Skip to main content
Erschienen in: Inflammation Research 10/2018

28.07.2018 | Original Research Paper

Fascin protein stabilization by miR-146a implicated in the process of a chronic inflammation-related colon carcinogenesis model

verfasst von: Yusuke Kanda, Tokuichi Kawaguchi, Mitsuhiko Osaki, Kunishige Onuma, Takahiro Ochiya, Tomoyuki Kitagawa, Futoshi Okada

Erschienen in: Inflammation Research | Ausgabe 10/2018

Einloggen, um Zugang zu erhalten

Abstract

Objective

In sporadic colon tumors, multistep process of well-known genetic alterations accelerates carcinogenesis; however, this does not appear to be the case in inflammation-related ones. We previously established a model of inflammation-related colon carcinogenesis using human colonic adenoma cells, and identified fascin as a driver gene of this process. We analyzed the microRNAs involved in the stable fascin expression in colon adenocarcinoma cells.

Materials and methods

miRNA microarray analysis was performed using FPCK-1-1 adenoma cells and its-derived FPCKpP1-4 adenocarcinoma cells through chronic inflammation. To assess the involvement of miRNA in the inflammation-related carcinogenesis, sphere-forming ability, expression of colon cancer stemness markers, and stability of fascin protein via the proteasome using tough decoy RNA technique.

Results

We found that 17 miRNAs including miR-146a were upregulated and 16 miRNAs were downregulated in FPCKpP1-4 adenocarcinoma cells. We revealed that miR-146a in the adenocarcinoma cells brought about acquisition of sphere formation, cancer stemness, and inhibition of proteasomal degradation of the fascin protein.

Conclusions

We found that stable fascin expression is brought about via the inhibition of proteasome degradation by miR-146a in the process of a chronic inflammation-related colon carcinogenesis.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66:683–91.CrossRefPubMed Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66:683–91.CrossRefPubMed
2.
Zurück zum Zitat Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, Berry DA. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control. 2013;24:1207–22.CrossRefPubMedPubMedCentral Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI, Levin B, Berry DA. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control. 2013;24:1207–22.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–67.CrossRefPubMed Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–67.CrossRefPubMed
4.
Zurück zum Zitat Tarmin L, Yin J, Harpaz N, Kozam M, Noordzij J, Antonio LB, Jiang HY, Chan O, Cymes K, Meltzer SJ. Adenomatous polyposis coli gene mutations in ulcerative colitis-associated dysplasias and cancers versus sporadic colon neoplasms. Cancer Res. 1995;55:2035–8.PubMed Tarmin L, Yin J, Harpaz N, Kozam M, Noordzij J, Antonio LB, Jiang HY, Chan O, Cymes K, Meltzer SJ. Adenomatous polyposis coli gene mutations in ulcerative colitis-associated dysplasias and cancers versus sporadic colon neoplasms. Cancer Res. 1995;55:2035–8.PubMed
5.
Zurück zum Zitat Burmer GC, Levine DS, Kulander BG, Haggitt RC, Rubin CE, Rabinovitch PS. c-Ki-ras mutations in chronic ulcerative colitis and sporadic colon carcinoma. Gastroenterology. 1990;99:416–20.CrossRefPubMed Burmer GC, Levine DS, Kulander BG, Haggitt RC, Rubin CE, Rabinovitch PS. c-Ki-ras mutations in chronic ulcerative colitis and sporadic colon carcinoma. Gastroenterology. 1990;99:416–20.CrossRefPubMed
6.
Zurück zum Zitat Baker SJ, Preisinger AC, Jessup JM, Paraskeva C, Markowitz S, Willson JK, Hamilton S, Vogelstein B. p53 gene mutations occur in combination with 17p allelic deletions as late events in colorectal tumorigenesis. Cancer Res. 1990;50:7717–22.PubMed Baker SJ, Preisinger AC, Jessup JM, Paraskeva C, Markowitz S, Willson JK, Hamilton S, Vogelstein B. p53 gene mutations occur in combination with 17p allelic deletions as late events in colorectal tumorigenesis. Cancer Res. 1990;50:7717–22.PubMed
8.
Zurück zum Zitat Chaubert P, Benhattar J, Saraga E, Costa J. K-ras mutations and p53 alterations in neoplastic and nonneoplastic lesions associated with longstanding ulcerative colitis. Am J Pathol. 1994;144:767–75.PubMedPubMedCentral Chaubert P, Benhattar J, Saraga E, Costa J. K-ras mutations and p53 alterations in neoplastic and nonneoplastic lesions associated with longstanding ulcerative colitis. Am J Pathol. 1994;144:767–75.PubMedPubMedCentral
9.
Zurück zum Zitat Connelly TM, Berg AS, Harris DL 3rd, Brinton DL, Hegarty JP, Deiling SM, Stewart DB, Koltun WA. Ulcerative colitis neoplasia is not associated with common inflammatory bowel disease single-nucleotide polymorphisms. Surgery. 2014;156:253–62.CrossRefPubMed Connelly TM, Berg AS, Harris DL 3rd, Brinton DL, Hegarty JP, Deiling SM, Stewart DB, Koltun WA. Ulcerative colitis neoplasia is not associated with common inflammatory bowel disease single-nucleotide polymorphisms. Surgery. 2014;156:253–62.CrossRefPubMed
10.
Zurück zum Zitat Okada F, Kawaguchi T, Habelhah H, Kobayashi T, Tazawa H, Takeichi N, Kitagawa T, Hosokawa M. Conversion of human colonic adenoma cells to adenocarcinoma cells through inflammation in nude mice. Lab Investig. 2000;80:1617–28.CrossRefPubMed Okada F, Kawaguchi T, Habelhah H, Kobayashi T, Tazawa H, Takeichi N, Kitagawa T, Hosokawa M. Conversion of human colonic adenoma cells to adenocarcinoma cells through inflammation in nude mice. Lab Investig. 2000;80:1617–28.CrossRefPubMed
11.
Zurück zum Zitat Tazawa H, Kawaguchi T, Kobayashi T, Kuramitsu Y, Wada S, Satomi Y, Nishino H, Kobayashi M, Kanda Y, Osaki M, Kitagawa T, Hosokawa M, Okada F. Chronic inflammation-derived nitric oxide causes conversion of human colonic adenoma cells into adenocarcinoma cells. Exp Cell Res. 2013;319:2835–44.CrossRefPubMed Tazawa H, Kawaguchi T, Kobayashi T, Kuramitsu Y, Wada S, Satomi Y, Nishino H, Kobayashi M, Kanda Y, Osaki M, Kitagawa T, Hosokawa M, Okada F. Chronic inflammation-derived nitric oxide causes conversion of human colonic adenoma cells into adenocarcinoma cells. Exp Cell Res. 2013;319:2835–44.CrossRefPubMed
12.
Zurück zum Zitat Kanda Y, Kawaguchi T, Kuramitsu Y, Kitagawa T, Kobayashi T, Takahashi N, Tazawa H, Habelhah H, Hamada J, Kobayashi M, Hirahata M, Onuma K, Osaki M, Nakamura K, Kitagawa T, Hosokawa M, Okada F. Fascin regulates chronic inflammation-related human colon carcinogenesis by inhibiting cell anoikis. Proteomics. 2014;14:1031–41.CrossRefPubMed Kanda Y, Kawaguchi T, Kuramitsu Y, Kitagawa T, Kobayashi T, Takahashi N, Tazawa H, Habelhah H, Hamada J, Kobayashi M, Hirahata M, Onuma K, Osaki M, Nakamura K, Kitagawa T, Hosokawa M, Okada F. Fascin regulates chronic inflammation-related human colon carcinogenesis by inhibiting cell anoikis. Proteomics. 2014;14:1031–41.CrossRefPubMed
13.
Zurück zum Zitat Kanda Y, Osaki M, Okada F. Chemopreventive Strategies for inflammation-related carcinogenesis: Current status and future direction. Int J Mol Sci. 2017;18:E867.CrossRefPubMed Kanda Y, Osaki M, Okada F. Chemopreventive Strategies for inflammation-related carcinogenesis: Current status and future direction. Int J Mol Sci. 2017;18:E867.CrossRefPubMed
14.
Zurück zum Zitat Okada F. Beyond foreign-body-induced carcinogenesis: impact of reactive oxygen species derived from inflammatory cells in tumorigenic conversion and tumor progression. Int J Cancer. 2007;121:2364–72.CrossRefPubMed Okada F. Beyond foreign-body-induced carcinogenesis: impact of reactive oxygen species derived from inflammatory cells in tumorigenic conversion and tumor progression. Int J Cancer. 2007;121:2364–72.CrossRefPubMed
15.
Zurück zum Zitat Kawaguchi T, Miyaki M, Masui T, Watanabe M, Ohta H, Maruyama M, Utakoji T, Kitagawa T. Establishment and characterization of an epithelial cell line with quasi-normal chromosomes from a tubular adenoma of a familial polyposis coli patient. Jpn J Cancer Res. 1991;82:138–41.CrossRefPubMedPubMedCentral Kawaguchi T, Miyaki M, Masui T, Watanabe M, Ohta H, Maruyama M, Utakoji T, Kitagawa T. Establishment and characterization of an epithelial cell line with quasi-normal chromosomes from a tubular adenoma of a familial polyposis coli patient. Jpn J Cancer Res. 1991;82:138–41.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Okayama H, Schetter AJ, Harris CC. MicroRNAs and inflammation in the pathogenesis and progression of colon cancer. Dig Dis. 2012;30(Suppl 2):9–15.CrossRefPubMed Okayama H, Schetter AJ, Harris CC. MicroRNAs and inflammation in the pathogenesis and progression of colon cancer. Dig Dis. 2012;30(Suppl 2):9–15.CrossRefPubMed
17.
Zurück zum Zitat Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, Brant SR, Chakravarti S, Kwon JH. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624–35.CrossRefPubMed Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, Brant SR, Chakravarti S, Kwon JH. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624–35.CrossRefPubMed
18.
Zurück zum Zitat Iwamoto H, Kanda Y, Sejima T, Osaki M, Okada F, Takenaka A. Serum miR-210 as a potential biomarker of early clear cell renal cell carcinoma. Int J Oncol. 2014;44:53–8.CrossRefPubMed Iwamoto H, Kanda Y, Sejima T, Osaki M, Okada F, Takenaka A. Serum miR-210 as a potential biomarker of early clear cell renal cell carcinoma. Int J Oncol. 2014;44:53–8.CrossRefPubMed
19.
Zurück zum Zitat Kanda Y, Osaki M, Onuma K, Sonoda A, Kobayashi M, Hamada J, Nicolson GL, Ochiya T, Okada F. Amigo2-upregulation in tumour cells facilitates their attachment to liver endothelial cells resulting in liver metastases. Sci Rep. 2017;7:43567.CrossRefPubMedPubMedCentral Kanda Y, Osaki M, Onuma K, Sonoda A, Kobayashi M, Hamada J, Nicolson GL, Ochiya T, Okada F. Amigo2-upregulation in tumour cells facilitates their attachment to liver endothelial cells resulting in liver metastases. Sci Rep. 2017;7:43567.CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Kitajima S, Kohno S, Kondoh A, Sasaki N, Nishimoto Y, Li F, Mohammed A, Muranaka H, Nagatani N, Suzuki M, Kido Y, Takahashi C. Undifferentiated state induced by Rb-p53 double inactivation in mouse thyroid neuroendocrine cells and embryonic fibroblasts. Stem Cells. 2015;33:1657–69.CrossRefPubMed Kitajima S, Kohno S, Kondoh A, Sasaki N, Nishimoto Y, Li F, Mohammed A, Muranaka H, Nagatani N, Suzuki M, Kido Y, Takahashi C. Undifferentiated state induced by Rb-p53 double inactivation in mouse thyroid neuroendocrine cells and embryonic fibroblasts. Stem Cells. 2015;33:1657–69.CrossRefPubMed
21.
Zurück zum Zitat Vermeulen L, Todaro M, de Sousa Mello F, Sprick F, Kemper MR, Perez Alea K, Richel M, Stassi DJ, Medema G. JP. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA. 2008;105:13427–32.CrossRefPubMed Vermeulen L, Todaro M, de Sousa Mello F, Sprick F, Kemper MR, Perez Alea K, Richel M, Stassi DJ, Medema G. JP. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA. 2008;105:13427–32.CrossRefPubMed
22.
Zurück zum Zitat Haraguchi T, Ozaki Y, Iba H. Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic Acids Res. 2009;37:e43.CrossRefPubMedPubMedCentral Haraguchi T, Ozaki Y, Iba H. Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic Acids Res. 2009;37:e43.CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Lin J, Welker NC, Zhao Z, Li Y, Zhang J, Reuss SA, Zhang X, Lee H, Liu Y, Bronner MP. Novel specific microRNA biomarkers in idiopathic inflammatory bowel disease unrelated to disease activity. Mod Pathol. 2014;27:602–8.CrossRefPubMed Lin J, Welker NC, Zhao Z, Li Y, Zhang J, Reuss SA, Zhang X, Lee H, Liu Y, Bronner MP. Novel specific microRNA biomarkers in idiopathic inflammatory bowel disease unrelated to disease activity. Mod Pathol. 2014;27:602–8.CrossRefPubMed
25.
Zurück zum Zitat Qualtrough D, Smallwood K, Littlejohns D, Pignatelli M. The actin-bundling protein fascin is overexpressed in inflammatory bowel disease and may be important in tissue repair. BMC Gastroenterol. 2011;11:14.CrossRefPubMedPubMedCentral Qualtrough D, Smallwood K, Littlejohns D, Pignatelli M. The actin-bundling protein fascin is overexpressed in inflammatory bowel disease and may be important in tissue repair. BMC Gastroenterol. 2011;11:14.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Chen MB, Wei MX, Han JY, Wu XY, Li C, Wang J, Shen W, Lu PH. MicroRNA-451 regulates AMPK/mTORC1 signaling and fascin1 expression in HT-29 colorectal cancer. Cell Signal. 2014;26:102–9.CrossRefPubMed Chen MB, Wei MX, Han JY, Wu XY, Li C, Wang J, Shen W, Lu PH. MicroRNA-451 regulates AMPK/mTORC1 signaling and fascin1 expression in HT-29 colorectal cancer. Cell Signal. 2014;26:102–9.CrossRefPubMed
27.
Zurück zum Zitat Li YQ, Lu JH, Bao XM, Wang XF, Wu JH, Hong WQ. MiR-24 functions as a tumor suppressor in nasopharyngeal carcinoma through targeting FSCN1. J Exp Clin Cancer Res. 2015;34:130.CrossRefPubMedPubMedCentral Li YQ, Lu JH, Bao XM, Wang XF, Wu JH, Hong WQ. MiR-24 functions as a tumor suppressor in nasopharyngeal carcinoma through targeting FSCN1. J Exp Clin Cancer Res. 2015;34:130.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, Akutsu Y, Chiyomaru T, Enokida H, Nakagawa M, Matsubara H. miR-145, miR-133a and miR-133b: tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer. 2010;127:2804–14.CrossRefPubMed Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, Akutsu Y, Chiyomaru T, Enokida H, Nakagawa M, Matsubara H. miR-145, miR-133a and miR-133b: tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer. 2010;127:2804–14.CrossRefPubMed
29.
Zurück zum Zitat Liu R, Liao J, Yang M, Sheng J, Yang H, Wang Y, Pan E, Guo W, Pu Y, Kim SJ, Yin L. The cluster of miR-143 and miR-145 affects the risk for esophageal squamous cell carcinoma through co-regulating fascin homolog 1. PLoS One. 2012;7:e33987.CrossRefPubMedPubMedCentral Liu R, Liao J, Yang M, Sheng J, Yang H, Wang Y, Pan E, Guo W, Pu Y, Kim SJ, Yin L. The cluster of miR-143 and miR-145 affects the risk for esophageal squamous cell carcinoma through co-regulating fascin homolog 1. PLoS One. 2012;7:e33987.CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Li Y, Gao Y, Xu Y, Ma H, Yang M. Down-regulation of miR-326 is associated with poor prognosis and promotes growth and metastasis by targeting FSCN1 in gastric cancer. Growth Factors. 2015;33:267–74.CrossRefPubMed Li Y, Gao Y, Xu Y, Ma H, Yang M. Down-regulation of miR-326 is associated with poor prognosis and promotes growth and metastasis by targeting FSCN1 in gastric cancer. Growth Factors. 2015;33:267–74.CrossRefPubMed
31.
Zurück zum Zitat Zhang M, Dong BB, Lu M, Zheng MJ, Chen H, Ding JZ, Xu AM, Xu YH. miR-429 functions as a tumor suppressor by targeting FSCN1 in gastric cancer cells. Onco Targets Ther. 2016;9:1123–33.PubMedPubMedCentral Zhang M, Dong BB, Lu M, Zheng MJ, Chen H, Ding JZ, Xu AM, Xu YH. miR-429 functions as a tumor suppressor by targeting FSCN1 in gastric cancer cells. Onco Targets Ther. 2016;9:1123–33.PubMedPubMedCentral
32.
Zurück zum Zitat Xiao P, Liu W, Zhou H. miR-200b inhibits migration and invasion in non-small cell lung cancer cells via targeting FSCN1. Mol Med Rep. 2016;14:1835–40.CrossRefPubMed Xiao P, Liu W, Zhou H. miR-200b inhibits migration and invasion in non-small cell lung cancer cells via targeting FSCN1. Mol Med Rep. 2016;14:1835–40.CrossRefPubMed
33.
Zurück zum Zitat Liu Y, Hong W, Zhou C, Jiang Z, Wang G, Wei G, Li X. miR-539 inhibits FSCN1 expression and suppresses hepatocellular carcinoma migration and invasion. Oncol Rep. 2017;37:2593–602.CrossRefPubMedPubMedCentral Liu Y, Hong W, Zhou C, Jiang Z, Wang G, Wei G, Li X. miR-539 inhibits FSCN1 expression and suppresses hepatocellular carcinoma migration and invasion. Oncol Rep. 2017;37:2593–602.CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Yu S, Xie H, Zhang J, Wang D, Song Y, Zhang S, Zheng S, Wang J. MicroRNA663 suppresses the proliferation and invasion of colorectal cancer cells by directly targeting FSCN1. Mol Med Rep. 2017;16:9707–14.CrossRefPubMed Yu S, Xie H, Zhang J, Wang D, Song Y, Zhang S, Zheng S, Wang J. MicroRNA663 suppresses the proliferation and invasion of colorectal cancer cells by directly targeting FSCN1. Mol Med Rep. 2017;16:9707–14.CrossRefPubMed
35.
Zurück zum Zitat Mani A, Gelmann EP. The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol. 2005;23:4776–89.CrossRefPubMed Mani A, Gelmann EP. The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol. 2005;23:4776–89.CrossRefPubMed
36.
Zurück zum Zitat Fuchs SY. The role of ubiquitin-proteasome pathway in oncogenic signaling. Cancer Biol Ther. 2002;1:337–41.CrossRefPubMed Fuchs SY. The role of ubiquitin-proteasome pathway in oncogenic signaling. Cancer Biol Ther. 2002;1:337–41.CrossRefPubMed
37.
Zurück zum Zitat Leung CO, Deng W, Ye TM, Ngan HY, Tsao SW, Cheung AN, Pang RT, Yeung WS. miR-135a leads to cervical cancer cell transformation through regulation of beta-catenin via a SIAH1-dependent ubiquitin proteosomal pathway. Carcinogenesis. 2014;35:1931–40.CrossRefPubMed Leung CO, Deng W, Ye TM, Ngan HY, Tsao SW, Cheung AN, Pang RT, Yeung WS. miR-135a leads to cervical cancer cell transformation through regulation of beta-catenin via a SIAH1-dependent ubiquitin proteosomal pathway. Carcinogenesis. 2014;35:1931–40.CrossRefPubMed
38.
Zurück zum Zitat Sears R, Leone G, DeGregori J, Nevins JR. Ras enhances Myc protein stability. Mol Cell. 1999;3:169–79.CrossRefPubMed Sears R, Leone G, DeGregori J, Nevins JR. Ras enhances Myc protein stability. Mol Cell. 1999;3:169–79.CrossRefPubMed
40.
Zurück zum Zitat Voutsadakis IA. Proteasome expression and activity in cancer and cancer stem cells. Tumour Biol. 2017;39:1010428317692248.CrossRefPubMed Voutsadakis IA. Proteasome expression and activity in cancer and cancer stem cells. Tumour Biol. 2017;39:1010428317692248.CrossRefPubMed
41.
Zurück zum Zitat Hwang WL, Jiang JK, Yang SH, Huang TS, Lan HY, Teng HW, Yang CY, Tsai YP, Lin CH, Wang HW, Yang MH. MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells. Nat Cell Biol. 2014;16:268–80.CrossRefPubMed Hwang WL, Jiang JK, Yang SH, Huang TS, Lan HY, Teng HW, Yang CY, Tsai YP, Lin CH, Wang HW, Yang MH. MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells. Nat Cell Biol. 2014;16:268–80.CrossRefPubMed
42.
Zurück zum Zitat Lenos KJ, Vermeulen L. Cancer stem cells don’t waste their time cleaning-low proteasome activity, a marker for cancer stem cell function. Ann Transl Med. 2016;4:519.CrossRefPubMedPubMedCentral Lenos KJ, Vermeulen L. Cancer stem cells don’t waste their time cleaning-low proteasome activity, a marker for cancer stem cell function. Ann Transl Med. 2016;4:519.CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Abbaszadegan MR, Bagheri V, Razavi MS, Momtazi AA, Sahebkar A, Gholamin M. Isolation, identification, and characterization of cancer stem cells: a review. J Cell Physiol. 2017;232:2008–18.CrossRefPubMed Abbaszadegan MR, Bagheri V, Razavi MS, Momtazi AA, Sahebkar A, Gholamin M. Isolation, identification, and characterization of cancer stem cells: a review. J Cell Physiol. 2017;232:2008–18.CrossRefPubMed
Metadaten
Titel
Fascin protein stabilization by miR-146a implicated in the process of a chronic inflammation-related colon carcinogenesis model
verfasst von
Yusuke Kanda
Tokuichi Kawaguchi
Mitsuhiko Osaki
Kunishige Onuma
Takahiro Ochiya
Tomoyuki Kitagawa
Futoshi Okada
Publikationsdatum
28.07.2018
Verlag
Springer International Publishing
Erschienen in
Inflammation Research / Ausgabe 10/2018
Print ISSN: 1023-3830
Elektronische ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-018-1175-2

Weitere Artikel der Ausgabe 10/2018

Inflammation Research 10/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.