- Open Access
The association between S100A13 and HMGA1 in the modulation of thyroid cancer proliferation and invasion
- Jing Zhong†1,
- Chang Liu†1, 2,
- Ya-jun Chen1, 3,
- Qing-hai Zhang1,
- Jing Yang4,
- Xuan Kang1,
- Si-Rui Chen1,
- Ge-bo Wen1, 4,
- Xu-yu Zu1Email author and
- Ren-xian Cao1, 4Email author
© Zhong et al. 2016
Received: 2 September 2015
Accepted: 2 January 2016
Published: 23 March 2016
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.
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.
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.
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.
S100A13 is a small calcium (Ca2+)-binding protein which belongs to the S100 family. It is characterized by its specificity for diverse forms of cancer [1–3]. S100A13 could regulate secretion of FGF1 and IL1α and could be a marker for vessel density and on a cellular level [4, 5]. In addition S100A13 is also involved in cell cycle progression and differentiation, including cytokine and NF-κB signalling, suggesting that S100A13 may be related to increased aggressiveness of melanoma tumours [6, 7]. Several studies reported positive correlation between the elevated expression of S100A13 and risk of relapse and status of melanoma patients at follow-up, indicating that S100A13 may play a crucial role in melanoma chemoresistance [8, 9]. Moreover, S100A13 was found to be involved in the invasiveness of lung cancer cell lines , and also was detected in tumor cells circulating in blood of patients with metastatic cancer , indicating that this protein may be considered as a predictor of cancer metastases. Recently, a study on cystic papillary thyroid carcimoma (cPTC) confirmed a significant up-regulation of cytokeratin 19 and S100A13 in cPTC compared to benign lesions, suggesting their possible use in fine needle aspiration biopsy based preoperative diagnostics of cystic thyroid lesions . With multiplexed and targeted mass spectrometry method, S100A13 was also found to be elevated in papillary thyroid carcinoma (PTC) compared to normal tissue, suggesting that S100A13 may be considered as a novel candidate PTC biomarker .
High mobility group A (HMGA1) is an architectural transcription factor that encodes a nonhistone chromatin protein. Two isoforms, HMGA1a and HMGA1b are produced which do not show direct transcriptional regulation activities, but they regulate the transcriptional activity of several genes by altering the chromatin structure [14–16]. The expression of HMGA1 is absent or present only at low level in normal cell and adult tissues but are elevated in embryonic cells  and many malignant neoplasias, including breast , pancreas , lung , ovary , colon  and thyroid carcinomas . HMGA1 has been confirmed to associate with the initiation and progression of diverse types of tumors [24–27]. HMGA1 has also been reported to correlate with the presence of metastasis and reduced survival , and could be a poor prognostic marker.
In this study, we examined the effects of S100A13 and HMGA1 on thyroid cancer progression. The results suggest that HMGA1 was involved in the effect of S100A13 on thyroid cancer growth and invasion by modulating the expression of Snail and E-cadherin. In addition, a tissue microarray revealed that higher expressions of both S100A13 and HMGA1 were observed in thyroid cancer cases compared with that in normal thyroid cases. Statistical analysis also confirmed that S100A13 and HMGA1 expressions were positively correlated. This study establish the first link between S100A13 and HMGA1 in thyroid cancer, providing further evidence of the pivotal role of HMGA1 in thyroid cancer progression.
Human thyroid cancer cell line TT, TPC1 and SW579 were purchased from American Type Culture Collection (USA). After thawing, TT cells were cultured in F12 K (N3520; Sigma, USA) medium supplemented with 10 % fetal bovine serum (Gibco, USA) and NaHCO3 2.5 g/L at 37 °C in a humidified atmosphere containing 5 % CO2. TPC1 cells were cultured in DMEM medium supplemented with 10 % fetal bovine serum at 37 °C in a humidified atmosphere containing 5 % CO2. SW579 cells were cultured in L15 medium supplemented with 10 % fetal bovine serum at 37 °C in a humidified atmosphere without CO2. After three passages, cells were used for viral infection.
Western blot analysis
Total cell lysates were lysed on ice for 30 min. Soluble proteins (20 μg) were probed with anti-S100A13, anti-HMGA1, anti-Snail, and anti-E-cadherin antibodies (1:500, Abcam). Loading variations were normalized against β-actin, which was identified by anti-β-actin monoclonal antibody (1:1000, Abcam).
Construction and screening of lentiviral vectors harboring S100A13-specific siRNA
The siRNA sequences targeting to human S100A13 gene (GenBank accession No. NM_001024210) were selected: Target1: ATGAGTACTGGAGATTGAT; Target2: CTCGGAGCTCAAGTTCAAT; and Target3: TGGGCTCTCTTGATGAGAA. Three pairs of complementary oligonucleotides were then designed (Additional file 1: Table S1). The stem-loop oligonucleotides were synthesized and cloned into a lentivirus-based vector carrying the green fluorescent protein (GFP) gene (pGCSIL-GFP, Genechem, Shanghai, China). A universal sequence (PSC-NC: TTCTCCGAACGTGTCACGT) was used as a negative control for RNA interference. Lentiviral particles were prepared as previously described .
Three siRNA-carrying lentiviral vector constructs were used to infect TPC1 at a multiplicity of infection (MOI) of 20 (low MOI) and 40 (high MOI). Three days after infection, GFP expression was detected to calculate the infection efficiency. Five days after infection, cells were harvested. Real-time reverse transcription polymerase chain reaction (RT-PCR) was performed to determine S100A13 knockdown efficiency and screen for the siRNA with the highest knockdown efficiency which was then used for subsequent experiments.
RNA isolation and reverse transcription PCR (RT-PCR)
The SW579 were treated with Scramble RNA or HMGA1 siRNA (40, 80, 160 nM), and maintained in culture medium for 48 h. Total RNA was extracted from the SW579 cells using TRIzol reagent (Invitrogen) and the total RNA was reverse transcribed into cDNA using the first-strand synthesis kit (Gibco-BRL, Carlsbad, CA, USA). The mRNAs of HMGA1, E-cadherin, Snail and β-actin were amplified using the primers (Additional file 2: Table S2). The gene-specific primers were amplified with a denaturation step (95 °C for 2 min), followed by 35 cycles of denaturation (95 °C for 30 s), annealing (55 °C for 30 s) and extension (72 °C for 50 s). Samples from three separate experiments were analyzed in duplicate. The results from RT-PCR were expressed using β-actin as a reference.
Cell proliferation and colony formation assays
For cell proliferation assays, cells were seeded in a 96-well plate (2000 cells/well) and counted using an automated cell counter (Nexcelom Bioscience, Lawrence, MA, USA). For colony formation assay, cells were seeded in a 12-well plate (400 cells/well) and maintained for 8 days. Each experiment was carried out in triplicate and performed at least twice.
Cell invasion assays
For the invasion assays, 10,000 cells were resuspended in serum-free medium and placed in the upper chamber of a 24-well Matrigel™ Invasion Chamber (BD Biosciences, SanDiego, CA, USA) coated with Matrigel. Cell invasion was calculated as the percentage of total cells that had invaded the bottom chamber containing complete medium with serum.
For the scratch-wound assays, cells were transiently transfected with shRNA vectors and grown to confluence. A central linear wound area was carefully created by scraping the cell monolayer with a sterile 200 μl pipette tip, and images were taken after 24 h. Bars represent as the mean percentage of wound closure relative to the initial wound area.
Four-week-old BALB/c female nude mice were fed on the super-clean biological laminar flow shelf for 1 week. All of the in vivo experimental protocols were approved by the Animal Care Committee of South China University. The details of tumour xenografts assay were performed as described previously .
Transient transfection and luciferase activity assay
Transient gene delivery was carried out to assess the effect of HMGA1 on Snail and E-cadherin promoter activity in SW579 cells as described previously . A luciferase assay kit (Promega) was used to measure the reporter activity according to the manufacturer’s instructions. Luciferase activity was normalized by using a Renilla luciferase internal control.
Tissue microarray and immunohistochemical analysis
The tissue microarray (TH8010, US Biomax) consisting 70 thyroid cancer cases and 10 normal cases was utilized, and was histologically interpretable and analyzed for the correlation with clinicopathological parameters. IHC staining was performed as detailed in our previous studies . The mouse monoclonal S100A13 (1:25; ab55701, Abcam) antibody and the rabbit polyclonal HMGA1 antibody (1:150; ab4078, Abcam) were used.
All experiments were performed with three replicates and the results were expressed as the mean ± S.E.M or mean ± SD. Statistical analysis was done using SPSS, version 13.0. A statistical association between clinicopathological and molecular parameters was tested, using non-parametrically two-tailed Mann–Whitney U test. P values < 0.05 were considered significant. Spearman’s rank-correlation coefficients were used to assess the relationship between S100A13 and HMGA1 expression.
S100A13 overexpression increases tumor growth in a TT cell xenograft mouse model
S100A13 knockdown inhibits in vitro cell growth in the least/non-invasive cell line
Colony formation assay showed that the number of formed colonies from TPC1 cells with lentivirus-mediated S100A13 knockdown was markedly decreased compared to those of the control group and the NC group (Fig. 3b, P < 0.01). Whereas, the number of formed colonies of SW579 cells carrying with lentivirus-mediated S100A13 knockdown showed no significant difference to those of the control group and NC group (Additional file 4: Figure S2b). Those results indicated that S100A13 knockdown could inhibit the cell proliferation and colony formation of the least/non-invasive thyroid cancer TPC1 cells, but show no obvious effect on the proliferate ability of invasive thyroid cancer SW579 cells.
S100A13 knockdown inhibits the invasive and migration capabilities through decrease the expression of HMGA1 in thyroid cancer SW579 cells
To determine if S100A13 knockdown was able to affect the invasion properties of thyroid cancer TPC1 cells and SW579 cells, the transwell invasion assay and scratch-wound assay were performed. As shown in Fig. 3c, compared to those of the control group and the NC group, the invasion rate of SW579 cells in the S100A13 knockdown group decreased significantly (P < 0.05). As well as the result of invasion assay, the migration capability of the S100A13 knockdown group decreased significantly compared to those of the control group and the NC group (Fig. 3d, P < 0.01). The invasive and migration capabilities showed no significant difference between the control group and the NC group (Fig. 3c, d). The thyroid cancer TPC1 cells, however, showed no invasive capability even in the control group, and the migration capability of TPC1 cell with the S100A13 knockdown group showed no obvious difference compared to those of the NC group (Additional file 5: Figure S3). To determine if S100A13 knockdown was able to affect the expressions of invasion associated factors, the western blot was performed. As shown in Fig. 3e, S100A13 knockdown could lead to the downregulation of HMGA1 and Snail and the upregulation of E-cadherin in SW579 cells. Moreover, the ectopic S100A13 expression could increase both HMGA1 and Snail mRNA expressions (Additional file 6: Figure S4) and enhance the promoter activities (Additional file 7: Figure S5).
HMGA1 knockdown inhibits in vitro cell growth and invasion
S100A13 correlates with HMGA1 expression in thyroid carcinoma
Correlation of S100A13 and HMGA1 expression with clinicopathological parameters
Expressions of S100A13 and HMGA1 in thyroid normal tissue and cancer
Correlation of S100A13 and HMGA1 expression
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In this study, experiments were performed to determine the effects of S100A13 on cell proliferation, and we demonstrated that the ectopic expression of S100A13 could enhance cellular proliferation of thyroid cancer TT cells in vivo. To further define the effect of S100A13 on other thyroid cancer cells, three lentivirus-mediated S100A13 gene targeting shRNA (KD1, KD2 and KD3) were used to silence the expression of S100A13 in thyroid cancer TPC1 and SW579 cells. It was revealed that the downregulation of S100A13 could inhibit the TPC1 cells growth in vitro and lead to the decrease of invasive and migration ability of SW579 cell line in vitro. Those findings provide evidences for the involvement of S100A13 in the modulation of thyroid cancer cell proliferation and invasion. It was reported that the IL1α-S100A13 complex plays an important role in cell proliferation and angiogenesis, and would be an effective strategy to inhibit a wide range of cancers . It was also reported that S100A13 increased in human astrocytic gliomas, in which it correlates with VEGF-A expression, microvessel density and tumor grading  and it is also associated with a more aggressive, invasive phenotype in lung cancer-derived cell lines . Moreover, S100A13 was detected in tumor cells circulating in blood of patients with metastatic cancer, indicating that S100A13 could be considered as a predictor of metastases .
Intriguingly, the siRNA induced S100A13 downregualtion was found to cause the decreased expression of HMGA1 and Snail and increased E-cadherin expression in SW579 cells, indicating the involvements of HMGA1, Snail and E-cadherin in S100A13 induced celluar proliferation and invasion. Recent study reports silencing HMGA1 could block proliferation, migration and invasion of triple negative breast cancer MDA-MB-231 cells. Mesenchymal genes (Vimentin, Snail) are repressed, while E-cadherin is induced in the HMGA1 knock-down cells . In our study, the downregulation of HMGA1 was further confirmed to be able to decrease and increase the expression of Snail and E-cadherin respectively, resulting in the suppression of TPC1 cells proliferation and SW579 cells invasion. Those results indicate that S100A13 and HMGA1 show the consisitent effects on the proliferation and invasion of thyroid cancer cells.
The higher expressions of both S100A13 and HMGA1 were observed in thyroid cancer tissues compared with that in normal thyroid tissues through the analysis of tissue microarray, indicating that the elevated expression of S100A13 and HMGA1 in thyroid cancer tissue might play a role in the initiation and progression of thyroid cancer. Further analysis to the tissue microarray data unraveled a positive correlation between S100A13 and HMGA1 expression (P = 0.004) regardless of thyroid cancer types, which is consistent with the results from cells models, suggesting that S100A13 may be of importance in regulating HMGA1 expression in human thyroid cancer, and that S100A13 might be responsible for the increased ability of proliferation and invasion in thyroid cancer cells. Moreover, the expressions of S100A13 and HMGA1 in thyroid carcinoma were shown to be associated with the patient sex and tumor types, which is not be reported in other cancers previously. The further clarification of underlying molecular events would be helpful for understanding the role of S100A13 and HMGA1 in the progression of thyroid cancer.
In summary, 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.
JZ, XK, SC carried out the molecular studies and cellular assays. CL and YC carried out nude mice xenografts assays. QZ and JY carried out the immunoassays and performed the statistical analysis. JZ and GW participated in the design of the study and draft the manuscript. XZ and RC helped to design the study. All authors read and approved the final manuscript.
This work is supported by projects from the National Natural Science Foundation of People’s Republic of China (Grant No. 31200573, 81172542), Hunan Provincial Natural Science Foundation of China (12JJ3116, 13JJ6051), and The Health Department of Hunan Province (B2014-176).
The authors declare that they have no competing interests.
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- Dinarello CA. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int Rev Immunol. 1998;16:457–99.View ArticlePubMedGoogle Scholar
- Maini RN, Taylor PC. Anti-cytokine therapy for rheumatoid arthritis. Annu Rev Med. 2000;51:207–29.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta. 2010;1799:3–14.View ArticlePubMedPubMed CentralGoogle Scholar
- Resar LM. The high mobility group A1 gene: transforming inflammatory signals into cancer? Cancer Res. 2010;70:436–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Fusco A, Fedele M. Roles of HMGA proteins in cancer. Nat Rev Cancer. 2007;7:899–910.View ArticlePubMedGoogle Scholar
- Fedele M, Fusco A. HMGA and cancer. Biochim Biophys Acta. 2010;1799:48–54.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.PubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.PubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.PubMedGoogle Scholar
- 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.View ArticlePubMedPubMed CentralGoogle Scholar
- Salama I, Malone PS, Mihaimeed F, Jones JL. A review of the S100 proteins in cancer. Eur J Surg Oncol. 2008;34:357–64.View ArticlePubMedGoogle Scholar
- Garrett SC, Varney KM, Weber DJ, Bresnick AR. S100A4, a mediator of metastasis. J Biol Chem. 2006;281:677–80.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticleGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar
- 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.View ArticlePubMedGoogle Scholar