Exposure to early life stress regulates Bdnf expression in SERT mutant rats in an anatomically selective fashion

Journal of Neurochemistry

Volumn 132, Issue 1, 2015, Pages 146-154

  Calabrese, Francesca ^a   Van Der Doelen, Rick H A ^b   Guidotti, Gianluigi ^a   Racagni, Giorgio ^a   Kozicz, Tamas ^b   Homberg, Judith R ^b   Riva, Marco A ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b RADBOUD UNIVERSITY   (Netherlands)

Author keywords

maternal separation; neurotrophin; serotonin; ventral and dorsal hippocampus prefrontal cortex

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; SEROTONIN TRANSPORTER;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BDNF GENE; CONTROLLED STUDY; DORSOMEDIAL PREFRONTAL CORTEX; EARLY LIFE STRESS; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE ENVIRONMENT INTERACTION; HETEROZYGOTE; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SERT GENE; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; BIOSYNTHESIS; BRAIN LEVEL; GENE INACTIVATION; GENETICS; MENTAL STRESS; METABOLISM; MOLECULAR GENETICS; MUTATION; PSYCHOLOGY; SEPARATION ANXIETY; WISTAR RAT;

RATTUS;

ANIMALS; ANXIETY, SEPARATION; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; GENE KNOCKOUT TECHNIQUES; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; MOLECULAR SEQUENCE DATA; MUTATION; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL;

EID: 84923533467     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12846     Document Type: Article

References (41)

1. An J. J., Gharami K., Liao G. Y., et al,. (2008) Distinct role of long 3′ UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134, 175-187.
2. Baj G., Del Turco D., Schlaudraff J., Torelli L., Deller T., and, Tongiorgi E., (2013) Regulation of the spatial code for BDNF mRNA isoforms in the rat hippocampus following pilocarpine-treatment: a systematic analysis using laser microdissection and quantitative real-time PCR. Hippocampus 23, 413-423.
3. Calabrese F., Molteni R., Cattaneo A., Macchi F., Racagni G., Ellenbroek B.A., Gennarelli M., and, Riva M. A., (2010) Long-Term duloxetine treatment normalizes altered brain-derived neurotrophic factor expression in serotonin transporter knockout rats through the modulation of specific neurotrophin isoforms. Mol. Pharmacol. 77, 846-853.
4. Calabrese F., Molteni R., and, Riva M. A., (2011) Antistress properties of antidepressant drugs and their clinical implications. Pharmacol. Ther. 132, 39-56.
5. Calabrese F. Guidotti G., Middelman A., Racagni G., Homberg J., and, Riva M. A., (2013) Lack of serotonin transporter alters BDNF expression in the rat brain during early postnatal development. Mol. Neurobiol. 48, 244-256.
6. Caspi A., Sugden K., Moffitt T. E., et al,. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
7. Caspi A., Hariri A. R., Holmes A., Uher R., and, Moffitt T. E., (2010) Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry 167, 509-527.
8. Chourbaji S., Brandwein C., Vogt M. A., Dormann C., Hellweg R., and, Gass P., (2008) Nature vs. nurture: can enrichment rescue the behavioural phenotype of BDNF heterozygous mice? Behav. Brain Res. 192, 254-258.
9. Chourbaji S., Brandwein C., and, Gass P., (2011) Altering BDNF expression by genetics and/or environment: impact for emotional and depression-like behaviour in laboratory mice. Neurosci. Biobehav. Rev. 35, 599-611.
10. Chourbaji S., Hörtnagl H., Molteni R., Riva M. A., Gass P., and, Hellweg R., (2012) The impact of environmental enrichment on sex-specific neurochemical circuitries-effects on brain-derived neurotrophic factor and the serotonergic system. Neuroscience 220, 267-276.
11. van der Doelen R. H., Kozicz T., and, Homberg J. R., (2013) Adaptive fitness; early life adversity improves adult stress coping in heterozygous serotonin transporter knockout rats. Mol. Psychiatry 18, 1244-1245.
12. van der Doelen R. H., Deschamps W., D'Annibale C., Peeters D., Wevers R. A., Zelena D., Homberg J. R., and, Kozicz T., (2014) Early life adversity and serotonin transporter gene variation interact at the level of the adrenal gland to affect the adult hypothalamo-pituitary-adrenal axis. Transl. Psychiatry 4, e409.
13. Fanselow M. S., and, Dong H. W., (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19.
14. Fisher H. L., McGuffin P., Boydell J., et al,. (2014) Interplay between childhood physical abuse and familial risk in the onset of psychotic disorders. Schizophr. Bull. doi: 10.1093/schbul/sbt201 [Epub ahead of print].
15. Fumagalli F., Molteni R., Racagni G., and, Riva M. A., (2007) Stress during development: impact on neuroplasticity and relevance to psychopathology. Prog. Neurobiol. 81, 197-217.
16. Gluckman P. D., Hanson M. A., and, Beedle A. S., (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am. J. Hum. Biol. 19, 1-19.
17. Guidotti G., Calabrese F., Auletta F., Olivier J., Racagni G., Homberg J., and, Riva M. A., (2012) Developmental influence of the serotonin transporter on the expression of npas4 and GABAergic markers: modulation by antidepressant treatment. Neuropsychopharmacology 37, 746-758.
18. Gutman D. A., and, Nemeroff C. B., (2002) Neurobiology of early life stress: rodent studies. Semin. Clin. Neuropsychiatry 7, 89-95.
19. Heim C., Plotsky P. M., and, Nemeroff C. B., (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29, 641-648.
20. Homberg J. R., (2012) The stress-coping (mis)match hypothesis for nature x nurture interactions. Brain Res. 1432, 114-121.
21. Homberg J. R., and, Lesch K. P., (2011) Looking on the bright side of serotonin transporter gene variation. Biol. Psychiatry 69, 513-519.
22. Karg K., Burmeister M., Shedden K., and, Sen S., (2011) The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch. Gen. Psychiatry 68, 444-454.
23. Ladd C. O., Huot R. L., Thrivikraman K. V., Nemeroff C. B., Meaney M. J., and, Plotsky P. M., (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122, 81-103.
24. Lau A. G., Irier H. A., Gu J., et al,. (2010) Distinct 3′ UTRs differentially regulate activity-dependent translation of brain-derived neurotrophic factor (BDNF). Proc. Natl Acad. Sci. USA 107, 15945-15950.
25. Lesch K. P., Bengel D., Heils A., Sabol S. Z., Greenberg B. D., Petri S., Benjamin J., Müller C. R., Hamer D. H., and, Murphy D. L., (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.
26. Lippmann M., Bress A., Nemeroff C. B., Plotsky P. M., and, Monteggia L. M., (2007) Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 25, 3091-3098.
27. Meaney M. J., (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161-1192.
28. Molteni R., Cattaneo A., Calabrese F., Macchi F., Racagni G., Ellenbroek B. A., Gennarelli M., and, Riva M. A., (2010) Reduced function of the serotonin transporter is associated with decreased expression of BDNF in rodents as well as in humans. Neurobiol. Dis. 37, 747-755.
29. Munafò M. R., Durrant C., Lewis G., and, Flint J., (2009) Gene X environment interactions at the serotonin transporter locus. Biol. Psychiatry 65, 211-219.
30. Murphy D. L., and, Lesch K. P., (2008) Targeting the murine serotonin transporter: insights into human neurobiology. Nat. Rev. Neurosci. 9, 85-96.
31. Newport D. J., Stowe Z. N., and, Nemeroff C. B., (2002) Parental depression: animal models of an adverse life event. Am. J. Psychiatry 159, 1265-1283.
32. Olivier J. D., Van Der Hart M. G., Van Swelm R. P., Dederen P. J., Homberg J. R., Cremers T., Deen P. M., Cuppen E., Cools A. R., and, Ellenbroek B. A., (2008) A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 152, 573-584.
33. Orefice L. L., Waterhouse E. G., Partridge J. G., Lalchandani R. R., Vicini S,. and, Xu B,. (2013) Distinct roles for somatically and dendritically synthesized brain-derived neurotrophic factor in morphogenesis of dendritic spines. J. Neurosci. 33, 11618-11632.
34. Pruunsild P., Sepp M., Orav E., Koppel I., and, Timmusk T., (2011) Identification of cis-elements and transcription factors regulating neuronal activity-dependent transcription of human BDNF gene. J. Neurosci. 31, 3295-3308.
35. Roceri M., Hendriks W., Racagni G., Ellenbroek B. A., and, Riva M. A., (2002) Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol. Psychiatry 7, 609-616.
36. Roceri M., Cirulli F., Pessina C., Peretto P., Racagni G., and, Riva M. A., (2004) Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 55, 708-714.
37. Sánchez M. M., Ladd C. O., and, Plotsky P. M., (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13, 419-449.
38. Schmidt M. V., (2011) Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology 36, 330-338.
39. Smits B. M., Mudde J. B., van de Belt J,. et al. (2006) Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenet. Genomics 16, 159-169.
40. Waterhouse E. G., An J. J., Orefice L. L., Baydyuk M., Liao G. Y., Zheng K., Lu B., and, Xu B., (2012) BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J. Neurosci. 32, 14318-14330.
41. Weaver I. C., Cervoni N., Champagne F. A., D'Alessio A. C., Sharma S., Seckl J. R., Dymov S., Szyf M., and, Meaney M. J., (2004) Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854.