 |
 |
 |
 |
 |
 |
Sains Malaysiana 45(9)(2016): 1299–1310 Memory Enhancement in Rats by Soybean
and Tempeh Extracts is Associated with Improved Cholinergic
and Reduced Neuroinflammatory Activities (Peningkatan
Daya Ingatan dalam
Tikus oleh Ekstrak Soya dan Tempeh dikaitkan dengan Peningkatan Aktiviti
Kolinergik dan
Pengurangan Aktiviti Keradangan) ALIA
HAMAD1,
VASUDEVAN
MANI1,2,4*, KALAVATHY RAMASAMY1,2,
SIONG
MENG
LIM1,2
& ABU
BAKAR
ABDUL
MAJEED1,2 1Faculty of Pharmacy, Universiti Teknologi MARA, 42300
Bandar Puncak Alam,
Selangor Darul Ehsan, Malaysia 2Brain Degeneration and Therapeutics
Group, Pharmaceutical & Life Sciences Community of Research
(CoRe), Universiti Teknologi MARA, 40450 Shah Alam,
Selangor Darul Ehsan, Malaysia 3Collaborative Drug Discovery Research
(CDDR) Group, Pharmaceutical & Life Sciences Community of Research
(CoRe), Universiti
Teknologi MARA, 40450 Shah Alam,
Selangor Darul Ehsan, Malaysia 4Department of Pharmacology and Toxicology,
College of Pharmacy, Qassim University,
Buraidah Kingdom
of Saudi Arabia Received:
2 December 2015/Accepted: 3 May 2016 ABSTRACT The continued progression of
neurodegeneration may result in dementia. The present study compared
the neuroprotective activities between soybean and tempeh
extracts in rats. The extracts were administered orally at 10,
20 and 40 mg/kg for 15 days. Radial arm maze and elevated plus maze
served as exteroceptive behavioural models
for memory measuring. Brain cholinergic activities (acetylcholine
and acetylcholinesterase) and neuroinflammatory
related cytokines interleukin 1β and interleukin-10 were also
tested. Soybean and tempeh extracts significantly improved
memory, but overall 40 mg/kg tempeh showed better improvement
(p<0.05). The tempeh extracts at 20 and 40 mg/kg
exhibited a significant (p<0.05) increase and decrease
in the level of acetylcholine and acetylcholinesterase activities,
respectively. Tempeh extract (40 mg/kg) resulted in greater
reduction (p<0.05) of inflammation than soybean extract.
Altogether, tempeh extract may be beneficial in the management
and prevention of dementia and Alzheimer’s disease. Keywords: Cholinergic; memory;
neuroinflammation; soybean; Tempeh ABSTRAK Neurodegradasi yang
berlanjutan boleh
menyebabkan penyakit demensia. Kajian ini membandingkan keupayaan ekstrak soya dan tempeh untuk melindungi otak menggunakan tikus. Ekstrak tersebut telah diberi secara
oral pada 10, 20 dan
40 mg/kg selama 15 hari. Pengukuran
daya ingatan
dijalankan dengan menggunakan pagar sesat bentuk jejari
dan pagar sesat bersilang tinggi yang merupakan model rangsangan persekitaran. Aktiviti kolinergik otak (asetilkolina dan asetilkolinesterase) dan sitokin yang berkaitan dengan keradangan otak IL-1β
dan IL10 turut
diuji. Ekstrak
soya dan tempeh mampu meningkatkan daya ingatan, namun 40 mg/kg ekstrak tempeh menunjukkan peningkatan daya ingatan yang paling ketara (p<0.05).
Ekstrak tempeh (20 dan
40 mg/kg) menunjukkan peningkatan
dan penurunan
yang berkesan (p<0.05) dalam
aktiviti asetilkolina
(p<0.05) dan asetilkolinesterase.
Ekstrak tempeh 40 mg/kg mengurangkan
keradangan (p<0.05) yang lebih ketara berbanding
dengan ekstrak
soya. Sebagai kesimpulan, ekstrak tempeh mungkin berkesan mencegah demensia dan juga penyakit Alzheimer. Kata kunci: Daya
ingatan; kolinergik;
radang otak; soya; tempeh REFERENCES Ahmad,
A., Ramasamy, K., Majeed,
A.B.A. & Mani, V. 2015. Enhancement of β-secretase inhibition
and antioxidant activities of tempeh, a fermented soybean
cake through enrichment of bioactive aglycones.
Pharmaceutical Biology 53(5): 758-766. Ahmad,
A., Ramasamy, K., Jaafar,
S.M., Majeed, A.B.A. & Mani, V. 2014.
Total isoflavones from soybean and tempeh reversed scopolamine-induced
amnesia, improved cholinergic activities and reduced neuroinflammation. Food and Chemical Toxicology 65(3):
120-128. Akiyama,
H., Barger, S., Barnum, S., Bradt, B.,
Bauer, J. & Cole, G.M. 2000. Inflammation and Alzheimer’s disease.
Neurobiology of Aging 21(3): 383-421. Auld,
D.S., Kornecook, T.J., Bastianetto,
S. & Quirion, R. 2002. Alzheimer’s
disease and the basal forebrain cholinergic system: relations to
β-amyloid peptides, cognition, and treatment strategies. Progress
in Neurobiology 68(3): 209- 245. Bagheri, M., Joghataei,
M.T., Mohseni, S. & Roghani,
M. 2011. Genistein ameliorates learning
and memory deficits in amyloid β(1-40) rat model of Alzheimer’s
disease. Neurobiology of Learning and Memory 95(3): 270-276.
Barnes,
S. 2010. The biochemistry, chemistry and physiology of the isoflavones
in soybeans and their food products. Lymphatic Research and Biology
8(1): 89-98. Boast,
C.A., Walsh, T.J. & Bartolomeo, A. 2000. The delayed non-match-to-sample
radial arm maze task. Application to Models of Alzheimer’s Disease.
2nd ed. London: CRC Press. Chang,
C.T., Hsu, C.K., Chou, S.T., Chen, Y.C., Huang, F.S. & Chung,
Y.C. 2009. Effect of fermentation time on the antioxidant activities
of tempeh prepared from fermented soybean using Rhizopus
oligosporus. International Journal of Food Science
& Technology 44(4): 799-806. Danciu, C., Soica,
C., Csanyi, E., Ambrus,
R., Feflea, S., Peev,
C. & Dehelean, C. 2012. Changes in the anti-inflammatory activity
of soy isoflavonoid genistein
versus genistein incorporated in two types
of cyclodextrin derivatives. Chemistry Central Journal 6(1):
58. Devi,
M.K.A., Gondi, M., Sakthivelu, G., Giridhar, P., Rajasekaran, T. &
Ravishankar, G.A. 2009. Functional attributes
of soybean seeds and products, with reference to isoflavone
content and antioxidant activity. Food Chemistry 114(3):
771-776. Ding,
B.J., Ma, W.W., He, L.L., Zhou, X., Yuan, L.H., Yu, H.L., Feng,
J.F. & Xiao, R. 2011. Soybean isoflavone
alleviates β-amyloid 1-42 induced inflammatory response to
improve learning and memory ability by down regulation of Toll-like
receptor 4 expression and nuclear factor-κB
activity in rats. International Journal of Developmental Neuroscience
29(5): 537-542. Ecobichon, D.J. 1997. The Basis of Toxicity
Testing. 2nd ed. Boca Raton, Florida: CRC Press. Foyet, H.S., Hritcu, L., Ciobica,
A., Stefan, M., Kamtchouing, P. &
Cojocaru, D. 2011. Methanolic extract
of Hibiscus asper leaves improves spatial memory deficits
in the 6-hydroxydopamine-lesion rodent model of Parkinson’s disease.
Journal of Ethnopharmacology 133(2): 773-779. Glass,
C.K., Saijo, K., Winner, B., Marchetto,
M.C. & Gage, F.H. 2010. Mechanisms underlying inflammation in
neurodegeneration. Cell 140(6): 918-934. Goodman,
M.T., Wilkens, L.R., Hankin, J.H., Lyu, L.C., Wu, A.H. & Kolonel,
L.N. 1997. Association of soy and fiber consumption with the risk
of endometrial cancer. American Journal of Epidemiology 146(4):
294-306. Hwang,
Y.W., Kim, S.Y., Jee, S.H., Kim, Y.N.
& Nam, C.M. 2009. Soy food consumption and risk of prostate
cancer: A meta-analysis of observational studies. Nutrition and
Cancer 61(5): 598-606. Korde, L.A., Wu, A.H., Fears, T., Nomura, A.M.Y., West, D.W., Kolonel, L.N., Pike, M.C., Hoover, R.N. & Ziegler, R.G.
2009. Childhood soy intake and breast cancer risk in Asian American
women. Cancer Epidemiology Biomarkers & Prevention 18(4):
1050-1059. Kovarik, Z., Radic,
Z., Berman, H.A., Simeon-Rudolf, V., Reiner, E. & Taylor, P.
2003. Acetylcholinesterase active centre
and gorge conformations analysed by combinatorial
mutations and enantiomeric phosphonates. Biochemical Journal
373(1): 33-40. Kreijkamp-Kaspers, S., Kok,
L., Grobbee, D.E., de Haan,
E.H., Aleman, A., Lampe, J.W. & Van der Schouw, Y.T. 2004. Effect
of soy protein containing isoflavones
on cognitive function, bone mineral density, and plasma lipids in
postmenopausal women: a randomized controlled trial. JAMA 292(1):
65-74. Liang,
W., Lee, A.H., Binns, C.W., Huang, R.,
Hu, D. & Shao, H. 2009. Soy consumption reduces risk of ischemic
stroke: A case-control study in Southern China. Neuroepidemiology
33(2): 111-116. Lio, D., Licastro, F., Scola, L., Chiappelli, M., Grimald, L.M., Crivello, A., Colonna-Romano, G., Candore,
G., Franceschi, C. & Caruso, C. 2003.
Interleukin-10 promoter polymorphism in sporadic Alzheimer’s disease.
Genes and Immunity 4(3): 234-238. Mani,
V., Ramasamy, K., Ahmad, A., Parle, M.,
Shah, S.A.A. & Majeed, A.B.A. 2012.
Protective effects of total alkaloidal extract from Murraya
koenigii leaves on experimentally induced dementia. Food
and Chemical Toxicology 50(3-4): 1036-1044. Nagarajan, S., Burris, R.L., Stewart, B.W., Wilkerson,
J.E. & Badger, T.M. 2008. Dietary soy protein isolate ameliorates
atherosclerotic lesions in apolipoprotein E-deficient mice potentially
by inhibiting monocyte chemoattractant protein-1 expression. The
Journal of Nutrition 138(2): 332-337. Overk, C.R., Felder, C.C., Tu, Y., Schober, D.A., Bales, K.R., Wuu,
J. & Mufson, E.J. 2010. Cortical M1
receptor concentration increases without a concomitant change in
function in Alzheimer’s disease. Journal of Chemical Neuroanatomy
40(1): 63-70. Pan,
M.H., Lai, C.S. & Ho, C.T. 2010. Anti-inflammatory activity
of natural dietary flavonoids. Food & Function 1(1):
15-31. Patel,
N., Paris, D., Mathura, V., Quadros, A.,
Crawford, F. & Mullan, M. 2005. Inflammatory
cytokine levels correlate with amyloid load in transgenic mouse
models of Alzheimer’s disease. Journal of Neuroinflammation
2(1): 9. Pepeu, G. & Giovannini, M.G. 2010. Cholinesterase
inhibitors and memory. Chemico-Biological
Interactions 187(1-3): 403-408. Pipe,
E.A., Gobert, C.P., Capes, S.E., Darlington,
G.A., Lampe, J.W. & Duncan, A.M. 2009. Soy protein reduces serum
LDL cholesterol and the LDL cholesterol: HDL Cholesterol and Apolipoprotein
B: Apolipoprotein A-I ratios in adults with Type 2 Diabetes. The
Journal of Nutrition 139(9): 1700-1706. Pyo, Y.H. & Seong, K.S. 2009. Hypolipidemic effects of Monascus-fermented
soybean extracts in rats fed a high-fat and -cholesterol diet. Journal
of Agricultural and Food Chemistry 57(18): 8617-8622. Reynolds, K., Chin, A., Lees, K.A.,
Nguyen, A., Bujnowski, D. & He, J.
2006. A meta-analysis of the effect of soy protein supplementation
on serum lipids. The American Journal of Cardiology 98(5):
633-640. Rubio-Perez, J.M. & Morillas-Ruiz, J.M. 2012. A Review: Inflammatory process in
Alzheimer’s disease, role of cytokines. The Scientific World
Journal 2012: Article ID. 756357. Samadi, A., Chioua,
M., Bolea, I., de Los Rios, C., Iriepa,
I., Moraleda, I., Bastida,
A., Esteban, G., Unzeta, M., Galvez, E.
& Marco-Contelles, J. 2011. Synthesis, biological assessment and molecular
modelling of new multipotent MAO and cholinesterase inhibitors as
potential drugs for the treatment of Alzheimer’s disease. European
Journal of Medicinal Chemistry 46(9): 4665-4668. Titus, A.D.J., Shankaranarayana Rao, B.S., Harsha, H.N., Ramkumar, K., Srikumar, B.N., Singh,
S.B., Chattarji, S. & Raju, T.R. 2007.
Hypobaric hypoxia-induced dendritic atrophy of hippocampal neurons
is associated with cognitive impairment in adult rats. Neuroscience
145(1): 265-278. Town, T., Nikolic, V. & Tan,
J. 2005. The microglial “activation” continuum: from innate to adaptive
responses. Journal of Neuroinflammation
2(1): 1-10. Vasudevan, M. & Parle, M. 2006. Pharmacological
actions of Thespesia populnea relevant to Alzheimer’s disease. Phytomedicine 13(9-10): 677-687. Vasudevan, M. & Parle, M. 2007. Memory
enhancing activity of Anwala churna
(Emblica officinalis Gaertn.):
an Ayurvedic preparation. Physiology
& Behavior 91(1): 46-54. Villa, P., Costantini,
B., Suriano, R., Perri,
C., Macrì, F., Ricciardi,
L., Panunzi, S. & Lanzone, A.
2009. The differential effect of the phytoestrogen genistein
on cardiovascular risk factors in postmenopausal women: Relationship
with the metabolic status. Journal of Clinical Endocrinology
& Metabolism 94(2): 552-558. Vizi, E.S., Harsinc
Jr, L., Duncalf, D., Nagashima,
H., Potter, P. & Foldes, F.F. 1985.
A simple and sensitive method of acetylcholine identification and
assay: Bioassay combined with minicolumn
gel filtration or high-performance liquid chromatography. Journal
of Pharmacological Methods 13(3): 201-211. Wei, Q.K., Jone,
W.W. & Fang, T.J. 2004. Study on isoflavones
isomers contents in Taiwan’s Soybean and GM Soybean. Journal
of Food and Drug Analysis 12(4): 324-331. Winter, C.D., Iannotti,
F., Pringle, A.K., Trikkas, C., Clough,
G.F. & Church, M.K. 2002. A microdialysis
method for the recovery of IL-1β, IL-6 and nerve growth factor
from human brain in vivo. Journal of Neuroscience Methods
119(1): 45-50. Yang, H., Jin,
G., Ren, D., Luo, S. & Zhou, T. 2011. Mechanism of isoflavone
aglycone’s effect on cognitive performance
of senescence-accelerated mice. Brain Cognition 76(1): 206-210.
Zheng, H., Youdim,
M.B.H. & Fridkin, M. 2010. Site-activated
chelators targeting acetylcholinesterase and monoamine oxidase for
Alzheimer’s therapy. ACS Chemical Biology 5(6): 603-610.
*Corresponding author; email: vasudevan@puncakalam.uitm.edu.my
|
|||
|
