Inhibition of MDA-MB-231 breast cancer cell migration and invasion activity by andrographolide via suppression of nuclear factor-κB-dependent matrix metalloproteinase-9 expression Corrigendum in /10.3892/mmr.2019.9833

Zhai,Zanjing; Qu,Xinhua; Li,Haowei; Ouyang,Zhengxiao; Yan,Wei; Liu,Guangwang; Liu,Xuqiang; Fan,Qiming; Tang,Tingting; Dai,Kerong; Qin,An

doi:10.3892/mmr.2014.2872

Inhibition of MDA-MB-231 breast cancer cell migration and invasion activity by andrographolide via suppression of nuclear factor-κB-dependent matrix metalloproteinase-9 expression

Corrigendum in: /10.3892/mmr.2019.9833

Authors:
- Zanjing Zhai
- Xinhua Qu
- Haowei Li
- Zhengxiao Ouyang
- Wei Yan
- Guangwang Liu
- Xuqiang Liu
- Qiming Fan
- Tingting Tang
- Kerong Dai
- An Qin
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Affiliations: Shanghai Key Laboratory of Orthopaedic Implants, Department of Orthopaedics, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, P.R. China, Department of Orthopaedics, Wendeng Zhenggu Hospital of Shandong Province, Weihai, Shandong 264400, P.R. China, Department of Orthopedic Surgery, The Central Hospital of Xuzhou, Affiliated Hospital of Medical College of Southeast University, Xuzhou, Jiangsu 221009, P.R. China
Published online on: November 5, 2014 https://doi.org/10.3892/mmr.2014.2872
Pages: 1139-1145

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Abstract

Breast cancer is one of the most common types of cancer worldwide. The majority of patients with cancer succumb to the disease as a result of distant metastases (for example, in the bones), which cause severe complications. Despite advancements in breast cancer treatment, chemotherapeutic outcomes remain far from satisfactory, prompting a search for effective natural agents with few side‑effects. Andrographolide (AP), a natural diterpenoid lactone isolated from Andrographis paniculata, inhibits cancer cell growth. The current study aimed to examine the effect of AP on breast cancer cell proliferation, survival and progression in vitro and also its inhibitory activity on breast cancer bone metastasis in vivo. To achieve this, CCK8, flow cytometry, migration, invasion, western blot, PCR and luciferase reporter assay analyses were performed in vitro as well as establishing intratibial xenograft model of breast cancer bone metastasis in vivo. The results demonstrated that AP inhibits the migration and invasion of the MBA‑MD‑231 aggressive breast cancer cell line at non‑lethal concentrations, in addition to suppressing proliferation and inducing apoptosis at high concentrations in vitro. In vivo, AP significantly inhibited the growth of tumors planted in bone and attenuated cancer‑induced osteolysis. Tartrate‑resistant acid phosphatase staining revealed osteoclast activation in tumor‑bearing mice and AP was observed to attenuate this activation. The anti‑tumor activity of AP in vitro and in vivo correlates with the downregulation of the nuclear factor κB signaling pathway and the inhibition of matrix metalloproteinase‑9 expression levels. These results indicate that AP may be an effective anti‑tumor agent for the treatment of breast cancer bone metastasis.

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1	American Cancer Society. Breast cancer facts & figures 2007–2008. American Cancer Society, Inc; Atlanta, GA: pp. 1–13. 2007
2	Gonzalez-Angulo AM, Morales-Vasquez F and Hortobagyi GN: Overview of resistance to systemic therapy in patients with breast cancer. Breast Cancer Chemosensitivity. Yu D and Hung MC: Springer; New York, NY: pp. 1–22. 2007
3	Lin CW, Shen SC, Hou WC, Yang LY and Chen YC: Heme oxygenase-1 inhibits breast cancer invasion via suppressing the expression of matrix metalloproteinase-9. Mol Cancer Ther. 7:1195–1206. 2008. View Article : Google Scholar : PubMed/NCBI
4	Gialeli C, Theocharis AD and Karamanos NK: Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278:16–27. 2011. View Article : Google Scholar
5	Kessenbrock K, Plaks V and Werb Z: Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 141:52–67. 2010. View Article : Google Scholar : PubMed/NCBI
6	Deryugina EI and Quigley JP: Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochim Biophys Acta. 1803:103–120. 2010. View Article : Google Scholar :
7	Shuman Moss LA, Jensen-Taubman S and Stetler-Stevenson WG: Matrix metalloproteinases: changing roles in tumor progression and metastasis. Am J Pathol. 181:1895–1899. 2012. View Article : Google Scholar : PubMed/NCBI
8	Brinckerhoff CE and Matrisian LM: Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 3:207–214. 2002. View Article : Google Scholar : PubMed/NCBI
9	Overall CM and López-Otín C: Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer. 2:657–672. 2002. View Article : Google Scholar : PubMed/NCBI
10	Chakraborti S, Mandal M, Das S, Mandal A and Chakraborti T: Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem. 253:269–285. 2003. View Article : Google Scholar : PubMed/NCBI
11	Egeblad M and Werb Z: New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2:161–174. 2002. View Article : Google Scholar : PubMed/NCBI
12	Sato H and Seiki M: Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene. 8:395–405. 1993.PubMed/NCBI
13	Ling H, Zhang Y, Ng KY and Chew EH: Pachymic acid impairs breast cancer cell invasion by suppressing nuclear factor-κB-dependent matrix metalloproteinase-9 expression. Breast Cancer Res Treat. 126:609–620. 2011. View Article : Google Scholar
14	Weng CJ, Chau CF, Hsieh YS, Yang SF and Yen GC: Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis. 29:147–156. 2008. View Article : Google Scholar
15	Coon JT and Ernst E: Andrographis paniculata in the treatment of upper respiratory tract infections: a systematic review of safety and efficacy. Planta Med. 70:293–298. 2004. View Article : Google Scholar : PubMed/NCBI
16	Jiang X, Yu P, Jiang J, et al: Synthesis and evaluation of antibacterial activities of andrographolide analogues. Eur J Med Chem. 44:2936–2943. 2009. View Article : Google Scholar : PubMed/NCBI
17	Wang LJ, Zhou X, Wang W, et al: Andrographolide inhibits oral squamous cell carcinogenesis through NF-κB inactivation. J Dental Res. 90:1246–1252. 2011. View Article : Google Scholar
18	Rajagopal S, Kumar RA, Deevi DS, Satyanarayana C and Rajagopalan R: Andrographolide, a potential cancer therapeutic agent isolated from Andrographis paniculata. J Exp Ther Oncol. 3:147–158. 2003. View Article : Google Scholar : PubMed/NCBI
19	Chiou WF, Lin JJ and Chen CF: Andrographolide suppresses the expression of inducible nitric oxide synthase in macrophage and restores the vasoconstriction in rat aorta treated with lipopolysaccharide. Br J Pharmacol. 125:327–334. 1998. View Article : Google Scholar : PubMed/NCBI
20	Shen YC, Chen CF and Chiou WF: Andrographolide prevents oxygen radical production by human neutrophils: possible mechanism(s) involved in its anti-inflammatory effect. Br J Pharmacol. 135:399–406. 2002. View Article : Google Scholar : PubMed/NCBI
21	Trivedi NP, Rawal UM and Patel BP: Potency of andrographolide as an antitumor compound in BHC-induced liver damage. Integr Cancer Ther. 8:177–189. 2009. View Article : Google Scholar : PubMed/NCBI
22	Handa SS and Sharma A: Hepatoprotective activity of andrographolide against galactosamine & paracetamol intoxication in rats. Indian J Med Res. 92:284–292. 1990.PubMed/NCBI
23	Harjotaruno S, Widyawaruyanti A, Sismindari and Zaini NC: Apoptosis inducing effect of andrographolide on TF-47 human breast cancer cell line. Afr J Tradit Complement Altern Med. 4:345–351. 2007.
24	Kumar S, Patil SH, Sharma P, et al: Andrographolide inhibits osteopontin expression and breast tumor growth through down regulation of PI3 kinase/Akt signaling pathway. Curr Mol Med. 12:952–966. 2012. View Article : Google Scholar : PubMed/NCBI
25	Chao CY, Lii CK, Hsu YT, et al: Induction of heme oxygenase-1 and inhibition of TPA-induced matrix metalloproteinase-9 expression by andrographolide in MCF-7 human breast cancer cells. Carcinogenesis. 34:1843–1851. 2013. View Article : Google Scholar : PubMed/NCBI
26	Ooi LL, Zhou H, Kalak R, et al: Vitamin D deficiency promotes human breast cancer growth in a murine model of bone metastasis. Cancer Res. 70:1835–1844. 2010. View Article : Google Scholar : PubMed/NCBI
27	Zheng Y, Zhou H, Modzelewski JR, et al: Accelerated bone resorption, due to dietary calcium deficiency, promotes breast cancer tumor growth in bone. Cancer Res. 67:9542–9548. 2007. View Article : Google Scholar : PubMed/NCBI
28	Traxler P, Allegrini PR, Brandt R, et al: AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res. 64:4931–4941. 2004. View Article : Google Scholar : PubMed/NCBI
29	Wu W, Onn A, Isobe T, et al: Targeted therapy of orthotopic human lung cancer by combined vascular endothelial growth factor and epidermal growth factor receptor signaling blockade. Mol Cancer Ther. 6:471–483. 2007. View Article : Google Scholar : PubMed/NCBI
30	Li H, Zhai Z, Liu G, et al: Sanguinarine inhibits osteoclast formation and bone resorption via suppressing RANKL-induced activation of NF-κB and ERK signaling pathways. Biochem Biophys Res Commun. 430:951–956. 2013. View Article : Google Scholar
31	Ooi LL, Zheng Y, Zhou H, et al: Vitamin D deficiency promotes growth of MCF-7 human breast cancer in a rodent model of osteosclerotic bone metastasis. Bone. 47:795–803. 2010. View Article : Google Scholar : PubMed/NCBI
32	Ghosh S and Hayden MS: New regulators of NF-kappaB in inflammation. Nat Rev Immunol. 8:837–848. 2008. View Article : Google Scholar : PubMed/NCBI
33	Ghosh S and Baltimore D: Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 344:678–682. 1990. View Article : Google Scholar : PubMed/NCBI
34	Duffy MJ, Maguire TM, Hill A, McDermott E and O’Higgins N: Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res. 2:252–257. 2000. View Article : Google Scholar
35	Park JM, Kim A, Oh JH and Chung AS: Methylseleninic acid inhibits PMA-stimulated pro-MMP-2 activation mediated by MT1-MMP expression and further tumor invasion through suppression of NF-kappaB activation. Carcinogenesis. 28:837–847. 2007. View Article : Google Scholar
36	Takada Y, Ichikawa H, Badmaev V and Aggarwal BB: Acetyl-11-keto-beta-boswellic acid potentiates apoptosis, inhibits invasion, and abolishes osteoclastogenesis by suppressing NF-kappa B and NF-kappa B-regulated gene expression. J Immunol. 176:3127–3140. 2006. View Article : Google Scholar : PubMed/NCBI
37	Huang Q, Shen HM and Ong CN: Inhibitory effect of emodin on tumor invasion through suppression of activator protein-1 and nuclear factor-kappaB. Biochem Pharmacol. 68:361–371. 2004. View Article : Google Scholar : PubMed/NCBI