The coumarin derivative osthole stimulates Adult neural stem cells, promotes neurogenesis in the hippocampus, and ameliorates cognitive impairment in APP/PS1 transgenic mice

Biological and Pharmaceutical Bulletin

Volumn 38, Issue 9, 2015, Pages 1290-1301

  Kong, Liang ^a   Hu, Yu ^a   Yao, Yingjia ^a   Jiao, Yanan ^a   Li, Shaoheng ^a   Yang, Jingxian ^a  

^a LIAONING UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Alzheimer's disease; Cognitive impairment; Neural stem cell; Notch signaling; Osthole

Indexed keywords

MESSENGER RNA; NOTCH RECEPTOR; NOTCH1 RECEPTOR; OSTHOLE; TRANSCRIPTION FACTOR HES 1; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; COUMARIN DERIVATIVE; NEUROPROTECTIVE AGENT; PRESENILIN 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; COGNITIVE DEFECT; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IN VITRO STUDY; LEARNING; MEMORY; MORRIS WATER MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; COGNITION DISORDERS; CYTOLOGY; DRUG EFFECTS; GENETICS; MAZE TEST; METABOLISM;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; COGNITION DISORDERS; COUMARINS; HIPPOCAMPUS; MAZE LEARNING; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; NEUROPROTECTIVE AGENTS; PRESENILIN-1;

EID: 84941200477     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b15-00142     Document Type: Article

References (70)

1. Zhongling F, Gang Z, Lei Y. Neural stem cells and Alzheimer's disease: challenges and hope. Am. J. Alzheimers Dis. Other Demen., 24, 52-57 (2009).
2. Marx MJ. J. Neuroscience. New leads on the 'how' of Alzheimer's. Science, 293, 2192-2194 (20 01).
3. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science, 297, 353-356 (2002).
4. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science, 300, 486-489 (2003).
5. Pluchino S, Furlan R, Martino G. Cell-based remyelinating therapies in multiple sclerosis: evidence from experimental studies. Curr. Opin. Neurol., 17, 247-255 (2004).
6. Magnus T, Rao MS. Neural stem cells in inflammatory CNS diseases: mechanisms and therapy. J. Cell. Mol. Med., 9, 303-319 (2005).
7. Yang J, Jiang Z, Fitzgerald DC, Ma C, Yu S, Li H, Zhao Z, Li Y, Ciric B, Curtis M, Rostami A, Zhang GX. Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelin-ation in experimental autoimmune encephalitis. J. Clin. Invest., 119, 3678-3691 (2009).
8. Zhang N, Kang T, Xia Y, Wen Q, Zhang X, Li H, Hu Y, Hao H, Zhao D, Sun D, Yan Y, Zhang GX, Yang J. Effects of salvianolic acid B on survival, self-renewal and neuronal differentiation of bone marrow derived neural stem cells. Eur. J. Pharmacol., 697, 32-39 (2012).
9. Yang J, Rostami A, Zhang GX. Cellular remyelinating therapy in multiple sclerosis. J. Neurol. Sci., 276, 1-5 (2009).
10. Yang J, Yan Y, Ciric B, Yu S, Guan Y, Xu H, Rostami A, Zhang GX. Evaluation of bone marrow- and brain-derived neural stem cells in therapy of central nervous system autoimmunity. Am. J. Pathol., 177, 1989-20 01 (2010).
11. Bi XB, Deng YB, Gan DH, Wang YZ. Salvianolic acid B promotes survival of transplanted mesenchymal stem cells in spinal cord-injured rats. Acta Pharmacol. Sin., 29, 169-176 (2008).
12. Vescovi AL, Snyder EY. Establishment and properties of neural stem cell clones: plasticity in vitro and in vivo. Brain Pathol., 9, 569-598 (1999).
13. Zompa EA, Cain LD, Everhart AW, Moyer MP, Hulsebosch CE. Transplant therapy: recovery of function after spinal cord injury. J. Neurotrauma, 14, 479-506 (1997).
14. Park KI, Liu S, Flax JD, Nissim S, Stieg PE, Snyder EY. Transplantation of neural progenitor and stem cells: developmental insights may suggest new therapies for spinal cord and other CNS dysfunction. J. Neurotrauma, 16, 675-687 (1999).
15. Fricker-Gates RA, Winkler C, Kirik D, Rosenblad C, Carpenter MK, Björklund A. EGF infusion stimulates the proliferation and migration of embryonic progenitor cells transplanted in the adult rat striatum. Exp. Neurol., 165, 237-247 (2000).
16. Coyne TM, Marcus AJ, Woodbury D, Black IB. Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. Stem Cells, 24, 2483-2492 (2006).
17. Yi SH, Jo AY, Park CH, Koh HC, Park RH, Suh-Kim H, Shin I, Lee YS, Kim J, Lee SH. Mash1 and neurogenin 2 enhance survival and differentiation of neural precursor cells after transplantation to rat brains via distinct modes of action. Mol. Ther., 16, 1873-1882 (2008).
18. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703-716 (1999).
19. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell, 96, 25-34 (1999).
20. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med., 8, 963-970 (2002).
21. Magavi SS, Leavit BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature, 405, 951-955 (2000).
22. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci., 30, 3489-3498 (2010).
23. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci., 3, 517-530 (2002).
24. Ross SE, Greenberg ME, Stiles CD. Basic helix-loop-helix factors in cortical development. Neuron, 39, 13-25 (2003).
25. Kageyama R, Ohtsuka T, Shimojo H, Imayoshi I. Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci., 11, 1247-1251 (2008).
26. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res., 306, 343-348 (2005).
27. Leker RR, Lasri V, Chernoguz D. Growth factors improve neu-rogenesis and outcome after focal cerebral ischemia. J. Neural Tran sm., 116, 1397-1402 (2009).
28. Arsenijevic Y, Weiss S. Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J. Neurosci., 18, 2118-2128 (1998).
29. Yabe T, Hirahara H, Harada N, Ito N, Nagai T, Sanagi T, Yamada H. Ferulic acid induces neural progenitor cell proliferation in vitro and in vivo. Neuroscience, 165, 515-524 (2010).
30. Heurteaux C, Gandin C, Borsotto M, Widmann C, Brau F, Lhuillier M, Onteniente B, Lazdunski M. Neuroprotective and neuroprolif-erative activities of NeuroAid (MLC601, MLC901), a Chinese medicine, in vitro and in vivo. Neuropharmacology, 58, 987-1001 (2010).
31. Zhuang P, Zhang Y, Cui G, Bian Y, Zhang M, Zhang J, Liu Y, Yang X, Isaiah AO, Lin Y, Jiang Y. Direct stimulation of adult neural stem/progenitor cells in vitro and neurogenesis in vivo by salviano-lic acid B. PLoS ONE, 7, e35636 (2012).
32. Dong S, Zeng Q, Mitchell ES, Xiu J, Duan Y, Li CX, Tiwari JK, Hu YH, Cao XH, Zhao Z. Curcumin enhances neurogenesis and cognition in aged rats: implications for transcriptional interactions related to growth and synaptic plasticity. PLoS ONE, 7, e31211 (2012).
33. Chao X, Zhou J, Chen T, Liu W, Dong W, Qu Y, Jiang X, Ji X, Zhen H, Fei Z. Neuroprotective effect of osthole against acute isch-emic stroke on middle cerebral ischemia occlusion in rats. Brain Res., 1363, 206-211 (2010).
34. Gao Z, Wen Q, Xia Y, Yang J, Gao P, Zhang N, Li H, Zou S. Os-thole augments therapeutic efficiency of neural stem cells-based therapy in experimental autoimmune encephalomyelitis. J. Pharmacol. Sci., 124, 54-65 (2014).
35. Chen T, Liu W, Chao X, Qu Y, Zhang L, Luo P, Xie K, Huo J, Fei Z. Neuroprotective effect of osthole against oxygen and glucose deprivation in rat cortical neurons: involvement of mitogen-activated protein kinase pathway. Neuroscience, 183, 2 0 3-211 (2 011).
36. Chen X, Pi R, Zou Y, Liu M, Ma X, Jiang Y, Mao X, Hu X. Attenuation of experimental autoimmune encephalomyelitis in C57BL/6 mice by osthole, a natural coumarin. Eur. J. Pharmacol., 629, 40-46 (2010).
37. McLenachan S, Lum MG, Waters MJ, Turnley AM. Growth hormone promotes proliferation of adult neurosphere cultures. Growth Horm. IGF Res., 19, 212-218 (20 09).
38. Schonk DM, Kuijpers HJ, Van Drunen E, Van Dalen CH, Geurts Van Kessel AH, Verheijen R, Ramaekers FC. Assignment of the gene (s) involved in the expression of the proliferation-related Ki-67 antigen to human chromosome 10. Hum. Genet., 83, 297-299 (1989).
39. Bullwinkel J, Baron-Lühr B, Lüdemann A, Wohlenberg C, Gerdes J, Scholzen T. Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J. Cell. Physiol., 206, 624-635 (2006).
40. Rahmanzadeh R, Huttmann G, Gerdes J, Scholzen T. Chromophore-assisted light in activation of pKi-67 leads to inhibition of ribosomal RNA synthesis. Cell Prolif., 40, 422-430 (2007).
41. Yang J, Bridges K, Chen KY, Liu AY. Riluzole increases the amount of latent HSF1 for an amplified heat shock response and cytoprotection. PLoS ONE, 3, e2864 (2008).
42. Guo Y, Wang P, Sun H, Cai R, Xia W, Wang S. Advanced glycation end product-induced astrocytic differentiation of cultured neuro-spheres through inhibition of Notch-Hes1 pathway-mdiated neuro-genesis. Int. J. Mol. Sci., 15, 157-170 (2013).
43. Hu J, Huang X, Hong X, Lu Q, Zhu X. Arsenic trioxide inhibits the proliferation of myeloma cell line through notch signaling pathway. Cancer Cell Int., 13, 25 (2013).
44. Johnstone DM, Graham RM, Trinder D, Riveros C, Olynyk JK, Scott RJ, Moscato P, Milward EA. Changes in brain transcripts related to Alzheimer's disease in a model of HFE hemochromatosis are not consistent with increased Alzheimer's disease risk. J. Alzheimer's Dis., 30, 791-803 (2012).
45. Zhuang PW, Cui GZ, Zhang YJ, Zhang MX, Guo H, Zhang JB, Lu ZQ, Isaiah AO, Lin YX. Baicalin regulates neuronal fate decision in neural stem/progenitor cells and stimulates hippocampal neurogen-esis in adult rats. CNS Neurosci. Ther., 19, 154-162 (2013).
46. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland JN, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet., 13, 159-170 (2004).
47. McClean PL, Hölscher C. Liraglutide can reverse memory impairment, synaptic loss and reduce plaque load in aged APP/PS1 mice, a model of Alzheimer's disease. Neuropharmacology, 76(Pt. A), 57-67 (2014).
48. Yan P, Bero AW, Cirrito JR, Xiao Q, Hu X, Wang Y, Gonzales E, Holtzman DM, Lee JM. Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice. J. Neurosci., 29, 10706-10714 (2009).
49. Li X, Guo F, Zhang Q, Huo T, Liu L, Wei H, Xiong L, Wang Q. Electroacupuncture decreases cognitive impairment and promotes neurogenesis in the APP/PS1 transgenic mice. BMC Complement. Altern. Med., 14, 37 (2014).
50. Teng Y, Zhang MQ, Wang W, Liu LT, Zhou LM, Miao SK, Wan LH. Compound danshen tablet ameliorated aβ25-35-induced spatial memory impairment in mice via rescuing imbalance between cyto-kines and neurotrophins. BMC Complement. Altern. Med., 14, 23 (2 014).
51. Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature, 449, 351-355 (2007).
52. Crawford TQ, Roelink H. The notch response inhibitor DAPT enhances neuronal differentiation in embryonic stem cell-derived embryoid bodies independently of sonic hedgehog signaling. Dev. Dyn., 236, 886-892 (2007).
53. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol., 182, 311-322 (2000).
54. Hu Y, Wen Q, Liang W, Kang T, Ren L, Zhang N, Zhao D, Sun D, Yang J. Osthole reverses beta-amyloid peptide cytotoxicity on neural cells by enhancing cyclic amp response element-binding protein phosphorylation. Biol. Pharm. Bull., 36, 1950-1958 (2013).
55. Bruel-Jungerman E, Rampon C, Laroche S. Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev. Neurosci., 18, 93-114 (2007).
56. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci., 11, 339-350 (2010).
57. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol., 39, 569-578 (1999).
58. Mook-Jung I, Hong HS, Boo JH, Lee KH, Yun SH, Cheong MY, Joo I, Huh K, Jung MW. Ginsenoside Rb1 and Rg1 improve spatial learning and increase hippocampal synaptophysin level in mice. J. Neurosci. Res., 63, 509-515 (2001).
59. Kim SJ, Son TG, Park HR, Park M, Kim MS, Kim HS, Chung HY, Mattson MP, Lee J. Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. J. Biol. Chem., 283, 1449 7-14505 (2008).
60. Ji HJ, Hu JF, Wang YH, Chen XY, Zhou R, Chen NH. Osthole improves chronic cerebral hypoperfusion induced cognitive deficits and neuronal damage in hippocampus. Eur. J. Pharmacol., 636, 96-101 (2010).
61. Fernandes-Alnemri T, Litwack G, Alnemri ES. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J. Biol. Chem., 269, 30761-30764 (1994).
62. Aliaghaei A, Digaleh H, Khodagholi F, Ahmadiani A. Encapsulated choroid plexus epithelial cells actively protect against intrahippo-campal aβ-induced long-term memory dysfunction; upregulation of effective neurogenesis with the abrogated apoptosis and neuroin-flammation. J. Mol. Neurosci., 56, 708-721(2015), Epub ahead of print.
63. Qin Y, Chen Z, Han X, Wu H, Yu Y, Wu J, Liu S, Hou Y. Progesterone attenuates Aβ25-35-induced neuronal toxicity via JNK inactivation and progesterone receptor membrane component 1-de-pendent inhibition of mitochondrial apoptotic pathway. J. Steroid Biochem. Mol. Biol., (2015), Epub ahead of print.
64. Zare N, Motamedi F, Digaleh H, Khodagholi F, Maghsoudi N. Collaboration of geldanamycin-activated P70S6K and Hsp70 against beta-amyloid-induced hippocampal apoptosis: an approach to long-term memory and learning. Cell Stress Chaperones, 20, 309-319 (2015).
65. Selkoe D, Kopan R. Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. Annu. Rev. Neuro-sci., 26, 565-597 (2003).
66. Dovey HF, John V, Anderson J P, Chen LZ, De Saint Andrieu P, Fang LY, Freedman SB, Folmer B, Goldbach E, Holsztynska EJ, Hu KL, Johnson-Wood KL, Kennedy SL, Kholodenko D, Knops JE, Latimer LH, Lee M, Liao Z, Lieberburg IM, Motter RN, Mutter LC, Nietz J, Quinn KP, Sacchi KL, Seubert PA, Shopp GM, Thorsett ED, Tung JS, Wu J, Yang S, Yin CT, Schenk DB, May PC, Altstiel LD, Bender MH, Boggs LN, Britton TC, Clemens JC, Czilli DL, Dieckman-McGinty DK, Droste JJ, Fuson KS, Gitter BD, Hyslop PA, Johnstone EM, Li W-Y, Little SP, Mabry TE, Miller FD, Ni B, Nissen JS, Porter WJ, Potts BD, Reel JK, Stephenson D, Su Y, Shipley LA, Whitesitt CA, Yin T, Audia JE. Functional gamma-secretase inhibitors reduce beta amyloid peptide levels in brain. J. Neurochem., 76, 173-181 (2001).
67. Sastre M, Steiner H, Fuchs K, Capell A, Multhaup G, Condron MM, Teplow D, Haass C. Presenilin-dependent gamma-secretase processing of beta amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep., 2, 835-841 (2001).
68. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C. A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep., 3, 688-694 (2002).
69. Netzer WJ, Dou F, Cai D, Veach D, Jean S, Li Y, Bornmann WG, Clarkson B, Xu H, Greengard P. Gleevec inhibits beta-amyloid production but not Notch cleavage. Proc. Natl. Acad. Sci. U. S. A., 100, 12444-12449 (2003).
70. Fraering PC, Ye W, La Voie MJ, Ostaszewski BL, Selkoe DJ, Wolfe MS. γ-Secretase substrate selectivity can be modulated directly via interaction with a nucleotide-binding site. J. Biol. Chem., 280, 41987-419 96 (20 05).