Top

Published in:

Open Access 01-12-2016 | Research

The association between S100A13 and HMGA1 in the modulation of thyroid cancer proliferation and invasion

Authors: Jing Zhong, Chang Liu, Ya-jun Chen, Qing-hai Zhang, Jing Yang, Xuan Kang, Si-Rui Chen, Ge-bo Wen, Xu-yu Zu, Ren-xian Cao

Published in: Journal of Translational Medicine | Issue 1/2016

Abstract

Background

S100A13 and high mobility group A (HMGA1) are known to play essential roles in the carcinogenesis and progression of cancer. However, the correlation between S100A13 and HMGA1 during cancer progression is not yet well understood. In this study, we determined the effects of S100A13 on HMGA1 expression in thyroid cancer cells and examined the role of HMGA1 in thyroid cancer progression.

Methods

Stable ectopic S100A13 expression TT cellular proliferation was evaluated by nude mice xenografts assays. The effect of lentivirus-mediated S100A13 knockdown on thyroid cancer cellular oncogenic properties were evaluated by MTT, colony formation assays and transwell assays in TPC1 and SW579 cells. The effect of siRNA-mediated HMGA1 knockdown on thyroid cancer cellular proliferation and invasion were evaluated by MTT, colony formation assays and transwell assays. The tissue microarray was performed to investigate the correlation between S100A13 and HMGA1 expression in tumor tissues.

Results

The ectopic expression of S100A13 could increase tumor growth in a TT cell xenograft mouse model. Moreover, lentivirus-mediated S100A13 knockdown led to the inhibition of cellular oncogenic properties in thyroid cancer cells, and HMGA1 was found to be involved in the effect of S100A13 on thyroid cancer growth and invasion. Furthermore, siRNA-mediated HMGA1 knockdown was proved to inhibit the growth of TPC1 cells and invasive abilities of SW579 cells. Clinically, it was revealed that both S100A13 and HMGA1 showed a higher expression levels in thyroid cancer cases compared with those in matched normal thyroid cases (P = 0.007 and P = 0.000); S100A13 and HMGA1 expressions were identified to be positively correlated (P = 0.004, R = 0.316) when analyzed regardless of thyroid cancer types.

Conclusions

This is the first report for the association between HMGA1 and S100A13 expression in the modulation of thyroid cancer growth and invasion. Those results would provide an essential insight into the effect of S100A13 on carcinogenesis of thyroid tumor, rending S100A13 to be potential biological marker for the diagnosis of thyroid cancer.

Available only for authorised users

Dinarello CA. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int Rev Immunol. 1998;16:457–99.CrossRefPubMed

Maini RN, Taylor PC. Anti-cytokine therapy for rheumatoid arthritis. Annu Rev Med. 2000;51:207–29.CrossRefPubMed

Kawaguchi Y, Nishimagi E, Tochimoto A, Kawamoto M, Katsumata Y, Soejima M, et al. Intracellular IL-1α-binding proteins contribute to biological functions of endogenous IL-1α in systemic sclerosis fibroblasts. Proc Natl Acad Sci USA. 2006;103:14501–6.CrossRefPubMedPubMedCentral

Cao R, Yan B, Yang H, Zu X, Wen G, Zhong J. Effect of human S100A13 gene silencing on FGF-1 transportation in human endothelial cells. J Formos Med Assoc. 2010;109:632–40.CrossRefPubMed

Mohan SK, Yu C. The IL1α-S100A13 heterotetrameric complex structure: a component in the non-classical pathway for interleukin 1α secretion. J Biol Chem. 2011;286:14608–17.CrossRefPubMedPubMedCentral

Hsieh HL, Schafer BW, Weigle B, Heizmann CW. S100 protein translocation in response to extracellular S100 is mediated by receptor for advanced glycation endproducts in human endothelial cells. Biochem Biophys Res Commun. 2004;316:949–59.CrossRefPubMed

Massi D, Landriscina M, Piscazzi A, Cosci E, Kirov A, Paglierani M, et al. S100A13 is a new angiogenic marker in human melanoma. Mod Pathol. 2010;23:804–13.CrossRefPubMedPubMedCentral

Azimi A, Pernemalm M, Frostvik Stolt M, Hansson J, Lehtio J, Egyhazi Brage S, et al. Proteomics analysis of melanoma metastases: association between S100A13 expression and chemotherapy resistance. Br J Cancer. 2014;110:2489–95.CrossRefPubMedPubMedCentral

Paulitschke V, Haudek-Prinz V, Griss J, Berger W, Mohr T, Pehamberger H, et al. Functional classification of cellular proteome profiles support the identification of drug resistance signatures in melanoma cells. J Proteome Res. 2013;12:3264–76.CrossRefPubMedPubMedCentral

10.

Pierce A, Barron N, Linehan R, Ryan E, O’Driscoll L, Daly C, et al. Identification of a novel, functional role for S100A13 in invasive lung cancer cell lines. Eur J Cancer. 2008;44:151–9.CrossRefPubMed

11.

Smirnov DA, Zweitzig DR, Foulk BW, Miller MC, Doyle GV, Pienta KJ, et al. Global gene expression profiling of circulating tumor cells. Cancer Res. 2005;65:4993–7.CrossRefPubMed

12.

Dinets A, Pernemalm M, Kjellin H, Sviatoha V, Sofiadis A, Juhlin CC, et al. Differential protein expression profiles of cyst fluid from papillary thyroid carcinoma and benign thyroid lesions. PLoS One. 2015;10:e0126472.CrossRefPubMedPubMedCentral

13.

Martinez-Aguilar J, Clifton-Bligh R, Molloy MP. A multiplexed, targeted mass spectrometry assay of the S100 protein family uncovers the isoform-specific expression in thyroid tumours. BMC Cancer. 2015;15:199.CrossRefPubMedPubMedCentral

14.

Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta. 2010;1799:3–14.CrossRefPubMedPubMedCentral

15.

Resar LM. The high mobility group A1 gene: transforming inflammatory signals into cancer? Cancer Res. 2010;70:436–9.CrossRefPubMedPubMedCentral

16.

Fusco A, Fedele M. Roles of HMGA proteins in cancer. Nat Rev Cancer. 2007;7:899–910.CrossRefPubMed

17.

Fedele M, Fusco A. HMGA and cancer. Biochim Biophys Acta. 2010;1799:48–54.CrossRefPubMed

18.

Shah SN, Cope L, Poh W, Belton A, Roy S, Talbot CC Jr, et al. HMGA1: a master regulator of tumor progression in triple-negative breast cancer cells. PLoS One. 2013;8:e63419.CrossRefPubMedPubMedCentral

19.

Abe N, Watanabe T, Masaki T, Mori T, Sugiyama M, Uchimura H, et al. Pancreatic duct cell carcinomas express high levels of high mobility group I(Y) proteins. Cancer Res. 2000;60:3117–22.PubMed

20.

Meyer B, Loeschke S, Schultze A, Weigel T, Sandkamp M, Goldmann T, et al. HMGA2 overexpression in non-small cell lung cancer. Mol Carcinog. 2007;46:503–11.CrossRefPubMed

21.

Masciullo V, Baldassarre G, Pentimalli F, Berlingieri MT, Boccia A, Chiappetta G, et al. HMGA1 protein over-expression is a frequent feature of epithelial ovarian carcinomas. Carcinogenesis. 2003;24:1191–8.CrossRefPubMed

22.

Belton A, Gabrovsky A, Bae YK, Reeves R, Iacobuzio-Donahue C, Huso DL, et al. HMGA1 induces intestinal polyposis in transgenic mice and drives tumor progression and stem cell properties in colon cancer cells. PLoS One. 2012;7:e30034.CrossRefPubMedPubMedCentral

23.

Chiappetta G, Tallini G, De Biasio MC, Manfioletti G, Martinez-Tello FJ, Pentimalli F, et al. Detection of high mobility group I HMGI(Y) protein in the diagnosis of thyroid tumors: HMGI(Y) expression represents a potential diagnostic indicator of carcinoma. Cancer Res. 1998;58:4193–8.PubMed

24.

Puca F, Colamaio M, Federico A, Gemei M, Tosti N, Bastos AU, et al. HMGA1 silencing restores normal stem cell characteristics in colon cancer stem cells by increasing p53 levels. Oncotarget. 2014;5:3234–45.CrossRefPubMedPubMedCentral

25.

Karp JE, Smith BD, Resar LS, Greer JM, Blackford A, Zhao M, et al. Phase 1 and pharmacokinetic study of bolus-infusion flavopiridol followed by cytosine arabinoside and mitoxantrone for acute leukemias. Blood. 2011;117:3302–10.CrossRefPubMedPubMedCentral

26.

Nelson DM, Joseph B, Hillion J, Segal J, Karp JE, Resar LM. Flavopiridol induces BCL-2 expression and represses oncogenic transcription factors in leukemic blasts from adults with refractory acute myeloid leukemia. Leuk Lymphoma. 2011;52:1999–2006.CrossRefPubMedPubMedCentral

27.

Pegoraro S, Ros G, Piazza S, Sommaggio R, Ciani Y, Rosato A, et al. HMGA1 promotes metastatic processes in basal-like breast cancer regulating EMT and stemness. Oncotarget. 2013;4:1293–308.CrossRefPubMedPubMedCentral

28.

Huang R, Huang D, Dai W, Yang F. Overexpression of HMGA1 correlates with the malignant status and prognosis of breast cancer. Mol Cell Biochem. 2015;404:251–7.CrossRefPubMed

29.

Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science. 2002;295:868–72.CrossRefPubMed

30.

Zhong J, Cao RX, Liu JH, Liu YB, Wang J, Liu LP, et al. Nuclear loss of protein arginine N-methyltransferase 2 in breast carcinoma is associated with tumor grade and overexpression of cyclin D1 protein. Oncogene. 2014;33:5546–58.CrossRefPubMed

31.

Zhong J, Cao RX, Zu XY, Hong T, Yang J, Liu L, et al. Identification and characterization of novel spliced variants of PRMT2 in breast carcinoma. FEBS J. 2012;279:316–35.CrossRefPubMed

32.

Cao RX, Tian LN, Wen F, Liu X, Zhong J, Wen GB. Overexpressing exogenous S100A13 gene and its effect on proliferation of human thyroid cancer cell line TT. Ai Zheng. 2008;27:822–7.PubMed

33.

Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, et al. Functions of S100 proteins. Curr Mol Med. 2013;13:24–57.CrossRefPubMedPubMedCentral

34.

Salama I, Malone PS, Mihaimeed F, Jones JL. A review of the S100 proteins in cancer. Eur J Surg Oncol. 2008;34:357–64.CrossRefPubMed

35.

Garrett SC, Varney KM, Weber DJ, Bresnick AR. S100A4, a mediator of metastasis. J Biol Chem. 2006;281:677–80.CrossRefPubMed

36.

Krop I, Marz A, Carlsson H, Li X, Bloushtain-Qimron N, Hu M, et al. A putative role for psoriasin in breast tumor progression. Cancer Res. 2005;65:11326–34.CrossRefPubMed

37.

Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O. Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int J Cancer. 1997;74:464–9.CrossRefPubMed

38.

Nipp M, Elsner M, Balluff B, Meding S, Sarioglu H, Ueffing M, et al. S100-A10, thioredoxin, and S100-A6 as biomarkers of papillary thyroid carcinoma with lymph node metastasis identified by MALDI imaging. J Mol Med (Berl). 2012;90:163–74.CrossRef

39.

Zhang L, Fogg DK, Waisman DM. RNA interference-mediated silencing of the S100A10 gene attenuates plasmin generation and invasiveness of Colo 222 colorectal cancer cells. J Biol Chem. 2004;279:2053–62.CrossRefPubMed

40.

Landriscina M, Bagala C, Mandinova A, Soldi R, Micucci I, Bellum S, et al. Copper induces the assembly of a multiprotein aggregate implicated in the release of fibroblast growth factor 1 in response to stress. J Biol Chem. 2001;276:25549–57.CrossRefPubMed

41.

Matsunaga H, Ueda H. Stress-induced non-vesicular release of prothymosin-alpha initiated by an interaction with S100A13, and its blockade by caspase-3 cleavage. Cell Death Differ. 2010;17:1760–72.CrossRefPubMed

42.

Rani SG, Mohan SK, Yu C. Molecular level interactions of S100A13 with amlexanox: inhibitor for formation of the multiprotein complex in the nonclassical pathway of acidic fibroblast growth factor. Biochemistry. 2010;49:2585–92.CrossRefPubMed

43.

Matsunaga H, Ueda H. Synergistic Ca2+ and Cu2+ requirements of the FGF1-S100A13 interaction measured by quartz crystal microbalance: an initial step in amlexanox-reversible non-classical release of FGF1. Neurochem Int. 2008;52:1076–85.CrossRefPubMed

Title: The association between S100A13 and HMGA1 in the modulation of thyroid cancer proliferation and invasion
Authors: Jing Zhong
Chang Liu
Ya-jun Chen
Qing-hai Zhang
Jing Yang
Xuan Kang
Si-Rui Chen
Ge-bo Wen
Xu-yu Zu
Ren-xian Cao
Publication date: 01-12-2016
Publisher: BioMed Central
Published in: Journal of Translational Medicine / Issue 1/2016
Electronic ISSN: 1479-5876
DOI: https://doi.org/10.1186/s12967-016-0824-x

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2016

Increased expression of upstream TH2-cytokines in a mouse model of viral-induced asthma exacerbation

Slow induction of brain death leads to decreased renal function and increased hepatic apoptosis in rats

Single nucleotide polymorphisms in apoptosis pathway are associated with response to imatinib therapy in chronic myeloid leukemia

The fibrolytic potentials of vitamin D and thymoquinone remedial therapies: insights from liver fibrosis established by CCl4 in rats

Effects of the intramyocardial implantation of stromal vascular fraction in patients with chronic ischemic cardiomyopathy

The role of cancer-associated fibroblasts in esophageal cancer

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials