Chotosan ameliorates cognitive and emotional deficits in an animal model of type 2 diabetes: Possible involvement of cholinergic and VEGF/PDGF mechanisms in the brain

BMC Complementary and Alternative Medicine

Volumn 12, Issue , 2012, Pages

  Zhao, Qi ^a   Niu, Yimin ^a   Matsumoto, Kinzo ^a   Tsuneyama, Koichi ^b   Tanaka, Ken ^a   Miyata, Takeshi ^a,c   Yokozawa, Takako ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b UNIVERSITY OF TOYAMA   (Japan)

^c SOJO UNIVERSITY   (Japan)

Author keywords

Cholinergic system; Chotosan; Cognitive deficits; Diabetes; VEGF PDGF systems

Indexed keywords

ANGIOGENIC FACTOR; CHOLINERGIC RECEPTOR; CHOTOSAN; KAMPO; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE C ALPHA; TACRINE; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ANXIETY DISORDER; ARTICLE; BRAIN; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ELEVATED PLUS MAZE TEST; EMOTIONAL DISORDER; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MOUSE; NEUROCHEMISTRY; NEUROPSYCHOLOGICAL TEST; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBJECT RECOGNITION TEST; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TREATMENT DURATION; WATER MAZE TEST; WESTERN BLOTTING; Y MAZE TEST;

EID: 84867607875     PISSN: None     EISSN: 14726882     Source Type: Journal    
DOI: 10.1186/1472-6882-12-188     Document Type: Article

References (68)

1. de la Torre JC. Pathophysiology of neuronal energy crisis in Alzheimer's disease. Neurodegener Dis 2008, 5(3-4):126-132.
2. Zhao WQ, Townsend M. Insulin resistance and amyloidogenesis as common molecular foundation for type 2 diabetes and Alzheimer's disease. Biochim Biophys Acta 2009, 1792(5):482-496. 10.1016/j.bbadis.2008.10.014, 19026743.
3. Janson J, Laedtke T, Parisi JE, O'Brien P, Petersen RC, Butler PC. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 2004, 53(2):474-481. 10.2337/diabetes.53.2.474, 14747300.
4. Brennan AM, Mantzoros CS. Drug Insight: the role of leptin in human physiology and pathophysiology-emerging clinical applications. Nat Clin Pract Endocrinol Metab 2006, 2(6):318-327. 10.1038/ncpendmet0196, 16932309.
5. Zhao Q, Matsumoto K, Tsuneyama K, Tanaka K, Li F, Shibahara N, Miyata T, Yokozawa T. Diabetes-induced central cholinergic neuronal loss and cognitive deficit are attenuated by tacrine and a Chinese herbal prescription, kangen-karyu: elucidation in type 2 diabetes db/db mice. J Pharmacol Sci 2011, 117:230-242. 10.1254/jphs.11115FP, 22083044.
6. Dinel AL, Andre C, Aubert A, Ferreira G, Laye S, Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One 2011, 6(9):e24325. 10.1371/journal.pone.0024325, 3174932, 21949705.
7. Terasawa K, Shimada Y, Kita T, Yamamoto T, Tosa H, Tanaka N, Saito E, Kanaki E, Goto S, Mizushima N, et al. Choto-san in the treatment of vascular dementia: a double-blind, placebo-controlled study. Phytomedicine 1997, 4:15-22. 10.1016/S0944-7113(97)80022-0, 23195240.
8. Yamaguchi S, Matsubara M, Kobayashi S. Event-related brain potential changes after Choto-san administration in stroke patients with mild cognitive impairments. Psychopharmacology (Berl) 2004, 171(3):241-249.
9. Suzuki T, Futami S, Igari Y, Matsumura N, Watanabe K, Nakano H, Oba K, Murata Y, Koibuchi H, Kigawa Y. A Chinese herbal medicine, choto-san, improves cognitive function and activities of daily living of patients with dementia: a double-blind, randomized, placebo-controlled study. J Am Geriatr Soc 2005, 53(12):2238-2240. 10.1111/j.1532-5415.2005.00512_7.x, 16398922.
10. Sugimoto A, Goto K, Ishige A, Komatsu Y, Miyamoto KI. Effect of Choto-san, a Kampo medicine, on the cerebral blood flow autoregulation in spontaneously hypertensive rats. Jpn J Pharmacol 2000, 83(2):135-142. 10.1254/jjp.83.135, 10928326.
11. Watanabe H, Zhao Q, Matsumoto K, Tohda M, Murakami Y, Zhang SH, Kang TH, Mahakunakorn P, Maruyama Y, Sakakibara I, et al. Pharmacological evidence for antidementia effect of Choto-san (Gouteng-san), a traditional Kampo medicine. Pharmacol Biochem Behav 2003, 75(3):635-643. 10.1016/S0091-3057(03)00109-6, 12895681.
12. Murakami Y, Zhao Q, Harada K, Tohda M, Watanabe H, Matsumoto K. Choto-san, a Kamp formula, improves chronic cerebral hypoperfusion-induced spatial learning deficit via stimulation of muscarinic M1 receptor. Pharmacol Biochem Behav 2005, 81:616-625. 10.1016/j.pbb.2005.05.004, 15936808.
13. Zhao Q, Murakami Y, Tohda M, Obi R, Shimada Y, Matsumoto K. Chotosan, a Kampo formula, ameliorates chronic cerebral hypoperfusion-induced deficits in object recognition. J Pharmacol Sci 2007, 103:360-373. 10.1254/jphs.FP0061457, 17409635.
14. De Vriese AS, Tilton RG, Stephan CC, Lameire NH. Vascular endothelial growth factor is essential for hyperglycemia-induced structural and functional alterations of the peritoneal membrane. J Am Soc Nephrol 2001, 12(8):1734-1741.
15. Khamaisi M, Schrijvers BF, De Vriese AS, Raz I, Flyvbjerg A. The emerging role of VEGF in diabetic kidney disease. Nephrol Dial Transplant 2003, 18(8):1427-1430. 10.1093/ndt/gfg242, 12897074.
16. Emerich DF, Schneider P, Bintz B, Hudak J, Thanos CG. Aging reduces the neuroprotective capacity, VEGF secretion, and metabolic activity of rat choroid plexus epithelial cells. Cell Transplant 2007, 16:697-705.
17. Uysal N, Sisman AR, Dayi A, Aksu I, Cetin F, Gencoglu C, Tas A, Buyuk E. Maternal exercise decreases maternal deprivation induced anxiety of pups and correlates to increased prefrontal cortex BDNF and VEGF. Neurosci Lett 2011, 505(3):273-278. 10.1016/j.neulet.2011.10.039, 22044872.
18. Ding YH, Zhou Y, Rafols JA, Clark JC, Ding Y. Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr Neurovasc Res 2006, 3:15-23. 10.2174/156720206775541787, 16472122.
19. Valenzuela MJ, Breakspear M, Sachdev P. Complex mental activity and the aging brain: Molecular, cellular and cortical network mechanisms. Brain Res Rev 2007, 56:198-213. 10.1016/j.brainresrev.2007.07.007, 17870176.
20. Zhao Q, Yokozawa T, Tsuneyama K, Tanaka K, Miyata T, Shibahara N, Matsumoto K. Chotosan (Diaoteng San)-induced improvement of cognitive deficits in senescence-accelerated mouse (SAMP8) involves the amelioration of angiogenic/neurotrophic factors and neuroplasticity systems in the brain. Chin Med 2011, 6:33. 10.1186/1749-8546-6-33, 3189182, 21943225.
21. Zhao Q, Yokozawa T, Yamabe N, Tsuneyama K, Li X-H, Matsumoto K. Kangen-karyu improves memory deficit caused by aging through normalization of neuroplasticity-related signaling system and VEGF system in the brain. J Ethnopharmacol 2010, 131(2):377-385. 10.1016/j.jep.2010.07.016, 20637274.
22. Zhao H-F, Li Q, Zhang Z-F, Pei X-R, Wang J, Li Y. Long-term ginsenoside consumption prevents memory loss in aged SAMP8 mice by decreasing oxidative stress and up-regulating the plasticity-related proteins in hippocampus. Brain Res 2009, 1256:111-122.
23. Horai H, Arita M, Kanaya S, Nihei Y, Ikeda T, Suwa K, Ojima Y, Tanaka K, Tanaka S, Aoshima K, et al. MassBank: a public repository for sharing mass spectral data for life sciences. J Mass Spectrom 2010, 45(7):703-714. 10.1002/jms.1777, 20623627.
24. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, Berardi N, Cattaneo A. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proceedings of National Academy of Science USA 2005, 102:3811-3816.
25. Dellu F, Contarino A, Simon H, Koob GF, Gold LH. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol Learn Mem 2000, 73(1):31-48. 10.1006/nlme.1999.3919, 10686122.
26. Yamada M, Hayashida M, Zhao Q, Shibahara N, Tanaka K, Miyata T, Matsumoto K. Ameliorative effects of yokukansan on learning and memory deficits in olfactory bulbectomized mice. J Ethnopharmacol 2011, 135(3):737-746. 10.1016/j.jep.2011.04.010, 21513784.
27. Curran-Everett D, Benos DJ. Guidelines for reporting statistics in journals published by the American Physiological Society: the seque. Adv Physiol Educ 2007, 31:295-298. 10.1152/advan.00022.2007, 18057394.
28. Hu Y, Schett G, Zou Y, Dietrich H, Xu G. Abundance of platelet-derived growth factors (PDGFs), PDGF receptors and activation of mitogen-activated protein kinases in brain decline with age. Brain Res 1998, 53:251-258.
29. Nait Oumesmar B, Vignais L, Baron-Van Evercooren A. Developmental expression of platelet-derived growth factor α-receptor in neurons and glial cells of the mouse CNS. J Neurosci 1997, 17:125-139.
30. Zheng L, Ishii Y, Tokunaga A, Hamashima T, Shen J, Zhao Q-L, Ishizawa S, Fujimori T, Nabeshima Y-I, Mori H, et al. Neuroprotective effects of PDGF against oxidative stress and the signaling pathway involved. J Neurosci Res 2010, 88:1273-1284.
31. Penn JS, Madan A, Caldwell RB, Bartoli M, Caldwell RW, Hartnett ME. Vascular endothelial growth factor in eye disease. Prog Retin Eye Res 2008, 27(4):331-371. 10.1016/j.preteyeres.2008.05.001, 18653375.
32. Wirostko B, Wong TY, Simo R. Vascular endothelial growth factor and diabetic complications. Prog Retin Eye Res 2008, 27(6):608-621. 10.1016/j.preteyeres.2008.09.002, 18929676.
33. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006, 1(2):848-858. 10.1038/nprot.2006.116, 2895266, 17406317.
34. Sharma AN, Elased KM, Garrett TL, Lucot JB. Neurobehavioral deficits in db/db diabetic mice. Physiol Behav 2010, 101(3):381-388. 10.1016/j.physbeh.2010.07.002, 3098504, 20637218.
35. Oomura Y, Aou S, Fukunaga K. Prandial increase of leptin in the brain activates spatial learning and memory. Pathophysiology 2010, 17(2):119-127. 10.1016/j.pathophys.2009.04.004, 19608390.
36. Gilbert DB, Patterson TA, Rose SP. Midazolam induces amnesia in a simple, one-trial, maze-learning task in young chicks. Pharmacol Biochem Behav 1989, 34(2):439-442. 10.1016/0091-3057(89)90340-7, 2623000.
37. Jensen HH, Poulsen JC. Amnesic effects of diazepam: " drug dependence" explained by state-dependent learning. Scand J Psychol 1982, 23(2):107-111.
38. Miyamoto M. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp Gerontol 1997, 32:139-148. 10.1016/S0531-5565(96)00061-7, 9088911.
39. Aksu I, Baykara B, Ozbal S, Cetin F, Sisman AR, Dayi A, Gencoglu C, Tas A, Buyuk E, Gonenc-Arda S, et al. Maternal treadmill exercise during pregnancy decreases anxiety and increases prefrontal cortex VEGF and BDNF levels of rat pups in early and late periods of life. Neurosci Lett 2012, 516(2):221-225. 10.1016/j.neulet.2012.03.091, 22503727.
40. Birnbaum SG, Yuan PX, Wang M, Vijayraghavan S, Bloom AK, Davis DJ, Gobeske KT, Sweatt JD, Manji HK, Arnsten AF. Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science 2004, 306(5697):882-884. 10.1126/science.1100021, 15514161.
41. Keranen LM, Dutil EM, Newton AC. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr Biol 1995, 5(12):1394-1403. 10.1016/S0960-9822(95)00277-6, 8749392.
42. Menne J, Meier M, Park JK, Haller H. Inhibition of protein kinase C in diabetic nephropathy-where do we stand?. Nephrol Dial Transplant 2009, 24(7):2021-2023. 10.1093/ndt/gfp150, 19349294.
43. Jolivalt CG, Lee CA, Beiswenger KK, Smith JL, Orlov M, Torrance MA, Masliah E. Defective insulin signaling pathway and increased glycogen synthase kinase-3 activity in the brain of diabetic mice: parallels with Alzheimer's disease and correction by insulin. J Neurosci Res 2008, 86(15):3265-3274. 10.1002/jnr.21787, 18627032.
44. Li ZG, Zhang W, Sima AA. Alzheimer-like changes in rat models of spontaneous diabetes. Diabetes 2007, 56(7):1817-1824. 10.2337/db07-0171, 17456849.
45. Clodfelder-Miller B, De Sarno P, Zmijewska AA, Song L, Jope RS. Physiological and pathological changes in glucose regulate brain Akt and glycogen synthase kinase-3. J Biol Chem 2005, 280(48):39723-39731. 10.1074/jbc.M508824200, 1361688, 16179343.
46. Takada-Takatori Y, Kume T, Sugimoto M, Katsuki H, Sugimoto H, Akaike A. Acetylcholinesterase inhibitors used in treatment of Alzheimer's disease prevent glutamate neurotoxicity via nicotinic acetylcholine receptors and phosphatidylinositol 3-kinase cascade. Neuropharmacology 2006, 51(3):474-486. 10.1016/j.neuropharm.2006.04.007, 16762377.
47. Tyagi E, Agrawal R, Nath C, Shukla R. Cholinergic protection via alpha7 nicotinic acetylcholine receptors and PI3K-Akt pathway in LPS-induced neuroinflammation. Neurochem Int 2010, 56(1):135-142. 10.1016/j.neuint.2009.09.011, 19781587.
48. Meier M, King GL. Protein kinase C activation and its pharmacological inhibition in vascular disease. Vasc Med 2000, 5(3):173-185.
49. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9(6):669-676. 10.1038/nm0603-669, 12778165.
50. Inui H, Kitami Y, Tani M, Kondo T, Inagami T. Differences in signal transduction between platelet-derived growth factor (PDGF) α and β receptors in vascular smooth muscle cells. J Biol Chem 1994, 269(48):30546-30552.
51. Flyvbjerg A. Putative pathophysiological role of growth factors and cytokines in experimental diabetic kidney disease. Diabetologia 2000, 43(10):1205-1223. 10.1007/s001250051515, 11079738.
52. Kilic E, Kilic U, Wang Y, Bassetti CL, Marti HH, Hermann DM. The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF's neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J 2006, 20(8):1185-1187. 10.1096/fj.05-4829fje, 16641198.
53. Arimura K, Ago T, Kamouchi M, Nakamura K, Ishitsuka K, Kuroda J, Sugimori H, Ooboshi H, Sasaki T, Kitazono T. PDGF receptor beta signaling in pericytes following ischemic brain injury. Curr Neurovasc Res 2012, 9(1):1-9. 10.2174/156720212799297100, 22272762.
54. Kakinuma Y, Ando M, Kuwabara M, Katare RG, Okudela K, Kobayashi M, Sato T. Acetylcholine from vagal stimulation protects cardiomyocytes against ischemia and hypoxia involving additive non-hypoxic induction of HIF-1alpha. FEBS Lett 2005, 579(10):2111-2118. 10.1016/j.febslet.2005.02.065, 15811327.
55. Kakinuma Y, Furihata M, Akiyama T, Arikawa M, Handa T, Katare RG, Sato T. Donepezil, an acetylcholinesterase inhibitor against Alzheimer's dementia, promotes angiogenesis in an ischemic hindlimb model. J Mol Cell Cardiol 2010, 48(4):680-693. 10.1016/j.yjmcc.2009.11.010, 19962381.
56. Gong Y, Liu L, Xie B, Liao Y-C, Yang E, Sun Z. Ameliorative effects of lotus seedpod proanthocyanidins on cognitive deficits and oxidative damage in senescence-accelerated mice. Behav Brain Res 2008, 194:100-107. 10.1016/j.bbr.2008.06.029, 18652848.
57. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 2004, 36:827-835. 10.1038/ng1395, 15258583.
58. Plaschke K, Staub J, Ernst E, Marti HH. VEGF overexpression improves mice cognitive abilities after unilateral common carotid artery occlusion. Exp Neurol 2008, 214:285-292. 10.1016/j.expneurol.2008.08.014, 18822285.
59. Nobel M, Murray K, Stroobant P, Waterfield MD, Riddle P. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of oligodendrocyte/type-2 astrocyte progenitor cell. Nature 1988, 333:560-562. 10.1038/333560a0, 3287176.
60. Matsui T, Sano K, Tsukamoto T, Ito M, Takaishi T, Nakata H, Nakamura H, Chihara K. Human neuroblastoma cells express α and β platelet-derived growth factor receptors coupling with neurotrophic and chemotactic signaling. J Clin Invest 1993, 92:1153-1160. 10.1172/JCI116684, 288252, 8376577.
61. Fan L, Zhao Z, Orr PT, Chambers CH, Lewis MC, Frick KM. Estradiol-induced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation. J Neurosci 2010, 30:4390-4400. 10.1523/JNEUROSCI.4333-09.2010, 2852263, 20335475.
62. Boulton M, Foreman D, Williams G, McLeod D. VEGF localisation in diabetic retinopathy. Br J Physiol Opt 1998, 82(5):561-568.
63. Ishida S, Shinoda K, Kawashima S, Oguchi Y, Okada Y, Ikeda E. Coexpression of VEGF receptors VEGF-R2 and neuropilin-1 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 2000, 41(7):1649-1656.
64. Hartig W, Bauer A, Brauer K, Grosche J, Hortobagyi T, Penke B, Schliebs R, Harkany T. Functional recovery of cholinergic basal forebrain neurons under disease conditions: old problems, new solutions?. Rev Neurosci 2002, 13(2):95-165.
65. Schliebs R, Arendt T. The cholinergic system in aging and neuronal degeneration. Behav Brain Res 2011, 221(2):555-563. 10.1016/j.bbr.2010.11.058, 21145918.
66. Araya R, Noguchi T, Yuhki M, Kitamura N, Higuchi M, Saido TC, Seki K, Itohara S, Kawano M, Tanemura K, et al. Loss of M5 muscarinic acetylcholine receptors leads to cerebrovascular and neuronal abnormalities and cognitive deficits in mice. Neurobiol Dis 2006, 24(2):334-344. 10.1016/j.nbd.2006.07.010, 16956767.
67. Poulin B, Butcher A, McWilliams P, Bourgognon JM, Pawlak R, Kong KC, Bottrill A, Mistry S, Wess J, Rosethorne EM, et al. The M3-muscarinic receptor regulates learning and memory in a receptor phosphorylation/arrestin-dependent manner. Proc Natl Acad Sci U S A 2010, 107(20):9440-9445. 10.1073/pnas.0914801107, 2889095, 20439723.
68. Volpicelli LA, Leve AI. Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog Brain Res 2004, 145:59-66.