Broccoli Cultivated with Deep Sea Water Mineral Fertilizer Enhances Anti-Cancer and Anti-Inflammatory Effects of AOM/DSS-Induced Colorectal Cancer in C57BL/6N Mice
Abstract
:1. Introduction
2. Results
2.1. Antioxidant Capacities and Mineral Analysis of Broccoli Samples
2.2. Mouse Body and Organ Weight, Colon Length, Number of Tumors, and Colon Weight/Length Ratio
2.3. Morphological Changes in the Mice Colon and Spleen Tissues
2.4. Levels of Inflammation-Related Cytokines Secreted by Mice Blood Serum
2.5. Levels of Inflammation-Related Cytokines Secreted by Mice Splenocytes
2.6. Effect of Broccoli on NK Cell Activity in Mice Splenocytes
2.7. Effects of the Samples on the mRNA and Protein Expression of Inflammation-Related Genes in Mice Liver Tissue
2.8. Effects of the Samples on the mRNA and Protein Expression of Apoptosis-Related Genes in Mice Colon Tissue
2.9. Metabolomics Analysis and PLS-DA Score Plot
3. Discussion
4. Materials and Methods
4.1. Broccoli Preparation
4.2. Animal Experiment Design
4.3. Assessment of the 2,2-Diphenyl-1-picrylhydrazyl (DPPH) Inhibition Rate in Broccoli
4.4. Assessment of the Total Phenolic (TP) Content
4.5. Assessment of the Total Flavonoid (TF) Content
4.6. Sample Collection
4.7. Histopathological Studies
4.8. Measurement of Inflammatory Cytokines Using Enzyme-Linked Immunosorbent Assay (ELISA)
4.9. Quantitative Reverse Transcription Polymerase Chain Reaction (qRT-PCR)
4.10. Western Blotting
4.11. Measurement of Natural Killer Cell Activity
4.12. Metabolomic Analysis and Multivariate Statistical Analysis
4.13. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ilahy, R.; Tlili, I.; Pek, Z.; Montefusco, A.; Siddiqui, M.W.; Homa, F.; Hdider, C.; R’Him, T.; Lajos, H.; Lenucci, M.S. Pre- and Post-harvest Factors Affecting Glucosinolate Content in Broccoli. Front. Nutr. 2020, 7, 147. [Google Scholar] [CrossRef]
- Li, Z.; Zheng, S.; Liu, Y.; Fang, Z.; Yang, L.; Zhuang, M.; Zhang, Y.; Lv, H.; Wang, Y.; Xu, D. Characterization of glucosinolates in 80 broccoli genotypes and different organs using UHPLC-Triple-TOF-MS method. Food Chem. 2021, 334, 127519. [Google Scholar] [CrossRef] [PubMed]
- Thomas, M.; Badr, A.; Desjardins, Y.; Gosselin, A.; Angers, P. Characterization of industrial broccoli discards (Brassica oleracea var. italica) for their glucosinolate, polyphenol and flavonoid contents using UPLC MS/MS and spectrophotometric methods. Food Chem. 2018, 245, 1204–1211. [Google Scholar] [CrossRef]
- Hwang, J.H.; Lim, S.B. Antioxidant and anticancer activities of broccoli by-products from different cultivars and maturity stages at harvest. Prev. Nutr. Food Sci. 2015, 20, 8–14. [Google Scholar] [CrossRef] [PubMed]
- Borowski, J.; Szajdek, A.; Borowska, E.J.; Ciska, E.; Zieliński, H. Content of selected bioactive components and antioxidant properties of broccoli (Brassica oleracea L.). Eur. Food Res. Technol. 2007, 226, 459–465. [Google Scholar] [CrossRef]
- Gu, H.F.; Mao, X.Y.; Du, M. Metabolism, absorption, and anti-cancer effects of sulforaphane: An update. Crit. Rev. Food Sci. Nutr. 2022, 62, 3437–3452. [Google Scholar] [CrossRef]
- Roberts, D.P.; Mattoo, A.K. Sustainable Crop Production Systems and Human Nutrition. Front. Sustain. Food Syst. 2019, 3, 72. [Google Scholar] [CrossRef]
- El-Ramady, H.; Hajdú, P.; Törős, G.; Badgar, K.; Llanaj, X.; Kiss, A.; Abdalla, N.; Omara, A.E.-D.; Elsakhawy, T.; Elbasiouny, H.; et al. Plant Nutrition for Human Health: A Pictorial Review on Plant Bioactive Compounds for Sustainable Agriculture. Sustainability 2022, 14, 8329. [Google Scholar] [CrossRef]
- Marles, R.J. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. J. Food Compost. Anal. 2017, 56, 93–103. [Google Scholar] [CrossRef]
- Shrivastava, P.; Kumar, R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 2015, 22, 123–131. [Google Scholar] [CrossRef]
- Rahman, K.; Zhang, D. Effects of Fertilizer Broadcasting on the Excessive Use of Inorganic Fertilizers and Environmental Sustainability. Sustainability 2018, 10, 759. [Google Scholar] [CrossRef]
- Lee, Y.-J.; Pan, Y.; Park, S.-H.; Sin, S.-I.; Park, K.-Y. Anticancer Effects in HT-29 Cells and Anti-Inflammatory Effects on Mouse Splenocytes of Broccoli Cultivated with Deep Sea Water Minerals in Organic Farming. Appl. Sci. 2023, 13, 9684. [Google Scholar] [CrossRef]
- Shawki, S.; Ashburn, J.; Signs, S.A.; Huang, E. Colon Cancer: Inflammation-Associated Cancer. Surg. Oncol. Clin. N. Am. 2018, 27, 269–287. [Google Scholar] [CrossRef] [PubMed]
- Lin, R.; Piao, M.; Song, Y.; Liu, C. Quercetin Suppresses AOM/DSS-Induced Colon Carcinogenesis through Its Anti-Inflammation Effects in Mice. J. Immunol. Res. 2020, 2020, 9242601. [Google Scholar] [CrossRef]
- Westbrook, A.M.; Szakmary, A.; Schiestl, R.H. Mechanisms of intestinal inflammation and development of associated cancers: Lessons learned from mouse models. Mutat. Res. 2010, 705, 40–59. [Google Scholar] [CrossRef]
- Wijnands, A.M.; Mahmoud, R.; Lutgens, M.; Oldenburg, B. Surveillance and man-agement of colorectal dysplasia and cancer in inflammatory bowel disease: Current practice and future perspectives. Eur. J. Intern. Med. 2021, 93, 35–41. [Google Scholar] [CrossRef]
- Briede, I.; Balodis, D.; Gardovskis, J.; Strumfa, I. Stemness, Inflammation and Epithelial–Mesenchymal Transition in Colorectal Carcinoma: The Intricate Network. Int. J. Mol. Sci. 2021, 22, 12891. [Google Scholar] [CrossRef]
- Zhang, D.; Bi, J.; Liang, Q.; Wang, S.; Zhang, L.; Han, F.; Li, S.; Qiu, B.; Fan, X.; Chen, W.; et al. VCAM1 Promotes Tumor Cell Invasion and Metastasis by Inducing EMT and Transendothelial Migration in Colorectal Cancer. Front. Oncol. 2020, 10, 1066. [Google Scholar] [CrossRef]
- Rubin, D.C.; Shaker, A.; Levin, M.S. Chronic intestinal inflammation: Inflammatory bowel disease and colitis-associated colon cancer. Front. Immunol. 2012, 3, 107. [Google Scholar] [CrossRef] [PubMed]
- Xi, Y.; Xu, P. Global colorectal cancer burden in 2020 and projections to 2040. Transl. Oncol. 2021, 14, 101174. [Google Scholar] [CrossRef] [PubMed]
- Leystra, A.A.; Clapper, M.L. Gut Microbiota Influences Experimental Outcomes in Mouse Models of Colorectal Cancer. Genes 2019, 10, 900. [Google Scholar] [CrossRef]
- Li, Q.; Chen, C.; Liu, C.; Sun, W.; Liu, X.; Ci, Y.; Song, Y. The Effects of Cellulose on AOM/DSS-Treated C57BL/6 Colorectal Cancer Mice by Changing Intestinal Flora Composition and Inflammatory Factors. Nutr. Cancer 2021, 73, 502–513. [Google Scholar] [CrossRef]
- Wu, M.; Li, J.; An, Y.; Li, P.; Xiong, W.; Li, J.; Yan, D.; Wang, M.; Zhong, G. Chitooligosaccharides Prevents the Development of Colitis-Associated Colorectal Cancer by Modulating the Intestinal Microbiota and Mycobiota. Front. Microbiol. 2019, 10, 2101. [Google Scholar] [CrossRef] [PubMed]
- Wu, R.; Wang, L.; Yin, R.; Hudlikar, R.; Li, S.; Kuo, H.D.; Peter, R.; Sargsyan, D.; Guo, Y.; Liu, X.; et al. Epigenetics/epigenomics and prevention by curcumin of early stages of inflammatory-driven colon cancer. Mol. Carcinog. 2020, 59, 227–236. [Google Scholar] [CrossRef] [PubMed]
- Janakiram, N.B.; Rao, C.V. The role of inflammation in colon cancer. Adv. Exp. Med. Biol. 2014, 816, 25–52. [Google Scholar] [CrossRef] [PubMed]
- Ju, J.; Song, J.L.; Park, E.S.; Do, M.S.; Park, K.Y. Korean solar salts reduce obesity and alter its related markers in diet-induced obese mice. Nutr. Res. Pract. 2016, 10, 629–634. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Lau, H.C.; Zhang, X.; Yu, J. Mouse Models for Application in Colorectal Cancer: Understanding the Pathogenesis and Relevance to the Human Condition. Biomedicines 2022, 10, 1710. [Google Scholar] [CrossRef]
- Gommeaux, J.; Cano, C.; Garcia, S.; Gironella, M.; Pietri, S.; Culcasi, M.; Pebusque, M.J.; Malissen, B.; Dusetti, N.; Iovanna, J.; et al. Colitis and colitis-associated cancer are exacerbated in mice deficient for tumor protein 53-induced nuclear protein 1. Mol. Cell Biol. 2007, 27, 2215–2228. [Google Scholar] [CrossRef] [PubMed]
- Latte, K.P.; Appel, K.E.; Lampen, A. Health benefits and possible risks of broccoli—An overview. Food Chem. Toxicol. 2011, 49, 3287–3309. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Tan, L.; Li, C.; Wu, H.; Ran, D.; Zhang, Z. Sulforaphane alter the microbiota and mitigate colitis severity on mice ulcerative colitis induced by DSS. AMB Express 2020, 10, 119. [Google Scholar] [CrossRef] [PubMed]
- Bessler, H.; Djaldetti, M. Broccoli and human health: Immunomodulatory effect of sulforaphane in a model of colon cancer. Int. J. Food Sci. Nutr. 2018, 69, 946–953. [Google Scholar] [CrossRef] [PubMed]
- De Robertis, M.; Massi, E.; Poeta, M.L.; Carotti, S.; Morini, S.; Cecchetelli, L.; Signori, E.; Fazio, V.M. The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies. J. Carcinog. 2011, 10, 9. [Google Scholar] [CrossRef]
- Xie, Y.; Shao, F.; Duan, X.; Ding, J.; Ning, Y.; Sun, X.; Xia, L.; Pan, J.; Chen, J.; He, S.; et al. Whole beta-glucan particle attenuates AOM/DSS-induced colorectal tumorigenesis in mice via inhibition of intestinal inflammation. Front. Pharmacol. 2023, 14, 1017475. [Google Scholar] [CrossRef]
- Parkins, K.M.; Dubois, V.P.; Hamilton, A.M.; Makela, A.V.; Ronald, J.A.; Foster, P.J. Multimodality cellular and molecular imaging of concomitant tumour enhancement in a syngeneic mouse model of breast cancer metastasis. Sci. Rep. 2018, 8, 8930. [Google Scholar] [CrossRef]
- Kim, E.R.; Chang, D.K. Colorectal cancer in inflammatory bowel disease: The risk, pathogenesis, prevention and diagnosis. World J. Gastroenterol. 2014, 20, 9872–9881. [Google Scholar] [CrossRef] [PubMed]
- Fantini, M.C.; Guadagni, I. From inflammation to colitis-associated colorectal cancer in inflammatory bowel disease: Pathogenesis and impact of current therapies. Dig. Liver Dis. 2021, 53, 558–565. [Google Scholar] [CrossRef] [PubMed]
- Janelle, C.A.; Christian, J. The struggle within: Microbial influences on colorectal cancer. Inflamm. Bowel Dis. 2011, 17, 396–409. [Google Scholar]
- Feagins, L.A. Role of transforming growth factor-beta in inflammatory bowel disease and colitis-associated colon cancer. Inflamm. Bowel Dis. 2010, 16, 1963–1968. [Google Scholar] [CrossRef]
- Grivennikov, S.I.; Karin, M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor. Rev. 2010, 21, 11–19. [Google Scholar] [CrossRef]
- Moriasi, C.; Subramaniam, D.; Awasthi, S.; Ramalingam, S.; Anant, S. Prevention of colitis-associated cancer: Natural compounds that target the IL-6 soluble receptor. Anticancer Agents Med. Chem. 2012, 12, 1221–1238. [Google Scholar] [CrossRef]
- Luo, J.L.; Maeda, S.; Hsu, L.C.; Yagita, H.; Karin, M. Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 2004, 6, 297–305. [Google Scholar] [CrossRef]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.C. NF-kappaB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef]
- Luo, C.; Zhang, H. The Role of Proinflammatory Pathways in the Pathogenesis of Colitis-Associated Colorectal Cancer. Mediat. Inflamm. 2017, 2017, 5126048. [Google Scholar] [CrossRef]
- Ji, S.Y.; Cha, H.J.; Molagoda, I.M.N.; Kim, M.Y.; Kim, S.Y.; Hwangbo, H.; Lee, H.; Kim, G.Y.; Kim, D.H.; Hyun, J.W.; et al. Suppression of Lipopolysaccharide-Induced Inflammatory and Oxidative Response by 5-Aminolevulinic Acid in RAW 264.7 Macrophages and Zebrafish Larvae. Biomol. Ther. 2021, 29, 685–696. [Google Scholar] [CrossRef] [PubMed]
- Wallace, J.L. Nitric oxide in the gastrointestinal tract: Opportunities for drug development. Br. J. Pharmacol. 2019, 176, 147–154. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, K.; Han, G.C.; Wang, R.X.; Xiao, H.; Hou, C.M.; Guo, R.F.; Dou, Y.; Shen, B.F.; Li, Y.; et al. Neutrophil infiltration favors colitis-associated tumorigenesis by activating the interleukin-1 (IL-1)/IL-6 axis. Mucosal Immunol. 2014, 7, 1106–1115. [Google Scholar] [CrossRef]
- Hamilton, K.E.; Simmons, J.G.; Ding, S.; Van Landeghem, L.; Lund, P.K. Cytokine induction of tumor necrosis factor receptor 2 is mediated by STAT3 in colon cancer cells. Mol. Cancer Res. 2011, 9, 1718–1731. [Google Scholar] [CrossRef] [PubMed]
- Nagasaki, T.; Hara, M.; Nakanishi, H.; Takahashi, H.; Sato, M.; Takeyama, H. Interleukin-6 released by colon cancer-associated fibroblasts is critical for tumour angiogenesis: Anti-interleukin-6 receptor antibody suppressed angiogenesis and inhibited tumour-stroma interaction. Br. J. Cancer 2014, 110, 469–478. [Google Scholar] [CrossRef]
- Alkhayyat, M.; Abureesh, M.; Gill, A.; Khoudari, G.; Abou Saleh, M.; Mansoor, E.; Regueiro, M. Lower Rates of Colorectal Cancer in Patients With Inflammatory Bowel Disease Using Anti-TNF Therapy. Inflamm. Bowel Dis. 2021, 27, 1052–1060. [Google Scholar] [CrossRef] [PubMed]
- Zheng, H.; Ban, Y.; Wei, F.; Ma, X. Regulation of Interleukin-12 Production in Antigen-Presenting Cells. Adv. Exp. Med. Biol. 2016, 941, 117–138. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Wang, B.; Yuan, X.; Lu, Y.; Hu, J.; Gao, J.; Lin, J.; Liang, J.; Hou, S.; Chen, S. Vitexin prevents colitis-associated carcinogenesis in mice through regulating macrophage polarization. Phytomedicine 2021, 83, 153489. [Google Scholar] [CrossRef]
- Al-Falahi, M.N.; Al-Dulaimi, K.H.; Ghani, E.T.A.; Al-Taey, D.K.; Farhan, K.J. Effect of humic acids and the amount of mineral fertilizer on some characteristics of saline soil, growth and yield of broccoli plant under salt stress conditions. J. Agric. Sci. 2022, 33, 11–20. [Google Scholar] [CrossRef]
- Torres, J.L.R.; da Cunha Gomes, F.R.; Barreto, A.C.; Tamburus, A.Y.; da Silva Vieira, D.M.; de Souza, Z.M.; Mazetto, J.C. Application of different cover crops and mineral fertilizer doses for no-till cultivation of broccoli, cauliflower and cabbage. Aust. J. Crop Sci. 2017, 11, 1339–1345. [Google Scholar] [CrossRef]
- ŠLosÁR, M.; Uher, A.; AndrejiovÁ, A.; JurÍKovÁ, T. Selected yield and qualitative parameters of broccoli in dependence on nitrogen, sulfur, and zinc fertilization. Turk. J. Agricul. For. 2016, 40, 465–473. [Google Scholar] [CrossRef]
- Ferguson, L.R.; Schlothauer, R.C. The potential role of nutritional genomics tools in validating high health foods for cancer control: Broccoli as example. Mol. Nutr. Food Res. 2012, 56, 126–146. [Google Scholar] [CrossRef] [PubMed]
- Jeffery, E.H.; Araya, M. Physiological effects of broccoli consumption. Phytochem. Rev. 2008, 8, 283–298. [Google Scholar] [CrossRef]
- Higdon, J.V.; Delage, B.; Williams, D.E.; Dashwood, R.H. Cruciferous vegetables and human cancer risk: Epidemiologic evidence and mechanistic basis. Pharmacol. Res. 2007, 55, 224–236. [Google Scholar] [CrossRef] [PubMed]
- Swaminathan, H.; Saravanamurali, K.; Yadav, S.A. Extensive review on breast cancer its etiology, progression, prognostic markers, and treatment. Med. Oncol. 2023, 40, 238. [Google Scholar] [CrossRef] [PubMed]
- Feitelson, M.A.; Arzumanyan, A.; Kulathinal, R.J.; Blain, S.W.; Holcombe, R.F.; Mahajna, J.; Marino, M.; Martinez-Chantar, M.L.; Nawroth, R.; Sanchez-Garcia, I.; et al. Sustained proliferation in cancer: Mechanisms and novel therapeutic targets. Semin. Cancer Biol. 2015, 35, S25–S54. [Google Scholar] [CrossRef] [PubMed]
- Pistritto, G.; Trisciuoglio, D.; Ceci, C.; Garufi, A.; D’Orazi, G. Apoptosis as anticancer mechanism: Function and dysfunction of its modulators and targeted therapeutic strategies. Aging 2016, 8, 603–619. [Google Scholar] [CrossRef]
- Chen, J. The Cell-Cycle Arrest and Apoptotic Functions of p53 in Tumor Initiation and Progression. Cold Spring Harb. Perspect. Med. 2016, 6, a026104. [Google Scholar] [CrossRef]
- Engeland, K. Cell cycle regulation: p53-p21-RB signaling. Cell Death Differ. 2022, 29, 946–960. [Google Scholar] [CrossRef]
- Bajwa, N.; Liao, C.; Nikolovska-Coleska, Z. Inhibitors of the anti-apoptotic Bcl-2 proteins: A patent review. Expert Opin. Ther. Pat. 2012, 22, 37–55. [Google Scholar] [CrossRef] [PubMed]
- Chota, A.; George, B.P.; Abrahamse, H. Interactions of multidomain pro-apoptotic and anti-apoptotic proteins in cancer cell death. Oncotarget 2021, 12, 1615–1626. [Google Scholar] [CrossRef] [PubMed]
- Zheng, C.; Liu, T.; Liu, H.; Wang, J. Role of BCL-2 Family Proteins in Apoptosis and its Regulation by Nutrients. Curr. Protein Pept. Sci. 2020, 21, 799–806. [Google Scholar] [CrossRef] [PubMed]
- Shukla, S.; Saxena, S.; Singh, B.K.; Kakkar, P. BH3-only protein BIM: An emerging target in chemotherapy. Eur. J. Cell Biol. 2017, 96, 728–738. [Google Scholar] [CrossRef] [PubMed]
- Modi, V.; Sankararamakrishnan, R. Binding affinity of pro-apoptotic BH3 peptides for the anti-apoptotic Mcl-1 and A1 proteins: Molecular dynamics simulations of Mcl-1 and A1 in complex with six different BH3 peptides. J. Mol. Graph. Model. 2017, 73, 115–128. [Google Scholar] [CrossRef] [PubMed]
- Osford, S.M.; Dallman, C.L.; Johnson, P.W.; Ganesan, A.; Packham, G. Current strategies to target the anti-apoptotic Bcl-2 protein in cancer cells. Curr. Med. Chem. 2004, 11, 1031–1039. [Google Scholar] [CrossRef]
- Wolf, P.; Schoeniger, A.; Edlich, F. Pro-apoptotic complexes of BAX and BAK on the outer mitochondrial membrane. Biochim. Biophys. Acta Mol. Cell Res. 2022, 1869, 119317. [Google Scholar] [CrossRef]
- Gogvadze, V.; Orrenius, S.; Zhivotovsky, B. Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim. Biophys. Acta 2006, 1757, 639–647. [Google Scholar] [CrossRef]
- Dadsena, S.; Zollo, C.; García-Sáez, A.J. Mechanisms of mitochondrial cell death. Biochem. Soc. Trans. 2021, 49, 663–674. [Google Scholar] [CrossRef]
- Vo, P.H.T.; Nguyen, T.D.T.; Tran, H.T.; Nguyen, Y.N.; Doan, M.T.; Nguyen, P.H.; Lien, G.T.K.; To, D.C.; Tran, M.H. Cytotoxic components from the leaves of Erythrophleum fordii induce human acute leukemia cell apoptosis through caspase 3 activation and PARP cleavage. Bioorg. Med. Chem. Lett. 2021, 31, 127673. [Google Scholar] [CrossRef]
- Dirican, E.; Ozcan, H.; Karabulut Uzuncakmak, S.; Takim, U. Evaluation Expression of the Caspase-3 and Caspase-9 Apoptotic Genes in Schizophrenia Patients. Clin. Psychopharmacol. Neurosci. 2023, 21, 171–178. [Google Scholar] [CrossRef]
- Jiang, M.; Qi, L.; Li, L.; Li, Y. The caspase-3/GSDME signal pathway as a switch between apoptosis and pyroptosis in cancer. Cell Death Discov. 2020, 6, 112. [Google Scholar] [CrossRef]
- Herr, I.; Buchler, M.W. Dietary constituents of broccoli and other cruciferous vegetables: Implications for prevention and therapy of cancer. Cancer Treat. Rev. 2010, 36, 377–383. [Google Scholar] [CrossRef] [PubMed]
- Tang, L.; Zhang, Y.; Jobson, H.E.; Li, J.; Stephenson, K.K.; Wade, K.L.; Fahey, J.W. Potent activation of mitochondria-mediated apoptosis and arrest in S and M phases of cancer cells by a broccoli sprout extract. Mol. Cancer Ther. 2006, 5, 935–944. [Google Scholar] [CrossRef] [PubMed]
- Zeng, W.; Yang, J.; Yan, G.; Zhu, Z. CaSO(4) Increases Yield and Alters the Nutritional Contents in Broccoli (Brassica oleracea L. Var. italica) Microgreens under NaCl Stress. Foods 2022, 11, 3485. [Google Scholar] [CrossRef] [PubMed]
- Dave, A.; Graham, I.A. Oxylipin Signaling: A Distinct Role for the Jasmonic Acid Precursor cis-(+)-12-Oxo-Phytodienoic Acid (cis-OPDA). Front. Plant Sci. 2012, 3, 42. [Google Scholar] [CrossRef] [PubMed]
- Guo, H.M.; Li, H.C.; Zhou, S.R.; Xue, H.W.; Miao, X.X. Cis-12-oxo-phytodienoic acid stimulates rice defense response to a piercing-sucking insect. Mol. Plant 2014, 7, 1683–1692. [Google Scholar] [CrossRef] [PubMed]
- Savchenko, T.; Kolla, V.A.; Wang, C.Q.; Nasafi, Z.; Hicks, D.R.; Phadungchob, B.; Chehab, W.E.; Brandizzi, F.; Froehlich, J.; Dehesh, K. Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol. 2014, 164, 1151–1160. [Google Scholar] [CrossRef] [PubMed]
- Taki-Nakano, N.; Ohzeki, H.; Kotera, J.; Ohta, H. Cytoprotective effects of 12-oxo phytodienoic acid, a plant-derived oxylipin jasmonate, on oxidative stress-induced toxicity in human neuroblastoma SH-SY5Y cells. Biochim. Biophys. Acta 2014, 1840, 3413–3422. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez-Bosch, C. Priming plant resistance by activation of redox-sensitive genes. Free Radic. Biol. Med. 2018, 122, 171–180. [Google Scholar] [CrossRef] [PubMed]
- Vicedo, B.; Flors, V.; de la, O.L.M.; Finiti, I.; Kravchuk, Z.; Real, M.D.; Garcia-Agustin, P.; Gonzalez-Bosch, C. Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol. Plant Microbe Interact. 2009, 22, 1455–1465. [Google Scholar] [CrossRef]
- Saidhareddy, P.; Ajay, S.; Shaw, A.K. ‘Chiron’ approach to the total synthesis of macrolide (+)-Aspicilin. RSC Adv. 2014, 4, 4253–4259. [Google Scholar] [CrossRef]
- Pant, R.; Joshi, A.; Joshi, T.; Maiti, P.; Nand, M.; Joshi, T.; Pande, V.; Chandra, S. Identification of potent Antigen 85C inhibitors of Mycobacterium tuberculosis via in-house lichen library and binding free energy studies Part-II. J. Mol. Graph. Model. 2021, 103, 107822. [Google Scholar] [CrossRef]
- Martins, T.; Oliveira, P.A.; Pires, M.J.; Neuparth, M.J.; Lanzarin, G.; Felix, L.; Venancio, C.; Pinto, M.L.; Ferreira, J.; Gaivao, I.; et al. Effect of a Sub-Chronic Oral Exposure of Broccoli (Brassica oleracea L. Var. Italica) By-Products Flour on the Physiological Parameters of FVB/N Mice: A Pilot Study. Foods 2022, 11, 120. [Google Scholar] [CrossRef]
- Nair, A.B.; Jacob, S. A simple practice guide for dose conversion between animals and human. J. Basic Clin. Pharm. 2016, 7, 27–31. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.A.; Kim, H.; Lee, K.W.; Park, K.Y. Dietary Nanosized Lactobacillus plantarum Enhances the Anticancer Effect of Kimchi on Azoxymethane and Dextran Sulfate Sodium—Induced Colon Cancer in C57BL/6J Mice. J. Environ. Pathol. Toxicol. Oncol. 2016, 35, 147–159. [Google Scholar] [CrossRef]
- Ju, J.; Lee, G.Y.; Kim, Y.S.; Chang, H.K.; Do, M.S.; Park, K.Y. Bamboo salt suppresses colon carcinogenesis in C57BL/6 mice with chemically induced colitis. J. Med. Food 2016, 19, 1015–1022. [Google Scholar] [CrossRef]
- Lee, S.Y.; Hong, G.H.; Chung, J.H.; Park, K.Y. Anticancer effects of washed-dehydrated solar salt doenjang on colon cancer-induced C57BL/6 mice. J. Med. Food 2023, 26, 672–682. [Google Scholar] [CrossRef]
- Li, T.; Shen, P.; Liu, W.; Liu, C.; Liang, R.; Yan, N.; Chen, J. Major Polyphenolics in Pineapple Peels and their Antioxidant Interactions. Int. J. Food Prop. 2014, 17, 1805–1817. [Google Scholar] [CrossRef]
- Li, X.; Wasila, H.; Liu, L.; Yuan, T.; Gao, Z.; Zhao, B.; Ahmad, I. Physicochemical characteristics, polyphenol compositions and antioxidant potential of pomegranate juices from 10 Chinese cultivars and the environmental factors analysis. Food Chem. 2015, 175, 575–584. [Google Scholar] [CrossRef] [PubMed]
NOR | CON | CFB | SFB | TFB | NFB | |
---|---|---|---|---|---|---|
Liver | 0.96 ± 0.06 b | 1.07 ± 0.08 a | 1.00 ± 0.10 ab | 0.94 ± 0.08 b | 0.94 ± 0.08 b | 0.92 ± 0.05 b |
Spleen | 0.05 ± 0.01 a | 0.18 ± 0.04 b | 0.16 ± 0.11 b | 0.08 ± 0.01 a | 0.07 ± 0.02 a | 0.06 ± 0.01 a |
Kidney | 0.31 ± 0.02 a | 0.26 ± 0.02 c | 0.27 ± 0.02 bc | 0.28 ± 0.01 bc | 0.28 ± 0.01 abc | 0.30 ± 0.02 ab |
Testis | 0.18 ± 0.02 a | 0.14 ± 0.02 b | 0.14 ± 0.02 b | 0.16 ± 0.02 b | 0.16 ± 0.01 b | 0.19 ± 0.01 a |
Gene Name | Primer Sequence |
---|---|
NF-κB p50 | F: 5′-CACCTAGCTGCCAAAGAAGG-3′ |
R: 5′-GCAGGCTATTGCTCATCACA-3′ | |
NF-κB p65 | F: 5′-ATGGCAGACGATGATCCCTAC-3′ |
R: 5′-CGGAATCGAAATCCCCTCTGTT-3′ | |
IFN-γ | F: 5′-GCTTTGCAGCTCTTCCTCAT-3′ |
R: 5′-GTCACCATCCTTTTGCCAGT-3′ | |
COX-2 | F: 5′-GGTGCCTGGTCTGATGATG-3′ |
R: 5′-TGCTGGTTTGGAATAGTTGCT-3′ | |
iNOS | F: 5′-ATGGCTTGCCCCTGGAA-3′ |
R: 5′-TATTGTTGGGCTGAGAA-3′ | |
IL-6 | F: 5′-ATGAAGTTCCTCTCTGCAA-3′ |
R: 5′-AGTGGTATCCTCTGTGAAG-3′ | |
IL-12 | F: 5′-CATCGATGAGCTGATGCAGT-3′ |
R: 5′-CAGATAGCCCATCACCCTGT-3′ | |
IL-10 | F: 5′-CCAAGCCTTATCGGAAATGA-3′ |
R: 5′-TTTTCACAGGGGAGAAATCG-3′ | |
IL-4 | F: 5′-TCAACCCCCAGCTAGTTGTC-3′ |
R: 5′-TGTTCTTCGTTGCTGTGAGG-3′ | |
p53 | F: 5′-ATGGAGGAGCCGCAGTCAGA-3′ |
R: 5′-TGCAGGGGCCGCCGGTGTAG-3′ | |
p21 | F: 5′-ATGTCAGAACCGGCTGGGG-3′ |
R: 5′-GCCGGGGCCCCGTGGGA-3′ | |
Bim | F: 5′-AGATCCCCGCTTTTCATCTT-3′ |
R: 5′-TCTTGGGCGATCCATATCTC-3′ | |
Bad | F: 5′-CAATGACCCCTTCATTGACC-3′ |
R: 5′-GACAAGCTTCCCGTTCTCAG-3′ | |
Bak | F: 5′-TCTGGCCCTACACGTCTACC-3′ |
R: 5′-AGTGATGCAGCATGAAGTCG-3′ | |
Bax | F: 5′-TGCTTCAGGGTTTCATCCAG-3′ |
R: 5′-GGCGGCAATCATCCTCTG-3′ | |
Bcl-2 | F: 5′-AAGATTGATGGGATCGTTGC-3′ |
R: 5′-GCGGAACACTTGATTCTGGT-3′ | |
Caspase-9 | F: 5′-CTAGTTTGCCCACACCCAGT-3′ |
R: 5′-CTGCTCAAAGATGTCGTCCA-3′ | |
Caspase-3 | F: 5′-TTTTTCAGAGGGGATCGTTG-3′ |
R: 5′-CGGCCTCCACTGGTATTTTA-3′ | |
GAPDH | F: 5′-AGGTCGGTGTGAACGGATTTG-3′ |
R: 5′-GGGGTCGTTGATGGCAACA-3′ |
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Lee, Y.-J.; Pan, Y.; Lim, D.; Park, S.-H.; Sin, S.-I.; Kwack, K.; Park, K.-Y. Broccoli Cultivated with Deep Sea Water Mineral Fertilizer Enhances Anti-Cancer and Anti-Inflammatory Effects of AOM/DSS-Induced Colorectal Cancer in C57BL/6N Mice. Int. J. Mol. Sci. 2024, 25, 1650. https://doi.org/10.3390/ijms25031650
Lee Y-J, Pan Y, Lim D, Park S-H, Sin S-I, Kwack K, Park K-Y. Broccoli Cultivated with Deep Sea Water Mineral Fertilizer Enhances Anti-Cancer and Anti-Inflammatory Effects of AOM/DSS-Induced Colorectal Cancer in C57BL/6N Mice. International Journal of Molecular Sciences. 2024; 25(3):1650. https://doi.org/10.3390/ijms25031650
Chicago/Turabian StyleLee, Yeon-Jun, Yanni Pan, Daewoo Lim, Seung-Hwan Park, Sin-Il Sin, KyuBum Kwack, and Kun-Young Park. 2024. "Broccoli Cultivated with Deep Sea Water Mineral Fertilizer Enhances Anti-Cancer and Anti-Inflammatory Effects of AOM/DSS-Induced Colorectal Cancer in C57BL/6N Mice" International Journal of Molecular Sciences 25, no. 3: 1650. https://doi.org/10.3390/ijms25031650