Sains Malaysiana 48(10)(2019): 2191–2199

http://dx.doi.org/10.17576/jsm-2019-4810-15

The Neuroprotective Effect of Nasturtium officinale on Learning Ability and Density of Parvalbumin Neurons in the Hippocampus of Neurodegenerative-Induced Mice Model

(Kesan Neuropelindung Nasturtium officinale pada Keupayaan Pembelajaran dan Kepadatan Neuron Parvalbumin di Hipokampus Model Tikus Teraruh Neurodegeneratif)

WARIT RUANGLERTBOON¹, EKKASIT KUMARNSIT², SUKANYA DEJ-ADISAI³,

URAPORN VONGVATCHARANON⁴ & WANDEE UDOMUKSORN¹*

¹Department of Pharmacology, Faculty of Science, Prince of Songkla University, Hatyai, Songkhla 90110, Thailand

²Department of Physiology, Faculty of Science, Prince of Songkla University, Hatyai, Songkhla 90110, Thailand

³Department of Pharmacognosy and Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Hatyai, Songkhla 90110, Thailand

⁴Department of Anatomy, Faculty of Science, Prince of Songkla University, Hatyai, Songkhla 90110, Thailand

Received: 14 February 2019/Accepted: 20 August 2019

ABSTRACT

According to European traditional pharmacopeia, as well as in Chinese traditional medicine, watercress (Nasturtium officinale) has a property in enhancing physical stamina during stress condition. The aim of the study was to evaluate the neuroprotective effects of watercress extract (WCE) on dexamethasone-induced neurodegeneration in mice. Swiss albino male mice (35-40 g) were divided into 6 groups: double distilled water (DW) and normal saline solution (NSS) (DW+NSS), DW and dexamethasone (DW+DEX)-treated for 21 days, 80 mg/kg of watercress extract (WCE) and NSS (80WCE+NSS), and WCE-treated (14 days prior to and during dexamethasone treatment) at variable doses of 20 mg/kg (20WCE+DEX), 40 mg/kg (40WCE+DEX), and 80 mg/kg (80WCE+DEX). At the end of the experiment, animals were tested for spatial memory and learning ability by Morris Water Maze apparatus to determine the escape latency time (ELT), and the density of parvalbumin (PV)-immunoreactive (PV-ir) neurons in the hippocampus of the brain, using immunohistochemistry. After dexamethasone treatment, the animals had significantly lower body weight, higher ELT and reduced density of PV-ir neurons in the CA1 and CA2 regions of the hippocampus, compared to the control animals. These parameters partially improved in animals supplemented with WCE but without a dose-related pattern. This study suggests that WCE may be beneficial for neuroprotection in stress-induced neurodegeneration.

Keywords: Hippocampus; Nasturtium officinale; neurodegeneration; parvalbumin neurons; spatial memory

ABSTRAK

Menurut farmakopeia tradisi Eropah dan perubatan tradisi China, selada air (Nasturtium officinale) mempunyai sifat dalam meningkatkan stamina fizikal semasa keadaan stres. Tujuan kajian ini adalah untuk menilai kesan neuropelindung daripada ekstrak selada air (WCE) pada deksametason-teraruh neurodegenerasi pada tikus. Tikus jantan Swiss Albino (35-40 g) telah dibahagikan kepada 6 kumpulan: Air suling dua kali (DW) dan larutan garam biasa (NSS) (DW + NSS), DW dan deksametason (DW + DEX)-dirawat selama 21 hari, 80 mg/kg daripada ekstrak selada air (WCE) dan NSS (80WCE + NSS), dan WCE-dirawat (14 hari sebelum dan semasa rawatan deksametason) pada pelbagai dos 20 mg/kg (20WCE + DEX), 40 mg/kg (40WCE + DEX), dan 80 mg/kg (80WCE + DEX). Pada akhir uji kaji, haiwan telah diuji untuk ingatan ruang dan keupayaan belajar menggunakan perkakasan Lorongan Keliru Morris untuk menentukan waktu lepas kependaman (ELT), dan ketumpatan neuron parvalbumin (PV)-imunoreaktif (PV-ir) pada hipokampus otak menggunakan imunohistokimia. Selepas rawatan deksametason, tikus mempunyai berat badan yang jauh lebih rendah, ELT lebih tinggi dan kurang ketumpatan neuron PV-ir di kawasan CA1 dan CA2 hipokampus berbanding dengan tikus kawalan. Parameter ini sebahagiannya bertambah baik pada haiwan yang diberikan WCE tetapi tanpa corak yang berkaitan dengan dos. Kajian ini menunjukkan bahawa WCE mungkin bermanfaat untuk neuropelindung dalam neurodegeneratif teraruh tekanan.

Kata kunci: Hipokampus; ingatan ruang; Nasturtium officinale; neurodegeneratif; parvalbumin neuron

REFERENCES

Almeida, O.F.X., Conde, G.L., Crochemore, C., Demeneix, B.A., Fischer, D., Hassan, A.H.S., Meyer, M., Holsboer, F. & Michaelidis, T.M. 2000. Subtle shifts in the ratio between pro-and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. Federation of American Societies for Experimental Biology Journal 14: 779-790.

Ballard, C., Gauthier, S., Corbett, A., Brayne, C., Aarsland, D. & Jones, E. 2011. Alzheimer’s disease. Lancet 377: 1019-1031.

Ball, M.J. 1978. Topographic distribution of neurofibrillary tangles and granulovacuolar degeneration in hippocampal cortex of aging and demented patients. A quantitative study. Acta Neuropathologica 42(2): 73-80.

Behl, C. 1998. Effects of glucocorticoids on oxidative stress-induced hippocampal cell death: Implications for the pathogenesis of Alzheimer’s disease. Experimental Gerontology 33(7-8): 689-696.

Bergmann, I., Nitsch, R. & Frotscher, M. 1991. Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anatomy and Embryology 184: 403-409.

Brown, E.S. 2009. Effects of glucocorticoids on mood, memory, and the hippocampus treatment and preventive therapy. Annals of the New York Academy of Sciences 1179: 41-55.

Caillard, O., Moreno, H., Schwaller, B., Llano, I., Celio, M.R. & Marty, A. 2000. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proceedings of the National Academy of Sciences 97(24): 13372-13377.

Celio, M.R. 1986. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231(4741): 995-997.

Chrousos, G.P. & Kino, T. 2009. Glucocorticoid signaling in the cell expanding clinical implications to complex human. behavioral and somatic disorders. Annals of the New York Academy of Sciences 1179: 153-166.

Coleman, P.D. & Flood, D.G. 1987. Neuron numbers and dendritic extent in normal aging and Alzheimer’s disease. Neurobiology of Aging 8(6): 521-545.

Cowan, R.L., Wilson, C.J., Emson, P.C. & Heizmann, C.W. 1990. Parvalbumin-containing GABAergic interneurons in the rat neostriatum. Journal of Comparative Neurology 302(2): 197-205.

D’Hooge, R. & De Deyn, P.P. 2001. Applications of the Morris water maze in the study of learning and memory. Brain Research Reviews 36(1): 60-90.

Filipović, D., Zlatković, J., Gass, P. & Inta, D. 2013.The differential effects of acute vs. chronic stress and their combination on hippocampal parvalbumin and inducible heat shock protein 70 expression. Neuroscience 236: 47-54.

Fogarty, M.C., Hughes, C.M., Burke, G., Brown, J.C. & Davison, G.W. 2013. Acute and chronic watercress supplementation attenuates exercise-induced peripheral mononuclear cell DNA damage and lipid peroxidation. British Journal of Nutrition 109(02): 293-301.

Gill, C.I., Haldar, S., Boyd, L.A., Bennett, R., Whiteford, J., Butler, M., Pearson, J.R., Bradbury, I. & Rowland, IR. 2007. Watercress supplementation in diet reduces lymphocyte DNA damage and alters blood antioxidant status in healthy adults. American Journal of Clinical Nutrition 85(2): 504- 510.

Hu, W., Zhang, M., Czéh, B., Flügge, G. & Zhang, W. 2010. Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network. Neuropsychopharmacology 35: 1693-1707.

Hun Lee, J., Shu, L., Fuentes, F., Su, Z.Y. & Tony Kong, A.N. 2013. Cancer chemoprevention by traditional chinese herbal medicine and dietary phytochemicals: Targeting Nrf2-mediated oxidative stress/anti-inflammatory responses, epigenetics, and cancer stem cells. Journal of Traditional and Complementary Medicine 3(1): 69-79.

Jeon, J., Bong, S.J., Park, J.S., Park, Y.K., Arasu, M.V., Al-Dhabi, N.A. & Park, S.U. 2017. De novo transcriptome analysis and glucosinolate profiling in watercress (Nasturtium officinale R. Br.). BMC Genomics 18(1): 401.

Johnson, I.T. 2002. Glucosinolates in the human diet. Bioavailability and implications for Health. Phytochemistry Reviews 1: 183-188.

Jothy, S.L., Zuraini, Z. & Sasidharan, S. 2011. Phytochemicals screening, DPPH free radical scavenging and xanthine oxidase inhibitiory activities of Cassia fistula seeds extract. Journal of Medicinal Plants Research 5(10): 1941-1947.

Kawata, M. 1995. Roles of steroid hormones and their receptors in structural organization in the nervous system. Neuroscience Research 24(1): 1-46.

Liu, X.Y., Shi, J.H., Du, W.H., Fan, Y.P., Hu, X.L., Zhang, C.C., Xu, H.B., Miao, Y.J., Zhou, H.Y., Xiang, P. & Chen, F.L. 2011. Glucocorticoids decrease body weight and food intake and inhibit appetite regulatory peptide expression in the hypothalamus of rats. Experimental and Therapeutic Medicine 2(5): 977-984.

McPhalen, C.A., Sielecki, A.R., Santarsiero, B.D. & James, M.N. 1994. Refined crystal structure of rat parvalbumin, a mammalian alpha-lineage parvalbumin, at 2.0A resolution. Journal of Molecular Biology 235(2): 718-732.

Morris, R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 11(1): 47-60.

Murray, A.J., Sauer, J.F., Riedel, G., McClure, C., Ansel, L., Cheyne, L., Bartos, M., Wisden, W. & Wulff, P. 2011. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nature Neuroscience 14(3): 297-299.

Ng, T.P. 2016. Cognitive health of older persons in longitudinal ageing cohort studies. Sains Malaysiana 45(9): 1351-1355.

Ognjanovski, N., Schaeffer, S., Wu, J., Mofakham, S., Maruyama, D., Zochowski, M. & Aton, S.J. 2017. Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nature Communications 8: 15039.

Plogmann, D. & Celio, M.R. 1993. Intracellular concentration of parvalbumin in nerve cells. Brain Research 600(2): 273-279.

Rashidy-Pour, A., Sadeghi, H., Taherain, A.A., Vafaei, A.A. & Fathollahi, Y. 2004. The effects of acute restraint stress and dexamethasone on retrieval of long-term memory in rats: An interaction with opiate system. Behavioural Brain Research 154(1): 193-198.

Reagan, L.P. & McEwen, B.S. 1997. Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. Journal of Chemical Neuroanatomy 13(3): 149-167.

Shahrokhi, N., Hadad, M.K., Keshavarzi, Z. & Shabani, M. 2009. Effects of aqueous extract of water cress on glucose and lipis plasma in streptozotocin induced diabetic rats. Pakistan Journal of Physiology 5(2): 6-10.

Sloviter, R.S. 1989. Calcium-binding protein (Calbindin-D_28k) and parvalbumin immunocytochemistry: Localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. Journal of Comparative Neurology 280(2): 183-196.

Tongjaroenbuangam, W., Ruksee, N., Chantiratikul, P., Pakdeenarong, N., Kongbuntad, W. & Govitrapong, P. 2011. Neuroprotective effects of quercetin, rutin and okra (Abelmoschus esculentus Linn.) in dexamethasone-treated mice. Neurochemistry International 59(5): 677-685.

Tulipano, G., Taylor, J.E., Halem, H.A., Datta, R., Dong, J.Z., Culler, M.D., Bianchi, I., Cocchi, D. & Giustina, A. 2007. Glucocorticoid inhibition of growth in rats: Partial reversal with the full-length ghrelin analog BIM-28125. Pituitary 10(3): 267-274.

Uabundit, N., Wattanathorn, J., Mucimapura, S. & Ingkaninan, K. 2010. Cognitive enhancement and neuroprotective effects of Bacopa monnieri in Alzheimer’s disease model. Journal of Ethnopharmacology 127(1): 26-31.

Udomuksorn, W., Mukem, S., Kumarnsit, E., Vongvatcharanon, S. & Vongvatcharanon, U. 2011. Effect of alcohol administration during adulthood on parvalbumin and glial fibrillary acidic protein immunoreactivity in rat cerebral cortex. Acta Histochemica 113(3): 283-289.

Verret, L., Mann, E.O., Hang, G.B., Barth, A.M., Cobos, I., Ho, K., Devidze, N., Masliah, E., Kreitzer, A.C., Mody, I., Mucke, L. & Palop, J.J. 2012. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149(3): 708-721.

Vongvatcharanon, U., Mukem, S., Udomuksorn, W., Kumarsit, E. & Vongvatcharanon, S. 2010. Alcohol administration during adulthood induces alterations of parvalbumin and glial fibrillary acidic protein immunoreactivity in rat hippocampus and cingulate cortex. Acta Histochemica 112(4): 392-401.

Voutsina, N., Payne, A.C., Hancock, R.D., Clarkson, G.J., Rothwell, S.D., Chapman, M.A. & Taylor, G. 2016. Characterization of the watercress (Nasturtium officinale R. Br.; Brassicaceae) transcriptome using RNASeq and identification of candidate genes for important phytonutrient traits linked to human health. BMC Genomics 17: 378.

Woolley, C.S., Gould, E. & McEwen, B.S. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Research 531(1-2): 225-231.

Yahaya, M.F., Zainodin, A., Pupathy, R., Min, E.O.H., Bakar, N.H.A., Zamri, N.A., Ismail, H. & Mohd Ramli, E.S. 2018. The effect of palm tocotrienol on surface osteoblast and osteoclast in excess glucocorticoid osteoporotic rat model. Sains Malaysiana 47(11): 2731-2739.

Yazdanparast, R., Bahramikia, S. & Ardestan, A. 2008. Nasturtium officinale reduces oxidative stress and enhances antioxidant capacity in hypercholesterolaemic rats. Chemico- Biological Interactions 172: 176-184.

Yun, S.J., Lee, D.J., Kim, M.O., Jung, B., Kim, S.O., Sohn, N.W. & Lee, E.H. 2003. Reduction but not cleavage of poly (ADP-ribose) polymerase during stress-mediated cell death in the rat hippocampus. NeuroReport 14(7): 935-939.

*Corresponding author; email: wandee.u@psu.ac.th