Allopregnanolone restores hippocampal-dependent learning and memory and neural progenitor survival in aging 3xTgAD and nonTg mice

Neurobiology of Aging

Volumn 33, Issue 8, 2012, Pages 1493-1506

  Singh, Chanpreet ^a   Liu, Lifei ^a   Wang, Jun Ming ^b   Irwin, Ronald W ^a   Yao, Jia ^a   Chen, Shuhua ^a   Henry, Sherry ^b   Thompson, Richard F ^a   Brinton, Roberta Diaz ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Adult neurogenesis; Allopregnanolone; Alzheimer's disease therapeutics; Mild cognitive impairment therapeutics; Trace eyeblink conditioning; Translational neuroscience

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; AMYLOID BETA PROTEIN;

AGING; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; COGNITION; CONDITIONING; CONTROLLED STUDY; DRUG EFFICACY; HABITUATION; HIPPOCAMPUS; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; STATE DEPENDENT LEARNING; TRAINING;

AGING; ALZHEIMER DISEASE; ANIMALS; CELL SURVIVAL; HIPPOCAMPUS; LEARNING; MEMORY; MICE; MICE, KNOCKOUT; NEURONS; PREGNANOLONE; RECOVERY OF FUNCTION; STEM CELLS; TREATMENT OUTCOME;

EID: 84861882571     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.06.008     Document Type: Article

References (71)

1. Aimone J.B., Deng W., Gage F.H. Adult neurogenesis: integrating theories and separating functions. Trends Cogn. Sci 2010, 14:325-337.
2. Alvarez-Buylla A., Kohwi M., Nguyen T.M., Merkle F.T. The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb Symp. Quant. Biol 2008, 73:357-365.
3. Bath K.G., Mandairon N., Jing D., Rajagopal R., Kapoor R., Chen Z.Y., Khan T., Proenca C.C., Kraemer R., Cleland T.A., Hempstead B.L., Chao M.V., Lee F.S. Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J. Neurosci 2008, 28:2383-2393.
4. Baulieu E.E., Robel P., Schumacher M. Neurosteroids: beginning of the story. Int. Review Neurobiol 2001, 46:1-32.
5. Bernardi F., Salvestroni C., Casarosa E., Nappi R.E., Lanzone A., Luisi S., Purdy R.H., Petraglia F., Genazzani A.R. Aging is associated with changes in allopregnanolone concentrations in brain, endocrine glands and serum in male rats. Eur. J. Endocrinol 1998, 138:316-321.
6. Billings L.M., Green K.N., McGaugh J.L., LaFerla F.M. Learning decreases A beta*56 and tau pathology and ameliorates behavioral decline in 3xTg-AD mice. J. Neurosci 2007, 27:751-761.
7. Billings L.M., Oddo S., Green K.N., McGaugh J.L., LaFerla F.M. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 2005, 45:675-688.
8. Bilsland J.G., Haldon C., Goddard J., Oliver K., Murray F., Wheeldon A., Cumberbatch J., McAllister G., Munoz-Sanjuan I. A rapid method for the quantification of mouse hippocampal neurogenesis in vivo by flow cytometry. Validation with conventional and enhanced immunohistochemical methods. J. Neurosci. Methods 2006, 157:54-63.
9. Blurton-Jones M., Kitazawa M., Martinez-Coria H., Castello N.A., Müller F.J., Loring J.F., Yamasaki T.R., Poon W.W., Green K.N., LaFerla F.M. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13594-13599.
10. Brinton R.D. Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol. Sci 2009, 30:212-222.
11. Brinton R.D., Thompson R.F., Foy M.R., Baudry M., Wang J., Finch C.E., Morgan T.E., Pike C.J., Mack W.J., Stanczyk F.Z., Nilsen J. Progesterone receptors: Form and function in brain. Front. Neuroendocrinol 2008, 29:313-339.
12. Brinton R.D., Wang J.M. Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer's disease: allopregnanolone as a proof of concept neurogenic agent. Curr. Alzheimer Res 2006, 3:185-190.
13. Chen S., Wang J.M., Irwin R.W., Yao J., Liu L., Brinton R.D. Chronic administration of allopregnanolone modifies progression of Alzheimer's pathology in the triple transgenic Alzheimer's disease mouse. Society for Neuroscience 2008, Neuroscience Meeting Planner Washington, D.C., Program No, p. 55411. http://www.sfn.org/index.aspx?pagename=abstracts_ampublications.
14. Chevallier N.L., Soriano S., Kang D.E., Masliah E., Hu G., Koo E.H. Perturbed neurogenesis in the adult hippocampus associated with presenilin-1 A246E mutation. Am. J. Pathol 2005, 167:151-159.
15. Demars M., Hu Y.S., Gadadhar A., Lazarov O. Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J. Neurosci. Res 2010, 88:2103-2117.
16. Djebaili M., Guo Q., Pettus E.H., Hoffman S.W., Stein D.G. The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J. Neurotrauma 2005, 22:106-118.
17. Ebert A.D., Beres A.J., Barber A.E., Svendsen C.N. Human neural progenitor cells over-expressing IGF-1 protect dopamine neurons and restore function in a rat model of Parkinson's disease. Exp. Neurol 2008, 209:213-223.
18. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
19. Ermini F.V., Grathwohl S., Radde R., Yamaguchi M., Staufenbiel M., Palmer T.D., Jucker M. Neurogenesis and alterations of neural stem cells in mouse models of cerebral amyloidosis. Am. J. Pathol 2008, 172:1520-1528.
20. Ewers M., Morgan D.G., Gordon M.N., Woodruff-Pak D.S. Associative and motor learning in 12-month-old transgenic APP+PS1 mice. Neurobiol. Aging 2006, 27:1118-1128.
21. Gage F.H. Neurogenesis in the Adult Brain. J. Neurosci 2002, 22:612-613.
22. Gago N., El-Etr M., Sananès N., Cadepond F., Samuel D., Avellana-Adalid V., Baron-Van Evercooren A., Schumacher M. 3alpha,5alpha-Tetrahydroprogesterone (allopregnanolone) and gamma-aminobutyric acid: autocrine/paracrine interactions in the control of neonatal PSA-NCAM+ progenitor proliferation. J. Neurosci. Res 2004, 78:770-783.
23. Hattiangady B., Rao M.S., Shetty G.A., Shetty A.K. Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp. Neurol 2005, 195:353-371.
24. Hattiangady B., Shetty A.K. Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol. Aging 2008, 29:129-147.
25. Hattiangady B., Shuai B., Cai J., Coksaygan T., Rao M.S., Shetty A.K. Increased dentate neurogenesis after grafting of glial restricted progenitors or neural stem cells in the aging hippocampus. Stem Cells 2007, 25:2104-2117.
26. Henry S., Bigler S., Wang J. High throughput analysis of neural progenitor cell proliferation in adult rodent hippocampus. Biosci. Trends 2009, 3:233-238.
27. Hong X.P., Peng C.X., Wei W., Tian Q., Liu Y.H., Yao X.Q., Zhang Y., Cao F.Y., Wang Q., Wang J.Z. Essential role of tau phosphorylation in adult hippocampal neurogenesis. Hippocampus 2010, 20:1339-1349.
28. Kim W.R., Kim Y., Eun B., Park O.H., Kim H., Kim K., Park C.H., Vinsant S., Oppenheim R.W., Sun W. Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J. Neurosci 2007, 27:14392-14403.
29. Kishimoto Y., Suzuki M., Kawahara S., Kirino Y. Age-dependent impairment of delay and trace eyeblink conditioning in mice. Neuroreport 2001, 12:3349-3352.
30. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci 1996, 16:2027-2033.
31. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci 1997, 17:5820-5829.
32. Lauber M.E., Lichtensteiger W. Ontogeny of 5 alpha-reductase (type 1) messenger ribonucleic acid expression in rat brain: early presence in germinal zones. Endocrinology 1996, 137:2718-2730.
33. Lazarini F., Mouthon M.A., Gheusi G., de Chaumont F., Olivo-Marin J.C., Lamarque S., Abrous D.N., Boussin F.D., Lledo P.M. Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 2009, 4:e7017.
34. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci 2010, 33:569-579.
35. Lee T., Kim J.J. Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. J. Neurosci 2004, 24:3242-3250.
36. Lie D.C., Song H., Colamarino S.A., Ming G.L., Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol 2004, 44:399-421.
37. Lu P., Jones L.L., Snyder E.Y., Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol 2003, 181:115-129.
38. Ma D.K., Bonaguidi M.A., Ming G.L., Song H. Adult neural stem cells in the mammalian central nervous system. Cell Res 2009, 19:672-682.
39. Marx C.E., Trost W.T., Shampine L.J., Stevens R.D., Hulette C.M., Steffens D.C., Ervin J.F., Butterfield M.I., Blazer D.G., Massing M.W., Lieberman J.A. The neurosteroid allopregnanolone is reduced in prefrontal cortex in Alzheimer's disease. Biol. Psychiatry 2006, 60:1287-1294.
40. Mellon S.H., Griffin L.D. Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab 2002, 13:35-43.
41. Mellon S.H., Griffin L.D. Synthesis, regulation, and function of neurosteroids. Endocr. Res 2002, 28:463.
42. Naylor J.C., Kilts J.D., Hulette C.M., Steffens D.C., Blazer D.G., Ervin J.F., Strauss J.L., Allen T.B., Massing M.W., Payne V.M., Youssef N.A., Shampine L.J., Marx C.E. Allopregnanolone levels are reduced in temporal cortex in patients with Alzheimer's disease compared to cognitively intact control subjects. Biochim. Biophys. Acta 2010, 1801:951-959.
43. Niidome T., Taniuchi N., Akaike A., Kihara T., Sugimoto H. Differential regulation of neurogenesis in two neurogenic regions of APPswe/PS1dE9 transgenic mice. Neuroreport 2008, 19:1361-1364.
44. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., LaFerla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 2003, 24:1063-1070.
45. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
46. Ohno M., Tseng W., Silva A.J., Disterhoft J.F. Trace eyeblink conditioning requires the hippocampus but not autophosphorylation of alphaCaMKII in mice. Learn. Mem 2005, 12:211-215.
47. Park K.I., Himes B.T., Stieg P.E., Tessler A., Fischer I., Snyder E.Y. Neural stem cells may be uniquely suited for combined gene therapy and cell replacement: Evidence from engraftment of Neurotrophin-3-expressing stem cells in hypoxic-ischemic brain injury. Exp. Neurol 2006, 199:179-190.
48. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur. J. Neurosci 2005, 21:464-476.
49. Rao M.S., Hattiangady B., Reddy D.S., Shetty A.K. Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. J. Neurosci. Res 2006, 83:1088-1105.
50. Rao M.S., Hattiangady B., Shetty A.K. Fetal hippocampal CA3 cell grafts enriched with FGF-2 and BDNF exhibit robust long-term survival and integration and suppress aberrant mossy fiber sprouting in the injured middle-aged hippocampus. Neurobiol. Dis 2006, 21:276-290.
51. Rao M.S., Hattiangady B., Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006, 5:545-558.
52. Rodríguez J.J., Jones V.C., Tabuchi M., Allan S.M., Knight E.M., LaFerla F.M., Oddo S., Verkhratsky A. Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS One 2008, 3:e2935.
53. Rodríguez J.J., Jones V.C., Verkhratsky A. Impaired cell proliferation in the subventricular zone in an Alzheimer's disease model. Neuroreport 2009, 20:907-912.
54. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17501-17506.
55. Sayeed I., Guo Q., Hoffman S.W., Stein D.G. Allopregnanolone, a progesterone metabolite, is more effective than progesterone in reducing cortical infarct volume after transient middle cerebral artery occlusion. Ann. Emerg. Med 2006, 47:381-389.
56. Sayeed I., Parvez S., Wali B., Siemen D., Stein D.G. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism for better neuroprotective effects of allopregnanolone over progesterone. Brain Res 2009, 1263:165-173.
57. Shetty A.K., Hattiangady B., Shetty G.A. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: Role of astrocytes. Glia 2005, 51:173-186.
58. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
59. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
60. Taniuchi N., Niidome T., Goto Y., Akaike A., Kihara T., Sugimoto H. Decreased proliferation of hippocampal progenitor cells in APPswe/PS1dE9 transgenic mice. Neuroreport 2007, 18:1801-1805.
61. Taupin P., Ray J., Fischer W.H., Suhr S.T., Hakansson K., Grubb A., Gage F.H. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 2000, 28:385-397.
62. Tseng W., Guan R., Disterhoft J.F., Weiss C. Trace eyeblink conditioning is hippocampally dependent in mice. Hippocampus 2004, 14:58-65.
63. Verret L., Jankowsky J.L., Xu G.M., Borchelt D.R., Rampon C. Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J. Neurosci 2007, 27:6771-6780.
64. Vossel K.A., Zhang K., Brodbeck J., Daub A.C., Sharma P., Finkbeiner S., Cui B., Mucke L. Tau reduction prevents Abeta-induced defects in axonal transport. Science 2010, 330:198.
65. Waddell J., Shors T.J. Neurogenesis, learning and associative strength. Eur. J. Neurosci 2008, 27:3020-3028.
66. Wang J.M., Johnston P.B., Ball B.G., Brinton R.D. The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J. Neurosci 2005, 25:4706-4718.
67. Wang J.M., Singh C., Liu L., Irwin R.W., Chen S., Chung E.J., Thompson R.F., Brinton R.D. Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6498-6503.
68. Weill-Engerer S., David J.P., Sazdovitch V., Liere P., Eychenne B., Pianos A., Schumacher M., Delacourte A., Baulieu E.E., Akwa Y. Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J. Clin. Endocrinol. Metab 2002, 87:5138-5143.
69. Woodruff-Pak D.S., Finkbiner R.G., Sasse D.K. Eyeblink conditioning discriminates Alzheimer's patients from non-demented aged. Neuroreport 1990, 1:45-48.
70. Zhang C., McNeil E., Dressler L., Siman R. Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp. Neurol 2007, 204:77-87.
71. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.