Top

Published in:

01-07-2018 | Laboratory Investigation

AnnexinA5 promote glioma cell invasion and migration via the PI3K/Akt/NF-κB signaling pathway

Authors: Chenxing Ji, Hua Guo, Pei Zhang, Wei Kuang, Yanghua Fan, Lei Wu

Published in: Journal of Neuro-Oncology | Issue 3/2018

Abstract

As an important member of the Annexins, AnnexinA5 has been attributed important functions in trophoblast membrane repair, anticoagulation and cellular signal transduction. Accumulated studies show that AnnexinA5 is closely associated with various types of carcinomas. However, the potential contribution of AnnexinA5 to glioma cancer progression remains unclear. In this study, we report that AnnexinA5 is significantly upregulated in both high-grade glioma samples and glioma cell lines. Moreover, overexpression of AnnexinA5 promotes cell migration and invasion in vitro and tumorigenicity of glioma cells in nude mice, while knockdown of AnnexinA5 manifests a repressive function during these cellular processes. Importantly, mechanistic studies further reveal that AnnexinA5 is an essential transcriptional target of Snail via activating the PI3K/Akt/NF-κB signaling pathway. Taken together, these findings suggest that AnnexinA5 or the PI3K/Akt/NF-κB pathway may be promising therapeutic molecules to eradicate glioma metastases.

Available only for authorised users

Chhabda S, Carney O, D’Arco F, Jacques TS, Mankad K (2016) The 2016 World Health Organization Classification of tumours of the Central Nervous System: what the paediatric neuroradiologist needs to know. Quant Imaging Med Surg 6:486–489. https://doi.org/10.21037/qims.2016.10.01 CrossRefPubMedPubMedCentral

Komori T, Sasaki H, Yoshida K (2016) Revised WHO classification of tumours of the central nervous system: summary of the revision and perspective. No shinkei geka Neurol Surg 44:625–635. https://doi.org/10.11477/mf.1436203347 CrossRef

Jansen M, Yip S, Louis DN (2010) Molecular pathology in adult gliomas: diagnostic, prognostic, and predictive markers. Lancet Neurol 9:717–726. https://doi.org/10.1016/S1474-4422(10)70105-8 CrossRefPubMedPubMedCentral

Rock K, McArdle O, Forde P, Dunne M, Fitzpatrick D, O’Neill B, Faul C (2012) A clinical review of treatment outcomes in glioblastoma multiforme–the validation in a non-trial population of the results of a randomised Phase III clinical trial: has a more radical approach improved survival? Br J Radiol 85:e729-733. https://doi.org/10.1259/bjr/83796755 CrossRef

Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109. https://doi.org/10.1007/s00401-007-0243-4 CrossRefPubMedPubMedCentral

Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ (2010) Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA 60:166–193. https://doi.org/10.3322/caac.20069 PubMedPubMedCentralCrossRef

Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15:1311–1333. https://doi.org/10.1101/gad.891601 CrossRefPubMed

Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371. https://doi.org/10.1152/physrev.00030.2001 CrossRefPubMed

Xue G, Hao LQ, Ding FX, Mei Q, Huang JJ, Fu CG, Yan HL, Sun SH (2009) Expression of annexin a5 is associated with higher tumor stage and poor prognosis in colorectal adenocarcinomas. J Clin Gastroenterol 43:831–837. https://doi.org/10.1097/MCG.0b013e31819cc731 CrossRefPubMed

10.

Sun B, Bai Y, Zhang L, Gong L, Qi X, Li H, Wang F, Chi X, Jiang Y, Shao S (2016) Quantitative proteomic profiling the molecular signatures of annexin A5 in lung squamous carcinoma cells. PloS ONE 11:e0163622. https://doi.org/10.1371/journal.pone.0163622 CrossRefPubMedPubMedCentral

11.

Lee EK, Cho H, Kim CW (2011) Proteomic analysis of cancer stem cells in human prostate cancer cells. Biochem Biophys Res Commun 412:279–285. https://doi.org/10.1016/j.bbrc.2011.07.083 CrossRefPubMed

12.

Martin M, Leffler J, Blom AM (2012) Annexin A2 and A5 serve as new ligands for C1q on apoptotic cells. J Biol Chem 287:33733–33744. https://doi.org/10.1074/jbc.M112.341339 CrossRefPubMedPubMedCentral

13.

Li X, Chen L, Liang XJ, Gao YF, Wang XJ, Xu Q, Yan Y, Gao FL (2012) Annexin A5 protein expression is associated with the histological differentiation of uterine cervical squamous cell carcinoma in patients with an increased serum concentration. Mol Med Rep 6:1249–1254. https://doi.org/10.3892/mmr.2012.1078 CrossRefPubMed

14.

Rajcevic U, Petersen K, Knol JC, Loos M, Bougnaud S, Klychnikov O, Li KW, Pham TV, Wang J, Miletic H, Peng Z, Bjerkvig R, Jimenez CR, Niclou SP (2009) iTRAQ-based proteomics profiling reveals increased metabolic activity and cellular cross-talk in angiogenic compared with invasive glioblastoma phenotype. Mol Cell Proteomics 8:2595–2612. https://doi.org/10.1074/mcp.M900124-MCP200 CrossRefPubMedPubMedCentral

15.

Shi X, Zhan L, Xiao C, Lei Z, Yang H, Wang L, Zhao J, Zhang HT (2015) miR-1238 inhibits cell proliferation by targeting LHX2 in non-small cell lung cancer. Oncotarget 6:19043–19054. https://doi.org/10.18632/oncotarget.4232 PubMedPubMedCentralCrossRef

16.

Duan R, Han L, Wang Q, Wei J, Chen L, Zhang J, Kang C, Wang L (2015) HOXA13 is a potential GBM diagnostic marker and promotes glioma invasion by activating the Wnt and TGF-beta pathways. Oncotarget 6:27778–27793. https://doi.org/10.18632/oncotarget.4813 PubMedPubMedCentralCrossRef

17.

Li W, Zheng J, Deng J, You Y, Wu H, Li N, Lu J, Zhou Y (2014) Increased levels of the long intergenic non-protein coding RNA POU3F3 promote DNA methylation in esophageal squamous cell carcinoma cells. Gastroenterology 146:1714–1726 e1715. https://doi.org/10.1053/j.gastro.2014.03.002 CrossRefPubMed

18.

Wang J, Zhang Y, Liu X, Ma J, Liu P, Hu C, Zhang G (2014) Annexin A5 inhibits diffuse large B-cell lymphoma cell invasion and chemoresistance through phosphatidylinositol 3-kinase signaling. Oncol Rep 32:2557–2563. https://doi.org/10.3892/or.2014.3547 CrossRefPubMed

19.

Wu L, Yang L, Xiong Y, Guo H, Shen X, Cheng Z, Zhang Y, Gao Z, Zhu X (2014) Annexin A5 promotes invasion and chemoresistance to temozolomide in glioblastoma multiforme cells. Tumour Biol 35:12327–12337. https://doi.org/10.1007/s13277-014-2545-1 CrossRefPubMed

20.

Singh AR, Joshi S, George E, Durden DL (2014) Anti-tumor effect of a novel PI3-kinase inhibitor, SF1126, in (12) V-Ha-Ras transgenic mouse glioma model. Cancer Cell Int 14:105. https://doi.org/10.1186/s12935-014-0105-9 CrossRefPubMedPubMedCentral

21.

Shingu T, Yamada K, Hara N, Moritake K, Osago H, Terashima M, Uemura T, Yamasaki T, Tsuchiya M (2003) Synergistic augmentation of antimicrotubule agent-induced cytotoxicity by a phosphoinositide 3-kinase inhibitor in human malignant glioma cells. Cancer Res 63:4044–4047PubMed

22.

Gaelzer MM, Coelho BP, de Quadros AH, Hoppe JB, Terra SR, Guerra MC, Usach V, Guma FC, Goncalves CA, Setton-Avruj P, Battastini AM, Salbego CG (2016) Phosphatidylinositol 3-Kinase/AKT pathway inhibition by doxazosin promotes glioblastoma cells death, upregulation of p53 and triggers low neurotoxicity. PloS ONE 11:e0154612. https://doi.org/10.1371/journal.pone.0154612 CrossRefPubMedPubMedCentral

23.

Moss SE, Morgan RO (2004) The annexins. Genome Biol 5:219. https://doi.org/10.1186/gb-2004-5-4-219 CrossRefPubMedPubMedCentral

24.

Laohavisit A, Davies JM (2011) Annexins. New Phytol 189:40–53. https://doi.org/10.1111/j.1469-8137.2010.03533.x CrossRefPubMed

25.

Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. J Exp Bot 59:533–544. https://doi.org/10.1093/jxb/erm344 CrossRefPubMed

26.

Shin DW, Kwon YJ, Ye DJ, Baek HS, Lee JE, Chun YJ (2016) Auranofin suppresses plasminogen activator inhibitor-2 expression through annexin A5 induction in human prostate cancer cells. Biomol Ther. https://doi.org/10.4062/biomolther.2016.223 CrossRef

27.

Hong M, Park N, Chun YJ (2014) Role of annexin a5 on mitochondria-dependent apoptosis induced by tetramethoxystilbene in human breast cancer cells. Biomol Ther 22:519–524. https://doi.org/10.4062/biomolther.2014.112 CrossRef

28.

Park N, Chun YJ (2014) Auranofin promotes mitochondrial apoptosis by inducing annexin A5 expression and translocation in human prostate cancer cells. J Toxicol Environ Health A 77:1467–1476. https://doi.org/10.1080/15287394.2014.955834 CrossRefPubMed

29.

Tang Y, Lv P, Sun Z, Han L, Luo B, Zhou W (2015) 14-3-3zeta up-regulates hypoxia-inducible factor-1alpha in hepatocellular carcinoma via activation of PI3K/Akt/NF-small ka, CyrillicB signal transduction pathway. Int J Clin Exp Pathol 8:15845–15853PubMedPubMedCentral

30.

Shan RF, Zhou YF, Peng AF, Jie ZG (2014) Inhibition of Aurora-B suppresses HepG2 cell invasion and migration via the PI3K/Akt/NF-kappaB signaling pathway in vitro. Exp Ther Med 8:1005–1009. https://doi.org/10.3892/etm.2014.1844 CrossRefPubMedPubMedCentral

31.

Rodriguez M, Luo W, Weng J, Zeng L, Yi Z, Siwko S, Liu M (2014) PSGR promotes prostatic intraepithelial neoplasia and prostate cancer xenograft growth through NF-kappaB. Oncogenesis 3:e114. https://doi.org/10.1038/oncsis.2014.29 CrossRefPubMedPubMedCentral

32.

Felx M, Guyot MC, Isler M, Turcotte RE, Doyon J, Khatib AM, Leclerc S, Moreau A, Moldovan F (2006) Endothelin-1 (ET-1) promotes MMP-2 and MMP-9 induction involving the transcription factor NF-kappaB in human osteosarcoma. Clin Sci 110:645–654. https://doi.org/10.1042/CS20050286 CrossRefPubMed

33.

Ahmad A, Biersack B, Li Y, Kong D, Bao B, Schobert R, Padhye SB, Sarkar FH (2013) Targeted regulation of PI3K/Akt/mTOR/NF-kappaB signaling by indole compounds and their derivatives: mechanistic details and biological implications for cancer therapy. Anti-cancer Agents Med Chem 13:1002–1013CrossRef

34.

Zhang LL, Mu GG, Ding QS, Li YX, Shi YB, Dai JF, Yu HG (2015) Phosphatase and tensin homolog (PTEN) represses colon cancer progression through inhibiting paxillin transcription via PI3K/AKT/NF-kappaB pathway. J Biol Chem 290:15018–15029. https://doi.org/10.1074/jbc.M115.641407 CrossRefPubMed

35.

Jiao Y, Li H, Liu Y, Guo A, Xu X, Qu X, Wang S, Zhao J, Li Y, Cao Y (2015) Resveratrol inhibits the invasion of glioblastoma-initiating cells via down-regulation of the PI3K/Akt/NF-kappaB signaling pathway. Nutrients 7:4383–4402. https://doi.org/10.3390/nu7064383 CrossRefPubMedPubMedCentral

Title: AnnexinA5 promote glioma cell invasion and migration via the PI3K/Akt/NF-κB signaling pathway
Authors: Chenxing Ji
Hua Guo
Pei Zhang
Wei Kuang
Yanghua Fan
Lei Wu
Publication date: 01-07-2018
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 3/2018
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-018-2818-4

At a glance: The STEP trials

Springer Medicine

AnnexinA5 promote glioma cell invasion and migration via the PI3K/Akt/NF-κB signaling pathway

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2018

Repeat stereotactic radiosurgery for Cushing’s disease: outcomes of an international, multicenter study

A surgical strategy using a fusion image constructed from 11C-methionine PET, 18F-FDG-PET and MRI for glioma with no or minimum contrast enhancement

Multi-institutional study of treatment patterns in Korean patients with WHO grade II gliomas: KNOG 15-02 and KROG 16-04 intergroup study

Sym004-induced EGFR elimination is associated with profound anti-tumor activity in EGFRvIII patient-derived glioblastoma models

Timing of re-irradiation in recurrent high-grade gliomas: a single institution study

Malignancy probability map as a novel imaging biomarker to predict malignancy distribution: employing MRS in GBM patients