Abstract
Sargassum fulvellum (Turner) C. Agardh is an edible brown macroalgae having pharmacological importance. In previous reports, we described the screening of marine algae for their neuritogenic activity in developing hippocampal neurons and found that ethanol extract of S. fulvellum (SFE) possesses promising neurite-outgrowth-promoting activity. In this study, we evaluated whether the initial neurite promoting effect of SFE was followed on the further neuronal maturation and synapse formation. SFE exhibited dose-dependent effect on neurite maturation with an optimum concentration of 5 μg/mL. The initial neuronal differentiation is significantly promoted by SFE. Subsequently, compared with control culture, SFE increased the indices of axonal and dendritic developments such as the number and the length of primary processes, and branching frequencies. In addition to its effect on neurite development, SFE significantly increased the number of puncta for postsynaptic density-95, synaptic vesicle 2, and synapse (about 35%, 67%, and 125%, respectively, of control). Moreover, SFE dose-dependently protects neurons from naturally occurring death in normal culture condition. Taken together, our data demonstrate that SFE can promote neuronal maturation and synaptogenesis and support neuronal survival, suggesting the beneficial effect of this alga in nervous system.
Similar content being viewed by others
References
Brewer G. J.; Torricelli J. R.; Evege E. K.; Price P. J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal™, a new serum-free medium combination. J. Neurosci. Res. 35: 567–576; 1993.
Connor B.; Dragunow M. The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res. Brain Res. Rev. 27: 1–39; 1998.
Donguibogam Committee. Donguibogam Committee, translated Donguibogam. Bubinmunwha Press, Seoul, South Korea. 2198;1999.
Dotti C. G.; Sullivan C. A.; Banker G. A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8: 1454–1488; 1988.
Goslin K.; Asmussen H.; Banker G. Rat hippocampal neurons in low-density culture. In: Banker G.; Goslin K. (eds) Culturing nerve cells. MIT Press, Cambridge, MA, pp 339–370; 1998.
Greene L. A.; Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73: 2424–2428; 1976.
Hannan M. A.; Kang J. Y.; Hong Y. K.; Lee H.; Choi J. S.; Choi I. S.; Moon I. S. The marine alga Gelidium amansii promotes the development and complexity of neuronal cytoarchitecture. Phytother. Res; 2012. doi:10.1002/ptr.4684.
Hefti F. Is Alzheimer’s disease caused by lack of nerve growth factor? Ann. Neurol. 13: 109–110; 1983.
Henderson C. E. Role of neurotrophic factors in neuronal development. Curr. Opin. Neurobiol. 6: 64–70; 1996.
Ina A.; Hayashi K.-I.; Nozaki H.; Kamei Y. Pheophytin a, a low molecular weight compound found in the marine brown alga Sargassum fulvellum, promotes the differentiation of PC12 cells. Int. J. Dev. Neurosci. 25: 63–68; 2007.
Ippolito D. M.; Eroglu C. Quantifying synapses: an immunocytochemistry-based assay to quantify synapse number. J. Vis. Exp. 45: e2270; 2010.
Jo E. H.; Cho S. D.; Ahn N. S.; Jung J. W.; Yang S. R.; Park J. S.; Hwang J. W.; Lee S. H.; Park J. R.; Kim S. J.; Park H. K.; Lee Y. S.; Kang K. S. Inhibition of human breast carcinoma by BLC (Sargassum fulvellum) and BLC/HEN egg in vitro and in vivo. Korean J. Vet. Res. 45: 85–91; 2005.
Kamei Y.; Tsang C. K. Sargaquinoic acid promotes neurite outgrowth via protein kinase A and MAP kinases-mediated signaling pathways in PC12D cells. Int. J. Dev. Neurosci. 21: 255–262; 2003.
Kang J. Y.; Khan M. N. A.; Park N. H.; Cho J. Y.; Lee M. C.; Fujii H.; Hong Y. K. Antipyretic, analgesic, and anti-inflammatory activities of the seaweed Sargassum fulvellum and Sargassum thunbergii in mice. J. Ethnopharmacol. 116: 187–190; 2008.
Koh J. Y.; Choi D. W. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Meth. 20: 83–90; 1987.
Lee E.; Son H. Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 42: 239–244; 2009.
Moon I. S.; Cho S. J.; Jin I.; Walikonis R. A simple method for combined fluorescence in situ hybridization and immunocytochemistry. Mol. Cell 24: 76–82; 2007.
Schaeffer E. L.; Novaes B. A.; da Silva E. R.; Skaf H. D.; Mendes-Neto A. G. Strategies to promote differentiation of newborn neurons into mature functional cells in Alzheimer brain. Prog. Neuropsychopharmacol. Biol. Psychiatry 33: 1087–1102; 2009.
Seress L. Morphological changes of the human hippocampal formation from midgestation to early childhood. In: Nelson C. A.; Luciana M. (eds) Handbook of developmental cognitive neuroscience. MIT Press, Cambridge, MA, pp 45–58; 2001.
Sholl D. A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87: 387–406; 1953.
Siegel G. J.; Chauhan N. B. Neurotrophic factors in Alzheimer’s and Parkinson’s disease brain. Brain Res. Brain Res. Rev. 33: 199–227; 2000.
Suh K. T. Classification of herbs in decoction part of Donguibogam. Ph.D. Thesis. Kyungsung University, Busan, Korea; 138; 1997.
Supèr H.; Soriano E. The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J. Comp. Neurol. 344: 101–120; 1994.
Tsang C. K.; Ina A.; Goto T.; Kamei Y. Sargachromenol, a novel nerve growth factor-potentiating substance isolated from Sargassum macrocarpum, promotes neurite outgrowth and survival via distinct signaling pathways in PC12D cells. Neurosci. 132: 633–643; 2005.
Acknowledgment
This work was supported by Global Healthcare Industry RIS Center, Ministry of Knowledge Economy, Korea. MAH wishes to thank National Institute for International Education (NIIED), Korea, for financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Editor: T. Okamoto
Rights and permissions
About this article
Cite this article
Hannan, M.A., Kang, JY., Hong, YK. et al. A brown alga Sargassum fulvellum facilitates neuronal maturation and synaptogenesis. In Vitro Cell.Dev.Biol.-Animal 48, 535–544 (2012). https://doi.org/10.1007/s11626-012-9537-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11626-012-9537-5