Chlorogenic acid induces apoptosis and cell-cycle arrest in colorectal cancer cells.


Journal

Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234

Informations de publication

Date de publication:
Dec 2023
Historique:
received: 14 05 2023
accepted: 26 09 2023
medline: 27 11 2023
pubmed: 17 10 2023
entrez: 17 10 2023
Statut: ppublish

Résumé

Apoptotic agents from natural products like phenolic compounds can be used effectively in the treatment of cancer. Chlorogenic acid (CGA) is one of the phenolic compounds in medicinal plants with anti-cancer properties. In this research, we aimed to explore the anti-cancer mode of action of CGA on colorectal cancer (CRC) cells in vitro conditions. HT-29 and HEK-293 cells were cultured after MTT assay for 24 h with CGA 100 µM, and without CGA. Then, flow cytometry assays and the expression of apoptosis-related genes including caspase 3 and 9, Bcl-2 and Bax, and cell cycle-related genes including P21, P53 and NF-κB at mRNA and protein levels were examined. Finally, we measured the amount of intracellular reactive oxygen species (ROS). The cell viability of all two-cell lines decreased in a dose-dependent manner. Moreover, CGA induces cell cycle arrest in HT-29 cells by increasing the expression of P21 and P53. It also induces apoptosis in HT-29 cells by mitigating Bcl-2 and NF-κB expression and elevating caspase 3 and 9 expression and ROS levels. Considering the cytotoxicity and cell cycle arrest and induction of apoptosis in the colon cancer cell line by CGA, it can be concluded that CGA is a suitable option for the treatment of colon cancer.

Sections du résumé

BACKGROUND BACKGROUND
Apoptotic agents from natural products like phenolic compounds can be used effectively in the treatment of cancer. Chlorogenic acid (CGA) is one of the phenolic compounds in medicinal plants with anti-cancer properties. In this research, we aimed to explore the anti-cancer mode of action of CGA on colorectal cancer (CRC) cells in vitro conditions.
METHODS METHODS
HT-29 and HEK-293 cells were cultured after MTT assay for 24 h with CGA 100 µM, and without CGA. Then, flow cytometry assays and the expression of apoptosis-related genes including caspase 3 and 9, Bcl-2 and Bax, and cell cycle-related genes including P21, P53 and NF-κB at mRNA and protein levels were examined. Finally, we measured the amount of intracellular reactive oxygen species (ROS).
RESULTS RESULTS
The cell viability of all two-cell lines decreased in a dose-dependent manner. Moreover, CGA induces cell cycle arrest in HT-29 cells by increasing the expression of P21 and P53. It also induces apoptosis in HT-29 cells by mitigating Bcl-2 and NF-κB expression and elevating caspase 3 and 9 expression and ROS levels.
CONCLUSIONS CONCLUSIONS
Considering the cytotoxicity and cell cycle arrest and induction of apoptosis in the colon cancer cell line by CGA, it can be concluded that CGA is a suitable option for the treatment of colon cancer.

Identifiants

pubmed: 37847443
doi: 10.1007/s11033-023-08854-y
pii: 10.1007/s11033-023-08854-y
doi:

Substances chimiques

Chlorogenic Acid 318ADP12RI
Caspase 3 EC 3.4.22.-
Reactive Oxygen Species 0
NF-kappa B 0
Tumor Suppressor Protein p53 0
Proto-Oncogene Proteins c-bcl-2 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

9845-9857

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Ranjbary AG, Mehrzad J, Dehghani H, Abdollahi A, Hosseinkhani S (2020) Variation in blood and colorectal epithelia’s key trace elements along with expression of mismatch repair proteins from localized and metastatic colorectal cancer patients. Biol Trace Elem Res 194(1):66–75
pubmed: 31172427
Ghorbani Ranjbary A, Mehrzad J, Rahbar N, Dehghani H (2023) Impacts of some clinicopathodemography and colorectal tissues key cell cycle and mucin stabilizing molecules on the metastasis trend in colorectal cancer patients. Mol Biol Rep. https://doi.org/10.1007/s11033-023-08766-x
doi: 10.1007/s11033-023-08766-x pubmed: 37644368
Azimi M, Mehrzad J, Ahmadi A, Ahmadi E, Ghorbani RA (2021) Apoptosis induced by Ziziphora tenuior essential oil in human colorectal cancer cells. Biomed Res Int 2021:5522964
pubmed: 34337019 pmcid: 8324347
Shaghayegh G, Alabsi AM, Ali-Saeed R, Ali AM, Vincent-Chong VK, Zain RB (2016) Cell cycle arrest and mechanism of apoptosis induction in H400 oral cancer cells in response to Damnacanthal and Nordamnacanthal isolated from Morinda citrifolia. Cytotechnology. https://doi.org/10.1007/s10616-016-0014-y
doi: 10.1007/s10616-016-0014-y pubmed: 27488882 pmcid: 5023568
Uzma F, Mohan CD, Hashem A, Konappa NM, Rangappa S, Kamath PV, Singh BP, Mudili V, Gupta VK, Siddaiah CN, Chowdappa S (2018) Endophytic fungi—alternative sources of cytotoxic compounds: a review. Front Pharmacol 9:309
pubmed: 29755344 pmcid: 5932204
Aubrey BJ, Kelly GL, Janic A, Herold MJ, Strasser A (2018) How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death Differ 25(1):104–113
pubmed: 29149101
Barnum KJ, O’Connell MJ (2014) Cell cycle regulation by checkpoints. Cell Cycle Control: Mech Protoc. https://doi.org/10.1007/978-1-4939-0888-2_2
doi: 10.1007/978-1-4939-0888-2_2
Vermeulen K, Berneman ZN, Van Bockstaele DR (2003) Cell cycle and apoptosis. Cell Prolif 36(3):165–175
pubmed: 12814432 pmcid: 6496173
Ranjbary AG, Saleh GK, Azimi M, Karimian F, Mehrzad J, Zohdi J (2023) Superparamagnetic iron oxide nanoparticles induce apoptosis in HT-29 cells by stimulating oxidative stress and damaging DNA. Biol Trace Elem Res 201(3):1163–1173
pubmed: 35451693
Chen J (2016) The cell-cycle arrest and apoptotic functions of p53 in tumor initiation and progression. Cold Spring Harb Perspect Med 6(3):a026104
pubmed: 26931810 pmcid: 4772082
Li T, Kon N, Jiang L, Tan M, Ludwig T, Zhao Y, Baer R, Gu W (2012) Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149(6):1269–1283
pubmed: 22682249 pmcid: 3688046
Büki A, Okonkwo DO, Wang KK, Povlishock JT (2000) Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 20(8):2825–2834
pubmed: 10751434 pmcid: 6772193
Chen Q, Gong B, Almasan A (2000) Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ 7(2):227–233
pubmed: 10713737
Robertson JD, Orrenius S (2000) Molecular mechanisms of apoptosis induced by cytotoxic chemicals. Crit Rev Toxicol 30(5):609–627
pubmed: 11055838
Vaux DL (2011) Apoptogenic factors released from mitochondria. Biochim Biophys Acta (BBA)—Mol Cell Res 1813(4):546–550
Singh SK, Banerjee S, Acosta EP, Lillard JW, Singh R (2017) Resveratrol induces cell cycle arrest and apoptosis with docetaxel in prostate cancer cells via a p53/p21WAF1/CIP1 and p27KIP1 pathway. Oncotarget 8(10):17216
pubmed: 28212547 pmcid: 5370034
Kubczak M, Khassenova AB, Skalski B, Michlewska S, Wielanek M, Skłodowska M, Aralbayeva AN, Nabiyeva ZS, Murzakhmetova MK, Zamaraeva M, Bryszewska M, Ionov M (2022) Hippophae rhamnoides L. leaf and twig extracts as rich sources of nutrients and bioactive compounds with antioxidant activity. Sci Rep 12(1):1095
pubmed: 35058528 pmcid: 8776824
Liang N, Kitts DD (2015) Role of chlorogenic acids in controlling oxidative and inflammatory stress conditions. Nutrients 8(1):16
pubmed: 26712785 pmcid: 4728630
Nabavi SF, Tejada S, Setzer WN, Gortzi O, Sureda A, Braidy N, Daglia M, Manayi A, Nabavi SM (2017) Chlorogenic acid and mental diseases: from chemistry to medicine. Curr Neuropharmacol 15(4):471–479
pubmed: 27012954 pmcid: 5543670
Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2(5):270–278
pubmed: 20716914 pmcid: 2835915
Wang L, Pan X, Jiang L, Chu Y, Gao S, Jiang X, Zhang Y, Chen Y, Luo S, Peng C (2022) The biological activity mechanism of chlorogenic acid and its applications in food industry: a review. Front Nutr 9:943911
pubmed: 35845802 pmcid: 9278960
Yang JS, Liu CW, Ma YS, Weng SW, Tang NY, Wu SH, Ji BC, Ma CY, Ko YC, Funayama S, Kuo CL (2012) Chlorogenic acid induces apoptotic cell death in U937 leukemia cells through caspase-and mitochondria-dependent pathways. In Vivo 26(6):971–978
pubmed: 23160680
Huang MT, Badmaev V, Ding Y, Liu Y, Xie JG, Ho CT (2000) Anti-tumor and anti-carcinogenic activities of triterpenoid, β-boswellic acid. BioFactors 13(1–4):225–230
pubmed: 11237186
Sakagami H, Jiang Y, Kusama K, Atsumi T, Ueha T, Toguchi M, Iwakura I, Satoh K, Fukai T, Nomura T (2000) Induction of apoptosis by flavones, flavonols (3-hydroxyflavones) and isoprenoid-substituted flavonoids in human oral tumor cell lines. Anticancer Res 20(1A):271–277
pubmed: 10769666
Bhattacharya S, Zheng H, Tzimas C, Carroll M, Baker DP, Fuchs SY (2011) Bcr-abl signals to desensitize chronic myeloid leukemia cells to IFNα via accelerating the degradation of its receptor. Blood, J Am Soc Hematol 118(15):4179–4187
Rakshit S, Mandal L, Pal BC, Bagchi J, Biswas N, Chaudhuri J, Chowdhury AA, Manna A, Chaudhuri U, Konar A, Mukherjee T (2010) Involvement of ROS in chlorogenic acid-induced apoptosis of Bcr-Abl+ CML cells. Biochem Pharmacol 80(11):1662–1675
pubmed: 20832390
Ge F, Ke C, Tang W, Yang X, Tang C, Qin G, Xu R, Li T, Chen X, Zuo J, Ye Y (2007) Isolation of chlorogenic acids and their derivatives from Stemona japonica by preparative HPLC and evaluation of their anti-AIV (H5N1) activity in vitro. Phytochem Anal 18(3):213–218
pubmed: 17500364
Vinson JA, Chen X, Garver DD (2019) Determination of total chlorogenic acids in commercial green coffee extracts. J Med Food 22(3):314–320
pubmed: 30888913 pmcid: 6445179
Salzillo A, Ragone A, Spina A, Naviglio S, Sapio L (2021) Chlorogenic acid enhances doxorubicin-mediated cytotoxic effect in osteosarcoma cells. Int J Mol Sci 22(16):8586
pubmed: 34445291 pmcid: 8395331
Du J, Chen C, Sun Y, Zheng L, Wang W (2015) Ponicidin suppresses HT29 cell growth via the induction of G1 cell cycle arrest and apoptosis. Mol Med Rep 12(4):5816–5820
pubmed: 26239027 pmcid: 4581821
Phang CW, Karsani SA, Abd Malek SN (2017) Induction of apoptosis and cell cycle arrest by flavokawain C on HT-29 human colon adenocarcinoma via enhancement of reactive oxygen species generation, upregulation of p21, p27, and Gadd153, and inactivation of inhibitor of apoptosis proteins. Pharmacogn Mag 13(Suppl 2):S321
pubmed: 28808400 pmcid: 5538174
Karimi A, Krähmer A, Herwig N, Schulz H, Hadian J, Meiners T (2020) variation of secondary metabolite profile of Zataria multiflora Boiss. populations linked to geographic, climatic, and edaphic factors. Front Plant Sci 11:969
pubmed: 32719699 pmcid: 7348666
Saei-Dehkordi SS, Tajik H, Moradi M, Khalighi-Sigaroodi F (2010) Chemical composition of essential oils in Zataria multiflora Boiss. from different parts of Iran and their radical scavenging and antimicrobial activity. Food Chem Toxicol 48(6):1562–1567
pubmed: 20332011
Saharkhiz MJ, Smaeili S, Merikhi M (2010) Essential oil analysis and phytotoxic activity of two ecotypes of Zataria multiflora Boiss. growing in Iran. Nat Prod Res 24(17):1598–1609
pubmed: 20954087
Zeng A, Liang X, Zhu S, Liu C, Wang S, Zhang Q, Zhao J, Song L (2021) Chlorogenic acid induces apoptosis, inhibits metastasis and improves antitumor immunity in breast cancer via the NF-κB signaling pathway. Oncol Rep 45(2):717–727
pubmed: 33416150
Sakai E, Farhana F, Yamaguchi Y, Tsukuba T (2022) Potentials of natural antioxidants from plants as antiosteoporotic agents. Stud Nat Prod Chem 72:1–28
Liu YJ, Zhou CY, Qiu CH, Lu XM, Wang YT (2013) Chlorogenic acid induced apoptosis and inhibition of proliferation in human acute promyelocytic leukemia HL-60 cells. Mol Med Rep 8(4):1106–1110
pubmed: 23982123
Wang L, Du H, Chen P (2020) Chlorogenic acid inhibits the proliferation of human lung cancer A549 cell lines by targeting annexin A2 in vitro and in vivo. Biomed Pharmacother 131:110673
pubmed: 32882585
Shi X, Zhou N, Cheng J, Shi X, Huang H, Zhou M, Zhu H (2019) Chlorogenic acid protects PC12 cells against corticosterone-induced neurotoxicity related to inhibition of autophagy and apoptosis. BMC Pharmacol Toxicol 20:1
Antonsson B (2001) Bax and other pro-apoptotic Bcl-2 family” killer-proteins” and their victim the mitochondrion. Cell Tissue Res 306:347–361
pubmed: 11735035
Kapoor I, Bodo J, Hill BT, Hsi ED, Almasan A (2020) Targeting BCL-2 in B-cell malignancies and overcoming therapeutic resistance. Cell Death Dis 11(11):941
pubmed: 33139702 pmcid: 7608616
Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH (2013) Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol 14:1–9
Li Y, Pu R, Zhou L, Wang D, Li X (2021) Effects of a chlorogenic acid-containing herbal medicine (LASNB) on colon cancer. Evid Based Complement Alternat Med 2021(20):9923467
pubmed: 34462643 pmcid: 8403046
Vélez-Vargas LC, Santa-González GA, Uribe D, Henao-Castañeda IC, Pedroza-Díaz J (2023) In Vitro and In silico study on the impact of chlorogenic acid in colorectal cancer cells: proliferation, apoptosis, and interaction with β-catenin and LRP6. Pharmaceuticals (Basel) 16(2):276
pubmed: 37259421
Cheng X, Xu X, Chen D, Zhao F, Wang W (2019) Therapeutic potential of targeting the Wnt/β-catenin signaling pathway in colorectal cancer. Biomed Pharmacother 110:473–481
pubmed: 30530050
Disoma C, Zhou Y, Li S, Peng J, Xia Z (2022) Wnt/β-catenin signaling in colorectal cancer: is therapeutic targeting even possible? Biochimie 195:39–53
pubmed: 35066101
Musaogullari A, Mandato A, Chai YC (2020) Role of glutathione depletion and reactive oxygen species generation on caspase-3 activation: a study with the kinase inhibitor staurosporine. Front Physiol 28(11):998
Collin F (2019) Chemical basis of reactive oxygen species reactivity and involvement in neurodegenerative diseases. Int J Mol Sci 20(10):2407
pubmed: 31096608 pmcid: 6566277
RedzaDutordoir M, Averill-Bates DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys—Mol Cell Res 1863(12):2977–2992
Hou N, Liu N, Han J, Yan Y, Li J (2017) Chlorogenic acid induces reactive oxygen species generation and inhibits the viability of human colon cancer cells. Anticancer Drugs 28(1):59–65
pubmed: 27603595
Liu Z, Liu H, Yuan X, Wang Y, Li L, Wang G, Song J, Shao Z, Fu R (2018) Downregulation of Pim-2 induces cell cycle arrest in the G0/G1 phase via the p53-non-dependent p21 signaling pathway. Oncol Lett 15(4):4079–4086
pubmed: 29541172 pmcid: 5835926
Abbas T, Dutta A (2009) p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9(6):400–414
pubmed: 19440234 pmcid: 2722839
Karimian A, Ahmadi Y, Yousefi B (2016) Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair 42:63–71
pubmed: 27156098
Xia M, Knezevic D, Vassilev LT (2011) p21 does not protect cancer cells from apoptosis induced by nongenotoxic p53 activation. Oncogene 30(3):346–355
pubmed: 20871630
Sadeghi Ekbatan S, Li XQ, Ghorbani M, Azadi B, Kubow S (2018) Chlorogenic acid and its microbial metabolites exert anti-proliferative effects, S-phase cell-cycle arrest and apoptosis in human colon cancer Caco-2 cells. Int J Mol Sci 19(3):723
pubmed: 29510500 pmcid: 5877584

Auteurs

Ali Ghorbani Ranjbary (AG)

Department of Microbiology and Immunology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran. ali.ghorbaniranjbary@mail.um.ac.ir.

Ali Bagherzadeh (A)

Department of Immunology and Oncology, Faculty of Veterinary Medicine, Islamic Azad University-Garmsar Branch, Garmsar, Iran.

Seyed Sina Sabbaghi (SS)

Department of Immunology and Oncology, Faculty of Veterinary Medicine, Islamic Azad University-Garmsar Branch, Garmsar, Iran.

Arshida Faghihi (A)

Department of Chemistry, Faculty of Science Shiraz University, Shiraz, Iran.

Delaram Nassaj Karimi (DN)

Department of Immunology and Oncology, Faculty of Veterinary Medicine, Islamic Azad University-Garmsar Branch, Garmsar, Iran.

Shahryar Naji (S)

Department of Microbiology and Immunology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran.

Mohsen Kardani (M)

Department of Immunology and Oncology, Faculty of Veterinary Medicine, Islamic Azad University-Garmsar Branch, Garmsar, Iran.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH