Reactive oxygen species mediated apoptotic death of colon cancer cells: therapeutic potential of plant derived alkaloids

. 2023 ; 14 () : 1201198. [epub] 20230725

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37560308

Colorectal cancer (CRC) is one of the most deaths causing diseases worldwide. Several risk factors including hormones like insulin and insulin like growth factors (e.g., IGF-1) have been considered responsible for growth and progression of colon cancer. Though there is a huge advancement in the available screening as well as treatment techniques for CRC. There is no significant decrease in the mortality of cancer patients. Moreover, the current treatment approaches for CRC are associated with serious challenges like drug resistance and cancer re-growth. Given the severity of the disease, there is an urgent need for novel therapeutic agents with ideal characteristics. Several pieces of evidence suggested that natural products, specifically medicinal plants, and derived phytochemicals may serve as potential sources for novel drug discovery for various diseases including cancer. On the other hand, cancer cells like colon cancer require a high basal level of reactive oxygen species (ROS) to maintain its own cellular functions. However, excess production of intracellular ROS leads to cancer cell death via disturbing cellular redox homeostasis. Therefore, medicinal plants and derived phytocompounds that can enhance the intracellular ROS and induce apoptotic cell death in cancer cells via modulating various molecular targets including IGF-1 could be potential therapeutic agents. Alkaloids form a major class of such phytoconstituents that can play a key role in cancer prevention. Moreover, several preclinical and clinical studies have also evidenced that these compounds show potent anti-colon cancer effects and exhibit negligible toxicity towards the normal cells. Hence, the present evidence-based study aimed to provide an update on various alkaloids that have been reported to induce ROS-mediated apoptosis in colon cancer cells via targeting various cellular components including hormones and growth factors, which play a role in metastasis, angiogenesis, proliferation, and invasion. This study also provides an individual account on each such alkaloid that underwent clinical trials either alone or in combination with other clinical drugs. In addition, various classes of phytochemicals that induce ROS-mediated cell death in different kinds of cancers including colon cancer are discussed.

Zobrazit více v PubMed

Ma X, Yu H. Global burden of cancer. Yale J Biol Med (2006) 79(3-4):85–94. PubMed PMC

Nelson VK, Sahoo NK, Sahu M, Sudhan HH, Pullaiah CP, Muralikrishna KS. In vitro anticancer activity of eclipta alba whole plant extract on colon cancer cell HCT-116. BMC Complement Med Ther (2020) 20(1):355. doi: 10.1186/s12906-020-03118-9 PubMed DOI PMC

Abane R, Mezger V. Roles of heat shock factors in gametogenesis and development. FEBS J (2010) 277(20):4150–72. doi: 10.1111/j.1742-4658.2010.07830.x PubMed DOI

Zaytseva Y. Lipid metabolism as a targetable metabolic vulnerability in colorectal cancer. Cancers (Basel) (2021) 13(2):1–5. doi: 10.3390/cancers13020301 PubMed DOI PMC

Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet (2019) 394(10207):1467–80. doi: 10.1016/s0140-6736(19)32319-0 PubMed DOI

Sawicki T, Ruszkowska M, Danielewicz A, Niedźwiedzka E, Arłukowicz T, Przybyłowicz KE. A review of colorectal cancer in terms of epidemiology, risk factors, development, symptoms and diagnosis. Cancers (Basel) (2021) 13(9):1–23. doi: 10.3390/cancers13092025 PubMed DOI PMC

Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol (2021) 14(10):101174. doi: 10.1016/j.tranon.2021.101174 PubMed DOI PMC

White A, Ironmonger L, Steele RJC, Ormiston-Smith N, Crawford C, Seims A. A review of sex-related differences in colorectal cancer incidence, screening uptake, routes to diagnosis, cancer stage and survival in the UK. BMC Cancer (2018) 18(1):906. doi: 10.1186/s12885-018-4786-7 PubMed DOI PMC

Brahmkhatri VP, Prasanna C, Atreya HS. Insulin-like growth factor system in cancer: novel targeted therapies. BioMed Res Int (2015) 2015:538019. doi: 10.1155/2015/538019 PubMed DOI PMC

Chainy GBN, Sahoo DK. Hormones and oxidative stress: an overview. Free Radic Res (2020) 54(1):1–26. doi: 10.1080/10715762.2019.1702656 PubMed DOI

Sahoo DK, Chainy GBN. Hormone-linked redox status and its modulation by antioxidants. Vitam Horm (2023) 121:197–246. doi: 10.1016/bs.vh.2022.10.007 PubMed DOI

Lukas M. Inflammatory bowel disease as a risk factor for colorectal cancer. Dig Dis (2010) 28(4-5):619–24. doi: 10.1159/000320276 PubMed DOI

Sahoo DK, Borcherding DC, Chandra L, Jergens AE, Atherly T, Bourgois-Mochel A, et al. . Differential transcriptomic profiles following stimulation with lipopolysaccharide in intestinal organoids from dogs with inflammatory bowel disease and intestinal mast cell tumor. Cancers (Basel) (2022) 14(14):1–59. doi: 10.3390/cancers14143525 PubMed DOI PMC

Gavrilas LI, Cruceriu D, Mocan A, Loghin F, Miere D, Balacescu O. Plant-derived bioactive compounds in colorectal cancer: insights from combined regimens with conventional chemotherapy to overcome drug-resistance. Biomedicines (2022) 10(8):1–14. doi: 10.3390/biomedicines10081948 PubMed DOI PMC

Braun MS, Seymour MT. Balancing the efficacy and toxicity of chemotherapy in colorectal cancer. Ther Adv Med Oncol (2011) 3(1):43–52. doi: 10.1177/1758834010388342 PubMed DOI PMC

Pardini B, Kumar R, Naccarati A, Novotny J, Prasad RB, Forsti A, et al. . 5-fluorouracil-based chemotherapy for colorectal cancer and MTHFR/MTRR genotypes. Br J Clin Pharmacol (2011) 72(1):162–3. doi: 10.1111/j.1365-2125.2010.03892.x PubMed DOI PMC

Dutta N, Ghosh S, Nelson VK, Sareng HR, Majumder C, Mandal SC, et al. . Andrographolide upregulates protein quality control mechanisms in cell and mouse through upregulation of mTORC1 function. Biochim Biophys Acta Gen Subj (2021) 1865(6):129885. doi: 10.1016/j.bbagen.2021.129885 PubMed DOI

Ghosh S, Hazra J, Pal K, Nelson VK, Pal M. Prostate cancer: therapeutic prospect with herbal medicine. Curr Res Pharmacol Drug Discovery (2021) 2:100034. doi: 10.1016/j.crphar.2021.100034 PubMed DOI PMC

Pullaiah CP, Nelson VK, Rayapu S, Nk G V, Kedam T. Exploring cardioprotective potential of esculetin against isoproterenol induced myocardial toxicity in rats: in vivo and in vitro evidence. BMC Pharmacol Toxicol (2021) 22(1):43. doi: 10.1186/s40360-021-00510-0 PubMed DOI PMC

Dutta N, Pemmaraju DB, Ghosh S, Ali A, Mondal A, Majumder C, et al. . Alkaloid-rich fraction of ervatamia coronaria sensitizes colorectal cancer through modulating AMPK and mTOR signalling pathways. J Ethnopharmacol (2022) 283:114666. doi: 10.1016/j.jep.2021.114666 PubMed DOI

Nelson VK, Paul S, Roychoudhury S, Oyeyemi IT, Mandal SC, Kumar N, et al. . Heat shock factors in protein quality control and spermatogenesis. Adv Exp Med Biol (2022) 1391:181–99. doi: 10.1007/978-3-031-12966-7_11 PubMed DOI

Nelson VK, Pullaiah CP, Saleem Ts M, Roychoudhury S, Chinnappan S, Vishnusai B, et al. . Natural products as the modulators of oxidative stress: an herbal approach in the management of prostate cancer. Adv Exp Med Biol (2022) 1391:161–79. doi: 10.1007/978-3-031-12966-7_10 PubMed DOI

De S, Paul S, Manna A, Majumder C, Pal K, Casarcia N, et al. . Phenolic phytochemicals for prevention and treatment of colorectal cancer: a critical evaluation of In vivo studies. Cancers (Basel) (2023) 15(3):1–66. doi: 10.3390/cancers15030993 PubMed DOI PMC

Badavenkatappa Gari S, Nelson VK, Peraman R. Tinospora sinensis (Lour.) merr alkaloid rich extract induces colon cancer cell death via ROS mediated, mTOR dependent apoptosis pathway: “an in-vitro study”. BMC Complement Med Ther (2023) 23(1):33. doi: 10.1186/s12906-023-03849-5 PubMed DOI PMC

Nelson VK, Ali A, Dutta N, Ghosh S, Jana M, Ganguli A, et al. . Azadiradione ameliorates polyglutamine expansion disease in drosophila by potentiating DNA binding activity of heat shock factor 1. Oncotarget (2016) 7(48):78281–96. doi: 10.18632/oncotarget.12930 PubMed DOI PMC

Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res (2010) 44(5):479–96. doi: 10.3109/10715761003667554 PubMed DOI PMC

Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discovery (2009) 8(7):579–91. doi: 10.1038/nrd2803 PubMed DOI

Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discovery (2013) 12(12):931–47. doi: 10.1038/nrd4002 PubMed DOI

NavaneethaKrishnan S, Rosales JL, Lee KY. Targeting Cdk5 for killing of breast cancer cells via perturbation of redox homeostasis. Oncoscience (2018) 5(5-6):152–4. doi: 10.18632/oncoscience.431 PubMed DOI PMC

Shimada Y, Yoshino M, Wakui A, Nakao I, Futatsuki K, Sakata Y, et al. . Phase II study of CPT-11, a new camptothecin derivative, in metastatic colorectal cancer. CPT-11 gastrointestinal cancer study group. J Clin Oncol (1993) 11(5):909–13. doi: 10.1200/jco.1993.11.5.909 PubMed DOI

Kapała A, Szlendak M, Motacka E. The anti-cancer activity of lycopene: a systematic review of human and animal studies. Nutrients (2022) 14(23):1–44. doi: 10.3390/nu14235152 PubMed DOI PMC

Farsad-Naeimi A, Alizadeh M, Esfahani A, Darvish Aminabad E. Effect of fisetin supplementation on inflammatory factors and matrix metalloproteinase enzymes in colorectal cancer patients. Food Funct (2018) 9(4):2025–31. doi: 10.1039/c7fo01898c PubMed DOI

Jiang X, Jiang Z, Jiang M, Sun Y. Berberine as a potential agent for the treatment of colorectal cancer. Front Med (Lausanne) (2022) 9:886996. doi: 10.3389/fmed.2022.886996 PubMed DOI PMC

Aggarwal V, Tuli HS, Varol A, Thakral F, Yerer MB, Sak K, et al. . Role of reactive oxygen species in cancer progression: molecular mechanisms and recent advancements. Biomolecules (2019) 9(11):1–26. doi: 10.3390/biom9110735 PubMed DOI PMC

Sahoo DK, Allenspach K, Mochel JP, Parker V, Rudinsky AJ, Winston JA, et al. . Synbiotic-IgY therapy modulates the mucosal microbiome and inflammatory indices in dogs with chronic inflammatory enteropathy: a randomized, double-blind, placebo-controlled study. Vet Sci (2022) 10(1):1–18. doi: 10.3390/vetsci10010025 PubMed DOI PMC

Guo YJ, Pan WW, Liu SB, Shen ZF, Xu Y, Hu LL. ERK/MAPK signalling pathway and tumorigenesis. Exp Ther Med (2020) 19(3):1997–2007. doi: 10.3892/etm.2020.8454 PubMed DOI PMC

Zhang Y, Gan B, Liu D. & paik J FoxO family members in cancer. Cancer Biol Ther (2011) 12:4. doi: 10.4161/cbt.12.4.15954 PubMed DOI

Dai L, Zhuang L, Zhang B, Wang F, Chen X, Xia C, et al. . DAG/PKCδ and IP3/Ca²⁺/CaMK IIβ operate in parallel to each other in PLCγ1-driven cell proliferation and migration of human gastric adenocarcinoma cells, through Akt/mTOR/S6 pathway. Int J Mol Sci (2015) 16(12):28510–22. doi: 10.3390/ijms161226116 PubMed DOI PMC

Hwang AB, Lee SJ. Regulation of life span by mitochondrial respiration: the HIF-1 and ROS connection. Aging (2011), 304–10. PubMed PMC

Guba M, Seeliger H, Kleespies A, Jauch KW, Bruns C. Vascular endothelial growth factor in colorectal cancer. Int J Colorectal Dis (2004) 19(6):510–7. doi: 10.1007/s00384-003-0576-y PubMed DOI

Lee YJ, Karl DL, Maduekwe UN, Rothrock C, Ryeom S, D'Amore PA, et al. . Differential effects of VEGFR-1 and VEGFR-2 inhibition on tumor metastases based on host organ environment. Cancer Res (2010) 70(21):8357–67. doi: 10.1158/0008-5472.CAN-10-1138 PubMed DOI PMC

Lan T, Chen L, Wei X. Inflammatory Cytokines in cancer: comprehensive understanding and clinical progress in gene therapy. Cells (2021) 10(1):100. doi: 10.3390/cells10010100 PubMed DOI PMC

NavaneethaKrishnan S, Rosales JL, Lee KY. ROS-mediated cancer cell killing through dietary phytochemicals. Oxid Med Cell Longev (2019) 2019:9051542. doi: 10.1155/2019/9051542 PubMed DOI PMC

Sreevalsan S, Safe S. REACTIVE OXYGEN SPECIES AND COLORECTAL CANCER. Curr Colorectal Cancer Rep (2013) 9(4):350–7. doi: 10.1007/s11888-013-0190-5 PubMed DOI PMC

Ahmed K, Zaidi SF, Cui ZG, Zhou D, Saeed SA, Inadera H. Potential proapoptotic phytochemical agents for the treatment and prevention of colorectal cancer. Oncol Lett (2019) 18(1):487–98. doi: 10.3892/ol.2019.10349 PubMed DOI PMC

Hill MM, Adrain C, Duriez PJ, Creagh EM, Martin SJ. Analysis of the composition, assembly kinetics and activity of native apaf-1 apoptosomes. EMBO J (2004) 23(10):2134–45. doi: 10.1038/sj.emboj.7600210 PubMed DOI PMC

Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ (2006) 13(9):1423–33. doi: 10.1038/sj.cdd.4401950 PubMed DOI

Silke J, Meier P. Inhibitor of apoptosis (IAP) proteins-modulators of cell death and inflammation. Cold Spring Harb Perspect Biol (2013) 5(2). doi: 10.1101/cshperspect.a008730 PubMed DOI PMC

Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol (2007) 35(4):495–516. doi: 10.1080/01926230701320337 PubMed DOI PMC

Bruckheimer EM, Cho SH, Sarkiss M, Herrmann J, McDonnell TJ. The bcl-2 gene family and apoptosis. Adv Biochem Eng Biotechnol (1998) 62:75–105. doi: 10.1007/BFb0102306 PubMed DOI

Hardwick JM, Soane L. Multiple functions of BCL-2 family proteins. Cold Spring Harb Perspect Biol (2013) 5(2). doi: 10.1101/cshperspect.a008722 PubMed DOI PMC

Hempel N, Trebak M. Crosstalk between calcium and reactive oxygen species signaling in cancer. Cell Calcium (2017) 63:70–96. doi: 10.1016/j.ceca.2017.01.007 PubMed DOI PMC

Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta (2016) 1863(12):2977–92. doi: 1016/j.bbamcr.2016.09.012 PubMed

Park DR, Thomsen AR, Frevert CW, Pham U, Skerrett SJ, Kiener PA, et al. . Fas (CD95) induces proinflammatory cytokine responses by human monocytes and monocyte-derived macrophages. J Immunol (2003) 170(12):6209–16. doi: 10.4049/jimmunol.170.12.6209 PubMed DOI

Volpe E, Sambucci M, Battistini L, Borsellino G. Fas-fas ligand: checkpoint of T cell functions in multiple sclerosis. Front Immunol (2016) 7:382. doi: 10.3389/fimmu.2016.00382 PubMed DOI PMC

Pobezinskaya YL, Liu Z. The role of TRADD in death receptor signaling. Cell Cycle (2012) 11(5):871–6. doi: 10.4161/cc.11.5.19300 PubMed DOI PMC

Huang YT, Liu CH, Yang YC, Aneja R, Wen SY, Huang CY, et al. . ROS- and HIF1α-dependent IGFBP3 upregulation blocks IGF1 survival signaling and thereby mediates high-glucose-induced cardiomyocyte apoptosis. J Cell Physiol (2019) 234(8):13557–70. doi: 10.1002/jcp.28034 PubMed DOI

Akhtar R, Chandel S, Sarotra P, Medhi B. Current status of pharmacological treatment of colorectal cancer. World J Gastrointest Oncol (2014) 6(6):177–83. doi: 10.4251/wjgo.v6.i6.177 PubMed DOI PMC

Cassidy J, Misset JL. Oxaliplatin-related side effects: characteristics and management. Semin Oncol (2002) 29(5 Suppl 15):11–20. doi: 10.1053/sonc.2002.35524 PubMed DOI

Reynolds NA, Wagstaff AJ. Cetuximab: in the treatment of metastatic colorectal cancer. Drugs (2004) 64(1):109–18. doi: 10.2165/00003495-200464010-00007 PubMed DOI

Willems E, Gerne L, George C, D’Hondt M. Adverse effects of bevacizumab in metastatic colorectal cancer: a case report and literature review. Acta Gastroenterol Belg (2019) 82(2):322–5. PubMed

Battaglin F, Puccini A, Ahcene Djaballah S, Lenz HJ. The impact of panitumumab treatment on survival and quality of life in patients with RAS wild-type metastatic colorectal cancer. Cancer Manag Res (2019) 11:5911–24. doi: 10.2147/cmar.S186042 PubMed DOI PMC

Hirsch BR, Zafar SY. Capecitabine in the management of colorectal cancer. Cancer Manag Res (2011) 3:79–89. doi: 10.2147/cmr.S11250 PubMed DOI PMC

Van der Jeught K, Xu HC, Li YJ, Lu XB, Ji G. Drug resistance and new therapies in colorectal cancer. World J Gastroenterol (2018) 24(34):3834–48. doi: 10.3748/wjg.v24.i34.3834 PubMed DOI PMC

Hasegawa K, Saiura A, Takayama T, Miyagawa S, Yamamoto J, Ijichi M, et al. . Adjuvant oral uracil-tegafur with leucovorin for colorectal cancer liver metastases: a randomized controlled trial. PloS One (2016) 11(9):e0162400. doi: 10.1371/journal.pone.0162400 PubMed DOI PMC

Hata T, Hagihara K, Tsutsui A, Akamatsu H, Ohue M, Shingai T, et al. . Administration method of adjuvant tegafur-uracil and leucovorin calcium in patients with resected colorectal cancer: a phase III study. Oncologist (2021) 26(5):e735–41. doi: 10.1002/onco.13724 PubMed DOI PMC

Singh V, Sheikh A, Abourehab MAS, Kesharwani P. Dostarlimab as a miracle drug: rising hope against cancer treatment. Biosensors (Basel) (2022) 12(8):1–14. doi: 10.3390/bios12080617 PubMed DOI PMC

Xie YH, Chen YX, Fang JY. Comprehensive review of targeted therapy for colorectal cancer. Signal Transduct Target Ther (2020) 5(1):22. doi: 10.1038/s41392-020-0116-z PubMed DOI PMC

Rotte A. Combination of CTLA-4 and PD-1 blockers for treatment of cancer. J Exp Clin Cancer Res (2019) 38(1):255. doi: 10.1186/s13046-019-1259-z PubMed DOI PMC

Savoia P, Astrua C, Fava P. Ipilimumab (Anti-Ctla-4 mab) in the treatment of metastatic melanoma: effectiveness and toxicity management. Hum Vaccin Immunother (2016) 12(5):1092–101. doi: 10.1080/21645515.2015.1129478 PubMed DOI PMC

Kooshkaki O, Derakhshani A, Hosseinkhani N, Torabi M, Safaei S, Brunetti O, et al. . Combination of ipilimumab and nivolumab in cancers: from clinical practice to ongoing clinical trials. Int J Mol Sci (2020) 21(12):1–28. doi: 10.3390/ijms21124427 PubMed DOI PMC

Wookey V, Grothey A. Update on the role of pembrolizumab in patients with unresectable or metastatic colorectal cancer. Therap Adv Gastroenterol (2021) 14:17562848211024460. doi: 10.1177/17562848211024460 PubMed DOI PMC

Berg D. Managing the side effects of chemotherapy for colorectal cancer. Semin Oncol (1998) 25(5 Suppl 11):53–9. PubMed

Golshani G, Zhang Y. Advances in immunotherapy for colorectal cancer: a review. Therap Adv Gastroenterol (2020) 13:1756284820917527. doi: 10.1177/1756284820917527 PubMed DOI PMC

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. . Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin (2021) 71(3):209–49. doi: 10.3322/caac.21660 PubMed DOI

Hashem S, Ali TA, Akhtar S, Nisar S, Sageena G, Ali S, et al. . Targeting cancer signaling pathways by natural products: exploring promising anti-cancer agents. BioMed Pharmacother (2022) 150:113054. doi: 10.1016/j.biopha.2022.113054 PubMed DOI

Choudhari AS, Mandave PC, Deshpande M, Ranjekar P, Prakash O. Phytochemicals in cancer treatment: from preclinical studies to clinical practice. Front Pharmacol (2019) 10:1614. doi: 10.3389/fphar.2019.01614 PubMed DOI PMC

Rahman MA, Hannan MA, Dash R, Rahman MH, Islam R, Uddin MJ, et al. . Phytochemicals as a complement to cancer chemotherapy: pharmacological modulation of the autophagy-apoptosis pathway. Front Pharmacol (2021) 12:639628. doi: 10.3389/fphar.2021.639628 PubMed DOI PMC

Greenwell M, Rahman PK. Medicinal plants: their use in anticancer treatment. Int J Pharm Sci Res (2015) 6(10):4103–12. doi: 10.13040/ijpsr.0975-8232.6(10).4103-12 PubMed DOI PMC

Seca AML, Pinto DCGA. Biological potential and medical use of secondary metabolites. Medicines (Basel) (2019) 6(2):1–6. doi: 10.3390/medicines6020066 PubMed DOI PMC

Dhyani P, Quispe C, Sharma E, Bahukhandi A, Sati P, Attri DC, et al. . Anticancer potential of alkaloids: a key emphasis to colchicine, vinblastine, vincristine, vindesine, vinorelbine and vincamine. Cancer Cell Int (2022) 22(1):206. doi: 10.1186/s12935-022-02624-9 PubMed DOI PMC

Huang M, Lu JJ, Ding J. Natural products in cancer therapy: past, present and future. Nat Prod Bioprospect (2021) 11(1):5–13. doi: 10.1007/s13659-020-00293-7 PubMed DOI PMC

Xu Y, Fang F, Miriyala S, Crooks PA, Oberley TD, Chaiswing L, et al. . KEAP1 is a redox sensitive target that arbitrates the opposing radiosensitive effects of parthenolide in normal and cancer cells. Cancer Res (2013) 73(14):4406–17. doi: 10.1158/0008-5472.Can-12-4297 PubMed DOI PMC

Khan H, Alam W, Alsharif KF, Aschner M, Pervez S, Saso L. Alkaloids and colon cancer: molecular mechanisms and therapeutic implications for cell cycle arrest. Molecules (2022) 27(3):1–26. doi: 10.3390/molecules27030920 PubMed DOI PMC

Heinrich M, Mah J, Amirkia V. Alkaloids used as medicines: structural phytochemistry meets biodiversity-an update and forward look. Molecules (2021) 26(7):1–26. doi: 10.3390/molecules26071836 PubMed DOI PMC

Gong X, Chen Z, Han Q, Chen C, Jing L, Liu Y, et al. . Sanguinarine triggers intrinsic apoptosis to suppress colorectal cancer growth through disassociation between STRAP and MELK. BMC Cancer (2018) 18(1):578. doi: 10.1186/s12885-018-4463-x PubMed DOI PMC

Matkar SS, Wrischnik LA, Hellmann-Blumberg U. Sanguinarine causes DNA damage and p53-independent cell death in human colon cancer cell lines. Chem Biol Interact (2008) 172(1):63–71. doi: 10.1016/j.cbi.2007.12.006 PubMed DOI

Yin HQ, Kim YH, Moon CK, Lee BH. Reactive oxygen species-mediated induction of apoptosis by a plant alkaloid 6-methoxydihydrosanguinarine in HepG2 cells. Biochem Pharmacol (2005) 70(2):242–8. doi: 10.1016/j.bcp.2005.04.020 PubMed DOI

Dai W, Mu L, Cui Y, Li Y, Chen P, Xie H, et al. . Berberine promotes apoptosis of colorectal cancer via regulation of the long non-coding RNA (lncRNA) cancer susceptibility candidate 2 (CASC2)/AU-binding factor 1 (AUF1)/B-cell CLL/Lymphoma 2 (Bcl-2) axis. Med Sci Monit (2019) 25:730–8. doi: 10.12659/msm.912082 PubMed DOI PMC

Wang L, Liu L, Shi Y, Cao H, Chaturvedi R, Calcutt MW, et al. . Berberine induces caspase-independent cell death in colon tumor cells through activation of apoptosis-inducing factor. PloS One (2012) 7(5):e36418. doi: 10.1371/journal.pone.0036418 PubMed DOI PMC

Park JJ, Seo SM, Kim EJ, Lee YJ, Ko YG, Ha J, et al. . Berberine inhibits human colon cancer cell migration via AMP-activated protein kinase-mediated downregulation of integrin β1 signaling. Biochem Biophys Res Commun (2012) 426(4):461–7. doi: 10.1016/j.bbrc.2012.08.091 PubMed DOI

Hsu WH, Hsieh YS, Kuo HC, Teng CY, Huang HI, Wang CJ, et al. . Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL. Arch Toxicol (2007) 81(10):719–28. doi: 10.1007/s00204-006-0169-y PubMed DOI

Li W, Hua B, Saud SM, Lin H, Hou W, Matter MS, et al. . Berberine regulates AMP-activated protein kinase signaling pathways and inhibits colon tumorigenesis in mice. Mol Carcinog (2015) 54(10):1096–109. doi: 10.1002/mc.22179 PubMed DOI PMC

Liu X, Ji Q, Ye N, Sui H, Zhou L, Zhu H, et al. . Berberine inhibits invasion and metastasis of colorectal cancer cells via COX-2/PGE2 mediated JAK2/STAT3 signaling pathway. PloS One (2015) 10(5):e0123478. doi: 10.1371/journal.pone.0123478 PubMed DOI PMC

Wu K, Yang Q, Mu Y, Zhou L, Liu Y, Zhou Q, et al. . Berberine inhibits the proliferation of colon cancer cells by inactivating wnt/β-catenin signaling. Int J Oncol (2012) 41(1):292–8. doi: 10.3892/ijo.2012.1423 PubMed DOI

Li D, Zhang Y, Liu K, Zhao Y, Xu B, Xu L, et al. . Berberine inhibits colitis-associated tumorigenesis via suppressing inflammatory responses and the consequent EGFR signaling-involved tumor cell growth. Lab Invest (2017) 97(11):1343–53. doi: 10.1038/labinvest.2017.71 PubMed DOI

Samadi P, Sarvarian P, Gholipour E, Asenjan KS, Aghebati-Maleki L, Motavalli R, et al. . Berberine: a novel therapeutic strategy for cancer. IUBMB Life (2020) 72(10):2065–79. doi: 10.1002/iub.2350 PubMed DOI

Zhao Y, Roy S, Wang C, Goel A. A combined treatment with berberine and andrographis exhibits enhanced anti-cancer activity through suppression of DNA replication in colorectal cancer. Pharm (Basel) (2022) 15(3):1–17. doi: 10.3390/ph15030262 PubMed DOI PMC

Guan X, Zheng X, Vong CT, Zhao J, Xiao J, Wang Y, et al. . Combined effects of berberine and evodiamine on colorectal cancer cells and cardiomyocytes in vitro . Eur J Pharmacol (2020) 875:173031. doi: 10.1016/j.ejphar.2020.173031 PubMed DOI

Rattanawong A, Payon V, Limpanasittikul W, Boonkrai C, Mutirangura A, Wonganan P. Cepharanthine exhibits a potent anticancer activity in p53-mutated colorectal cancer cells through upregulation of p21Waf1/Cip1. Oncol Rep (2018) 39(1):227–38. doi: 10.3892/or.2017.6084 PubMed DOI

Han B, Jiang P, Li Z, Yu Y, Huang T, Ye X, et al. . Coptisine-induced apoptosis in human colon cancer cells (HCT-116) is mediated by PI3K/Akt and mitochondrial-associated apoptotic pathway. Phytomedicine (2018) 48:152–60. doi: 10.1016/j.phymed.2017.12.027 PubMed DOI

Huang T, Xiao Y, Yi L, Li L, Wang M, Tian C, et al. . Coptisine from rhizoma coptidis suppresses HCT-116 cells-related tumor growth in vitro and in vivo . Sci Rep (2017) 7:38524. doi: 10.1038/srep38524 PubMed DOI PMC

Cao Q, Hong S, Li Y, Chen H, Shen Y, Shao K, et al. . Coptisine suppresses tumor growth and progression by down-regulating MFG-E8 in colorectal cancer. RSC Adv (2018) 8(54):30937–45. doi: 10.1039/c8ra05806g PubMed DOI PMC

Manogaran P, Beeraka NM, Huang CY, Vijaya Padma V. Neferine and isoliensinine enhance ‘intracellular uptake of cisplatin’ and induce ‘ROS-mediated apoptosis’ in colorectal cancer cells - a comparative study. Food Chem Toxicol (2019) 132:110652. doi: 10.1016/j.fct.2019.110652 PubMed DOI

Manogaran P, Somasundaram B, Viswanadha VP. Reversal of cisplatin resistance by neferine/isoliensinine and their combinatorial regimens with cisplatin-induced apoptosis in cisplatin-resistant colon cancer stem cells (CSCs). J Biochem Mol Toxicol (2022) 36(3):e22967. doi: 10.1002/jbt.22967 PubMed DOI

Liu X, Zhang Y, Wu S, Xu M, Shen Y, Yu M, et al. . Palmatine induces G2/M phase arrest and mitochondrial-associated pathway apoptosis in colon cancer cells by targeting AURKA. Biochem Pharmacol (2020) 175:113933. doi: 10.1016/j.bcp.2020.113933 PubMed DOI

Meng LH, Zhang H, Hayward L, Takemura H, Shao RG, Pommier Y. Tetrandrine induces early G1 arrest in human colon carcinoma cells by down-regulating the activity and inducing the degradation of G1-s-specific cyclin-dependent kinases and by inducing p53 and p21Cip1. Cancer Res (2004) 64(24):9086–92. doi: 10.1158/0008-5472.Can-04-0313 PubMed DOI

Qin R, Shen H, Cao Y, Fang Y, Li H, Chen Q, et al. . Tetrandrine induces mitochondria-mediated apoptosis in human gastric cancer BGC-823 cells. PloS One (2013) 8(10):e76486. doi: 10.1371/journal.pone.0076486 PubMed DOI PMC

Li X, Zhen D, Lu X, Xu H, Shao Y, Xue Q, et al. . Enhanced cytotoxicity and activation of ROS-dependent c-jun NH2-terminal kinase and caspase-3 by low doses of tetrandrine-loaded nanoparticles in lovo cells–a possible Trojan strategy against cancer. Eur J Pharm Biopharm (2010) 75(3):334–40. doi: 10.1016/j.ejpb.2010.04.016 PubMed DOI

Santos LS, Silva VR, Menezes LRA, Soares MBP, Costa EV, Bezerra DP. Xylopine induces oxidative stress and causes G(2)/M phase arrest, triggering caspase-mediated apoptosis by p53-independent pathway in HCT116 cells. Oxid Med Cell Longev (2017) 2017:7126872. doi: 10.1155/2017/7126872 PubMed DOI PMC

Lorence A, Medina-Bolivar F, Nessler CL. Camptothecin and 10-hydroxycamptothecin from camptotheca acuminata hairy roots. Plant Cell Rep (2004) 22(6):437–41. doi: 10.1007/s00299-003-0708-4 PubMed DOI

Ha SW, Kim YJ, Kim W, Lee CS. Antitumor effects of camptothecin combined with conventional anticancer drugs on the cervical and uterine squamous cell carcinoma cell line SiHa. Korean J Physiol Pharmacol (2009) 13(2):115–21. doi: 10.4196/kjpp.2009.13.2.115 PubMed DOI PMC

Park K, Abebe W, Fermin C, Reddy G, Habtemariam T, Chung J, et al. . Hypoxia inhibition of camptothecin-induced apoptosis by bax loss. Biologia (2012) 67:616–21. doi: 10.2478/s11756-012-0037-6 DOI

Liskova V, Kajsik M, Chovancova B, Roller L, Krizanova O. Camptothecin, triptolide, and apoptosis inducer kit have differential effects on mitochondria in colorectal carcinoma cells. FEBS Open Bio (2022) 12(5):913–24. doi: 10.1002/2211-5463.13401 PubMed DOI PMC

Wenzel U, Nickel A, Kuntz S, Daniel H. Ascorbic acid suppresses drug-induced apoptosis in human colon cancer cells by scavenging mitochondrial superoxide anions. Carcinogenesis (2004) 25(5):703–12. doi: 10.1093/carcin/bgh079 PubMed DOI

Guo Z, Wang Z, Liang R, Tian H, Chen X, Chen M. Reactive oxygen species activated by mitochondria-specific camptothecin prodrug for enhanced chemotherapy. Bosn J Basic Med Sci (2022) 22(6):934–48. doi: 10.17305/bjbms.2022.7194 PubMed DOI PMC

Fujita K, Kubota Y, Ishida H, Sasaki Y. Irinotecan, a key chemotherapeutic drug for metastatic colorectal cancer. World J Gastroenterol (2015) 21(43):12234–48. doi: 10.3748/wjg.v21.i43.12234 PubMed DOI PMC

Britten CD, Hilsenbeck SG, Eckhardt SG, Marty J, Mangold G, MacDonald JR, et al. . Enhanced antitumor activity of 6-hydroxymethylacylfulvene in combination with irinotecan and 5-fluorouracil in the HT29 human colon tumor xenograft model. Cancer Res (1999) 59(5):1049–53. PubMed

Raymond E, Louvet C, Tournigand C, Coudray AM, Faivre S, De Gramont A, et al. . Pemetrexed disodium combined with oxaliplatin, SN38, or 5-fluorouracil, based on the quantitation of drug interactions in human HT29 colon cancer cells. Int J Oncol (2002) 21(2):361–7. doi: 10.3892/ijo.21.2.361 PubMed DOI

Allegrini G, Goulette FA, Darnowski JW, Calabresi P. Thrombospondin-1 plus irinotecan: a novel antiangiogenic-chemotherapeutic combination that inhibits the growth of advanced human colon tumor xenografts in mice. Cancer Chemother Pharmacol (2004) 53(3):261–6. doi: 10.1007/s00280-003-0712-y PubMed DOI

Di Bartolomeo M, Ciarlo A, Bertolini A, Barni S, Verusio C, Aitini E, et al. . Capecitabine, oxaliplatin and irinotecan in combination, with bevacizumab (COI-b regimen) as first-line treatment of patients with advanced colorectal cancer. an Italian trials of medical oncology phase II study. Eur J Cancer (2015) 51(4):473–81. doi: 10.1016/j.ejca.2014.12.020 PubMed DOI

Cai Y, Deng R, Hu H, Zhang J, Ling J, Wu Z, et al. . [Analysis on safety and preliminary efficacy of dose-modified regimen of 5-fluorouracil plus oxaliplatin and irinotecan (FOLFOXIRI) in advanced colorectal cancer]. Zhonghua Wei Chang Wai Ke Za Zhi (2018) 21(9):1045–50. PubMed

Reyes-Escogido Mde L, Gonzalez-Mondragon EG, Vazquez-Tzompantzi E. Chemical and pharmacological aspects of capsaicin. Molecules (2011) 16(2):1253–70. doi: 10.3390/molecules16021253 PubMed DOI PMC

Yang KM, Pyo JO, Kim GY, Yu R, Han IS, Ju SA, et al. . Capsaicin induces apoptosis by generating reactive oxygen species and disrupting mitochondrial transmembrane potential in human colon cancer cell lines. Cell Mol Biol Lett (2009) 14(3):497–510. doi: 10.2478/s11658-009-0016-2 PubMed DOI PMC

Kim CS, Park WH, Park JY, Kang JH, Kim MO, Kawada T, et al. . Capsaicin, a spicy component of hot pepper, induces apoptosis by activation of the peroxisome proliferator-activated receptor gamma in HT-29 human colon cancer cells. J Med Food (2004) 7(3):267–73. doi: 10.1089/jmf.2004.7.267 PubMed DOI

Kim YM, Hwang JT, Kwak DW, Lee YK, Park OJ. Involvement of AMPK signaling cascade in capsaicin-induced apoptosis of HT-29 colon cancer cells. Ann N Y Acad Sci (2007) 1095:496–503. doi: 10.1196/annals.1397.053 PubMed DOI

Lu HF, Chen YL, Yang JS, Yang YY, Liu JY, Hsu SC, et al. . Antitumor activity of capsaicin on human colon cancer cells in vitro and colo 205 tumor xenografts in vivo . J Agric Food Chem (2010) 58(24):12999–3005. doi: 10.1021/jf103335w PubMed DOI

Clark R, Lee J, Lee SH. Synergistic anticancer activity of capsaicin and 3,3’-diindolylmethane in human colorectal cancer. J Agric Food Chem (2015) 63(17):4297–304. doi: 10.1021/jf506098s PubMed DOI

Kim MY, Trudel LJ, Wogan GN. Apoptosis induced by capsaicin and resveratrol in colon carcinoma cells requires nitric oxide production and caspase activation. Anticancer Res (2009) 29(10):3733–40. PubMed

Waziri PM, Abdullah R, Yeap SK, Omar AR, Kassim NK, Malami I, et al. . Clausenidin induces caspase-dependent apoptosis in colon cancer. BMC Complement Altern Med (2016) 16:256. doi: 10.1186/s12906-016-1247-1 PubMed DOI PMC

Song N, Ma J, Hu W, Guo Y, Hui L, Aamer M, et al. . Lappaconitine hydrochloride inhibits proliferation and induces apoptosis in human colon cancer HCT-116 cells via mitochondrial and MAPK pathway. Acta Histochem (2021) 123(5):151736. doi: 10.1016/j.acthis.2021.151736 PubMed DOI

Yaffe PB, Power Coombs MR, Doucette CD, Walsh M, Hoskin DW. Piperine, an alkaloid from black pepper, inhibits growth of human colon cancer cells via G1 arrest and apoptosis triggered by endoplasmic reticulum stress. Mol Carcinog (2015) 54(10):1070–85. doi: 10.1002/mc.22176 PubMed DOI

DA Silva Machado F, Munari FM, Scariot FJ, Echeverrigaray S, Aguzzoli C, Pich CT, et al. . Piperlongumine induces apoptosis in colorectal cancer HCT 116 cells independent of bax, p21 and p53 status. Anticancer Res (2018) 38(11):6231–6. doi: 10.21873/anticanres.12978 PubMed DOI

Chen W, Lian W, Yuan Y, Li M. The synergistic effects of oxaliplatin and piperlongumine on colorectal cancer are mediated by oxidative stress. Cell Death Dis (2019) 10(8):600. doi: 10.1038/s41419-019-1824-6 PubMed DOI PMC

Kim GD. Harmine hydrochloride triggers G2/M cell cycle arrest and apoptosis in HCT116 cells through ERK and PI3K/AKT/mTOR signaling pathways. Prev Nutr Food Sci (2021) 26(4):445–52. doi: 10.3746/pnf.2021.26.4.445 PubMed DOI PMC

Liu J, Li Q, Liu Z, Lin L, Zhang X, Cao M, et al. . Harmine induces cell cycle arrest and mitochondrial pathway-mediated cellular apoptosis in SW620 cells via inhibition of the akt and ERK signaling pathways. Oncol Rep (2016) 35(6):3363–70. doi: 10.3892/or.2016.4695 PubMed DOI

Liang L, Wu J, Luo J, Wang L, Chen ZX, Han CL, et al. . Oxymatrine reverses 5-fluorouracil resistance by inhibition of colon cancer cell epithelial-mesenchymal transition and NF-κB signaling in vitro . Oncol Lett (2020) 19(1):519–26. doi: 10.3892/ol.2019.11090 PubMed DOI PMC

Pan D, Zhang W, Zhang N, Xu Y, Chen Y, Peng J, et al. . Oxymatrine synergistically enhances doxorubicin anticancer effects in colorectal cancer. Front Pharmacol (2021) 12:673432. doi: 10.3389/fphar.2021.673432 PubMed DOI PMC

Kumar A, Singh B, Sharma PR, Bharate SB, Saxena AK, Mondhe DM. A novel microtubule depolymerizing colchicine analogue triggers apoptosis and autophagy in HCT-116 colon cancer cells. Cell Biochem Funct (2016) 34(2):69–81. doi: 10.1002/cbf.3166 PubMed DOI

Huang Z, Xu Y, Peng W. Colchicine induces apoptosis in HT−29 human colon cancer cells via the AKT and c-jun n-terminal kinase signaling pathways. Mol Med Rep (2015) 12(4):5939–44. doi: 10.3892/mmr.2015.4222 PubMed DOI

Seufferlein T, Ettrich TJ, Menzler S, Messmann H, Kleber G, Zipprich A, et al. . Green tea extract to prevent colorectal adenomas, results of a randomized, placebo-controlled clinical trial. Am J Gastroenterol (2022) 117(6):884–94. doi: 10.14309/ajg.0000000000001706 PubMed DOI

Singh AP, Singh R, Verma SS, Rai V, Kaschula CH, Maiti P, et al. . Health benefits of resveratrol: evidence from clinical studies. Med Res Rev (2019) 39(5):1851–91. doi: 10.1002/med.21565 PubMed DOI

Wu XY, Zhai J, Huan XK, Xu WW, Tian J, Farhood B. A systematic review of the therapeutic potential of resveratrol during colorectal cancer chemotherapy. Mini Rev Med Chem (2022) 23(10):1137–52. doi: 10.2174/1389557522666220907145153 PubMed DOI

Sharma RA, Euden SA, Platton SL, Cooke DN, Shafayat A, Hewitt HR, et al. . Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res (2004) 10(20):6847–54. doi: 10.1158/1078-0432.Ccr-04-0744 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...