Effect of Boswellia serrata Triana & Planch. gum resin administration during lactation on morphology of pyramidal neurons in hippocampus of rat

Document Type: Original article

Authors

1 Associate Professor, Department of Cell Biology and Anatomy, School of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran;

2 Professor of Department of Biomedical, Isfahan University of Medical Sciences, Isfahan, Iran;

Abstract

Background & Aim: In traditional medicine, Boswellia species gum resin known as Frankincense or Olibanum, has been administrated in elderly for enhancement of memory and also in pregnant women to increase memory and intelligence of progeny. However, it has been rarely scientifically documented so far. We have previously reported that maternal administration of Frankincense during lactation increased learning and memory performance. In this study, using animal model of rat, we investigated the morphological changes of pyramidal neurons of hippocampus, an important brain centre involved in learning and memory, following maternal administration of Frankincense during three week of lactation. Experimental: Two months-old male Wistar rats whose mothers were given by gavage the aqueous extract of the B. serrata (0.100 mg/kg/day) during lactation were deeply anesthetized and transcardially perfused with fixative solution. Each brain was then removed from skull and divided into two hemispheres. The right hemispheres were selected for morphometerical study. Transverse sections (100 μm thick) were cut through the entire extent of the hippocampus. In a Golgi study, the number of dendritic branching and segments was counted by Sholl’s method. Results & Discussion: Statistical analysis of data indicated that administration of Frankincense during lactation increase the number of dendritic segments, branching of Cornu Ammonis (CA) pyramidal cells in the hippocampus of rat offspring. There was no significant difference in the dendritic length of CA pyramidal cells between experimental and control groups. These results suggest that maternal administration of Frankincense during lactation increase dendritic arborization in the hippocampus. It can be concluded that such morphological changes leads to an increase in the synaptic contacts and it provides one of the bases for the memory improvement induced by Frankincense administration. Industrial/Practical recommendation: Our findings suggest that Boswellia resin and its active ingredients to be extensively studied in neurophysiology. It also suggests that compounds from Boswellia resin may be used in treatment of neurodegenerative disorders.

Keywords


Article Title [Persian]

اثر تجویز صمغ گیاه کندر (Boswellia serrata Triana & Planch) در دوره شیردهی بر مورفولوژی نورون های هیپوکامپی موالید موش صحرایی

Authors [Persian]

  • محمد حسینی شریف آباد 1
  • ابراهیم اسفندیاری 2
1 دانشیار گروه بیولوژی و علوم تشریح، دانشگاه علوم پزشکی شهید صدوقی یزد، یزد، ایران؛
2 استاد گروه زیست پزشکی، دانشکده پزشکی، دانشگاه علوم پزشکی اصفهان، اصفهان، ایران؛
Abstract [Persian]

مقدمه و هدف: کندر صمغ گونه­ Boswellia serrata است که طی سالیان دراز در طب سنتی برای افزایش حافظه افراد مسن و نیز مادران باردار برای افزایش هوش و حافظه فرزندان خود تجویز می شده است. با این حال تاکنون مستندات علمی اندکی در این رابطه موجود است. در این مطالعه با استفاده از مدل حیوانی موش بزرگ آزمایشگاهی(رت)، تغییرات مورفولوژیکی نورون­های هیپوکامپوس که مرکز مهم مغزی در روند یادگیری و حافظه می باشد متعاقب تجویز مادری کندر در سه هفته دوره شیردهی بررسی شد. روش تحقیق: موش­های صحرایی نر دو ماهه نژاد ویستار که به مادران آن­ها در دوره شیردهی به­مدت سه هفته به­صورت روزانه  mg/kg100 عصاره آبی کندر خورانده شده بود را عمیقاً بی­هوش کرد و با تزریق محلول ثابت کننده از راه قلب، مغز را ثابت نموده و از جمجمه خارج گردید. سپس آن را به دو نیم­کره تقسیم نموده و نیم­کره راست برای مطالعه مورفومتری انتخاب و مقاطع عرضی از کل هیپوکامپوس بریده شد. تعداد انشعابات و قطعات دندریتی با استفاده از روش Sholl شمرده شد. نتایج و بحث: تحلیل آماری داده­ها نشان داد که تجویز کندر در دوره شیردهی تعداد قطعات و انشعابات دندریتی سلول­های هرمی شاخ آمون هیپوکامپوس موالید رت را افزایش می دهد. اما تفاوت معنی داری از لحاظ طول دندریت سلول­های هرمی در گروه­های آزمایش و شاهد وجود نداشت. بر اساس این یافته ها پیشنهاد می­شود که تجویز مادری کندر در دوره شیردهی، شاخه های دندریتی در هیپوکامپوس را افزایش می­دهد و می­توان نتیجه گرفت که چنین تغییرات مورفولوژیکی منجر به افزایش تعداد تماس­های سیناپسی می­شود و این یکی از مبانی افزایش حافظه به دلیل تجویز کندر را فراهم می کند. توصیه کاربردی /صنعتی: با توجه به یافته های این مطالعه و سایر مطالعات پیشین ما مبنی بر تأثیر مصرف کندر در فراهم نمودن بستر مورفولوژیکی لازم برای افزایش قوای یادگیری و حافظه پیشنهاد می گردد این ماده و مشتقاتش در تحقیقات نوروفیزیولوژیک مورد ارزیابی بیشتر قرار گیرد و نتایج آن در پیش­گیری یا بهبود بیماری­های دژنراتیو عصبی که منجر به فراموشی می شود استفاده شود.

Keywords [Persian]

  • تکامل دندریت شاخ آمون کندر

Abdul Hameed, H. 1983. Avicenna’s Tract on Cardiac Drugs and Essays on Arab Cardiotherapy. Hamdard Foundation Press. New Delhi.

Alder, J., Cho, N.K. and Hatten, M.E. 1996. Embryonic precursor cells from the rhombic lip are specified to a cerebella granule neuron identity. Neuron, 17: 389-399.

Altmann, A., Poeckel, D. Fischer, L. Schubert-Zsilavecz, M. Steinhilber, D. and Wertz, O. 2004. Coupling of boswellic acid induced Ca2+ mobilization and MAPK activation to lipid metabolism and peroxide formation in human leucocytes. British Journal of Pharmacology, 141: 223-232.

Ammon H.P. 2006. Boswellic acids in chronic inflammatory diseases. Planta Medica, 12: 1100–1116.

Archier, P. and Vieillescazes, C. 2000. Characterization of various geographical origin incense based on chemical criteria. A European Journal on Analytical Chemistry, 28: 233-237.

Bayer, S.A. Altman, J. Russo, R.J. and Zhang, X. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology, 14: 83-144.

Büchele, B. Zugmaier, W. Estrada, A. Genze, F. Syrovets, T. and Paetz, C. 2006. Characterization of 3alpha-acetyl-11-ketoalpha-boswellic acid, a pentacyclic triterpenoid inducing apoptosis in vitro and in vivo. Planta Medica, 72: 1285–1289.

Dixit, V.P. Joshi, S. Sinha. R. Bharva Va, S.K. and Varma, M. 1980. Hypolipidemic activity of guggal resin and garlic in dogs and monkeys. Biochemistry and Experimental Biology, 16(4): 421-424.

Eckenhoff, M.F. and Rakic, R. 1986. Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural and immonocytochemical analysis in the developing Rhesus monkey. The Journal of Comparative Neurology, 223: 1-21.

Ernst, E. 2008. Frankincense: systematic review. British Medical Journal, 17: 337: a2813.

Farshchi, A. Ghiasi, G. Farshchi, S. and Malek Khatabi, P. 2010. Effects of Boswellia papyrifera Gum Extract on Learning and Memory in Mice and Rats. Iranian Journal of Basic Medical Sciences, 13(2) 9-15.

Horner, C.H. 1993. Plasticity of the dendritic spine. Progress in Neurobiology, 41: 281-321.

Hosseini, M. Hadjzad, M. Derekhshan, M. Havakhah, S. Behnam Rassouli, F. Rakhshandeh, H. and Saffarzadeh, F. 2010. The beneficial effects of olibanum on memory deficit induced by hypothyroidism in adult rats tested in Morris water maze. Archives of Pharmaceutical Research, 33(3): 463-468.

Hosseini-sharifabad, M. and Esfandiari, E. 2007. A morphometeric study on CA3 hippocampal field in young rats following maternal administration of Boswellia serrata resin during gestation. Iranian Journal of Basic Medical Sciences, 10(3): 176-182.

Hosseini-sharifabad, M. and Esfandiari, E. 2005. Quantitative analysis of hippocampal neuron number and size following prenatal administration of Boswellia serrata gum resin in adult rats. Journal of Isfahan Medical School, 76-77: 58-63.

Hosseini-sharifabad, M. Esfandiari, E. and Alaee, H. 2004. Effects of Frankincence aqueous extract during gestational period on increasing power of learning and memory in adult off springs. Journal of Isfahan Medical School, 71: 16-20. [in Farsi].

Hosseini-sharifabad, M., Esfandiari, E. Alaee, H. Moatar F. 2003. Effect of maternal consumption of aqueous extract of the gum resin of Boswellia serrata during lactation on increasing power of learning and memory in adult off springs. Iranian Journal of Basic Medical Sciences, 6(3): 207-211. [in Farsi].

Huan, M.T., Badmaev, V. Ding, Y. Liu, Y. Xie, J.G. and Ho, C.T. 2000. Anti-tumor and anti carcinogenic activities of triterpenoid, beta boswellic acid. BioFactors, 13(1-4): 225-30.

Jauch, J. and Bergmann, J. 2003. An efficient method for the largescale preparation of 3-O-acetyl-11-oxo-b-boswellic acid and other boswellic acids. European Journal of Organic Chemistry, 24: 4752-4756

Karima, O. Riazi, G. Yousefi, R. and Moosavi Movahedi, A.A. 2010. The enhancement effect of beta-boswellic acid on hippocampal neurites outgrowth and branching (an in vitro study). Neurological Sciences, 31: 315-320.

Mahmoudi, A. Hosseini-Sharifabad, A. Monsef-Esfahani, H.R. Yazdinejad, A.R. Khanavi, M., Roghani, A. Beyer C. and Sharifzadeh, M. 2011. Evaluation of systemic administration of Boswellia papyrifera extracts on spatial memory retention in male rats. Journal of Natural Medicines, 65(3-4): 519-525.

Marshall, S. 2003. Frankincense: festive pharmacognosy. The Pharmaceutical Journal, 271: 862-864.

Menon, M.K. and Kar, A. 1971. Analgesic and psychopharmacological effects of the gum resin of Boswellia serrata. Planta Medica, 19: 333-341.

Moore, P.D. 2006. Conservation biology: unkind cuts for incense. Nature, 14; 444(7121): 829.

Moussaieff, A., Shein, N. A., Tsenter, J., Grigoriadis, S., Simeonidou, C., Alexandrovich, A.G. Trembovler, V. Ben-Neriah, Y. Schmitz M.L. Fiebich, B.L. Munoz, E., Mechoulam, R. and Shohami, E. 2008a. Incensole acetate-a novel neuroprotective agent isolated from Boswellia carterii. .Journal of Cerebral Blood Flow & Metabolism, 28(7): 1341-1352.

Moussaieff, A. Rimmerman, N. Bregman, T. Straiker, A. Felder, C.C. Shoham, S. Kashman, Y. Huang S.M. Lee, H. Shohami, E. Mackie, K. Caterina, M.J. Walker, J.M. Fride, E. and Mechoulam, R. 2008b. Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain. The Federation of American Societies for Experimental Biology Journal, 22(8): 3024-3034.

Moussaieff, A. Shohami, E. Kashman, Y. Fride, E. Schmitz, M.L. Renner, F. Fiebich, B.L. Munoz, E. Ben-Neriah, Y. and Mechoulam, R. 2007. Incensole acetate, a novel anti-inflammatory compound isolated from Boswellia resin, inhibits nuclear factor-kappa B activation. Molecular Pharmacology, 72: 1657-1664.

Nguyen, P.V. and Woo, N.H. 2003. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Progress in Neurobiology, 71: 401-437.

Poeckel, D. and Werz, O. 2006. Boswellic acids: biological actions and molecular targets. Current Medicinal Chemistry, 13: 3359-3369.

Rusakov, D.A., Davies, H.A. and Harrison, E. 1997. Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neuroscience, 80: 69-77.

Sousa, N., Lukoyanov, N.V. Madeira, M.D. Almeida, O.F. and Paula-Barbosa, M.M. 2000. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience, 97: 253-266.

Thulin, M. and Warfa, A.M. 1985. The frankincense trees (Boswellia spp., Burseraceae) of Northern Somalia and Southern Arabia. Kew Bulletin, 42: 487-500.

Uemura, E., Carriquiry, A., Kliemann, W. and Goodwin, J. 1995. Mathematical modeling of dendritic growth in vitro. Brain Research, 671: 187-194.

Uylings, H.B.M., Ruiz-Marcos, A. and Van Pelt, J. 1986. The metric analysis of three- dimensional dendritic patterns: a methodological review. Journal of Neuroscience Methods, 18: 127-151.

West, M.J., Slomianka, L. and Gundersen, H.J.G. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anatomical Record, 231: 482-497.

Zola-Morgan, S. and Squire, L.R. 1993. Neuroanatomy of memory. The Annual Review of Neuroscience, 16: 547-563.