nach oben

Tumor Biology

Erschienen in:

28.03.2016 | Original Article

Discoidin domain receptor 1 (DDR1), a promising biomarker, induces epithelial to mesenchymal transition in renal cancer cells

verfasst von: Jingyuan Song, Xiao Chen, Jin Bai, Qinghua Liu, Hui Li, Jianwan Xie, Hui Jing, Junnian Zheng

Erschienen in: Tumor Biology | Ausgabe 8/2016

Einloggen, um Zugang zu erhalten

Abstract

Discoidin domain receptor I (DDR1) is confirmed as a receptor tyrosine kinase (RTK), which plays a consequential role in a variety of cancers. Nevertheless, the influence of DDR1 expression and development in renal clear cell carcinoma (RCCC) are still not well corroborated. In our research, we firstly discovered that the expression level of DDR1 was remarkable related to TNM stage (p = 0.032), depth of tumor invasion (p = 0.047), and lymph node metastasis (p = 0.034) in 119 RCCC tissue samples using tissue microarray. The function of DDR1 was then evaluated in vitro using collagen I and DDR1 small interfering RNA (siRNA) to regulate the expression of DDR1 in OS-RC-2 and ACHN renal cancer cells (RCC). DDR1 expression correlated with increased RCC cell migration, invasion, and angiogenesis. Further study revealed that high expression of DDR1 can result in epithelial to mesenchymal transition (EMT) activation. Western blot assay showed that the N-cadherin protein and vimentin were induced while E-cadherin was reduced after DDR1 over expression. Our results suggest that DDR1 is both a prognostic marker for RCCC and a potential functional target for therapy.

Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62:220–41.CrossRefPubMed

Finley DS, Pantuck AJ, Belldegrun AS. Tumor biology and prognostic factors in renal cell carcinoma. Oncologist. 2011;16 Suppl 2:4–13.CrossRefPubMedPubMedCentral

Coppin C, Kollmannsberger C, Le L, Porzsolt F, Wilt TJ. Targeted therapy for advanced renal cell cancer (rcc): a cochrane systematic review of published randomised trials. BJU Int. 2011;108:1556–63.CrossRefPubMed

Valiathan RR, Marco M, Leitinger B, Kleer CG, Fridman R. Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 2012;31:295–321.CrossRefPubMedPubMedCentral

Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell. 1997;1:13–23.CrossRefPubMed

Shrivastava A, Radziejewski C, Campbell E, Kovac L, McGlynn M, Ryan TE, et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell. 1997;1:25–34.CrossRefPubMed

Vogel WF, Abdulhussein R, Ford CE. Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal. 2006;18:1108–16.CrossRefPubMed

Yamanaka R, Arao T, Yajima N, Tsuchiya N, Homma J, Tanaka R, et al. Identification of expressed genes characterizing long-term survival in malignant glioma patients. Oncogene. 2006;25:5994–6002.CrossRefPubMed

Johansson FK, Goransson H, Westermark B. Expression analysis of genes involved in brain tumor progression driven by retroviral insertional mutagenesis in mice. Oncogene. 2005;24:3896–905.CrossRefPubMed

10.

Heinzelmann-Schwarz VA, Gardiner-Garden M, Henshall SM, Scurry J, Scolyer RA, Davies MJ, et al. Overexpression of the cell adhesion molecules ddr1, claudin 3, and ep-cam in metaplastic ovarian epithelium and ovarian cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2004;10:4427–36.CrossRef

11.

Weiner HL, Huang H, Zagzag D, Boyce H, Lichtenbaum R, Ziff EB. Consistent and selective expression of the discoidin domain receptor-1 tyrosine kinase in human brain tumors. Neurosurgery. 2000;47:1400–9.CrossRefPubMed

12.

Park HS, Kim KR, Lee HJ, Choi HN, Kim DK, Kim BT, et al. Overexpression of discoidin domain receptor 1 increases the migration and invasion of hepatocellular carcinoma cells in association with matrix metalloproteinase. Oncol Rep. 2007;18:1435–41.PubMed

13.

Edwards DR, Murphy G. Cancer. Proteases—invasion and more. Nature. 1998;394:527–8.CrossRefPubMed

14.

Yoshimoto M, Itoh F, Yamamoto H, Hinoda Y, Imai K, Yachi A. Expression of mmp-7(pump-1) mrna in human colorectal cancers. Int J Cancer J Int Cancer. 1993;54:614–8.CrossRef

15.

Senota A, Itoh F, Yamamoto H, Adachi Y, Hinoda Y, Imai K. Relation of matrilysin messenger rna expression with invasive activity in human gastric cancer. Clin Exp Metastasis. 1998;16:313–21.CrossRefPubMed

16.

Uhm JH, Dooley NP, Villemure JG, Yong VW. Glioma invasion in vitro: regulation by matrix metalloprotease-2 and protein kinase c. Clin Exp Metastasis. 1996;14:421–33.CrossRefPubMed

17.

Mikami S, Oya M, Mizuno R, Kosaka T, Katsube K, Okada Y. Invasion and metastasis of renal cell carcinoma. Med Mol Morphol. 2014;47:63–7.CrossRefPubMed

18.

Sato A, Nagase H, Obinata D, Fujiwara K, Fukuda N, Soma M, et al. Inhibition of mmp-9 using a pyrrole-imidazole polyamide reduces cell invasion in renal cell carcinoma. Int J Oncol. 2013;43:1441–6.PubMed

19.

Lu H, Yang Z, Zhang H, Gan M, Zhou T, Wang S. The expression and clinical significance of matrix metalloproteinase 7 and tissue inhibitor of matrix metalloproteinases 2 in clear cell renal cell carcinoma. Exp Ther Med. 2013;5:890–6.PubMed

20.

Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol. 2003;15:740–6.CrossRefPubMed

21.

Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006;172:973–81.CrossRefPubMedPubMedCentral

22.

Shintani Y, Fukumoto Y, Chaika N, Svoboda R, Wheelock MJ, Johnson KR. Collagen i-mediated up-regulation of n-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J Cell Biol. 2008;180:1277–89.CrossRefPubMedPubMedCentral

23.

Borza CM, Pozzi A. Discoidin domain receptors in disease. Matrix Biol J Int Soc Matrix Biol. 2014;34:185–92.CrossRef

24.

L’Hote CG, Thomas PH, Ganesan TS. Functional analysis of discoidin domain receptor 1: effect of adhesion on ddr1 phosphorylation. FASEB J Off Publ Fed Am Soc Exp Biol. 2002;16:234–6.

25.

Alves F, Saupe S, Ledwon M, Schaub F, Hiddemann W, Vogel WF. Identification of two novel, kinase-deficient variants of discoidin domain receptor 1: differential expression in human colon cancer cell lines. FASEB J Off Publ Fed Am Soc Exp Biol. 2001;15:1321–3.

26.

Sanchez MP, Tapley P, Saini SS, He B, Pulido D, Barbacid M. Multiple tyrosine protein kinases in rat hippocampal neurons: Isolation of ptk-3, a receptor expressed in proliferative zones of the developing brain. Proc Natl Acad Sci U S A. 1994;91:1819–23.CrossRefPubMedPubMedCentral

27.

Johnson JD, Edman JC, Rutter WJ. A receptor tyrosine kinase found in breast carcinoma cells has an extracellular discoidin i-like domain. Proc Natl Acad Sci U S A. 1993;90:5677–81.CrossRefPubMedPubMedCentral

28.

Laval S, Butler R, Shelling AN, Hanby AM, Poulsom R, Ganesan TS. Isolation and characterization of an epithelial-specific receptor tyrosine kinase from an ovarian cancer cell line. Cell Growth Differ Mol Biol J Am Assoc Cancer Res. 1994;5:1173–83.

29.

Vogel WF, Aszodi A, Alves F, Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol. 2001;21:2906–17.CrossRefPubMedPubMedCentral

30.

Alves F, Vogel W, Mossie K, Millauer B, Hofler H, Ullrich A. Distinct structural characteristics of discoidin i subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene. 1995;10:609–18.PubMed

31.

Miao L, Zhu S, Wang Y, Li Y, Ding J, Dai J, et al. Discoidin domain receptor 1 is associated with poor prognosis of non-small cell lung cancer and promotes cell invasion via epithelial-to-mesenchymal transition. Med Oncol. 2013;30:626.CrossRefPubMed

32.

Toy KA, Valiathan RR, Nunez F, Kidwell KM, Gonzalez ME, Fridman R, et al. Tyrosine kinase discoidin domain receptors ddr1 and ddr2 are coordinately deregulated in triple-negative breast cancer. Breast Cancer Res Treat. 2015;150:9–18.CrossRefPubMedPubMedCentral

33.

Huo Y, Yang M, Liu W, Yang J, Fu X, Liu D, et al. High expression of ddr1 is associated with the poor prognosis in Chinese patients with pancreatic ductal adenocarcinoma. J Exp Clin Cancer Res CR. 2015;34:88.CrossRefPubMed

34.

Rudra-Ganguly N, Lowe C, Mattie M, Chang MS, Satpayev D, Verlinsky A, et al. Discoidin domain receptor 1 contributes to tumorigenesis through modulation of tgfbi expression. PLoS One. 2014;9, e111515.CrossRefPubMedPubMedCentral

35.

Hou G, Vogel W, Bendeck MP. The discoidin domain receptor tyrosine kinase ddr1 in arterial wound repair. J Clin Invest. 2001;107:727–35.CrossRefPubMedPubMedCentral

36.

Ruiz PA, Jarai G. Collagen i induces discoidin domain receptor (ddr) 1 expression through ddr2 and a jak2-erk1/2-mediated mechanism in primary human lung fibroblasts. J Biol Chem. 2011;286:12912–23.CrossRefPubMedPubMedCentral

37.

Maeda M, Johnson KR, Wheelock MJ. Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J Cell Sci. 2005;118:873–87.CrossRefPubMed

38.

Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118:277–9.CrossRefPubMed

39.

Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871–90.CrossRefPubMed

40.

Sarkar FH, Li Y, Wang Z, Kong D. Pancreatic cancer stem cells and emt in drug resistance and metastasis. Minerva Chir. 2009;64:489–500.PubMedPubMedCentral

41.

Battaglia S, Benzoubir N, Ghigna MR, Guettier C, Brechot C, Bourgeade MF. Epithelial-mesenchymal transition and hepatocellular carcinoma. Ann Pathol. 2009;29(Spec No 1):S65–6.CrossRefPubMed

42.

Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249–57.CrossRefPubMed

43.

Ferrara N, Alitalo K. Clinical applications of angiogenic growth factors and their inhibitors. Nat Med. 1999;5:1359–64.CrossRefPubMed

44.

Weis SM, Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med. 2011;17:1359–70.CrossRefPubMed

45.

Cao YEG, Wang E, Pal K, Dutta SK, Bar-Sagi D, Mukhopadhyay D. Vegf exerts an angiogenesis-independent function in cancer cells to promote their malignant progression. Cancer Res. 2012;72:3912–8.CrossRefPubMedPubMedCentral

46.

Reel B, Korkmaz CG, Arun MZ, Yildirim G, Ogut D, Kaymak A, et al. The regulation of matrix metalloproteinase expression and the role of discoidin domain receptor 1/2 signalling in zoledronate-treated pc3 cells. J Cancer. 2015;6:1020–9.CrossRefPubMedPubMedCentral

47.

Fu HL, Sohail A, Valiathan RR, Wasinski BD, Kumarasiri M, Mahasenan KV, et al. Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. J Biol Chem. 2013;288:12114–29.CrossRefPubMedPubMedCentral

48.

Castro-Sanchez L, Soto-Guzman A, Guaderrama-Diaz M, Cortes-Reynosa P, Salazar EP. Role of ddr1 in the gelatinases secretion induced by native type iv collagen in mda-mb-231 breast cancer cells. Clin Exp Metastasis. 2011;28:463–77.CrossRefPubMed

49.

Kim HG, Tan L, Weisberg EL, Liu F, Canning P, Choi HG, et al. Discovery of a potent and selective ddr1 receptor tyrosine kinase inhibitor. ACS Chem Biol. 2013;8:2145–50.CrossRefPubMedPubMedCentral

50.

Carafoli F, Mayer MC, Shiraishi K, Pecheva MA, Chan LY, Nan R, et al. Structure of the discoidin domain receptor 1 extracellular region bound to an inhibitory fab fragment reveals features important for signaling. Structure. 2012;20:688–97.CrossRefPubMed

Titel: Discoidin domain receptor 1 (DDR1), a promising biomarker, induces epithelial to mesenchymal transition in renal cancer cells
verfasst von: Jingyuan Song
Xiao Chen
Jin Bai
Qinghua Liu
Hui Li
Jianwan Xie
Hui Jing
Junnian Zheng
Publikationsdatum: 28.03.2016
Verlag: Springer Netherlands
Erschienen in: Tumor Biology / Ausgabe 8/2016
Print ISSN: 1010-4283
Elektronische ISSN: 1423-0380
DOI: https://doi.org/10.1007/s13277-016-5021-2

Neu im Fachgebiet Onkologie

25.04.2024 | Nierenkarzinom | Nachrichten

Springer Medizin

Discoidin domain receptor 1 (DDR1), a promising biomarker, induces epithelial to mesenchymal transition in renal cancer cells

Abstract

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 8/2016

MicroRNA-134 modulates glioma cell U251 proliferation and invasion by targeting KRAS and suppressing the ERK pathway

The conglomeration of diagnostic, prognostic and therapeutic potential of serum miR-199a and its association with clinicopathological features in epithelial ovarian cancer

The potential role of CacyBP/SIP in tumorigenesis

Transforming growth factor (TGF) β1 acted through miR-130b to increase integrin α5 to promote migration of colorectal cancer cells

Overexpression of c-Myb is associated with suppression of distant metastases in colorectal carcinoma

Linc-ROR induces epithelial-mesenchymal transition and contributes to drug resistance and invasion of breast cancer cells

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie