Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals and Reagents
2.2. Preparation of Larrea tridentata (LT) Extracts
2.3. Cell Culture
2.4. Cytotoxicity Assays
2.5. Mitochondrial Membrane Potential (ΔΨm) Assay
2.6. ROS Production Assay
2.7. Annexin V-FITC and Propidium Iodide Staining Assay
2.8. Caspase-3 Activity Analysis
2.9. Western Blot Analysis
2.10. Cell Cycle Analysis
2.11. Statistical Analysis
3. Results
3.1. LT-e/w Extract Protected SH-SY5Y Cells Against H2O2-Induced Cytotoxicity
3.2. Four Fractions From LT-e/w Extract Exhibit Undetected Protective Activity on H2O2-Induced Toxicity on SH-SY5Y Cells
3.3. LT-e/w Extract Reduced The H2O2-Induced Mitochondrial Depolarization
3.4. LT-e/w Extract Attenuates H2O2-Induced Increase of Intracellular ROS Levels
3.5. LT-e/w Extract Interfered With H2O2-Induced Apoptosis In SH-SY5Y Cells
3.6. The LT-e/w Extract Cytoprotective Effect Involves a Decrease of Caspase-3 Activation
3.7. Analysis of the Cell Cycle Profile by Flow Cytometry
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Liu, Z.; Zhou, T.; Ziegler, A.C.; Dimitrion, P.; Zuo, L. Oxidative Stress in Neurodegenerative Diseases: From Molecular Mechanisms to Clinical Applications. Oxid. Med. Cell. Longev. 2017, 2017, 2525967. [Google Scholar] [CrossRef] [PubMed]
- Narayan, M. The Era of Neurodegenerative Metastasis. ACS Chem. Neurosci. 2019, 10, 3346–3348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thanan, R.; Oikawa, S.; Hiraku, Y.; Ohnishi, S.; Ma, N.; Pinlaor, S.; Yongvanit, P.; Kawanishi, S.; Murata, M. Oxidative Stress and Its Significant Roles in Neurodegenerative Diseases and Cancer. Int. J. Mol. Sci. 2015, 16, 193–217. [Google Scholar] [CrossRef] [PubMed]
- Skouta, R. Neuroprotective effect of antioxidant compounds. Neural Regen. Res. 2016, 11, 566–567. [Google Scholar] [CrossRef] [PubMed]
- Kabiraj, P.; Valenzuela, C.A.; Marin, J.E.; Ramirez, D.A.; Mendez, L.; Hwang, M.S.; Varela-Ramirez, A.; Fenelon, K.; Narayan, M.; Skouta, R. The Neuroprotective Role of Ferrostatin-1 Under Rotenone-Induced Oxidative Stress in Dopaminergic Neuroblastoma Cells. Protein J. 2015, 34, 349–358. [Google Scholar] [CrossRef]
- Iriti, M.; Vitalini, S.; Fico, G.; Faoro, F. Neuroprotective Herbs and Foods from Different Traditional Medicines and Diets. Molecules 2010, 15, 3517–3555. [Google Scholar] [CrossRef] [Green Version]
- Durães, F.; Pinto, M.; Sousa, E. Old Drugs as New Treatments for Neurodegenerative Diseases. Pharmaceuticals 2018, 11, 44. [Google Scholar] [CrossRef]
- Khalil, M.F.; Valenzuela, C.; Sisniega, D.; Skouta, R.; Narayan, M. ER Protein Processing Under Oxidative Stress: Implications and Prevention. Cell Biochem. Biophys. 2016, 74, 213–220. [Google Scholar] [CrossRef]
- González-Burgos, E.; Fernandez-Moriano, C.; Gómez-Serranillos, M.P. Potential Neuroprotective Activity of Ginseng in Parkinson’s Disease: A Review. J. Neuroimmune Pharmacol. 2015, 10, 14–29. [Google Scholar] [CrossRef]
- Uddin, S.; Al Mamun, A.; Iqbal, M.A.; Wahid, F.; Rony, R.K. Neuroprotective Activity of Asparagus racemosus Linn. Against Ethanol- Induced Cognitive Impairment and Oxidative Stress in Rats Brain: Auspicious for Controlling the Risk of Alzheimer’s Disease. J. Alzheimers Dis. Parkinsonism 2016, 6, 1–10. [Google Scholar] [CrossRef]
- Mathew, M.; Subramanian, S. In Vitro Screening for Anti-Cholinesterase and Antioxidant Activity of Methanolic Extracts of Ayurvedic Medicinal Plants Used for Cognitive Disorders. PLoS ONE 2014, 9, e86804. [Google Scholar] [CrossRef] [PubMed]
- Shahidi, F.; Ambigaipalan, P. Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects—A review. J. Funct. Foods 2015, 18, 820–897. [Google Scholar] [CrossRef]
- Yi, J.; Qu, H.; Wu, Y.; Wang, Z.; Wang, L. Study on antitumor, antioxidant and immunoregulatory activities of the purified polyphenols from pinecone of Pinus koraiensis on tumor-bearing S180 mice in vivo. Int. J. Biol. Macromol. 2017, 94, 735–744. [Google Scholar] [CrossRef] [PubMed]
- Kou, X.; Han, L.; Li, X.; Xue, Z.; Zhou, F. Antioxidant and antitumor effects and immunomodulatory activities of crude and puri fi ed polyphenol extract from blueberries. Front. Chem. Sci. Eng. 2016, 10, 108–119. [Google Scholar] [CrossRef]
- Morán-Santibañez, K.; Peña-Hernandez, M.A.; Cruz-Suárez, L.E.; Ricque-Marie, D.; Skouta, R.; Vasquez, A.H.; Rodriguez-Padilla, C.; Trejo-Avila, L.M. Virucidal and Synergistic Activity of Polyphenol-Rich Extracts of Seaweeds against Measles Virus. Viruses 2018, 10, 465. [Google Scholar] [CrossRef] [PubMed]
- Genskowsky, E.; Puente, L.A.; Pérez-Álvarez, J.A.; Fernández-López, J.; Muñoz, L.A.; Viuda-Martos, M. Determination of polyphenolic profile, antioxidant activity and antibacterial properties of maqui [Aristotelia chilensi s (Molina) Stuntz] a Chilean blackberry. J. Sci. Food Agric. 2016, 96, 4235–4242. [Google Scholar] [CrossRef] [PubMed]
- Elufioye, T.O.; Berida, T.I.; Habtemariam, S. Plants-Derived Neuroprotective Agents: Cutting the Cycle of Cell Death through Multiple Mechanisms. Evid. Based Complement. Altern. Med. 2017, 2017, 3574012. [Google Scholar] [CrossRef]
- Skouta, R.; Morán-Santibañez, K.; Valenzuela, C.A.; Vasquez, A.H.; Fenelon, K. Assessing the Antioxidant Properties of Larrea tridentata Extract as a Potential Molecular Therapy against Oxidative Stress. Molecules 2018, 23, 1826. [Google Scholar] [CrossRef]
- Bashyal, B.; Li, L.; Bains, T.; Debnath, A.; LaBarbera, D.V. Larrea tridentata: A novel source for anti-parasitic agents active against Entamoeba histolytica, Giardia lamblia and Naegleria fowleri. PLoS Negl. Trop. Dis. 2017, 11, e0005832. [Google Scholar] [CrossRef]
- Gnabre, J.; Bates, R.; Huang, R.C. Creosote bush lignans for human disease treatment and prevention: Perspectives on combination therapy. J. Tradit. Complement. Med. 2015, 5, 119–126. [Google Scholar] [CrossRef] [Green Version]
- Lema, C.; Varela-Ramirez, A.; Aguilera, R.J. Differential nuclear staining assay for high-throughput screening to identify cytotoxic compounds. Curr. Cell. Biochem. 2011, 1, 1–14. [Google Scholar] [PubMed]
- Gutierrez, D.A.; Dejesus, R.E.; Contreras, L.; Monterroza, L.; Larragoity, M.; Varela-ramirez, A.; Aguilera, R.J. A new pyridazinone exhibits potent cytotoxicity on human cancer cells via apoptosis and poly-ubiquitinated protein accumulation. Cell Biol. Toxicol. 2019, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Robles-Escajeda, E.; Das, U.; Ortega, N.M.; Parra, K.; Francia, G.; Dimmock, J.R.; Varela-Ramirez, A.; Aguilera, R.J. A novel curcumin-like dienone induces apoptosis in triple-negative breast cancer cells. Cell. Oncol. 2016, 39, 265–277. [Google Scholar] [CrossRef] [PubMed]
- Solis, L.H.; Ayala, Y.; Portillo, S.; Varela-Ramirez, A.; Aguilera, R.; Boland, T. Thermal inkjet bioprinting triggers the activation of the VEGF pathway in human microvascular endothelial cells in vitro. Biofabrication 2019, 11, 045005. [Google Scholar] [CrossRef] [PubMed]
- Smith, B.; Randle, D.; Mezencev, R.; Thomas, L.; Hinton, C.; Odero-Marah, V. Camalexin-Induced Apoptosis in Prostate Cancer Cells Involves Alterations of Expression and Activity of Lysosomal Protease Cathepsin D. Molecules 2014, 19, 3988–4005. [Google Scholar] [CrossRef] [Green Version]
- Segawa, K.; Nagata, S. An Apoptotic ‘Eat Me’ Signal: Phosphatidylserine Exposure. Trends Cell Biol. 2015, 25, 639–650. [Google Scholar] [CrossRef]
- Villanueva, P.J.; Martinez, A.; Baca, S.T.; Dejesus, R.E.; Larragoity, M.; Contreras, L.; Gutierrez, D.A.; Varela-Ramirez, A.; Aguilera, R.J. Pyronaridine exerts potent cytotoxicity on human breast and hematological cancer cells through induction of apoptosis. PLoS ONE 2018, 13, e0206467. [Google Scholar] [CrossRef]
- Iglesias-Figueroa, B.; Siqueiros-Cendón, T.S.; Gutierrez, D.A.; Aguilera, R.J.; Espinoza-Sánchez, E.A.; Arévalo-Gallegos, S.; Ramirez, A.V.; Rascón-Cruz, Q. Recombinant human lactoferrin induces apoptosis, disruption of F-actin structure and cell cycle arrest with selective cytotoxicity on human triple negative breast cancer cells. Apoptosis 2019, 24, 562–577. [Google Scholar] [CrossRef]
- Kovalevich, J.; Langford, D. Considerations for the Use of SH-SY5Y Neuroblastoma Cells in Neurobiology. In Neuronal Cell Culture: Methods and Protocols; Springer: Berlin/Heidelberg, Germany, 2013; Volume 1078, pp. 9–21. [Google Scholar]
- Veereshman, C. Natural products derived from plants as a source of drugs. J. Adv. Pharm. Technol. Res. 2012, 3, 200–201. [Google Scholar] [CrossRef]
- Arteaga, S.; Andrade-Cetto, A.; Cárdenas, R. Larrea tridentata (Creosote bush), an abundant plant of Mexican and US-American deserts and its metabolite nordihydroguaiaretic acid. J. Ethnopharmacol. 2005, 98, 231–239. [Google Scholar] [CrossRef]
- Kang, S.S.; Lee, J.Y.; Choi, Y.K.; Kim, G.S.; Han, B.H. Neuroprotective effects of flavones on hydrogen peroxide-induced apoptosis in SH-SY5Y neuroblostoma cells. Bioorganic Med. Chem. Lett. 2004, 14, 2261–2264. [Google Scholar] [CrossRef] [PubMed]
- Ismail, N.; Akhtar, M.N.; Ismail, M. Neuroprotective effect from stem bark extracts of Knema laurina against H2O2- and Aβ1-42-induced cell death in human SH-SY5Y cells. Nat. Prod. Res. 2015, 29, 1571–1574. [Google Scholar] [CrossRef] [PubMed]
- Law, B.N.T.; Ling, A.P.; Koh, R.Y.; Chye, S.M.; Wong, Y.P. Neuroprotective effects of orientin on hydrogen peroxide induced apoptosis in SH-SY5Y cells. Mol. Med. Rep. 2014, 9, 947–954. [Google Scholar] [CrossRef] [PubMed]
- Ruiz-Medina, B.E.; Lerma, D.; Hwang, M.; Ross, J.; Skouta, R.; Aguilera, R.J.; Kirken, R.A.; Varela-Ramirez, A.; Robles-Escajeda, E. Green barley mitigates cytotoxicity in human lymphocytes undergoing aggressive oxidative stress, via activation of both the Lyn/PI3K/Akt and MAPK/ERK pathways. Sci. Rep. 2019, 9, 6005. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Zhao, B.; Yew, D.T.; Kusiak, J.W.; Roth, G.S. Processing of Alzheimer’s Amyloid Precursor Protein during H2O2-Induced Apoptosis in Human Neuronal Cells. Biochem. Biophys. Res. Commun. 1997, 235, 845–848. [Google Scholar] [CrossRef] [PubMed]
- Clément, M.-V.; Ponton, A.; Pervaiz, S. Apoptosis induced by hydrogen peroxide is mediated by decreased superoxide anion concentration and reduction of intracellular milieu. FEBS Lett. 1998, 440, 13–18. [Google Scholar] [CrossRef] [Green Version]
- Ruffels, J.; Griffin, M.; Dickenson, J.M. Activation of ERK1/2, JNK and PKB by hydrogen peroxide in human SH-SY5Y neuroblastoma cells: Role of ERK1/2 in H2O2-induced cell death. Eur. J. Pharmacol. 2004, 483, 163–173. [Google Scholar] [CrossRef]
- Sun, G.; Guzman, E.; Balasanyan, V.; Conner, C.M.; Wong, K.; Zhou, H.R.; Kosik, K.S.; Montell, D.J. A molecular signature for anastasis, recovery from the brink of apoptotic cell death. J. Cell Biol. 2017, 216, 3355–3368. [Google Scholar] [CrossRef] [Green Version]
- Li, P.; Li, Z. Neuroprotective effect of paeoniflorin on H2O2-induced apoptosis in PC12 cells by modulation of reactive oxygen species and the inflammatory response. Exp. Ther. Med. 2015, 9, 1768–1772. [Google Scholar] [CrossRef]
- Alvariño, R.; Alonso, E.; Tribalat, M.; Gegunde, S.; Thomas, O.P.; Botana, L.M. Evaluation of the Protective Effects of Sarains on H2O2-Induced Mitochondrial Dysfunction and Oxidative Stress in SH-SY5Y Neuroblastoma Cells. Neurotox. Res. 2017, 32, 368–380. [Google Scholar] [CrossRef]
- Steele, M.L.; Truong, J.; Govindaraghavan, S.; Ooi, L.; Sucher, N.J.; Münch, G. Neurochemistry International Cytoprotective properties of traditional Chinese medicinal herbal extracts in hydrogen peroxide challenged human U373 astroglia cells. Neurochem. Int. 2013, 62, 522–529. [Google Scholar] [CrossRef] [PubMed]
- Liu, R.H. Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals 1–4. Am. J. Clin. Nutr. 2003, 78, 3–6. [Google Scholar] [CrossRef] [PubMed]
- Eberhardt, M.; Lee, C.Y.; Liu, R.H. Antioxidant activity of fresh apples. Nature 2000, 405, 903–904. [Google Scholar] [CrossRef] [PubMed]
- Seeram Navindra, P.; Adams, L.S.; Hardy, M.L.; Heber, D. Total Cranberry Extract versus its Phytochemical Constituents: Antiproliferative and Synergistic Effects against Human Tumor. J. Agric. Food Chem. 2004, 52, 2512–2517. [Google Scholar] [CrossRef]
- Ryter, S.W.; Kim, H.P.; Hoetzel, A.; Park, J.W.; Nakahira, K.; Wang, X.; Choi, A.M. Mechanisms of Cell Death in Oxidative Stress. Antioxid. Redox Signal. 2007, 9, 50–89. [Google Scholar] [CrossRef]
- Park, S.-E.; Kim, S.; Sapkota, K.; Kim, S.-J. Neuroprotective Effect of Rosmarinus officinalis Extract on Human Dopaminergic Cell line, SH-SY5Y. Cell. Mol. Neurobiol. 2010, 30, 759–767. [Google Scholar] [CrossRef]
- Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol. 2015, 4, 180–183. [Google Scholar] [CrossRef]
- Satoh, T.; Numakawa, T.; Abiru, Y.; Yamagata, T.; Ishikawa, Y.; Enokido, Y.; Hatanaka, H. Production of Reactive Oxygen Species and Release of L-Glutamate During Superoxide Anion-Induced Cell Death of Cerebellar Granule Neurons. J. Neurochem. 1998, 70, 316–324. [Google Scholar] [CrossRef]
- Li, H.; Zhu, H.; Xu, C.; Yuan, J. Cleavage of BID by Caspase 8 Mediates the Mitochondrial Damage in the Fas Pathway of Apoptosis. Cell 1998, 94, 491–501. [Google Scholar] [CrossRef] [Green Version]
- Robles-Escajeda, E.; Lerma, D.; Nyakeriga, A.M.; Ross, J.A.; Kirken, R.A.; Aguilera, R.J.; Varela-Ramirez, A. Searching in Mother Nature for Anti-Cancer Activity: Anti-Proliferative and Pro-Apoptotic Effect Elicited by Green Barley on Leukemia/Lymphoma Cells. PLoS ONE 2013, 8, e73508. [Google Scholar]
- Santiago-Vázquez, Y.; Das, U.; Varela-Ramirez, A.; Baca, S.T.; Ayala-marin, Y.; Lema, C.; Das, S.; Baryyan, A.; Jonathan, R.; Aguilera, R.J. Tumor-selective cytotoxicity of a novel pentadiene analogue on human leukemia/lymphoma cells. Clin. Cancer Drugs 2016, 3, 138–146. [Google Scholar] [CrossRef] [PubMed]
- Nunes, L.M.; Hossain, M.; Ramirez, A.V.; Das, U.; Marin, Y.M.A.; Dimmock, J.R.; Aguilera, R.J. A novel class of piperidones exhibit potent, selective and pro-apoptotic anti-leukemia properties. Oncol. Lett. 2016, 11, 3842–3848. [Google Scholar] [CrossRef] [PubMed]
- Contreras, L.; Calderon, R.I.; Varela-Ramirez, A.; Zhang, H.-Y.; Quan, Y.; Das, U.; Dimmock, J.R.; Skouta, R.; Aguilera, R.J. Induction of apoptosis via proteasome inhibition in leukemia/lymphoma cells by two potent piperidones. Cell. Oncol. 2018, 41, 623–636. [Google Scholar] [CrossRef] [PubMed]
- Scola, G.; Louise, V.; Laliberte, M.; Kyunghee, H.; Pinguelo, A.; Salvador, M.; Young, L.T.; Cristina, A. Neurochemistry International Vitis labrusca extract effects on cellular dynamics and redox modulations in a SH-SY5Y neuronal cell model: A similar role to lithium. Neurochem. Int. 2014, 79, 12–19. [Google Scholar] [CrossRef] [PubMed]
- Sajjad, N.; Wani, A.; Sharma, A.; Ali, R.; Hassan, S.; Hamid, R. Artemisia amygdalina Upregulates Nrf2 and Protects Neurons Against Oxidative Stress in Alzheimer Disease. Cell. Mol. Neurobiol. 2019, 39, 387–399. [Google Scholar] [CrossRef] [PubMed]
- Nuzzo, D.; Presti, G.; Picone, P.; Galizzi, G.; Gulotta, E.; Giuliano, S.; Mannino, C.; Gambino, V.; Scoglio, S.; Di Carlo, M.; et al. Effects of the Aphanizomenon flos-aquae Extract (Klamin®) on a Neurodegeneration Cellular Model. Oxid. Med. Cell. Longev. 2018, 2018, 9089016. [Google Scholar] [CrossRef] [PubMed]
- Eron, S.J.; Raghupathi, K.; Hardy, J.A.; Eron, S.J.; Raghupathi, K.; Hardy, J.A. Dual Site Phosphorylation of Caspase-7 by PAK2 Blocks Apoptotic Activity by Two Distinct Mechanisms. Structure 2017, 25, 27–39. [Google Scholar] [CrossRef] [PubMed]
- Solary, E.; Droin, N.; Bettaieb, A.; Corcos, L.; Garrido, C. Positive and negative regulation of apoptotic pathways by cytotoxic agents in hematological malignancies. Leukemia 2000, 12, 1833–1849. [Google Scholar] [CrossRef]
- Ibrahim, A.; Negida, A.; Ahmed, H.; Abdel-daim, M.M. Neuroprotective mechanisms of plant extracts against MPTP induced neurotoxicity: Future applications in Parkinson’s disease. Biomed. Pharmacother. 2017, 85, 635–645. [Google Scholar]
- De Bruin, E.C.; Meersma, D.; De Wilde, J.; den Otter, I. A serine protease is involved in the initiation of DNA damage-induced apoptosis. Cell Death Differ. 2003, 10, 1204–1212. [Google Scholar] [CrossRef]
- Duriez, P.J.; Shah, G.M. Cleavage of poly (ADP-ribose) polymerase: A sensitive parameter to study cell death. Biochem. Cell Biol. 1997, 75, 337–349. [Google Scholar] [CrossRef] [PubMed]
- Ko, H.L.; Ren, E.C. Functional Aspects of PARP1 in DNA Repair and Transcription. Biomolecules 2012, 2, 524–548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaitanya, G.V.; Alexander, J.S.; Babu, P.P. PARP-1 cleavage fragments: Signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal. 2010, 8, 31. [Google Scholar] [CrossRef] [PubMed]
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Morán-Santibañez, K.; Vasquez, A.H.; Varela-Ramirez, A.; Henderson, V.; Sweeney, J.; Odero-Marah, V.; Fenelon, K.; Skouta, R. Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells. Antioxidants 2019, 8, 427. https://doi.org/10.3390/antiox8100427
Morán-Santibañez K, Vasquez AH, Varela-Ramirez A, Henderson V, Sweeney J, Odero-Marah V, Fenelon K, Skouta R. Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells. Antioxidants. 2019; 8(10):427. https://doi.org/10.3390/antiox8100427
Chicago/Turabian StyleMorán-Santibañez, Karla, Abimael H. Vasquez, Armando Varela-Ramirez, Veronica Henderson, Janae Sweeney, Valerie Odero-Marah, Karine Fenelon, and Rachid Skouta. 2019. "Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells" Antioxidants 8, no. 10: 427. https://doi.org/10.3390/antiox8100427
APA StyleMorán-Santibañez, K., Vasquez, A. H., Varela-Ramirez, A., Henderson, V., Sweeney, J., Odero-Marah, V., Fenelon, K., & Skouta, R. (2019). Larrea tridentata Extract Mitigates Oxidative Stress-Induced Cytotoxicity in Human Neuroblastoma SH-SY5Y Cells. Antioxidants, 8(10), 427. https://doi.org/10.3390/antiox8100427