showed some large organs and an increase in pathologies. We have found that mice derived from embryos cultured with FCS exhibited specific behavioral alterations in anxiety and displayed deficiencies in implicit memories. Our data indicate that long-term programming of postnatal development, growth, and physiology can be affected irreversibly during the preimplantation period of embryo development by suboptimal in vitro culture.

Integrity signals

Registry

Crossref · 10.1073/pnas.0308560101

Cites

47 of 47 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting
DeChiara, T. M., Efstratiadis, A., & Robertsen, E. J. (1990) · Nature · doi:10.1038/345078a0 · Cited by 1,663
Low and Very Low Birth Weight in Infants Conceived with Use of Assisted Reproductive Technology
Schieve, L. A., Meikle, S., Ferré, C. D., Peterson, H. B., Jeng, G. T., & Wilcox, L. S. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa010806 · Cited by 1,014
Large offspring syndrome in cattle and sheep
Young, L. E. (1998) · Reviews of Reproduction · doi:10.1530/ror.0.0030155 · Cited by 880
Culture of preimplantation embryos: facts and artifacts
Bavister, B. D. (1995) · Human Reproduction Update · doi:10.1093/humupd/1.2.91 · Cited by 867
Differential Effects of Culture on Imprinted H19 Expression in the Preimplantation Mouse Embryo1
Doherty, A. S., Mann, M. R. W., Tremblay, K. D., Bartolomei, M. S., & Schultz, R. M. (2000) · Biology of Reproduction · doi:10.1095/biolreprod62.6.1526 · Cited by 723
Bovine Embryo Culture in the Presence or Absence of Serum: Implications for Blastocyst Development, Cryotolerance, and Messenger RNA Expression1
Rizos, D. V., Gutiérrez‐Adán, A., Pérez‐Garnelo, S. S., de la Fuente, J., Boland, M. P., & Lonergan, P. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.007799 · Cited by 537
Self-citation
Lamb Birth Weight is Affected by Culture System Utilized during in Vitro Pre-Elongation Development of Ovine Embryos
Thompson, J. G., Gardner, D. K., Pugh, P. A., McMillan, W. H., & Tervit, H. R. (1995) · Biology of Reproduction · doi:10.1095/biolreprod53.6.1385 · Cited by 441
A two-trial memory task with automated recording: study in young and aged rats
Dellu, F., Mayo, W., Cherkaoui, J., Le Moal, M., & Simon, H. (1992) · Brain Research · doi:10.1016/0006-8993(92)91352-f · Cited by 390
Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes
Dean, W., Bowden, L., Aitchison, A., Klose, J., Moore, T., Meneses, J. J., Reik, W., & Feil, R. (1998) · Development · doi:10.1242/dev.125.12.2273 · Cited by 375
The production of unusually large offspring following embryo manipulation: Concepts and challenges
Walker, S. K., Hartwich, K. M., & Seamark, R. F. (1996) · Theriogenology · doi:10.1016/0093-691x(95)00360-k · Cited by 374
Analysis of Differential Messenger RNA Expression Between Bovine Blastocysts Produced in Different Culture Systems: Implications for Blastocyst Quality1
Rizos, D. V., Lonergan, P., Boland, M. P., Arroyo-García, R. A., Pintado, B., de la Fuente, J., & Gutiérrez‐Adán, A. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.3.589 · Cited by 362
Self-citation
Cloned mice have an obese phenotype not transmitted to their offspring
Tamashiro, K. L., Wakayama, T., Akutsu, H., Yamazaki, Y., Lachey, J. L., Wortman, M. D., Seeley, R. J., D’Alessio, D. A., Woods, S. C., Yanagimachi, R., et al. (2002) · Nature Medicine · doi:10.1038/nm0302-262 · Cited by 356
The interplay of learning and anxiety in the elevated plus-maze
File, S. E. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90103-w · Cited by 334
The Neuropsychology of Attention
Cohen, R. A. (2014) · doi:10.1007/978-0-387-72639-7 · Cited by 332
Transactivation of Igf2 in a mouse model of Beckwith–Wiedemann syndrome
Sun, F.-L., Dean, W., Kelsey, G., Allen, N. D., & Reik, W. (1997) · Nature · doi:10.1038/39797 · Cited by 331
Analysis of apoptosis in the preimplantation bovine embryo using TUNEL
Byrne, A. T., Southgate, J., Brison, D. R., & Leese, H. J. (1999) · Reproduction · doi:10.1530/jrf.0.1170097 · Cited by 331
Temporal Divergence in the Pattern of Messenger RNA Expression in Bovine Embryos Cultured from the Zygote to Blastocyst Stage In Vitro or In Vivo
Lonergan, P. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.103.018168 · Cited by 306
Mechanisms of attention: A developmental study
Tipper, S. P., Bourque, T. A., Anderson, S. H., & Brehaut, J. (1989) · Journal of Experimental Child Psychology · doi:10.1016/0022-0965(89)90047-7 · Cited by 300
Beckwith-Wiedemann syndrome: imprinting in clusters revisited
Maher, E. R., & Reik, W. (2000) · Journal of Clinical Investigation · doi:10.1172/jci9340 · Cited by 299
Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro
Rizos, D. V., Fair, T., Papadopoulos, S., Boland, M. P., & Lonergan, P. (2002) · Molecular Reproduction and Development · doi:10.1002/mrd.10138 · Cited by 249
Imprinting in clusters: lessons from Beckwith-Wiedemann syndrome
Reik, W., & Maher, E. R. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01200-6 · Cited by 235
Culture of preimplantation embryos and its long-term effects on gene expression and phenotype
Khosla, S., Dean, W., Reik, W., & Feil, R. (2001) · Human Reproduction Update · doi:10.1093/humupd/7.4.419 · Cited by 232
Imprinting MechanismsPreprint
Constância, M., Pickard, B. S., Kelsey, G., & Reik, W. (1998) · Genome Research · doi:10.1101/gr.8.9.881 · Cited by 231
Trial 2 in the elevated plus-maze: a different form of fear?
File, S. E., Zangrossi, H., Viana, M. D. B., & Graeff, F. G. (1993) · Psychopharmacology · doi:10.1007/bf02253541 · Cited by 216
Mammalian embryo culture in the absence of serum or somatic cell support
Gardner, D. K. (1994) · Cell Biology International · doi:10.1006/cbir.1994.1043 · Cited by 194
Adult phenotype in the mouse can be affected by epigenetic events in the early embryo
Reik, W., Römer, I., Barton, S. C., Surani, M. A., Howlett, S., & Klose, J. (1993) · Development · doi:10.1242/dev.119.3.933 · Cited by 182
Morphology and biochemistry of in-vitro produced bovine embryos: implications for their cryopreservation
Massip, A., Mermillod, P., & Dinnyés, A. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135837 · Cited by 173
The Influence of Sex Hormones on Obesity across the Female Life Span
Lovejoy, J. C. (1998) · Journal of Women s Health · doi:10.1089/jwh.1998.7.1247 · Cited by 161
Identification of the Meg1 / Grb10 imprinted gene on mouse proximal chromosome 11, a candidate for the Silver–Russell syndrome gene
Miyoshi, N., Kuroiwa, Y., Kohda, T., Shitara, H., Yonekawa, H., Kawabe, T., Hasegawa, H., Barton, S. C., Surani, M. A., Kaneko‐Ishino, T., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.1102 · Cited by 156
Towards a single embryo transfer
Gardner, D. K., & Lane, M. (2003) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62170-0 · Cited by 153
Pregnancies after in vitro fertilization and transfer of human blastocysts
Bolton, V. N., Wren, M. E., & Parsons, J. H. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54257-5 · Cited by 137
Effect of the in vitro culture system on the kinetics of blastocyst development and sex ratio of bovine embryos
Gutiérrez‐Adán, A., Lonergan, P., Rizos, D. V., Ward, F., Boland, M. P., Pintado, B., & de la Fuente, J. (2001) · Theriogenology · doi:10.1016/s0093-691x(01)00471-x · Cited by 132
Self-citation
Imprinted genes, cognition and behaviour
Isles, A. R., & Wilkinson, L. S. (2000) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01504-7 · Cited by 118
Outcome of Low Birthweight
Barker, D. J. P. (2008) · Hormone Research · doi:10.1159/000184197 · Cited by 107
The effect of protein on preimplantation mouse embryo development in vitro
Caro, C. M., & Trounson, A. O. (1984) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf01139212 · Cited by 90
Genetic conflict in early development: parental imprinting in normal and abnormal growth
Moore, T. (1996) · Reviews of Reproduction · doi:10.1530/ror.0.0010073 · Cited by 87
Developmental consequences of embryo and cell manipulation in mice and farm animals
McEvoy, T., Robinson, J. J., & Sinclair, K. D. (2001) · Reproduction · doi:10.1530/rep.0.1220507 · Cited by 72
Female Gender Exacerbates Respiratory Depression in Leptin-deficient Obesity
Polotsky, V. Y., Wilson, J. A., Smaldone, M. C., HAINES, A. S., Hurn, P. D., Tankersley, C. G., SMITH, P. L., Schwartz, A. R., & O'Donnell, C. P. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.164.8.2101100 · Cited by 67
The effect of preimplantation culture conditions on murine embryo implantation and fetal development
Arny, M., Nachtigall, L. E., & Quagliarello, J. (1987) · Fertility and Sterility · doi:10.1016/s0015-0282(16)59545-4 · Cited by 45
Obesity – a chronic health problem in cloned mice?
Inui, A. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(02)00051-2 · Cited by 37
Expression and regulation of LRP-2/megalin in epithelial cells lining the efferent ducts and epididymis during postnatal development
Hermo, L., Lustig, M., Lefrançois, S., Argraves, W. S., & Morales, C. R. (1999) · Molecular Reproduction and Development · doi:10.1002/(sici)1098-2795(199907)53:3 · Cited by 32
An improved medium for long-term culture of human embryos overcomes the in vitro developmental block and increases blastocyst formation
FitzGerald, L., & DiMattina, M. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54914-0 · Cited by 32
Clones: A Hard Act to Follow
Pennisi, E., & Vogel, G. (2000) · Science · doi:10.1126/science.288.5472.1722 · Cited by 31
Manipulation of Domestic Animal Embryos and Implications for Development
McEvoy, T. (2003) · Reproduction in Domestic Animals · doi:10.1046/j.1439-0531.2003.00443.x · Cited by 25
Male-female differences in the relationship between obesity and lipids/lipoproteins.
Margolis, C. F., Sprecher, D. L., Simbartl, L. A., & Campaigne, B. N. (1996) · PubMed · Cited by 20
Ontogeny and adult behavior of mice with congenital neural tube defects
Cripps, M. M., & Nash, D. J. (1983) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(83)90474-0 · Cited by 6
Contributions of Behavioral Psychology to the Study of Attention
Cohen, R. A., & Sparling-Cohen, Y. A. (1993) · Critical issues in neuropsychology · doi:10.1007/978-1-4419-7463-1_4 · Cited by 3

Flagged first, then by citations

Research works printed but not linked: 5

Stojkovic, M., Kölle, S., Zakhartchenko, V., Stojkovic, P., Sinowatz, F., Wolf, E. (2000) Adv. Reprod. 5, 35–44.
Reik, W., Romer, I., Barton, S. C., Surani, M. A., Howlett, S. K. & Klose, J. (1993) Development (Cambridge, U.K.) 119, 933–942.
Dean, W., Bowden, L., Aitchison, A., Klose, J., Moore, T., Meneses, J. J., Reik, W. & Feil, R. (1998) Development (Cambridge, U.K.) 125, 2273–2282.
File, S. E., Zangrossi, H., Jr., Viana, M. & Graefff, F. G. (1996) Psychopharmacologia 111, 491–494.
Margolis, C. F., Sprecher, D. L., Simbartl, L. A. & Campaigne, B. N. (1996) Int. J. Obes. Relat Metab Disord 20, 784–790.8856404

Sorted by citations

Autism risk factors: genes, environment, and gene-environment interactions
Chaste, P., & Leboyer, M. (2012) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2012.14.3/pchaste · Cited by 807
Kaskadenreaktionen in der Totalsynthese
Nicolaou, K. C., Edmonds, D. J., & Bulger, P. G. (2006) · Angewandte Chemie · doi:10.1002/ange.200601872 · Cited by 634
Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation developmentPreprint
Hirasawa, R., Chiba, H., Kaneda, M., Tajima, S., Li, E., Jaenisch, R., & Sasaki, H. (2008) · Genes & Development · doi:10.1101/gad.1667008 · Cited by 488
Errors in development of fetuses and placentas from in vitro-produced bovine embryos
Farin, P. W., Piedrahita, J. A., & Farin, C. E. (2005) · Theriogenology · doi:10.1016/j.theriogenology.2005.09.022 · Cited by 444
Stress, genes and the mechanism of programming the brain for later life
de Kloet, E. R., Sibug, R. M., Helmerhorst, F. M., & Schmidt, M. V. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.008 · Cited by 370

See all 370

Authors: Fernández-Gonzalez, R., Moreira, P., Bilbao, A., Jiménez, A., Pérez-Crespo, M., Ramírez, M. A., De Fonseca, F. R., Pintado, B., & Gutiérrez-Adán, A.
Affiliations: Departamento de Reproducción Animal, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Carretera de la Coruña Km 5.9, 28040 Madrid, Spain; and Fundación Hospital Carlos Haya, Avenida Carlos Haya 82, 29010 Málaga, Spain
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (ES)
ORCID: Moreira, Pedro
Bilbao, Ainhoa
Pintado, Belén
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2004-04-12
Volume: 101
Issue: 16
Pages: 5880-5885
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0308560101
PMC: PMC395892
OpenAlex: W2147536097
Cited by: 370
References: 47
Citations by year: 2026: 4 · 2025: 4 · 2024: 6 · 2023: 11 · 2022: 8 · 2021: 9 · 2020: 18 · 2019: 12 · 2018: 17 · 2017: 22 · 2016: 16 · 2015: 18 · 2014: 25 · 2013: 11 · 2012: 27
FWCI: 13.57
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: embryo culture, fetal bovine serum, genomic imprinting, imprinted genes, blastocyst, preimplantation embryo development, developmental programming, anxiety-like behavior, implicit memory, locomotor activity, growth, organ enlargement
MeSH terms: Animals, Behavior, Animal, Blood, Embryo, Mammalian, Growth, RNA, Messenger, Transcription, Genetic, Genomic Imprinting, Culture Techniques, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks