Abstract
Background: Cardamonin is a naturally occurring chalcone from the Alpinia species. It is known to possess antioxidant and anti-inflammatory properties. Our previous studies have shown that cardamonin has antihyperalgesic and antiallodynic effects on CCI-induced neuropathic pain in mice. Although the evidence of the association between cardamonin and neuropathic pain has been reported in animal studies, specific targets using in vitro models are still lacking. Objectives/Methods: This study aims to investigate the effect of cardamonin on nitric oxide production using the LPS-induced neuropathic pain-like SH-SY5Y in vitro model through NMDA receptor expression. Results: Cardamonin administration in differentiated SH-SY5Y cells significantly reduced nitric oxide production assessed using Griess reagent. Western blot analysis demonstrated a significant reduction in GluN2B receptor expression in the cardamonin treated SH-SY5Y cells compared to the vehicle treated group. Conclusions: These data suggest that cardamonin reduces nitric oxide production modulated through NMDA GluN2B receptor subunit. Our results provides preliminary data to support the in vivo studies using cardamonin and may contribute to further understanding the mechanisms of action of cardamonin.
References
Ahlawat, A., Rana, A., Goyal, N., & Sharma, S. (2014). Potential role of nitric oxide synthase isoforms in pathophysiology of neuropathic pain. Inflammopharmacology, 22(5), 269-278.
https://doi.org/10.1007/s10787-014-0213-0
Andaloussi-Lilja, J. E., Lundqvist, J., & Forsby, A. (2009). TRPV1 expression and activity during retinoic acid-induced neuronal differentiation. Neurochemistry international, 55(8), 768-774.
https://doi.org/10.1016/j.neuint.2009.07.011
Attal, N., Lanteri-Minet, M., Laurent, B., Fermanian, J., & Bouhassira, D. (2011). The specific disease burden of neuropathic pain: results of a French nationwide survey. Pain, 152(12), 2836-2843.
https://doi.org/10.1016/j.pain.2011.09.014
Bajgai, S. P., Prachyawarakorn, V., Mahidol, C., Ruchirawat, S., & Kittakoop, P. (2011). Hybrid flavan-chalcones, aromatase and lipoxygenase inhibitors, from Desmos cochinchinensis. Phytochemistry, 72(16), 2062-2067.
https://doi.org/10.1016/j.phytochem.2011.07.002
Bansal, D., Bhansali, A., Hota, D., Chakrabarti, A., & Dutta, P. (2009). Amitriptyline vs. pregabalin in painful diabetic neuropathy: a randomized double blind clinical trial. Diabetic medicine, 26(10), 1019-1026.
https://doi.org/10.1111/j.1464-5491.2009.02806.x
Baron, R., Binder, A., & Wasner, G. (2010). Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment. The Lancet Neurology, 9(8), 807-819.
https://doi.org/10.1016/S1474-4422(10)70143-5
Boje, K. M., Jaworowicz, D., & Raybon, J. J. (2003). Neuroinflammatory role of prostaglandins during experimental meningitis: evidence suggestive of an in vivo relationship between nitric oxide and prostaglandins. Journal of Pharmacology and Experimental Therapeutics, 304(1), 319-325.
https://doi.org/10.1124/jpet.102.041533
Bryan, N. S., & Grisham, M. B. (2007). Methods to detect nitric oxide and its metabolites in biological samples. Free Radical Biology and Medicine, 43(5), 645-657.
https://doi.org/10.1016/j.freeradbiomed.2007.04.026
Calvo, M., Dawes, J. M., & Bennett, D. L. (2012). The role of the immune system in the generation of neuropathic pain. The Lancet Neurology, 11(7), 629-642.
https://doi.org/10.1016/S1474-4422(12)70134-5
Campbell, J. N., & Meyer, R. A. (2006). Mechanisms of neuropathic pain. Neuron, 52(1), 77-92.
https://doi.org/10.1016/j.neuron.2006.09.021
Caroff, M., & Karibian, D. (2003). Structure of bacterial lipopolysaccharides. Carbohydrate research, 338(23), 2431-2447.
https://doi.org/10.1016/j.carres.2003.07.010
Chen, Y.-C., Shen, S.-C., Chen, L.-G., Lee, T. J., & Yang, L.-L. (2001). Wogonin, baicalin, and baicalein inhibition of inducible nitric oxide synthase and cyclooxygenase-2 gene expressions induced by nitric oxide synthase inhibitors and lipopolysaccharide. Biochemical pharmacology, 61(11), 1417-1427.
https://doi.org/10.1016/S0006-2952(01)00594-9
Chia, J. S. M., Izham, N. A. M., Farouk, A. A. O., Sulaiman, M. R., Mustafa, S., Hutchinson, M. R., & Perimal, E. K. (2020). Zerumbone Modulates α2A-Adrenergic, TRPV1, and NMDA NR2B Receptors Plasticity in CCI-Induced Neuropathic Pain In Vivo and LPS-Induced SH-SY5Y Neuroblastoma In Vitro Models. Frontiers in Pharmacology, 11(92).
https://doi.org/10.3389/fphar.2020.00092
Clark, A. K., Old, E. A., & Malcangio, M. (2013). Neuropathic pain and cytokines: current perspectives. Journal of pain research, 6, 803.
https://doi.org/10.2147/JPR.S53660
Clark, A. K., Staniland, A. A., Marchand, F., Kaan, T. K., McMahon, S. B., & Malcangio, M. (2010). P2X7-dependent release of interleukin-1β and nociception in the spinal cord following lipopolysaccharide. Journal of Neuroscience, 30(2), 573-582.
https://doi.org/10.1523/JNEUROSCI.3295-09.2010
Colburn, R., Rickman, A., & DeLeo, J. (1999). The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Experimental neurology, 157(2), 289-304.
https://doi.org/10.1006/exnr.1999.7065
Cull-Candy, S., Brickley, S., & Farrant, M. (2001). NMDA receptor subunits: diversity, development and disease. Current opinion in neurobiology, 11(3), 327-335.
https://doi.org/10.1016/S0959-4388(00)00215-4
Cury, Y., Picolo, G., Gutierrez, V. P., & Ferreira, S. H. (2011). Pain and analgesia: the dual effect of nitric oxide in the nociceptive system. Nitric oxide, 25(3), 243-254.
https://doi.org/10.1016/j.niox.2011.06.004
El-Naga, R. N. (2014). Pre-treatment with cardamonin protects against cisplatin-induced nephrotoxicity in rats: impact on NOX-1, inflammation and apoptosis. Toxicology and applied pharmacology, 274(1), 87-95.
https://doi.org/10.1016/j.taap.2013.10.031
Ellis, A., & Bennett, D. (2013). Neuroinflammation and the generation of neuropathic pain. British journal of anaesthesia, 111(1), 26-37.
https://doi.org/10.1093/bja/aet128
Forstermann, U., & Sessa, W. C. (2011). Nitric oxide synthases: regulation and function. European heart journal, 33(7), 829-837.
https://doi.org/10.1093/eurheartj/ehr304
Gilron, I., Baron, R., & Jensen, T. (2015). Neuropathic pain: principles of diagnosis and treatment. Paper presented at the Mayo Clinic Proceedings.
https://doi.org/10.1016/j.mayocp.2015.01.018
Hatziieremia, S., Gray, A., Ferro, V., Paul, A., & Plevin, R. (2006). The effects of cardamonin on lipopolysaccharide‐induced inflammatory protein production and MAP kinase and NFκB signalling pathways in monocytes/macrophages. British journal of pharmacology, 149(2), 188-198.
https://doi.org/10.1038/sj.bjp.0706856
Inada, H., Shindo, H., Tawata, M., & Onaya, T. (1998). cAMP regulates nitric oxide production and ouabain sensitive Na+, K+-ATPase activity in SH-SY5Y human neuroblastoma cells. Diabetologia, 41(12), 1451-1458.
https://doi.org/10.1007/s001250051091
Inoue, K., & Tsuda, M. (2018). Microglia in neuropathic pain: cellular and molecular mechanisms and therapeutic potential. Nature Reviews Neuroscience, 19(3), 138.
https://doi.org/10.1038/nrn.2018.2
Joca, S. R., Sartim, A. G., Roncalho, A. L., Diniz, C. F., & Wegener, G. (2019). Nitric oxide signalling and antidepressant action revisited. Cell and tissue research, 1-14.
https://doi.org/10.1007/s00441-018-02987-4
Kim, Y.-J., Ko, H., Park, J.-S., Han, I.-H., Amor, E. C., Lee, J. W., & Yang, H. O. (2010). Dimethyl cardamonin inhibits lipopolysaccharide-induced inflammatory factors through blocking NF-κB p65 activation. International immunopharmacology, 10(9), 1127-1134.
https://doi.org/10.1016/j.intimp.2010.06.017
Kovalevich, J., & Langford, D. (2013). Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology Neuronal cell culture (pp. 9-21): Springer.
https://doi.org/10.1007/978-1-62703-640-5_2
Lee, M.-Y., Seo, C.-S., Lee, J.-A., Shin, I.-S., Kim, S.-J., Ha, H., & Shin, H.-K. (2012). Alpinia katsumadai H AYATA Seed Extract Inhibit LPS-Induced Inflammation by Induction of Heme Oxygenase-1 in RAW264. 7 Cells. Inflammation, 35(2), 746-757.
https://doi.org/10.1007/s10753-011-9370-0
Leung, L., & Cahill, C. M. (2010). TNF-α and neuropathic pain-a review. Journal of neuroinflammation, 7(1), 27.
https://doi.org/10.1186/1742-2094-7-27
Levy, D., & Zochodne, D. W. (2004). NO pain: potential roles of nitric oxide in neuropathic pain. Pain Practice, 4(1), 11-18.
https://doi.org/10.1111/j.1533-2500.2004.04002.x
Li, J.-H., Vicknasingam, B., Cheung, Y.-w., Zhou, W., Nurhidayat, A. W., Des Jarlais, D. C., & Schottenfeld, R. (2011). To use or not to use: an update on licit and illicit ketamine use. Substance abuse and rehabilitation, 2, 11.
https://doi.org/10.2147/SAR.S15458
Lin, W., Wu, R. T., Wu, T., Khor, T.-O., Wang, H., & Kong, A.-N. (2008). Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochemical pharmacology, 76(8), 967-973.
https://doi.org/10.1016/j.bcp.2008.07.036
Luo, Z. D., & Cizkova, D. (2000). The role of nitric oxide in nociception. Current review of pain, 4(6), 459-466.
https://doi.org/10.1007/s11916-000-0070-y
Lurie, D. I. (2018). An integrative approach to neuroinflammation in psychiatric disorders and neuropathic pain. Journal of experimental neuroscience, 12.
https://doi.org/10.1177/1179069518793639
Luscher, C., & Malenka, R. C. (2012). NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harbor perspectives in biology, 4(6), a005710.
https://doi.org/10.1101/cshperspect.a005710
Maruyama, K., Okamoto, T., & Shimaoka, M. (2012). Integrins and nitric oxide in the regulation of glia cells: potential roles in pathological pain. J Anesth Clin Res, 4(292), 2.
https://doi.org/10.4172/2155-6148.S7-008
Mengke, N. S., Hu, B., Han, Q. P., Deng, Y. Y., Fang, M., Xie, D., Li, A., & Zeng, H. K. (2016). Rapamycin inhibits lipopolysaccharide-induced neuroinflammation in vitro and in vivo. Molecular medicine reports, 14(6), 4957-4966.
https://doi.org/10.3892/mmr.2016.5883
Milligan, E. D., Twining, C., Chacur, M., Biedenkapp, J., O'Connor, K., Poole, S., Tracey, K., Martin, D., Maier, S. F., & Watkins, L. R. (2003). Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. Journal of Neuroscience, 23(3), 1026-1040.
https://doi.org/10.1523/JNEUROSCI.23-03-01026.2003
Miyamoto, T., Dubin, A. E., Petrus, M. J., & Patapoutian, A. (2009). TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice. PloS one, 4(10).
https://doi.org/10.1371/journal.pone.0007596
Moalem, G., & Tracey, D. J. (2006). Immune and inflammatory mechanisms in neuropathic pain. Brain research reviews, 51(2), 240-264.
https://doi.org/10.1016/j.brainresrev.2005.11.004
Mohammed Izham, N. A., Chia, J. S. M., Vidyadaran, S., Sulaiman, M. R., Bharatham, B. H., & Perimal, E. K. (2018). The Effect of DMEM and DMEM:F12 Culture Media on the Growth of SH-SY5Y Cells. Life Sciences, Medicine and Biomedicine, 2(3).
https://doi.org/10.28916/lsmb.2.3.2018.23
Mukherjee, P., Cinelli, M. A., Kang, S., & Silverman, R. B. (2014). Development of nitric oxide synthase inhibitors for neurodegeneration and neuropathic pain. Chemical Society Reviews, 43(19), 6814-6838.
https://doi.org/10.1039/C3CS60467E
Naik, A. K., Tandan, S. K., Kumar, D., & Dudhgaonkar, S. P. (2006). Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats. European journal of pharmacology, 530(1-2), 59-69.
https://doi.org/10.1016/j.ejphar.2005.11.029
Niesters, M., Martini, C., & Dahan, A. (2014). Ketamine for chronic pain: risks and benefits. British journal of clinical pharmacology, 77(2), 357-367.
https://doi.org/10.1111/bcp.12094
Obata, K., Yamanaka, H., Kobayashi, K., Dai, Y., Mizushima, T., Katsura, H., Fukuoka, T., Tokunaga, A., & Noguchi, K. (2006). The effect of site and type of nerve injury on the expression of brain-derived neurotrophic factor in the dorsal root ganglion and on neuropathic pain behavior. Neuroscience, 137(3), 961-970.
https://doi.org/10.1016/j.neuroscience.2005.10.015
Ortiz-Ortiz, M. A., Moran, J. M., Gonzalez-Polo, R. A., Niso-Santano, M., Soler, G., Bravo-San Pedro, J. M., & Fuentes, J. M. (2009). Nitric oxide-mediated toxicity in paraquat-exposed SH-SY5Y cells: a protective role of 7-nitroindazole. Neurotoxicity research, 16(2), 160-173.
https://doi.org/10.1007/s12640-009-9065-6
Park, S., Gwak, J., Han, S. J., & Oh, S. (2013). Cardamonin suppresses the proliferation of colon cancer cells by promoting β-catenin degradation. Biological and Pharmaceutical Bulletin, b13-00158.
https://doi.org/10.1248/bpb.b13-00158
Pascoal, A. C. R. F., Ehrenfried, C. A., Lopez, B. G.-C., De Araujo, T. M., Pascoal, V., Gilioli, R., Anhe, G. F., Ruiz, A. L. T. G., Carvalho, J. E. d., & Stefanello, M. E. A. (2014). Antiproliferative activity and induction of apoptosis in PC-3 cells by the chalcone cardamonin from Campomanesia adamantium Myrtaceae) in a bioactivity-guided study. Molecules, 19(2), 1843-1855.
https://doi.org/10.3390/molecules19021843
Petrenko, A. B., Yamakura, T., Baba, H., & Shimoji, K. (2003). The role of N-methyl-D-aspartate (NMDA) receptors in pain: a review. Anesthesia & Analgesia, 97(4), 1108-1116.
https://doi.org/10.1213/01.ANE.0000081061.12235.55
Qiu, Q., Sun, L., Wang, X. M., Lo, A. C., Wong, K. L., Gu, P., Wong, S. C. S., & Cheung, C. W. (2017). Propofol produces preventive analgesia via GluN2B-containing NMDA receptor/ERK1/2 signaling pathway in a rat model of inflammatory pain. Molecular pain, 13.
https://doi.org/10.1177/1744806917737462
Rao, C. B., Rao, T. N., & Suryaprakasam, S. (1976). Cardamonin and alpinetin from the seeds of Amomum subulatum. Planta Medica, 29(04), 391-392.
https://doi.org/10.1055/s-0028-1097682
Renauld, A., & Spengler, R. (2002). Tumor necrosis factor expressed by primary hippocampal neurons and SH‐SY5Y cells is regulated by α2‐adrenergic receptor activation. Journal of neuroscience research, 67(2), 264-274.
https://doi.org/10.1002/jnr.10101
Sambasevam, Y., Farouk, A. A. O., Mohamad, T. A. S. T., Sulaiman, M. R., Bharatham, B. H., & Perimal, E. K. (2017). Cardamonin attenuates hyperalgesia and allodynia in a mouse model of chronic constriction injury-induced neuropathic pain: Possible involvement of the opioid system. European journal of pharmacology, 796, 32-38.
https://doi.org/10.1016/j.ejphar.2016.12.020
Scholz, J., & Woolf, C. J. (2007). The neuropathic pain triad: neurons, immune cells and glia. Nature neuroscience, 10(11), 1361.
https://doi.org/10.1038/nn1992
Sharma, J., Al-Omran, A., & Parvathy, S. (2007). Role of nitric oxide in inflammatory diseases. Inflammopharmacology, 15(6), 252-259.
https://doi.org/10.1007/s10787-007-0013-x
Sharma, K., Sharma, D., Sharma, M., Sharma, N., Bidve, P., Prajapati, N., Kalia, K., & Tiwari, V. (2018). Astaxanthin ameliorates behavioral and biochemical alterations in in-vitro and in-vivo model of neuropathic pain. Neuroscience letters, 674, 162-170.
https://doi.org/10.1016/j.neulet.2018.03.030
Sousa, A. M., & Prado, W. A. (2001). The dual effect of a nitric oxide donor in nociception. Brain research, 897(1-2), 9-19.
https://doi.org/10.1016/S0006-8993(01)01995-3
Tanga, F. Y., Nutile-McMenemy, N., & DeLeo, J. A. (2005). The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proceedings of the National Academy of Sciences, 102(16), 5856-5861.
https://doi.org/10.1073/pnas.0501634102
Thacker, M. A., Clark, A. K., Marchand, F., & McMahon, S. B. (2007). Pathophysiology of peripheral neuropathic pain: immune cells and molecules. Anesthesia & Analgesia, 105(3), 838-847.
https://doi.org/10.1213/01.ane.0000275190.42912.37
Thomson, K. S., & Moland, E. S. (2000). Version 2000: the new β-lactamases of Gram-negative bacteria at the dawn of the new millennium. Microbes and Infection, 2(10), 1225-1235.
https://doi.org/10.1016/S1286-4579(00)01276-4
Uceyler, N., Rogausch, J. P., Toyka, K. V., & Sommer, C. (2007). Differential expression of cytokines in painful and painless neuropathies. Neurology, 69(1), 42-49.
https://doi.org/10.1212/01.wnl.0000265062.92340.a5
Van Hecke, O., Austin, S. K., Khan, R. A., Smith, B., & Torrance, N. (2014). Neuropathic pain in the general population: a systematic review of epidemiological studies. PAIN, 155(4), 654-662.
https://doi.org/10.1016/j.pain.2013.11.013
Xie, H.-r., Hu, L.-s., & Li, G.-y. (2010). SH-SY5Y human neuroblastoma cell line: in vitrocell model of dopaminergic neurons in Parkinson's disease. Chinese medical journal, 123(8), 1086-1092.
Xu, Z.-Z., Berta, T., & Ji, R.-R. (2013). Resolvin E1 inhibits neuropathic pain and spinal cord microglial activation following peripheral nerve injury. Journal of neuroimmune pharmacology, 8(1), 37-41.
https://doi.org/10.1007/s11481-012-9394-8
Yoon, S.-Y., Patel, D., & Dougherty, P. M. (2012). Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience, 221, 214-224.
https://doi.org/10.1016/j.neuroscience.2012.06.024
Zhao, B. (2009). Natural antioxidants protect neurons in Alzheimer's disease and Parkinson's disease. Neurochemical Research, 34(4), 630-638.
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Copyright (c) 2020 Array