Mouse model of panic disorder: Vulnerability to early environmental instability is strain-dependent.
6%CO2
C57BL/6J and DBA/2
instability of early environment
interference with maternal care
mouse model of panic disorder
repeated cross-fostering
respiratory endophenotype
tidal volume
ultrasonic vocalizations
unrestrained plethysmograph
Journal
Developmental psychobiology
ISSN: 1098-2302
Titre abrégé: Dev Psychobiol
Pays: United States
ID NLM: 0164074
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
26
04
2021
received:
29
01
2021
accepted:
05
05
2021
pubmed:
2
7
2021
medline:
26
3
2022
entrez:
1
7
2021
Statut:
ppublish
Résumé
Early life experiences and genetic background shape phenotypic variation. Several mouse models based on early treatments have evaluated short- and long-term phenotypic alterations and explored their molecular mechanisms. The instability of maternal cues was used to model human separation anxiety in outbred mice, one of the etiopathogenetic factors that predict panic disorder (PD). Application of the repeated cross-fostering (RCF) protocol to inbred strains (C57 and DBA) allowed us to measure differential responses to the same experimental manipulation. Ultrasounds emitted during isolation indicated that after RCF, pups from both strains lose their ability to be comforted by nest cues, but the frequency modulation of separation calls increased in RCF-C57 and decreased in RCF-DBA mice. No strain-specific difference in olfactory ability explained these responses in RCF-exposed mice. Rather, disruption of the infant-mother bond may differentially affect separation calls in the two strains. Moreover, the RCF-associated increased respiratory response to hypercapnia-an endophenotype of human PD documented among mice outbred strains-was replicated in the C57 strain only. We suggest that RCF-induced instability of the early environment affects emotionality and respiratory physiology differentially, depending on pups' genetic background. These strain-specific responses provide a lead to understand differential vulnerability to emotional disorders.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e22135Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Anderson, D. J., Noyes, R. Jr., & Crowe, R. R. (1984). A comparison of panic disorder and generalized anxiety disorder. American Journal of Psychiatry, 141(4), 572-575. https://doi.org/10.1176/ajp.141.4.572
Andolina, D., Puglisi-Allegra, S., & Ventura, R. (2015). Strain-dependent differences in corticolimbic processing of aversive or rewarding stimuli. Frontiers in Systems Neuroscience, 8, 207. https://doi.org/10.3389/fnsys.2014.00207
Barron, S., Kelly, S. J., & Riley, E. P. (1992). Neonatal alcohol exposure alters suckling behavior in neonatal rat pups. Pharmacology Biochemistry and Behavior, 39, 423-427. https://doi.org/10.1016/0091-3057(91)90202-D
Battaglia, M. (2012). Challenges in the appraisal and application of gene-environment interdependence. European Journal of Developmental Psychology, 9(4), 419-425. https://doi.org/10.1080/17405629.2012.689819
Battaglia, M., Ogliari, A., D'Amato, F. R., & Kinkead, R. (2014). Early-life risk factors for panic and separation anxiety disorder: Insights and outstanding questions arising from human and animal studies of CO2 sensitivity. Neurosciences and Biobehavioral Review, 46(Pt3), 455-464. https://doi.org/10.1016/j.neubiorev.2014.04.005
Battaglia, M., Ogliari, A., Harris, J.,, Spatola, C. A., Pesenti-Gritti, P., Reichborn-Kjennerud, T., Torgersen, S., Kringlen, E., & Tambs, K. (2007). A genetic study of the acute anxious response to carbon dioxide stimulation in man. Journal of Psychiatric Research, 41(11), 906-917. https://doi.org/10.1016/j.jpsychires.2006.12.002
Battaglia, M., Pesenti-Gritti, P., Medland, S. E., Ogliari, A., Tambs, K., & Spatola, C. A. (2009). A genetically informed study of the association between childhood separation anxiety, sensitivity to CO2, panic disorder, and the effect of childhood parental loss. Archives of General Psychiatry, 66(1), 64-71. https://doi.org/10.1001/archgenpsychiatry.2008.513
Battaglia, M., Pesenti-Gritti, P., Spatola, C. A., Ogliari, A., & Tambs, K. (2008). A twin study of the common vulnerability between heightened sensitivity to hypercapnia and panic disorder. American Journal of Medical Genetics part B Neuropsychiatric Genetics, 147B(5), 586-593. https://doi.org/10.1002/ajmg.b.30647
Battaglia, M., Rossignol, O., Bachand, K., D'Amato, F. R., & Koninck, Y. (2019). Amiloride modulation of carbon dioxide hypersensitivity and thermal nociceptive hypersensitivity induced by interference with early maternal environment. Journal of Psychopharmacoogy, 33(1), 101-108. https://doi.org/10.1177/0269881118784872. PMID: 29968500
Brown, R. E., Mathieson, W. B., Stapleton, J., & Neumann, P. E. (1999). Maternal behavior in female C57BL/6J and DBA/2J inbred mice. Physiology & Behavior, 67(4), 599-605. https://doi.org/10.1016/s0031-9384(99)00109-2
Cabib, S., Puglisi-Allegra, S., & Ventura, R. (2002). The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behavioral and Brain Research, 130(1-2), 103-109. https://doi.org/10.1016/S0166-4328(01)00422-3
Caruso, A., Sabbioni, M., Scattoni, M. L., & Branchi, I. (2018). Quantitative and qualitative features of neonatal vocalizations in mice. Handbook of Behavioral Neuroscience, 25, 138-147. https://doi.org/10.1016/B978-0-12-809600-0.00013-5
Czamara, D., Tissink, E., Tuhkanen, J., Martins, J., Awaloff, Y., Drake, A. J., Khulan, B., Palotie, A., Winter, S. M., Nemeroff, C. B., Craighead, W. E., Dunlop, B. W., Mayberg, H. S., Kinkead, B., Mathew, S. J., Iosifescu, D. V., Neylan, T. C., Heim, C. M., Lahti, J., … Binder, E. B. (2021). Combined effects of genotype and childhood adversity shape variability of DNA methylation across age. Translatioal Psychiatry, 11(1), 88. https://doi.org/10.1038/s41398-020-01147-z
Cinque, C., Pondiki, S., Oddi, D., Di Certo, M. G., Marinelli, S.,, Troisi, A., Moles, A., & D'Amato, F. R. (2012). Modeling socially anhedonic syndromes: Genetic and pharmacological manipulation of opioid neurotransmission in mice. Translational Psychiatry, 2(8), e155. https://doi.org/10.1038/tp.2012.83
Cittaro, D., Lampis, V., Luchetti, A., Coccurello, R., Guffanti, A., Felsani, A., Moles, A., Stupka, E., D' Amato, F. R., & Battaglia, M. (2016). Histone modifications in a mouse model of early adversities and panic disorder: Role for Asic1 and neurodevelopmental genes. Scientific Reports, 6, 25131. https://do.org/10.1038/srep25131
D'Amato, F. R., Scalera, E., Sarli, C., & Moles, A. (2005). Pups call, mothers rush: Does maternal responsiveness affect the amount of ultrasonic vocalizations in mouse pups? Behavioural Genetics, 35(1), 103-112. https://doi.org/10.1007/s10519-004-0860-9
D'Amato, F. R., Zanettini, C., Lampis, V., Coccurello, R., Pascucci, T., Ventura, R., Puglisi-Allegra, S., Spatola, C. A., Pesenti-Gritti, P., Oddi, D., Moles, A., & Battaglia, M. (2011). Unstable maternal environment, separation anxiety, and heightened CO2 sensitivity induced by gene-by-environment interplay. PLoS One, 6(4), e18637. https://doi.org/10.1371/journal.pone.0018637
Di Segni, M., Andolina, D., Luchetti, A., Babicola, L., D'Apolito, L. I., Pascucci, T., Conversi, D., Accoto, A., D'Amato, F. R., & Ventura, R. (2016). Unstable maternal environment affects stress response in adult mice in a genotype-dependent manner. Cerebral Cortex, 26(11), 4370-4380. https://doi.org/10.1093/cercor/bhv204
Dumont, F. S., Biancardi, V., & Kinkead, R. (2011). Hypercapnic ventilatory response of anesthetized female rats subjected to neonatal maternal separation: Insight into the origins of panic attacks? Respiratory Physiology and Neurobiology, 175(2), 288-295. https://doi.org/10.1016/j.resp.2010.12.004
Giannese, F., Luchetti, A., Barbiera, G., Lampis, V., Zanettini, C., Knudsen, G. P., Scaini, S., Lazarevic, D., Cittaro, D., D'Amato, F. R., & Battaglia, M. (2018). Conserved DNA methylation signatures in early maternal separation and in twins discordant for CO2 sensitivity. Scientific Reports, 8(1), 2258. https://doi.org/10.1038/s41598-018-20457-3
Grice, D. E., Reenilä, I., Männistö, P. T., Brooks, A. I., Smith, G. G., Golden, G. T., Buxbaum, J. D., & Berrettini, W. H. (2007). Transcriptional profiling of C57 and DBA strains of mice in the absence and presence of morphine. BMC Genomics, 8(8), 76. https://doi.org/10.1186/1471-2164-8-76
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49(12), 1023-1039. https://doi.org/10.1016/S0006-3223(01)01157-X
Horesh, N., Amir, M., Kedem, P., Goldberger, Y., & Kotler, M. (1997). Life events in childhood, adolescence and adulthood and the relationship to panic disorder. Acta Psychiatrica Scandinavica, 96(5), 373-378. https://doi.org/10.1111/j.1600-0447.1997.tb09932.x
Kelly, S. J., Day, N., & Streissguth, A. P. (2000). Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicology and Teratology, 22(2), 143-149. https://doi.org/10.1016/s0892-0362(99)00073-2
Klein, D. F. (1993). False suffocationalarms, spontaneouspanic, and relatedconditions. Archives of General Psychiatry, 50(4), 306-317. https://doi.org/10.1001/archpsyc.1993.01820160076009
Leibold, N. K., van den Hove, D. L., Viechtbauer, W., Buchanan, G. F., Goossens, L., Lange, I., Knuts, I., Lesch, K. P., Steinbusch, H. W., & Schruers, K. R. (2016). CO2 exposure as translational cross-species experimental model for panic. Translational Psychiatry, 6(9), e885. https://doi.org/10.1038/tp.2016.162
Luchetti, A., Battaglia, M., & D'Amato, F. R. (2016). Repeated cross-fostering protocol as a mouse model of early environmental instability. Bio-protocol, 6(4), e1734. https://doi.org/10.21769/BioProtoc.1734
Luchetti, A., Oddi, D., Lampis, V., Centofante, E., Felsani, A., Battaglia, M., & D'Amato, F. R. (2015). Early handling and repeated cross-fostering have opposite effect on mouse emotionality. Frontiers in Behavioral Neuroscience, 9, 93. https://doi.org/10.3389/fnbeh.2015.00093
McEwen, B. S. (2000). Effects of adverse experiences for brain structure and function. Biological Psychiatry, 48(8), 721-731. https://doi.org/10.1016/S0006-3223(00)00964-1
Millstein, R. A., & Holmes, A. (2007). Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neuroscience and Biobehavioral Review, 31(1), 3-17. https://doi.org/10.1016/j.neubiorev.2006.05.003
Moles, A., Kieffer, B. L., & D'Amato, F. R. (2004). Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science, 304(5679), 1983-1986. https://doi.org/10.1126/science.1095943
Ness, J. W., & Franchina, J. J. (1990). Effects of prenatal alcohol exposure on rat pups' ability to elicit retrieval behavior from dams. Developmental Psychobiology, 23(1), 85-99. https://doi.org/10.1002/dev.420230109
Quindry, J. C., Ballmann, C. G., Epstein, E. E., & Selsby, J. T. (2016). Plethysmography measurements of respiratory function in conscious unrestrained mice. Journal of Physiological Science, 66(2), 157-164. https://doi.org/10.1007/s12576-015-0408-1
Rockwood, G. A., & Riley, E. P. (1990). Nipple attachment behavior in rat pups exposed to alcohol in utero. Neurotoxicology and Teratology, 12, 383-389. https://doi.org/10.1016/0892-0362(90)90058-K
Schlenker, E., Shi, Y., Johnson, C., & Wipf, J. (2006). Acetazolamide affects breathing differently in ICR and C57 mice. Respiratory Physiology and Neurobiology, 152(2), 119-127. https://doi.org/10.1016/j.resp.2005.07.006
Schmidt, M. V., Enthoven, L., van der Mark, M., Levine, S., de Kloet, E. R., & Oitzl, M. S. (2003). The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. International Journal of Developmental Neuroscience, 21(3), 125-132. https://doi.org/10.1016/S0736-5748(03)00030-3
Shahrier, M. A., & Wada, H. (2018). Effects of prenatal ethanol exposure on acoustic characteristics of ultrasonic vocalizations in rat pups. Neurotoxicology, 69, 29-36. https://doi.org/10.1016/j.neuro.2018.08.006
Spatola, C. A., Scaini, S., Pesenti-Gritti, P., Medland, S. E., Moruzzi, S., Ogliari, A., Tambs, K., & Battaglia, M. (2011). Gene-environment interactions in panic disorder and CO₂ sensitivity: Effects of events occurring early in life. American Journal of Medical Genetics part B Neuropsychiatric Genetics, 156(1), 79-88. https://doi.org/10.1002/ajmg.b.31144
Szyf, M., & Bick, J. (2013). DNA methylation: A mechanism for embedding early life experiences in the genome. Child Development, 84(1), 49-57. https://doi.org/10.1111/j.1467-8624.2012.01793.x
Tankersley, C. G., Fitzgerald, R. S., & Kleeberger, S. R. (1994). Differential control of ventilation among inbred strains of mice. American Journal of Physiology, 267(5 Pt 2):R1371-R1377. https://doi.org/10.1152/ajpregu.1994.267.5.R1371
Vázquez, D. M. (1998). Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology, 23(7), 663-700. https://doi.org/10.1016/S0306-4530(98)00029-8
Ventura, R., Coccurello, R., Andolina, D., Latagliata, E. C., Zanettini, C., Lampis, V., Battaglia, M., D'Amato, F. R., & Moles, A. (2013). Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cerebral Cortex, 23(7), 1606-1617. https://doi.org/10.1093/cercor/bhs145
Vollmer, L. L., Strawn, J. R., & Sah, R. (2015). Acid-base dysregulation and chemosensory mechanisms in panic disorder: A translational update. Translational Psychiatry, 5(5), e572. https://doi.org/10.1038/tp.2015.67
Ward, R. (1980). Some effects of strain differences in the maternal behavior of inbred mice. Developmental Psychobiology, 13(2), 181-190. https://doi.org/10.1002/dev.420130209
Wiese, A. D., & Boutros, N. N. (2019). Diagnostic utility of sodium lactate infusion and CO2-35% inhalation for panic disorder. Neuropsychobiology, 78(2), 59-69. https://doi.org/10.1159/000499136
Winter, A., Ahlbrand, R., Naik, D., & Sah, R. (2017). Differential behavioral sensitivity to carbon dioxide (CO2) inhalation in rats. Neuroscience, 346, 423-433. https://doi.org/10.1016/j.neuroscience.2017.01.003
Wöhr, M., Dahlhoff, M., Wolf, E., Holsboer, F., Schwarting, R. K., & Wotjak, C. T. (2008). Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: An embryo-transfer study. Behavior Genetics, 38(6), 579-595. https://doi.org/10.1007/s10519-008-9221-4
Di Segni Matteo, Andolina Diego, Coassin Alessandra, Accoto Alessandra, Luchetti Alessandra, Pascucci Tiziana, Luzi Carla, Lizzi Anna Rita, D'Amato Francesca R., Ventura Rossella (2017). Sensitivity to cocaine in adult mice is due to interplay between genetic makeup, early environment and later experience. Neuropharmacology, 125, 87-98. http://doi.org/10.1016/j.neuropharm.2017.07.014.