α4βδ-GABAARs in the hippocampal CA1 as a biomarker for resilience to activity-based anorexia

Neuroscience

Volumn 265, Issue , 2014, Pages 108-123

  Aoki, C ^a   Wable, G ^a   Chowdhury, T G ^a   Sabaliauskas, N A ^a   Laurino, K ^b,c   Barbarich Marsteller, N C ^b,c  

^a NEW YORK UNIVERSITY   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Adolescence; Alpha4 GABA receptor; Anxiety; Hippocampus; Neuromodulation; Stress

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA4BETADELTA GABA A RECEPTOR; PROTEIN P42; PROTEIN P44; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; GABRA4 PROTEIN, RAT; PROTEIN SUBUNIT;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA NERVOSA; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; DENDRITIC SPINE; DIET RESTRICTION; FEMALE; HIPPOCAMPAL CA1 REGION; HYPERACTIVITY; IMMUNOREACTIVITY; NERVE CELL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; STRATUM RADIATUM; WEIGHT REDUCTION; ANALYSIS; ANIMAL; CHEMISTRY; DISEASE MODEL; EATING; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; MOUSE; PROTEIN SUBUNIT; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; ANOREXIA NERVOSA; BIOLOGICAL MARKERS; CA1 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; EATING; FEMALE; MICE; MOTOR ACTIVITY; PROTEIN SUBUNITS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RESILIENCE, PSYCHOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84896701176     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.01.011     Document Type: Article

References (71)

1. Aigner M., Treasure J., Kaye W., Kasper S. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the pharmacological treatment of eating disorders. World J Biol Psychiatry 2011, 12:400-443. WTFOE Disorders.
2. Aoki C., Sabaliauskas N., Chowdhury T., Min J.Y., Colacino A.R., Laurino K., Barbarich-Marsteller N.C. Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor alpha4 and delta subunits at the plasma membrane of hippocampal CA1 spines. Synapse 2012, 66:391-407.
3. Aoki C., Wu K., Elste A., Len G., Lin S., McAuliffe G., Black I.B. Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex. J Neurosci Res 2000, 59:454-463.
4. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders DSM-5. Washington, DC.
5. Araujo F., Ruano D., Vitorica J. Absence of association between delta and gamma2 subunits in native GABA(A) receptors from rat brain. Eur J Pharmacol 1998, 347:347-353.
6. Barbarich-Marsteller N.C., Laurino K., Colacino A.R. Pharmacological treatments for anorexia nervosa 2012, NOVA Science Publishers.
7. Barbarich-Marsteller N.C., Underwood M.D., Foltin R.W., Meyers M.M., Walsh B.T., Barrett J.S., Marsteller D.A. Identifying novel phenotypes of vulnerability and resistance to activity-based anorexia in adolescent female rats. Int J Eat Disord 2013, 46:737-746.
8. Bath K.G., Chuang J., Spencer-Segal J.L., Amso D., Altemus M., McEwen B.S., Lee F.S. Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biol Psychiatry 2012, 72:499-504.
9. Bath K.G., Schilit A., Lee F.S. Stress effects on BDNF expression: effects of age, sex, and form of stress. Neuroscience 2013, 239:149-156.
10. Birmingham C.L., Su J., Hlynsky J.A., Goldner E.M., Gao M. The mortality rate from anorexia nervosa. Int J Eat Disord 2005, 38:143-146.
11. Bulik C.M., Slof-Op't Landt M.C., van Furth E.F., Sullivan P.F. The genetics of anorexia nervosa. Annu Rev Nutr 2007, 27:263-275.
12. Chowdhury T.G., Wable G.S., Sabaliauskas N.A., Aoki C. Adolescent female C57BL/6 mice with vulnerability to activity-based anorexia exhibit weak inhibitory input onto hippocampal CA1 pyramidal cells. Neuroscience 2013, 241:250-267.
13. Davis C., Katzman D.K., Kaptein S., Kirsh C., Brewer H., Kalmbach K., Olmsted M.P., Woodside D.B., Kaplan A.S. The prevalence of high-level exercise in the eating disorders: etiological implications. Compr Psychiatry 1997, 38:321-326.
14. Davis C., Katzman D.K., Kirsh C. Compulsive physical activity in adolescents with anorexia nervosa: a psychobehavioral spiral of pathology. J Nerv Ment Dis 1999, 187:336-342.
15. Dellava J.E., Thornton L.M., Hamer R.M., Strober M., Plotnicov K., Klump K.L., Brandt H., Crawford S., Fichter M.M., Halmi K.A., Jones I., Johnson C., Kaplan A.S., Lavia M., Mitchell J., Rotondo A., Treasure J., Woodside D.B., Berrettini W.H., Kaye W.H., Bulik C.M. Childhood anxiety associated with low BMI in women with anorexia nervosa. Behav Res Ther 2010, 48:60-67.
16. Deslandes A., Moraes H., Ferreira C., Veiga H., Silveira H., Mouta R., Pompeu F.A., Coutinho E.S., Laks J. Exercise and mental health: many reasons to move. Neuropsychobiology 2009, 59:191-198.
17. Dixon D.P., Ackert A.M., Eckel L.A. Development of, and recovery from, activity-based anorexia in female rats. Physiol Behav 2003, 80:273-279.
18. Duman C.H., Schlesinger L., Russell D.S., Duman R.S. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 2008, 1199:148-158.
19. Fuss J., Ben Abdallah N.M., Hensley F.W., Weber K.J., Hellweg R., Gass P. Deletion of running-induced hippocampal neurogenesis by irradiation prevents development of an anxious phenotype in mice. PLoS One 2010, 5.
20. Gelegen C., van den Heuvel J., Collier D.A., Campbell I.C., Oppelaar H., Hessel E., Kas M.J. Dopaminergic and brain-derived neurotrophic factor signalling in inbred mice exposed to a restricted feeding schedule. Genes Brain Behav 2008, 7:552-559.
21. Gomez-Pinilla F., Ying Z., Roy R.R., Molteni R., Edgerton V.R. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 2002, 88:2187-2195.
22. Gorba T., Wahle P. Expression of TrkB and TrkC but not BDNF mRNA in neurochemically identified interneurons in rat visual cortex in vivo and in organotypic cultures. Eur J Neurosci 1999, 11:1179-1190.
23. Griffiths J., Lovick T. Withdrawal from progesterone increases expression of alpha4, beta1, and delta GABA(A) receptor subunits in neurons in the periaqueductal gray matter in female Wistar rats. J Comp Neurol 2005, 486:89-97.
24. Griffiths J.L., Lovick T.A. GABAergic neurones in the rat periaqueductal grey matter express alpha4, beta1 and delta GABAA receptor subunits: plasticity of expression during the estrous cycle. Neuroscience 2005, 136:457-466.
25. Gutierrez E. A rat in the labyrinth of anorexia nervosa: contributions of the activity-based anorexia rodent model to the understanding of anorexia nervosa. Int J Eat Disord 2013, 46:289-301.
26. Hare B.D., D'Onfro K.C., Hammack S.E., Falls W.A. Prior stress interferes with the anxiolytic effect of exercise in C57BL/6J mice. Behav Neurosci 2012, 126:850-856.
27. Hebebrand J., Exner C., Hebebrand K., Holtkamp C., Casper R.C., Remschmidt H., Herpertz-Dahlmann B., Klingenspor M. Hyperactivity in patients with anorexia nervosa and in semistarved rats: evidence for a pivotal role of hypoleptinemia. Physiol Behav 2003, 79:25-37.
28. Herring M.P., O'Connor P.J., Dishman R.K. The effect of exercise training on anxiety symptoms among patients: a systematic review. Arch Intern Med 2010, 170:321-331.
29. Hodes G.E., Shors T.J. Distinctive stress effects on learning during puberty. Horm Behav 2005, 48:163-171.
30. Huang Z.J., Scheiffele P. GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr Opin Neurobiol 2008, 18:77-83.
31. Hudson J.I., Hiripi E., Pope H.G., Kessler R.C. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry 2007, 61:348-358.
32. Huttunen P., Myers R.D. Tetrahydro-beta-carboline micro-injected into the hippocampus induces an anxiety-like state in the rat. Pharmacol Biochem Behav 1986, 24:1733-1738.
33. Joshi S., Kapur J. Slow intracellular accumulation of GABA(A) receptor delta subunit is modulated by brain-derived neurotrophic factor. Neuroscience 2009, 164:507-519.
34. Kataoka Y., Shibata K., Miyazaki A., Inoue Y., Tominaga K., Koizumi S., Ueki S., Niwa M. Involvement of the dorsal hippocampus in mediation of the antianxiety action of tandospirone, a 5-hydroxytryptamine1A agonistic anxiolytic. Neuropharmacology 1991, 30:475-480.
35. Kaye W.H., Bulik C.M., Thornton L., Barbarich N., Masters K. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry 2004, 161:2215-2221.
36. Kaye W.H., Fudge J.L., Paulus M. New insights into symptoms and neurocircuit function of anorexia nervosa. Nat Rev Neurosci 2009, 10:573-584.
37. Kitamura T., Mishina M., Sugiyama H. Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor epsilon 1 subunit. Neurosci Res 2003, 47:55-63.
38. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 2002, 82:1367-1375.
39. Lu B. BDNF and activity-dependent synaptic modulation. Learn Mem 2003, 10:86-98.
40. Lucas A.R., Beard C.M., O'Fallon W.M., Kurland L.T. 50-year trends in the incidence of anorexia nervosa in Rochester, Minn.: a population-based study. Am J Psychiatry 1991, 148:917-922.
41. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 1996, 726:49-56.
42. Nusser Z., Sieghart W., Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 1998, 18:1693-1703.
43. Onksen J.L., Briand L.A., Galante R.J., Pack A.I., Blendy J.A. Running-induced anxiety is dependent on increases in hippocampal neurogenesis. Genes Brain Behav 2012, 11:529-538.
44. Powers P.S., Bruty H. Pharmacotherapy for eating disorders and obesity. Child Adolesc Psychiatr Clin N Am 2009, 18:175-187.
45. Racz B., Weinberg R.J. Microdomains in forebrain spines: an ultrastructural perspective. Mol Neurobiol 2013, 47:77-89.
46. Riddle M.C., McKenna M.C., Yoon Y.J., Pattwell S.S., Santos P.M., Casey B.J., Glatt C.E. Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology 2013, 38:930-937.
47. Roberts D.S., Hu Y., Lund I.V., Brooks-Kayal A.R., Russek S.J. Brain-derived neurotrophic factor (BDNF)-induced synthesis of early growth response factor 3 (Egr3) controls the levels of type A GABA receptor alpha 4 subunits in hippocampal neurons. J Biol Chem 2006, 281:29431-29435.
48. Routtenberg A., Kuznesof A.W. Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 1967, 64:414-421.
49. Sabaliauskas N., Shen H., Homanics G.E., Smith S.S., Aoki C. Knockout of the gamma-aminobutyric acid receptor subunit alpha4 reduces functional delta-containing extrasynaptic receptors in hippocampal pyramidal cells at the onset of puberty. Brain Res 2012, 1450:11-23.
50. Sanna E., Mostallino M.C., Busonero F., Talani G., Tranquilli S., Mameli M., Spiga S., Follesa P., Biggio G. Changes in GABA(A) receptor gene expression associated with selective alterations in receptor function and pharmacology after ethanol withdrawal. J Neurosci 2003, 23:11711-11724.
51. Schoenfeld T.J., Rada P., Pieruzzini P.R., Hsueh B., Gould E. Physical exercise prevents stress-induced activation of granule neurons and enhances local inhibitory mechanisms in the dentate gyrus. J Neurosci 2013, 33:7770-7777.
52. Seeburg P.H., Wisden W., Verdoorn T.A., Pritchett D.B., Werner P., Herb A., Luddens H., Sprengel R., Sakmann B. The GABAA receptor family: molecular and functional diversity. Cold Spring Harb Symp Quant Biol 1990, 55:29-40.
53. Shen H., Gong Q.H., Aoki C., Yuan M., Ruderman Y., Dattilo M., Williams K., Smith S.S. Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 2007, 10:469-477.
54. Shen H., Sabaliauskas N., Sherpa A., Fenton A.A., Stelzer A., Aoki C., Smith S.S. A critical role for alpha4betadelta GABAA receptors in shaping learning deficits at puberty in mice. Science 2010, 327:1515-1518.
55. Sherwin C.M. Voluntary wheel running: a review and novel interpretation. Anim Behav 1998, 56:11-27.
56. Smith S.S. Neurosteroid regulation of GABA(A) receptors: Focus on the alpha4 and delta subunits. Pharmacol Ther 2007, 116:58-76.
57. Smith S.S., Gong Q.H., Li X., Moran M.H., Bitran D., Frye C.A., Hsu F.C. Withdrawal from 3alpha-OH-5alpha-pregnan-20-One using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor alpha4 subunit in association with increased anxiety. J Neurosci 1998, 18:5275-5284.
58. Spencer-Segal J.L., Waters E.M., Bath K.G., Chao M.V., McEwen B.S., Milner T.A. Distribution of phosphorylated TrkB receptor in the mouse hippocampal formation depends on sex and estrous cycle stage. J Neurosci 2011, 31:6780-6790.
59. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9:526-533.
60. Stranahan A.M., Lee K., Martin B., Maudsley S., Golden E., Cutler R.G., Mattson M.P. Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 2009, 19:951-961.
61. Sullivan P.F. Mortality in anorexia nervosa. Am J Psychiatry 1995, 152:1073-1074.
62. Talaenko A.N. The neurochemical profiles of the dorsal hippocampus and the antiaversive effects of anxiolytics in different models of anxiety in rats. J Nerv Ment Dis 1993, 43:621-626.
63. Tan J., Widjaja S., Xu J., Shepherd R.K. Cochlear implants stimulate activity-dependent CREB pathway in the deaf auditory cortex: implications for molecular plasticity induced by neural prosthetic devices. Cereb Cortex 2008, 18:1799-1813.
64. Thornton L.M., Dellava J.E., Root T.L., Lichtenstein P., Bulik C.M. Anorexia nervosa and generalized anxiety disorder: further explorations of the relation between anxiety and body mass index. J Anxiety Disord 2011, 25:727-730.
65. Tretter V., Jacob T.C., Mukherjee J., Fritschy J.M., Pangalos M.N., Moss S.J. The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J Neurosci 2008, 28:1356-1365.
66. Van der Borght K., Kobor-Nyakas D.E., Klauke K., Eggen B.J., Nyakas C., Van der Zee E.A., Meerlo P. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009, 19:928-936.
67. van Praag H. Neurogenesis and exercise: past and future directions. Neuromolecular Med 2008, 10:128-140.
68. Wable G.S., Barbarich-Marsteller N.C., Chowdhury T.G., Sabaliauskas N.A., Farb C.R., Aoki C. Excitatory synapses on dendritic shafts of the caudal basal amygdala exhibit elevated levels of GABAA receptor α4 subunits following the induction of activity-based anorexia. Synapse 2014, 68:1-15.
69. Wable G.S., Min J.-Y., Chowdhury T.G., Tateyama K., Aoki C. Activity-based anorexia: correlation of food restriction-induced hyperactivity with trait anxiety and GABAergic innervation of hippocampal pyramidal cells. Society for Neuroscience Annual Meeting Abstract 2013, #732.18.
70. Wei W., Zhang N., Peng Z., Houser C.R., Mody I. Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 2003, 23:10650-10661.
71. Xu H., Kotak V.C., Sanes D.H. Normal hearing is required for the emergence of long-lasting inhibitory potentiation in cortex. J Neurosci 2010, 30:331-341.