Effects of Embryo Transfer on Emotional Behaviors in C57BL/6 Mice.

Microbiologic standardization plays a key role in the management of animal facilities because contamination of stock could affect the health status and wellbeing of animals and thereby induce artifacts in biomedical research. One common method to avoid the dissemination of pathogens is embryo transfer (ET). Although disturbances in the perinatal environment may cause long-lasting effects on the behavior and physiology of mouse offspring, the influences of ET during this sensitive phase have not yet been addressed. Our study investigated the effects of various components of ET (anesthesia, surgery, recipient strain) on the behavior of dams (exploration, nest-building) and offspring (nest-building, exploration, anxiety, and social and depressive-like behaviors). For ET, the donor strain C57BL/6N and a standard protocol were used. Whereas treatment with anesthesia-analgesia did not affect maternal behavior, female offspring demonstrated overall effects on weight gain and corticosterone levels. Compared with naturally delivered female offspring, dams obtained through ET demonstrated decreased exploration and nest-building. In addition, female ET-derived offspring had enhanced levels of anxiety and increased social interest. Furthermore, ET-derived dams obtained by using NMRI as the recipient strain showed increased exploratory behavior compared with that of dams obtained by using C57 mice as recipients. Compared with using C57 as recipients, both sexes of offspring transferred into NMRI recipients weighed more, and female mice showed a depressive-like phenotype. Our findings suggest that ET, now considered to be a routine procedure in animal husbandry, bears the risk of introducing artifacts.

[1]  J. Fox,et al.  The Mammalian Microbiome and Its Importance in Laboratory Animal Research. , 2015, ILAR journal.

[2]  John F. Cryan,et al.  Gut microbiota depletion from early adolescence in mice: Implications for brain and behaviour , 2015, Brain, Behavior, and Immunity.

[3]  R. Lorenz,et al.  Cross-fostering immediately after birth induces a permanent microbiota shift that is shaped by the nursing mother , 2015, Microbiome.

[4]  B. Gelaye,et al.  Association of decreased serum brain-derived neurotrophic factor (BDNF) concentrations in early pregnancy with antepartum depression , 2015, BMC Psychiatry.

[5]  P. Gass,et al.  Bred to breed?! Implications of continuous mating on the emotional status of mouse offspring , 2015, Behavioural Brain Research.

[6]  M. Arenas,et al.  Influence of trait anxiety on the effects of acute stress on learning and retention of the passive avoidance task in male and female mice , 2014, Behavioural Processes.

[7]  A. Fodor,et al.  Behavioral effects of perinatal opioid exposure. , 2014, Life sciences.

[8]  M. Raspa,et al.  FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units , 2014, Laboratory animals.

[9]  L. Desbonnet,et al.  Microbiota is essential for social development in the mouse , 2013, Molecular Psychiatry.

[10]  J. Quevedo,et al.  Fenproporex Increases Locomotor Activity and Alters Energy Metabolism, and Mood Stabilizers Reverse These Changes: a Proposal for a New Animal Model of Mania , 2014, Molecular Neurobiology.

[11]  Joseph P. Garner,et al.  Nest Building as an Indicator of Health and Welfare in Laboratory Mice , 2013, Journal of visualized experiments : JoVE.

[12]  J. Deussing Targeted mutagenesis tools for modelling psychiatric disorders , 2013, Cell and Tissue Research.

[13]  A. O'Carroll,et al.  Stress-dependent and gender-specific neuroregulatory roles of the apelin receptor in the hypothalamic–pituitary–adrenal axis response to acute stress , 2012, The Journal of endocrinology.

[14]  Robert Lalonde,et al.  Cognitive and non-cognitive behaviors in the triple transgenic mouse model of Alzheimer's disease expressing mutated APP, PS1, and Mapt (3xTg-AD) , 2012, Behavioural Brain Research.

[15]  E. Coonen,et al.  Further evidence that culture media affect perinatal outcome: findings after transfer of fresh and cryopreserved embryos. , 2012, Human reproduction.

[16]  E. Marcantonio,et al.  Anesthetics isoflurane and desflurane differently affect mitochondrial function, learning, and memory , 2012, Annals of neurology.

[17]  J. Guillen FELASA guidelines and recommendations. , 2012, Journal of the American Association for Laboratory Animal Science : JAALAS.

[18]  A. Brunetti,et al.  Mice anesthesia, analgesia, and care, Part I: anesthetic considerations in preclinical research. , 2012, ILAR journal.

[19]  T. Rülicke,et al.  Repeated Use of Surrogate Mothers for Embryo Transfer in the Mouse , 2012, Biology of reproduction.

[20]  F. J. V. van Steensel,et al.  Anxiety Disorders in Children and Adolescents with Autistic Spectrum Disorders: A Meta-Analysis , 2011, Clinical child and family psychology review.

[21]  E. Byrnes,et al.  Adolescent Opiate Exposure in the Female Rat Induces Subtle Alterations in Maternal Care and Transgenerational Effects on Play Behavior , 2011, Frontiers in Psychiatry.

[22]  S. Meltzer-Brody New insights into perinatal depression: pathogenesis and treatment during pregnancy and postpartum , 2011, Dialogues in clinical neuroscience.

[23]  J. Roder,et al.  Assessment of Social Interaction Behaviors , 2011, Journal of visualized experiments : JoVE.

[24]  Loren J. Martin,et al.  Short-term Memory Impairment after Isoflurane in Mice Is Prevented by the &agr;5 &ggr;-Aminobutyric Acid Type A Receptor Inverse Agonist L-655,708 , 2010, Anesthesiology.

[25]  M. Maze,et al.  Tumor necrosis factor-α triggers a cytokine cascade yielding postoperative cognitive decline , 2010, Proceedings of the National Academy of Sciences.

[26]  B. Hagman,et al.  Housing environment influences the need for pain relief during post-operative recovery in mice , 2010, Physiology & Behavior.

[27]  E. Coonen,et al.  Effect of in vitro culture of human embryos on birthweight of newborns. , 2010, Human reproduction.

[28]  R. Hellweg,et al.  Voluntary exercise induces anxiety‐like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis , 2009, Hippocampus.

[29]  Hanno Würbel,et al.  Effects of foraging demand on maternal behaviour and adult offspring anxiety and stress response in C57BL/6 mice , 2009, Behavioural Brain Research.

[30]  H. C. Cromwell,et al.  The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. , 2009, Developmental psychobiology.

[31]  L. Vatten,et al.  Effects of technology or maternal factors on perinatal outcome after assisted fertilisation: a population-based cohort study , 2008, The Lancet.

[32]  M. Vogt,et al.  Evaluation of effects of previous exposure to an acute stressor before testing for depression-like behaviours in mice , 2008, Stress.

[33]  M. Hanson,et al.  Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure , 2007, Proceedings of the National Academy of Sciences.

[34]  J. Hanke,et al.  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 , 2006, Behavioural Brain Research.

[35]  R. Deacon Assessing nest building in mice , 2006, Nature Protocols.

[36]  P. Gass,et al.  IL-6 knockout mice exhibit resistance to stress-induced development of depression-like behaviors , 2006, Neurobiology of Disease.

[37]  A. G. Nasello,et al.  A comparative study of morphine treatment regimen prior to mating and during late pregnancy , 2006, Brain Research Bulletin.

[38]  E. Byrnes Transgenerational consequences of adolescent morphine exposure in female rats: effects on anxiety-like behaviors and morphine sensitization in adult offspring , 2005, Psychopharmacology.

[39]  H. Flor,et al.  Mice with Genetically Altered Glucocorticoid Receptor Expression Show Altered Sensitivity for Stress-Induced Depressive Reactions , 2005, The Journal of Neuroscience.

[40]  G. Robinson,et al.  Sociogenomics: social life in molecular terms , 2005, Nature Reviews Genetics.

[41]  A. Trounson,et al.  The effect of protein on preimplantation mouse embryo development in vitro , 1984, Journal of in Vitro Fertilization and Embryo Transfer.

[42]  M. Hahn,et al.  A Review of the Methods of Studies on Infant Ultrasound Production and Maternal Retrieval in Small Rodents , 2005, Behavior genetics.

[43]  J. Piven,et al.  Sociability and preference for social novelty in five inbred strains: an approach to assess autistic‐like behavior in mice , 2004, Genes, brain, and behavior.

[44]  D. Ecker,et al.  Long-term effects of culture of preimplantation mouse embryos on behavior. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Thomas R. Insel,et al.  Epigenetic sources of behavioral differences in mice , 2003, Nature Neuroscience.

[46]  B. Zörner,et al.  Memory retrieval after contextual fear conditioning induces c‐Fos and JunB expression in CA1 hippocampus , 2003, Genes, brain, and behavior.

[47]  P. Rehbinder,et al.  Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units , 2002, Laboratory animals.

[48]  Richard Paylor,et al.  The use of behavioral test batteries: Effects of training history , 2001, Physiology & Behavior.

[49]  D. G. Baker Natural Pathogens of Laboratory Mice, Rats, and Rabbits and Their Effects on Research , 1998, Clinical Microbiology Reviews.

[50]  G. Anderson,et al.  Effects of maternal and embryonic genotype on prenatal survival in two selected mouse lines. , 1980, Journal of animal science.

[51]  R. Porsolt,et al.  Behavioral despair in mice: a primary screening test for antidepressants. , 1977, Archives internationales de pharmacodynamie et de therapie.

[52]  P. Bedford Adverse cerebral effects of anaesthesia on old people. , 1955, Lancet.