Adult-onset hypothyroidism induces the amyloidogenic pathway of amyloid precursor protein processing in the rat hippocampus

Journal of Neuroendocrinology

Volumn 22, Issue 8, 2010, Pages 951-959

  Ghenimi, N ^a   Alfos, S ^a   Redonnet, A ^a   Higueret, P ^a   Pallet, V ^a   Enderlin, Valerie ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Adult; Amyloidogenic pathway of APP processing; Hippocampus; Hypothyroidism; Non amyloidogenic pathway of APP processing; Triiodothyronine nuclear receptors

Indexed keywords

3,5,3' TRIIODOTHYRONINE NUCLEAR RECEPTOR; ADAM PROTEIN; ALPHA SECRETASE; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; ISOPROTEIN; SECRETASE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

ADULT ONSET HYPOTHYROIDISM; AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; HYPOTHYROIDISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WISTAR RAT; ADULT; ANIMAL; BRAIN CORTEX; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; RANDOMIZATION;

ADULT; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; HYPOTHYROIDISM; PROTEIN ISOFORMS; RANDOM ALLOCATION; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; AMYLOID BETA-PEPTIDES;

EID: 77954731894     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02002.x     Document Type: Article

References (61)

1. Bernal J. Thyroid hormones and brain development. Vitam Horm 2005, 71:95-122.
2. Bernal J. Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 2007, 3:249-259.
3. Gulseren S, Gulseren L, Hekimsoy Z, Cetinay P, Ozen C, Tokatlioglu B. Depression, anxiety, health-related quality of life, and disability in patients with overt and subclinical thyroid dysfunction. Arch Med Res 2006, 37:133-139.
4. Davis JD, Tremont G. Neuropsychiatric aspects of hypothyroidism and treatment reversibility. Minerva Endocrinol 2007, 32:49-65.
5. Sui L, Wang F, Li BM. Adult-onset hypothyroidism impairs paired-pulse facilitation and long-term potentiation of the rat dorsal hippocampo-medial prefrontal cortex pathway in vivo. Brain Res 2006, 1096:53-60.
6. Vallortigara J, Alfos S, Micheau J, Higueret P, Enderlin V. T3 administration in adult hypothyroid mice modulates expression of proteins involved in striatal synaptic plasticity and improves motor behavior. Neurobiol Dis 2008, 31:378-385.
7. Tan ZS, Vasan RS. Thyroid function and Alzheimer's disease. J Alzheimers Dis 2009, 16:503-507.
8. Sampaolo S, Campos-Barros A, Mazziotti G, Carlomagno S, Sannino V, Amato G, Carella C, Di Iorio G. Increased cerebrospinal fluid levels of 3,3′,5′-triiodothyronine in patients with Alzheimer's disease. J Clin Endocrinol Metab 2005, 90:198-202.
9. Selkoe DJ. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 2001, 3:75-80.
10. Laudon H, Winblad B, Naslund J. The Alzheimer's disease-associated gamma-secretase complex: functional domains in the presenilin 1 protein. Physiol Behav 2007, 92:115-120.
11. Vassar R. BACE1: the beta-secretase enzyme in Alzheimer's disease. J Mol Neurosci 2004, 23:105-114.
12. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
13. Belandia B, Latasa MJ, Villa A, Pascual A. Thyroid hormone negatively regulates the transcriptional activity of the beta-amyloid precursor protein gene. J Biol Chem 1998, 273:30366-30371.
14. Latasa MJ, Belandia B, Pascual A. Thyroid hormones regulate beta-amyloid gene splicing and protein secretion in neuroblastoma cells. Endocrinology 1998, 139:2692-2698.
15. O'Barr SA, Oh JS, Ma C, Brent GA, Schultz JJ. Thyroid hormone regulates endogenous amyloid-beta precursor protein gene expression and processing in both in vitro and in vivo models. Thyroid 2006, 16:1207-1213.
16. Tanzi RE, McClatchey AI, Lamperti ED, Villa-Komaroff L, Gusella JF, Neve RL. Protease inhibitor domain encoded by an amyloid protein precursor mRNA associated with Alzheimer's disease. Nature 1988, 331:528-530.
17. LeBlanc AC, Xue R, Gambetti P. Amyloid precursor protein metabolism in primary cell cultures of neurons, astrocytes, and microglia. J Neurochem 1996, 66:2300-2310.
18. Simons M, de Strooper B, Multhaup G, Tienari PJ, Dotti CG, Beyreuther K. Amyloidogenic processing of the human amyloid precursor protein in primary cultures of rat hippocampal neurons. J Neurosci 1996, 16:899-908.
19. Gao Y, Pimplikar SW. The gamma -secretase-cleaved C-terminal fragment of amyloid precursor protein mediates signaling to the nucleus. Proc Natl Acad Sci USA 2001, 98:14979-14984.
20. Duyckaerts C. Looking for the link between plaques and tangles. Neurobiol Aging 2004, 25:735-739.
21. Edelberg HK, Wei JY. The biology of Alzheimer's disease. Mech Ageing Dev 1996, 91:95-114.
22. Irizarry MC, Hyman BT. Alzheimer disease therapeutics. J Neuropathol Exp Neurol 2001, 60:923-928.
23. Irizarry MC, Locascio JJ, Hyman BT. beta-site APP cleaving enzyme mRNA expression in APP transgenic mice: anatomical overlap with transgene expression and static levels with aging. Am J Pathol 2001, 158:173-177.
24. Vickers JC, Dickson TC, Adlard PA, Saunders HL, King CE, McCormack G. The cause of neuronal degeneration in Alzheimer's disease. Prog Neurobiol 2000, 60:139-165.
25. Coustaut M, Pallet V, Garcin H, Higueret P. The influence of dietary vitamin A on triiodothyronine, retinoic acid, and glucocorticoid receptors in liver of hypothyroid rats. Br J Nutr 1996, 76:295-306.
26. Bonnet E, Touyarot K, Alfos S, Pallet V, Higueret P, Abrous DN. Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS ONE 2008, 3:e3487.
27. Feart C, Pallet V, Boucheron C, Higueret D, Alfos S, Letenneur L, Dartigues JF, Higueret P. Aging affects the retinoic acid and the triiodothyronine nuclear receptor mRNA expression in human peripheral blood mononuclear cells. Eur J Endocrinol 2005, 152:449-458.
28. Borghi R, Patriarca S, Traverso N, Piccini A, Storace D, Garuti A, Gabriella C, Patrizio O, Massimo T. The increased activity of BACE1 correlates with oxidative stress in Alzheimer's disease. Neurobiol Aging 2007, 28:1009-1014.
29. Fukuzaki E, Takuma K, Himeno Y, Yoshida S, Funatsu Y, Kitahara Y, Mizoguchi H, Ibi D, Koike K, Inoue M, Yamada K. Enhanced activity of hippocampal BACE1 in a mouse model of postmenopausal memory deficits. Neurosci Lett 2008, 433:141-145.
30. Zhang L, Blomgren K, Kuhn HG, Cooper-Kuhn CM. Effects of postnatal thyroid hormone deficiency on neurogenesis in the juvenile and adult rat. Neurobiol Dis 2009, 34:366-374.
31. Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 2002, 23:38-89.
32. Cooper DS. Antithyroid drugs. N Engl J Med 2005, 352:905-917.
33. Jeannin E, Robyr D, Desvergne B. Transcriptional regulatory patterns of the myelin basic protein and malic enzyme genes by the thyroid hormone receptors alpha1 and beta1. J Biol Chem 1998, 273:24239-24248.
34. Enderlin V, Vallortigara J, Alfos S, Féart C, Pallet V, Higueret P. Retinoic acid reverses the PTU related decrease of its own nuclear receptors and neurogranin level in mice brain. J Physiol Biochem 2004, 60:191-198.
35. Iniguez MA, De Lecea L, Guadano-Ferraz A, Morte B, Gerendasy D, Sutcliffe JG, Bernal J. Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain. Endocrinology 1996, 137:1032-1041.
36. Piosik PA, van Groenigen M, Baas F. Effect of thyroid hormone deficiency on RC3/neurogranin mRNA expression in the prenatal and adult caprine brain. Brain Res Mol Brain Res 1996, 42:227-235.
37. Guadano-Ferraz A, Escamez MJ, Morte B, Vargiu P, Bernal J. Transcriptional induction of RC3/neurogranin by thyroid hormone: differential neuronal sensitivity is not correlated with thyroid hormone receptor distribution in the brain. Brain Res Mol Brain Res 1997, 49:37-44.
38. Bradley DJ, Young WS, Weinberger C. Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci USA 1989, 86:7250-7254.
39. Mellstrom B, Naranjo JR, Santos A, Gonzalez AM, Bernal J. Independent expression of the alpha and beta c-erbA genes in developing rat brain. Mol Endocrinol 1991, 5:1339-1350.
40. Ercan-Fang S, Schwartz HL, Oppenheimer JH. Isoform-specific 3,5,3′-triiodothyronine receptor binding capacity and messenger ribonucleic acid content in rat adenohypophysis: effect of thyroidal state and comparison with extrapituitary tissues. Endocrinology 1996, 137:3228-3233.
41. Vallortigara J, Chassande O, Higueret P, Enderlin V. TRα plays an essential role in the normalization of adult-onset hypothyroidism-related hypoexpression of synaptic plasticity target genes in striatum. J Neuroendocrinol 2009, 21:49-56.
42. Saido TC, Yamao-Harigaya W, Iwatsubo T, Kawashima S. Amino- and carboxyl-terminal heterogeneity of beta-amyloid peptides deposited in human brain. Neurosci Lett 1996, 215:173-176.
43. Sayre LM, Zagorski MG, Surewicz WK, Krafft GA, Perry G. Mechanisms of neurotoxicity associated with amyloid beta deposition and the role of free radicals in the pathogenesis of Alzheimer's disease: a critical appraisal. Chem Res Toxicol 1997, 10:518-526.
44. Selkoe DJ. Normal and abnormal biology of the beta-amyloid precursor protein. Annu Rev Neurosci 1994, 17:489-517.
45. Johnson SA, McNeill T, Cordell B, Finch CE. Relation of neuronal APP-751/APP-695 mRNA ratio and neuritic plaque density in Alzheimer's disease. Science 1990, 248:854-857.
46. Mishizen-Eberz AJ, Rissman RA, Carter TL, Ikonomovic MD, Wolfe BB, Armstrong DM. Biochemical and molecular studies of NMDA receptor subunits NR1/2A/2B in hippocampal subregions throughout progression of Alzheimer's disease pathology. Neurobiol Dis 2004, 15:80-92.
47. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 2007, 8:499-509.
48. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y. Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 2004, 101:3632-3637.
49. Benjannet S, Elagoz A, Wickham L, Mamarbachi M, Munzer JS, Basak A, Lazure C, Cromlish JA, Sisodia S, Checler F, Chretien M, Seidah NG. Post-translational processing of beta-secretase (beta-amyloid-converting enzyme) and its ectodomain shedding. The pro- and transmembrane/cytosolic domains affect its cellular activity and amyloid-beta production. J Biol Chem 2001, 276:10879-10887.
50. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, Sena-Esteves M, Hiltunen M, Yang SH, Zhong Z, Shen Y, Simpkins JW, Tanzi RE. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 2007, 54:721-737.
51. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G. Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann Neurol 2002, 51:783-786.
52. Zohar O, Cavallaro S, D'Agata V, Alkon DL. Quantification and distribution of beta-secretase alternative splice variants in the rat and human brain. Brain Res Mol Brain Res 2003, 115:63-68.
53. Fukumoto H, Rosene DL, Moss MB, Raju S, Hyman BT, Irizarry MC. Beta-secretase activity increases with aging in human, monkey, and mouse brain. Am J Pathol 2004, 164:719-725.
54. Giliberto L, Borghi R, Piccini A, Mangerini R, Sorbi S, Cirmena G, Garuti A, Ghetti B, Tagliavini F, Mughal MR, Mattson MP, Zhu X, Wang X, Guglielmotto M, Tamagno E, Tabaton M. Mutant presenilin 1 increases the expression and activity of BACE1. J Biol Chem 2009, 284:9027-9038.
55. Xia W. Role of presenilin in gamma-secretase cleavage of amyloid precursor protein. Exp Gerontol 2000, 35:453-460.
56. Kumar VB, Franko M, Banks WA, Kasinadhuni P, Farr SA, Vyas K, Choudhuri V, Morley JE. Increase in presenilin 1 (PS1) levels in senescence-accelerated mice (SAMP8) may indirectly impair memory by affecting amyloid precursor protein (APP) processing. J Exp Biol 2009, 212:494-498.
57. Findeis MA. The role of amyloid beta peptide 42 in Alzheimer's disease. Pharmacol Ther 2007, 116:266-286.
58. Terai K, Iwai A, Kawabata S, Tasaki Y, Watanabe T, Miyata K, Yamaguchi T. beta-amyloid deposits in transgenic mice expressing human beta-amyloid precursor protein have the same characteristics as those in Alzheimer's disease. Neuroscience 2001, 104:299-310.
59. Maccioni RB, Rojo LE, Fernandez JA, Kuljis RO. The role of neuroimmunomodulation in Alzheimer's disease. Ann NY Acad Sci 2009, 1153:240-246.
60. Hickman SE, Allison EK, El Khoury J. Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 2008, 28:8354-8360.
61. Boelen A, Kwakkel J, Alkemade A, Renckens R, Kaptein E, Kuiper G, Wiersinga WM, Visser TJ. Induction of type 3 deiodinase activity in inflammatory cells of mice with chronic local inflammation. Endocrinology 2005, 146:5128-5134.