Biochemical changes precede affective and cognitive anomalies in aging adult C57BL/6J mice with a prior history of adolescent alcohol binge-drinking.

Publisher: Wiley-Blackwell Country of Publication: United States NLM ID: 9604935 Publication Model: Print Cited Medium: Internet ISSN: 1369-1600 (Electronic) Linking ISSN: 13556215 NLM ISO Abbreviation: Addict Biol Subsets: MEDLINE

Publication: Hoboken, NJ : Wiley-Blackwell
Original Publication: Abingdon, Oxfordshire, UK ; Cambridge, MA : Carfax, c1996-

Binge Drinking*/metabolism ; Mice, Inbred C57BL* ; Aging*/metabolism ; Cognitive Dysfunction*/metabolism ; Cognitive Dysfunction*/etiology; Animals ; Female ; Mice ; Male ; tau Proteins/metabolism ; Amyloid Precursor Protein Secretases/metabolism ; Entorhinal Cortex/metabolism ; Brain/metabolism ; Underage Drinking ; Sensory Gating ; Amyloid beta-Protein Precursor/metabolism ; Amyloid beta-Protein Precursor/genetics ; Cognition ; Amyloid beta-Peptides/metabolism ; Prefrontal Cortex/metabolism ; Aspartic Acid Endopeptidases

The early initiation of binge-drinking and biological sex are critical risk factors for the development of affective disturbances and cognitive decline, as well as neurodegenerative diseases including Alzheimer's disease. Further, a history of excessive alcohol consumption alters normal age-related changes in the pattern of protein expression in the brain, which may relate to an acceleration of cognitive decline. Here, we aimed to disentangle the interrelation between a history of binge-drinking during adolescence, biological sex and normal aging on the manifestation of negative affect, cognitive decline and associated biochemical pathology. To this end, adolescent male and female C57BL/6J mice (PND 28-29) underwent 30 days of alcohol binge-drinking using a modified drinking-in-the-dark (DID) paradigm. Then, mice were assayed for negative affect, sensorimotor gating and cognition at three developmental stages during adulthood-mature adulthood (6 months), pre-middle age (9 months) and middle age (12 months). Behavioural testing was then followed by immunoblotting to index the protein expression of glutamate receptors, neuropathological markers [Tau, p (Thr217)-Tau, p (Ser396)-Tau, BACE, APP, Aβ], as well as ERK activation within the entorhinal cortex, prefrontal cortex and amygdala. Across this age span, we detected only a few age-related changes in our measures of negative affect or spatial learning/memory in the Morris water maze and all of these changes were sex-specific. Prior adolescent binge-drinking impaired behaviour only during reversal learning in 9-month-old females and during radial arm maze testing in 12-month-old females. In contrast to behaviour, we detected a large number of protein changes related to prior binge-drinking history, several of which manifested as early as 6 months of age, with the prefrontal cortex particularly affected at this earlier age. While 6-month-old mice exhibited relatively few alcohol-related protein changes within the entorhinal cortex and amygdala, the number of alcohol-related protein changes within the entorhinal cortex increased with age, while the 12-month-old mice exhibited the largest number of protein changes within the amygdala. Approximately a third of the alcohol-related protein changes were sex-selective. Taken together, the results of our longitudinal study using a murine model of binge-drinking indicate that a prior history of heavy alcohol consumption, beginning in adolescence, is sufficient to induce what we presume to be latent changes in protein indices of cellular activity, glutamate transmission and neuropathology within key brain regions governing cognition, executive function and emotion that appear to precede the onset of robust behavioural signs of dysregulated affect and cognitive impairment.
(© 2024 The Author(s). Addiction Biology published by John Wiley & Sons Ltd on behalf of Society for the Study of Addiction.)

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AA024044 National institutes of Health/National Institute on Alcohol Abuse and Alcoholism (NIH/NIAAA); DA053328 National institutes of Health/National Institute on Alcohol Abuse and Alcoholism (NIH/NIAAA); 2139319 NSF Graduate Research Program Fellowship

Keywords: Alzheimer's disease; Morris water maze; glutamate receptors; negative affect; radial arm maze

0 (tau Proteins)
EC 3.4.- (Amyloid Precursor Protein Secretases)
EC 3.4.23.46 (Bace1 protein, mouse)
0 (Amyloid beta-Protein Precursor)
0 (Amyloid beta-Peptides)
EC 3.4.23.- (Aspartic Acid Endopeptidases)

Date Created: 20241212 Date Completed: 20241212 Latest Revision: 20241214

20241214

PMC11635696

10.1111/adb.70006

39665499