Tetrahydrohyperforin increases adult hippocampal neurogenesis in wild-type and APPswe/PS1ΔE9 Mice

Journal of Alzheimer's Disease

Volumn 34, Issue 4, 2013, Pages 873-885

  Abbott, Ana C ^a   Calderon Toledo, Carla ^a   Aranguiz, Florencia C ^a   Inestrosa, Nibaldo C ^a   Varela Nallar, Lorena ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Alzheimer's disease; hippocampus; long term memory; neural progenitor cells; neurogenesis; tetrahydrohyperforin

Indexed keywords

BROXURIDINE; CENTRAL NERVOUS SYSTEM AGENTS; HYPERFORIN; IDN 5706; TETRAHYDROHYPERFORIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG DOSE COMPARISON; DRUG EFFICACY; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM MEMORY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY; TASK PERFORMANCE; WILD TYPE;

EID: 84876393414     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-121714     Document Type: Article

References (66)

1. Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22, 629-634. (Pubitemid 34141742)
2. Ming GL, Song H (2011) Adult neurogenesis in the Mammalian brain: Significant answers and significant questions. Neuron 70, 687-702.
3. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. (Pubitemid 34193451)
4. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25, 10074-10086. (Pubitemid 41636203)
5. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29, 13532-13542.
6. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16, 147-154.
7. Koehl M, Abrous DN (2011) A new chapter in the field of memory: Adult hippocampal neurogenesis. Eur J Neurosci 33, 1101-1114.
8. Marin-Burgin A, Schinder AF (2012) Requirement of adultborn neurons for hippocampus-dependent learning. Behav Brain Res 227, 391-399.
9. Aimone JB, Deng W, Gage FH (2011) Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596.
10. Sahay A, Wilson DA, Hen R (2011) Pattern separation: A common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582-588.
11. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54, 559-566. (Pubitemid 46756142)
12. Inestrosa NC, Arenas E (2010) Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 11, 77-86.
13. Suh H, Deng W, Gage FH (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25, 253-275.
14. Johnson MA, Ables JL, Eisch AJ (2009) Cell-intrinsic signals that regulate adult neurogenesis in vivo: Insights from inducible approaches. BMB Rep 42, 245-259.
15. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2, 266-270. (Pubitemid 30491298)
16. Kempermann G,Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495. (Pubitemid 27164074)
17. Snyder JS, Radik R, Wojtowicz JM, Cameron HA (2009) Anatomical gradients of adult neurogenesis and activity: Young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19, 360-370.
18. Leal-Galicia P, Castaneda-Bueno M, Quiroz-Baez R, Arias C (2008) Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol Learn Mem 90, 511-518.
19. DeCarolis NA, Eisch AJ (2010) Hippocampal neurogenesis as a target for the treatment of mental illness: A critical evaluation. Neuropharmacology 58, 884-893.
20. Winner B, Kohl Z, Gage FH (2011) Neurodegenerative disease and adult neurogenesis. Eur J Neurosci 33, 1139-1151.
21. Varela-Nallar L, Aranguiz FC, Abbott AC, Slater PG, Inestrosa NC (2010) Adult hippocampal neurogenesis in aging and Alzheimer's disease. Birth Defects Res C Embryo Today 90, 284-296.
22. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J, Arango V (2009) Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34, 2376-2389.
23. Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S, Price J, Pariante CM (2011) Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry 16, 738-750.
24. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20, 9104-9110. (Pubitemid 32042912)
25. Fiorentini A, Rosi MC, Grossi C, Luccarini I, Casamenti F (2010) Lithium improves hippocampal neurogenesis, neuropathology and cognitive functions in APP mutant mice. PLoS One 5, e14382.
26. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
27. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer's disease: At the crossroads. Exp Neurol 223, 267-281.
28. Griffith TN, Varela-Nallar L, Dinamarca MC, Inestrosa NC (2010) Neurobiological effects of Hyperforin and its potential in Alzheimer's disease therapy. Curr Med Chem 17, 391-406.
29. Inestrosa NC, Tapia-Rojas C, Griffith TN, Carvajal FJ, Benito MJ, Rivera-Dictter A, Alvarez AR, Serrano FG, Hanke JL, Burgos PV, Parodi J, Varela-Nallar L (2011) Tetrahydrohyperforin prevents cognitive deficit, Aβ deposition, tau phosphorylation and synaptotoxicity in the APPswe/PSEN1ΔE9 model of Alzheimer's disease: A possible effect on APP processing. Transl Psychiatry 1, e20.
30. Cerpa W, Hancke JL, Morazzoni P, Bombardelli E, Riva A, Marin PP, Inestrosa NC (2010) The hyperforin derivative IDN5706 occludes spatial memory impairments and neuropathological changes in a double transgenic Alzheimer's mouse model. Curr Alzheimer Res 7, 126-133.
31. Encinas JM, Enikolopov G (2008) Identifying and quantitating neural stem and progenitor cells in the adult brain. Methods Cell Biol 85, 243-272.
32. Wojtowicz JM, Kee N (2006) BrdU assay for neurogenesis in rodents. Nat Protoc 1, 1399-1405.
33. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A 92, 11879-11883. (Pubitemid 26014213)
34. Peltier J, Ormerod BK, Schaffer DV (2010) Isolation of adult hippocampal neural progenitors. Methods Mol Biol 621, 57-63.
35. Toledo EM, Inestrosa NC (2010) Activation of Wnt signaling by lithium and rosiglitazone reduced spatial memory impairment and neurodegeneration in brains of an APPswe/ PSEN1DeltaE9 mouse model of Alzheimer's disease. Mol Psychiatry 15, 272-285.
36. Suh H, Consiglio A, Ray J, Sawai T, D'Amour KA, Gage FH (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1, 515-528. (Pubitemid 350056408)
37. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460, 563-572. (Pubitemid 36528662)
38. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G (2011) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8, 566-579.
39. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez GR, Kronenberg G, KempermannG(2006)Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7, 77.
40. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852. (Pubitemid 40094618)
41. Maei HR, Zaslavsky K, Teixeira CtM, Frankland PW (2009) What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 3, 4.
42. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, FroschMP(2006) Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24, 516-524. (Pubitemid 44716680)
43. Hu YS, Xu P, Pigino G, Brady ST, Larson J, Lazarov O (2010) Complex environment experience rescues impaired neurogenesis, enhances synaptic plasticity, and attenuates neuropathology in familial Alzheimer's disease-linked APPswe/ PS1DeltaE9 mice. FASEB J 24, 1667-1681.
44. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16, 2027-2033. (Pubitemid 26144015)
45. Olariu A, CleaverKM, Cameron HA(2007) Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol 501, 659-667. (Pubitemid 46622502)
46. Snyder JS, Cameron HA (2012) Could adult hippocampal neurogenesis be relevant for human behavior? Behav Brain Res 227, 384-390.
47. Laakmann G, Schule C, Baghai T, KieserM(1998) St. John's wort in mild to moderate depression: The relevance of hyperforin for the clinical efficacy. Pharmacopsychiatry 31(Suppl 1), 54-59. (Pubitemid 28294226)
48. Zanoli P (2004) Role of hyperforin in the pharmacological activities of St. John's wort. CNS Drug Rev 10, 203-218. (Pubitemid 39391315)
49. Rozio M, Fracasso C, Riva A, Morazzoni P, Caccia S (2005) High-performance liquid chromatography measurement of hyperforin and its reduced derivatives in rodent plasma. J Chromatogr B Analyt Technol Biomed Life Sci 816, 21-27. (Pubitemid 40143485)
50. Crupi R, Mazzon E, Marino A, La Spada G, Bramanti P, Battaglia F, Cuzzocrea S, Spina E (2011) Hypericum perforatum treatment: Effect on behaviour and neurogenesis in a chronic stress model in mice. BMC Complement Altern Med 11, 7.
51. Gibon J, Deloulme JC, Chevallier T, Ladeveze E, Abrous DN, Bouron A (2013) The antidepressant hyperforin increases the phosphorylation of CREB and the expression of TrkB in a tissue-specific manner. Int J Neuropsychopharmacol 16, 189-198.
52. Chung YH, Sun Ahn H, Kim D, Hoon Shin D, Su Kim S, Yong Kim K, Bok Lee W, Ik Cha C (2006) Immunohistochemical study on the distribution of TRPC channels in the rat hippocampus. Brain Res 1085, 132-137. (Pubitemid 43728203)
53. Otsuka Y, Sakagami H, Owada Y, Kondo H (1998) Differential localization of mRNAs for mammalian trps, presumptive capacitative calcium entry channels, in the adult mouse brain. Tohoku J Exp Med 185, 139-146. (Pubitemid 128473295)
54. Zhou J, Du W, Zhou K, Tai Y, Yao H, Jia Y, Ding Y, Wang Y (2008) Critical role of TRPC6 channels in the formation of excitatory synapses. Nat Neurosci 11, 741-743. (Pubitemid 351896670)
55. Merz K, Herold S, Lie DC (2011) CREB in adult neurogenesis-master and partner in the development of adultborn neurons? Eur J Neurosci 33, 1078-1086.
56. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage FH, Song H, Lie DC (2009) GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 29, 7966-7977.
57. Fujioka T, Fujioka A, Duman RS (2004) Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci 24, 319-328. (Pubitemid 38112363)
58. Chatterjee SS, Bhattacharya SK, Wonnemann M, Singer A, Muller WE (1998) Hyperforin as a possible antidepressant component of hypericum extracts. Life Sci 63, 499-510. (Pubitemid 28367402)
59. Chatterjee SS, Biber A, Weibezahn C (2001) Stimulation of glutamate, aspartate and gamma-aminobutyric acid release from synaptosomes by hyperforin. Pharmacopsychiatry 34(Suppl 1), S11-S19.
60. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593. (Pubitemid 43185382)
61. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803-815. (Pubitemid 41266948)
62. Sun B, Halabisky B, Zhou Y, Palop JJ, Yu G, Mucke L, Gan L (2009) Imbalance between GABAergic and glutamatergic transmission impairs adult neurogenesis in an animal model of Alzheimer's disease. Cell Stem Cell 5, 624-633.
63. Li G, Bien-Ly N, Andrews-Zwilling Y, Xu Q, Bernardo A, Ring K, Halabisky B, Deng C, Mahley RW, Huang Y (2009) GABAergic interneuron dysfunction impairs hippocampal neurogenesis in adult apolipoprotein E4 knockin mice. Cell Stem Cell 5, 634-645.
64. Marin-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012) Unique processing during a period of high excitation/ inhibition balance in adult-born neurons. Science 335, 1238-1242.
65. DengW, Aimone JB, Gage FH (2010) New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11, 339-350.
66. Rodriguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM, Oddo S, Verkhratsky A (2008) Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS One 3, e2935.