Tissue mRNA for S100A4, S100A6, S100A8, S100A9, S100A11 and S100P Proteins in Colorectal Neoplasia: A Pilot Study
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
academic project PROGRES Q40-15
Univerzita Karlova v Praze
PubMed
33466593
PubMed Central
PMC7828666
DOI
10.3390/molecules26020402
PII: molecules26020402
Knihovny.cz E-resources
- Keywords
- S100 proteins, colorectal neoplasia, large intestine, mRNA,
- MeSH
- Adenoma genetics metabolism pathology MeSH
- Calgranulin A genetics metabolism MeSH
- Calgranulin B genetics metabolism MeSH
- Colorectal Neoplasms genetics metabolism pathology MeSH
- Middle Aged MeSH
- Humans MeSH
- RNA, Messenger genetics metabolism MeSH
- Biomarkers, Tumor genetics metabolism MeSH
- Neoplasm Proteins genetics metabolism MeSH
- Follow-Up Studies MeSH
- Pilot Projects MeSH
- Prognosis MeSH
- S100 Calcium Binding Protein A6 genetics metabolism MeSH
- Cell Cycle Proteins genetics metabolism MeSH
- S100 Proteins genetics metabolism MeSH
- Calcium-Binding Proteins genetics metabolism MeSH
- S100 Calcium-Binding Protein A4 genetics metabolism MeSH
- Aged MeSH
- Case-Control Studies MeSH
- Check Tag
- Middle Aged MeSH
- Humans MeSH
- Male MeSH
- Aged MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Calgranulin A MeSH
- Calgranulin B MeSH
- RNA, Messenger MeSH
- Biomarkers, Tumor MeSH
- Neoplasm Proteins MeSH
- S100 Calcium Binding Protein A6 MeSH
- Cell Cycle Proteins MeSH
- S100 Proteins MeSH
- Calcium-Binding Proteins MeSH
- S100 Calcium-Binding Protein A4 MeSH
- S100A11 protein, human MeSH Browser
- S100A4 protein, human MeSH Browser
- S100A6 protein, human MeSH Browser
- S100A8 protein, human MeSH Browser
- S100A9 protein, human MeSH Browser
- S100P protein, human MeSH Browser
S100 proteins are involved in the pathogenesis of sporadic colorectal carcinoma through different mechanisms. The aim of our study was to assess tissue mRNA encoding S100 proteins in patients with non-advanced and advanced colorectal adenoma. Mucosal biopsies were taken from the caecum, transverse colon and rectum during diagnostic and/or therapeutic colonoscopy. Another biopsy was obtained from adenomatous tissue in the advanced adenoma group. The tissue mRNA for each S100 protein (S100A4, S100A6, S100A8, S100A9, S100A11 and S100P) was investigated. Eighteen biopsies were obtained from the healthy mucosa in controls and the non-advanced adenoma group (six individuals in each group) and thirty biopsies in the advanced adenoma group (ten patients). Nine biopsies were obtained from advanced adenoma tissue (9/10 patients). Significant differences in mRNA investigated in the healthy mucosa were identified between (1) controls and the advanced adenoma group for S100A6 (p = 0.012), (2) controls and the non-advanced adenoma group for S100A8 (p = 0.033) and (3) controls and the advanced adenoma group for S100A11 (p = 0.005). In the advanced adenoma group, differences between the healthy mucosa and adenomatous tissue were found in S100A6 (p = 0.002), S100A8 (p = 0.002), S100A9 (p = 0.021) and S100A11 (p = 0.029). Abnormal mRNA expression for different S100 proteins was identified in the pathological adenomatous tissue as well as in the morphologically normal large intestinal mucosa.
See more in PubMed
Haigis K.M., editor. Molecular Pathogenesis of Colorectal Cancer. Springer; Berlin/Heidelberg, Germany: 2013.
Kohoutova D., Pejchal J., Bures J. Mitotic and apoptotic activity in colorectal neoplasia. BMC Gastroenterol. 2018;18:65. doi: 10.1186/s12876-018-0786-y. PubMed DOI PMC
Kohoutova D., Forstlova M., Moravkova P., Cyrany J., Bosak J., Smajs D., Rejchrt S., Bures J. Bacteriocin production by mucosal bacteria in current and previous colorectal neoplasia. BMC Cancer. 2020;20:39. doi: 10.1186/s12885-020-6512-5. PubMed DOI PMC
Nguyen L.H., Goel A., Chung D.C. Pathways of colorectal carcinogenesis. Gastroenterology. 2020;158:291–302. doi: 10.1053/j.gastro.2019.08.059. PubMed DOI PMC
Bresalier R.S. Colorectal cancer. In: Feldman M., Friedman L.S., Brandt L.J., editors. Sleisenger and Fordtran’s Gastrointestinal and Liver Disease. 11th ed. Elsevier; Philadelphia, PA, USA: 2021. pp. 2108–2152.
Stulík J., Osterreicher J., Koupilová K., Knízek J., Bures J., Jandík P., Langr F., Dedic K., Schäfer B.W., Heizmann C.W. Differential expression of the Ca2+ binding S100A6 protein in normal, preneoplastic and neoplastic colon mucosa. Eur. J. Cancer. 2000;36:1050–1059. doi: 10.1016/S0959-8049(00)00043-5. PubMed DOI
Wang W., Yu S., Huang S., Deng R., Ding Y., Wu Y., Li X., Wang A., Wang S., Chen W., et al. A complex role for calcium signaling in colorectal cancer development and progression. Mol. Cancer Res. 2019;17:2145–2153. doi: 10.1158/1541-7786.MCR-19-0429. PubMed DOI
Donato R., Cannon B.R., Sorci G., Riuzzi F., Hsu K., Weber D.J., Geczy C.L. Functions of S100 proteins. Curr. Mol. Med. 2013;13:1, 24–57. doi: 10.2174/156652413804486214. PubMed DOI PMC
Chen H., Xu C., Jin Q., Liu Z. S100 protein family in human cancer. Am. J. Cancer Res. 2014;4:89–115. PubMed PMC
Moravkova P., Kohoutova D., Rejchrt S., Cyrany J., Bures J. Role of S100 proteins in colorectal carcinogenesis. Gastroenterol. Res. Pract. 2016;2016:2632703. doi: 10.1155/2016/2632703. PubMed DOI PMC
Moravkova P., Kohoutova D., Vavrova J., Bures J. Serum S100A6, S100A8, S100A9 and S100A11 proteins in colorectal neoplasia: Results of a single centre prospective study. Scand. J. Clin. Lab. Investig. 2020;80:173–178. doi: 10.1080/00365513.2019.1704050. PubMed DOI
Stulík J., Kovárová H., Macela A., Bures J., Jandík P., Langr F., Otto A., Thiede B., Jungblut P. Overexpression of calcium-binding protein calgranulin B in colonic mucosal diseases. Clin. Chim. Acta. 1997;265:41–55. doi: 10.1016/S0009-8981(97)00101-0. PubMed DOI
Stulík J., Osterreicher J., Koupilová K., Knízek J., Macela A., Bures J., Jandík P., Langr F., Dedic K., Jungblut P.R. The analysis of S100A9 and S100A8 expression in matched sets of macroscopically normal colon mucosa and colorectal carcinoma: The S100A9 and S100A8 positive cells underlie and invade tumor mass. Electrophoresis. 1999;20:1047–1054. doi: 10.1002/(SICI)1522-2683(19990101)20:4/5<1047::AID-ELPS1047>3.0.CO;2-E. PubMed DOI
Stulík J., Koupilova K., Osterreicher J., Knízek J., Macela A., Bures J., Jandík P., Langr F., Dedic K., Jungblut P.R. Protein abundance alterations in matched sets of macroscopically normal colon mucosa and colorectal carcinoma. Electrophoresis. 1999;20:3638–3646. PubMed
Kang Y.G., Jung C.K., Lee A., Kang W.K., Oh S.T., Kang C.S. Prognostic significance of S100A4 mRNA and protein expression in colorectal cancer. J. Surg. Oncol. 2012;105:119–124. doi: 10.1002/jso.22070. PubMed DOI
Masuda T., Ishikawa T., Mogushi K., Okazaki S., Ishiguro M., Iida S., Mizushima H., Tanaka H., Uetake H., Sugihara K. Overexpression of the S100A2 protein as a prognostic marker for patients with stage II and III colorectal cancer. Int. J. Oncol. 2016;48:975–982. doi: 10.3892/ijo.2016.3329. PubMed DOI PMC
Goh J.Y., Feng M., Wang W., Oguz G., Yatim S.M.J.M., Lee P.L., Bao Y., Lim T.H., Wang P., Tam W.L., et al. Chromosome 1q21.3 amplification is a trackable biomarker and actionable target for breast cancer recurrence. Nat. Med. 2017;23:1319–1330. doi: 10.1038/nm.4405. PubMed DOI
Schäfer B.W., Wicki R., Engelkamp D., Mattei M.G., Heizmann C.W. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: Rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics. 1995;25:638–643. doi: 10.1016/0888-7543(95)80005-7. PubMed DOI
Orlando G., Law P.J., Cornish A.J., Dobbins S.E., Chubb D., Broderick P., Litchfield K., Hariri F., Pastinen T., Osborne C.S., et al. Promoter capture Hi-C-based identification of recurrent noncoding mutations in colorectal cancer. Nat. Genet. 2018;50:1375–1380. doi: 10.1038/s41588-018-0211-z. PubMed DOI PMC
Gibadulinova A., Oveckova I., Parkkila S., Pastorekova S., Pastorek J. Key promoter elements involved in transcriptional activation of the cancer-related gene coding for S100P calcium-binding protein. Oncol. Rep. 2008;20:391–396. PubMed
Nakamura N., Takenaga K. Hypomethylation of the metastasis-associated S100A4 gene correlates with gene activation in human colon adenocarcinoma cell lines. Clin. Exp. Metastasis. 1998;16:471–479. doi: 10.1023/A:1006589626307. PubMed DOI
Wang X.H., Zhang L.H., Zhong X.Y., Xing X.F., Liu Y.Q., Niu Z.J., Peng Y., Du H., Zhang G.G., Hu Y., et al. S100A6 overexpression is associated with poor prognosis and is epigenetically up-regulated in gastric cancer. Am. J. Pathol. 2010;177:586–597. doi: 10.2353/ajpath.2010.091217. PubMed DOI PMC
Liu K., Zhang Y., Zhang C., Zhang Q., Li J., Xiao F., Li Y., Zhang R., Dou D., Liang J., et al. Methylation of S100A8 is a promising diagnosis and prognostic marker in hepatocellular carcinoma. Oncotarget. 2016;7:56798–56810. doi: 10.18632/oncotarget.10792. PubMed DOI PMC
Zhang Y., Fang L., Zang Y., Xu Z. Identification of Core Genes and Key Pathways via Integrated Analysis of Gene Expression and DNA Methylation Profiles in Bladder Cancer. Med. Sci. Monit. 2018;24:3024–3033. doi: 10.12659/MSM.909514. PubMed DOI PMC
Kim J.H., Kim C.N., Kim S.Y., Lee J.S., Cho D., Kim J.W., Yoon S.Y. Enhanced S100A4 protein expression is clinicopathologically significant to metastatic potential and p53 dysfunction in colorectal cancer. Oncol. Rep. 2009;22:41–47. doi: 10.3892/or_00000404. PubMed DOI
Sorci G., Riuzzi F., Arcuri C., Bianchi R., Brozzi F., Tubaro C., Giambanco I. S100B’s double life: Intracellular regulator and extracellular signal. Biochim. Biophys. Acta. 2009;1793:1008–1022. doi: 10.1016/j.bbamcr.2008.11.009. PubMed DOI
Schmidt-Hansen B., Ornås D., Grigorian M., Klingelhöfer J., Tulchinsky E., Lukanidin E., Ambartsumian N. Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene. 2004;23:5487–5495. doi: 10.1038/sj.onc.1207720. PubMed DOI
Huang L., Xu Y., Cai G., Guan Z., Cai S. Downregulation of S100A4 expression by RNA interference suppresses cell growth and invasion in human colorectal cancer cells. Oncol. Rep. 2012;27:917–922. doi: 10.3892/or.2011.1598. PubMed DOI PMC
Marenholz I., Heizmann C.W., Fritz G. S100 proteins in mouse and man: From evolution to function and pathology (including an update of the nomenclature) Biochem. Biophys. Res. Commun. 2004;322:1111–1122. doi: 10.1016/j.bbrc.2004.07.096. PubMed DOI
Donato R., Sorci G., Giambanco I. S100A6 protein: Functional roles. Cell Mol. Life Sci. 2017;74:2749–2760. doi: 10.1007/s00018-017-2526-9. PubMed DOI PMC
Feng S., Zhou Q., Yang B., Li Q., Liu A., Zhao Y., Qiu C., Ge J., Zhai H. The effect of S100A6 on nuclear translocation of CacyBP/SIP in colon cancer cells. PLoS ONE. 2018;13:e0192208. doi: 10.1371/journal.pone.0192208. PubMed DOI PMC
Kilańczyk E., Graczyk A., Ostrowska H., Kasacka I., Leśniak W., Filipek A. S100A6 is transcriptionally regulated by β-catenin and interacts with a novel target, lamin A/C, in colorectal cancer cells. Cell Calcium. 2012;51:470–477. doi: 10.1016/j.ceca.2012.04.005. PubMed DOI
Króliczak W., Pietrzak M., Puzianowska-Kuznicka M. P53-dependent suppression of the human calcyclin gene (S100A6): The role of Sp1 and of NFkappaB. Acta Biochim. Pol. 2008;55:559–570. doi: 10.18388/abp.2008_3062. PubMed DOI
Komatsu K., Andoh A., Ishiguro S., Suzuki N., Hunai H., Kobune-Fujiwara Y., Kameyama M., Miyoshi J., Akedo H., Nakamura H. Increased expression of S100A6 (Calcyclin), a calcium-binding protein of the S100 family, in human colorectal adenocarcinomas. Clin. Cancer Res. 2000;6:172–177. PubMed
Gebhardt C., Németh J., Angel P., Hess J. S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 2006;72:1622–1631. doi: 10.1016/j.bcp.2006.05.017. PubMed DOI
Ehrchen J.M., Sunderkötter C., Foell D., Vogl T., Roth J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J. Leukoc. Biol. 2009;86:557–566. doi: 10.1189/jlb.1008647. PubMed DOI
Huang M., Wu R., Chen L., Peng Q., Li S., Zhang Y., Zhou L., Duan L. S100A9 regulates MDSCs-mediated immune suppression via the RAGE and TLR4 signaling pathways in colorectal carcinoma. Front. Immunol. 2019;10:2243. doi: 10.3389/fimmu.2019.02243. PubMed DOI PMC
Ghavami S., Kerkhoff C., Los M., Hashemi M., Sorg C., Karami-Tehrani F. Mechanism of apoptosis induced by S100A8/A9 in colon cancer cell lines: The role of ROS and the effect of metal ions. J. Leukoc. Biol. 2004;76:169–175. doi: 10.1189/jlb.0903435. PubMed DOI
Ghavami S., Rashedi I., Dattilo B.M., Eshraghi M., Chazin W.J., Hashemi M., Wesselborg S., Kerkhoff C., Los M. S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J. Leukoc. Biol. 2008;83:1484–1492. doi: 10.1189/jlb.0607397. PubMed DOI PMC
Luley K., Noack F., Lehnert H., Homann N. Local calprotectin production in colorectal cancer and polyps: Active neutrophil recruitment in carcinogenesis. Int. J. Color. Dis. 2011;26:603–607. doi: 10.1007/s00384-011-1165-0. PubMed DOI
Moris D., Spartalis E., Angelou A., Margonis G.A., Papalambros A., Petrou A., Athanasiou A., Schizas D., Dimitroulis D., Felekouras E. The value of calprotectin S100A8/A9 complex as a biomarker in colorectal cancer: A systematic review. J. BUON. 2016;21:859–866. PubMed
Turvill J., Aghahoseini A., Sivarajasingham N., Abbas K., Choudhry M., Polyzois K., Lasithiotakis K., Volanaki D., Kim B., Langlands F., et al. Faecal calprotectin in patients with suspected colorectal cancer: A diagnostic accuracy study. Br. J. Gen. Pract. 2016;66:e499–e506. doi: 10.3399/bjgp16X685645. PubMed DOI PMC
Andrés Cerezo L., Šumová B., Prajzlerová K., Veigl D., Damgaard D., Nielsen C.H., Pavelka K., Vencovský J., Šenolt L. Calgizzarin (S100A11): A novel inflammatory mediator associated with disease activity of rheumatoid arthritis. Arthritis Res. Ther. 2017;19:79. doi: 10.1186/s13075-017-1288-y. PubMed DOI PMC
Anania M.C., Miranda C., Vizioli M.G., Mazzoni M., Cleris L., Pagliardini S., Manenti G., Borrello M.G., Pierotti M.A., Greco A. S100A11 overexpression contributes to the malignant phenotype of papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 2013;98:1591–1600. doi: 10.1210/jc.2013-1652. PubMed DOI
Li Y., Zhang J. Expression of S100A11 is a prognostic factor for disease-free survival and overall survival in patients with high-grade serous ovarian vancer. Appl. Immunohistochem. Mol. Morphol. 2017;25:110–116. doi: 10.1097/PAI.0000000000000275. PubMed DOI
Zhang M., Zheng S., Jing C., Zhang J., Shen H., Xu X., Lin J., Zhang B. S100A11 promotes TGF-β1-induced epithelial-mesenchymal transition through SMAD2/3 signaling pathway in intrahepatic cholangiocarcinoma. Future Oncol. 2018;14:837–847. doi: 10.2217/fon-2017-0534. PubMed DOI
Ji Y.F., Li T., Jiang F., Ni W.K., Guan C.Q., Liu Z.X., Lu C.H., Ni R.Z., Wu W., Xiao M.B. Correlation between S100A11 and the TGF-β1/SMAD4 pathway and its effects on the proliferation and apoptosis of pancreatic cancer cell line PANC-1. Mol. Cell. Biochem. 2019;450:53–64. doi: 10.1007/s11010-018-3372-2. PubMed DOI
Xiao M., Li T., Ji Y., Jiang F., Ni W., Zhu J., Bao B., Lu C., Ni R. S100A11 promotes human pancreatic cancer PANC-1 cell proliferation and is involved in the PI3K/AKT signaling pathway. Oncol. Lett. 2018;15:175–182. doi: 10.3892/ol.2017.7295. PubMed DOI PMC
Koh S.A., Lee K.H. HGF-mediated S100A11 overexpression enhances proliferation and invasion of gastric cancer. Am. J. Transl. Res. 2018;10:3385–3394. PubMed PMC
Takamatsu H., Yamamoto K.I., Tomonobu N., Murata H., Inoue Y., Yamauchi A., Sumardika I.W., Chen Y., Kinoshita R., Yamamura M., et al. Extracellular S100A11 plays a critical role in spread of the fibroblast population in pancreatic cancers. Oncol. Res. 2019;27:713–727. doi: 10.3727/096504018X15433161908259. PubMed DOI PMC
Melle C., Ernst G., Schimmel B., Bleul A., Mothes H., Kaufmann R., Settmacher U., Von Eggeling F. Different expression of calgizzarin (S100A11) in normal colonic epithelium, adenoma and colorectal carcinoma. Int. J. Oncol. 2006;28:195–200. doi: 10.3892/ijo.28.1.195. PubMed DOI
Chiang J.M., Tan R., Wang J.Y., Chen J.S., Lee Y.S., Hsieh P.S., Changchien C.R., Chen J.R. S100P, a calcium-binding protein, is preferentially associated with the growth of polypoid tumors in colorectal cancer. Int. J. Mol. Med. 2015;35:675–683. doi: 10.3892/ijmm.2015.2065. PubMed DOI PMC
Zuo Z., Zhang P., Lin F., Shang W., Bi R., Lu F., Wu J., Jiang L. Interplay between Trx-1 and S100P promotes colorectal cancer cell epithelial-mesenchymal transition by up-regulating S100A4 through AKT activation. J. Cell. Mol. Med. 2018;22:2430–2441. doi: 10.1111/jcmm.13541. PubMed DOI PMC
Wang Q., Zhang Y.N., Lin G.L., Qiu H.Z., Wu B., Wu H.Y., Zhao Y., Chen Y.J., Lu C.M. S100P, a potential novel prognostic marker in colorectal cancer. Oncol. Rep. 2012;28:303–310. doi: 10.3892/or.2012.1794. PubMed DOI
Lam F.F., Jankova L., Dent O.F., Molloy M.P., Kwun S.Y., Clarke C., Chapuis P., Robertson G., Beale P., Clarke S., et al. Identification of distinctive protein expression patterns in colorectal adenoma. Proteom. Clin. Appl. 2010;4:60–70. doi: 10.1002/prca.200900084. PubMed DOI
Mahajan D., Downs-Kelly E., Liu X., Pai R.K., Patil D.T., Rybicki L., Bennett A.E., Plesec T., Cummings O., Rex D., et al. Reproducibility of the villous component and high-grade dysplasia in colorectal adenomas <1 cm: Implications for endoscopic surveillance. Am. J. Surg. Pathol. 2013;37:427–433. doi: 10.1097/PAS.0b013e31826cf50f. PubMed DOI
Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987;162:156–159. doi: 10.1016/0003-2697(87)90021-2. PubMed DOI
Bustin S.A., Mueller R. Real-time reverse transcription PCR (qRT-PCR) and its potential use in clinical diagnosis. Clin. Sci. (Lond.) 2005;109:365–379. doi: 10.1042/CS20050086. PubMed DOI
Rao X., Huang X., Zhou Z., Lin X. An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinform. Biomath. 2013;3:71–85. PubMed PMC