Discoidin domain receptor 2 (DDR2) promotes breast cancer cell metastasis and the mechanism implicates epithelial-mesenchymal transition programme under hypoxia

Journal of Pathology

Volumn 234, Issue 4, 2014, Pages 526-537

  Ren, Tingting ^a   Zhang, Wei ^a   Liu, Xinping ^a   Zhao, Hu ^a   Zhang, Jian ^a   Zhang, Jing ^a   Li, Xia ^a   Zhang, Yan ^a   Bu, Xin ^a   Shi, Man ^a   Yao, Libo ^a   Su, Jin ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Collagen receptor; DDR2; EMT; Hypoxia; Tumour metastasis

Indexed keywords

COLLAGEN RECEPTOR; DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UVOMORULIN; DISCOIDIN RECEPTOR; LECTIN RECEPTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST METASTASIS; CANCER GROWTH; CELL ACTIVATION; CELL ADHESION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; LYMPH NODE METASTASIS; MCF 7 CELL LINE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR INVASION; TUMOR XENOGRAFT; ANIMAL; BREAST TUMOR; CELL HYPOXIA; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL HYPOXIA; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HETEROGRAFTS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN;

EID: 84911991734     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4415     Document Type: Article

References (45)

1. McCormack VA, dos Santos Silva I. Breast density and parenchymalpatterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2006; 15: 1159-1169.
2. Sinkus R, Lorenzen J, Schrader D, et al. High-resolution tensor MRelastography for breast tumour detection. Phys Med Biol 2000; 45:1649-1664.
3. Butcher DT, Alliston T, Weaver VM. A tense situation: forcingtumour progression. Nature Rev Cancer 2009; 9: 108-122.
4. Lochter A, Bissell MJ. Involvement of extracellular matrix constituentsin breast cancer. Semin Cancer Biol 1995; 6: 165-173.
5. Provenzano PP, Eliceiri KW, Campbell JM, et al. Collagen reorganizationat the tumor-stromal interface facilitates local invasion. BMC Med 2006; 4: 38.
6. Provenzano PP, Inman DR, Eliceiri KW, et al. Collagen densitypromotes mammary tumor initiation and progression. BMC Med2008; 6: 11.
7. Li T, Sun L,Miller N, et al. The association ofmeasured breast tissuecharacteristics with mammographic density and other risk factorsfor breast cancer. Cancer Epidemiol Biomarkers Prev 2005; 14:343-349.
8. Vogel W, Gish GD, Alves F, et al. The discoidin domain receptortyrosine kinases are activated by collagen. Mol Cell 1997; 1: 13-23.
9. Leitinger B, Kwan AP. The discoidin domain receptor DDR2 is areceptor for type X collagen. Matrix Biol 2006; 25: 355-364.
10. Goldsmith EC, Zhang X, Watson J, et al. The collagen receptorDDR2 is expressed during early cardiac development. Anat Rec(Hoboken) 2010; 293: 762-769.
11. Goldsmith EC, Hoffman A, Morales MO, et al. Organization offibroblasts in the heart. Dev Dyn 2004; 230: 787-794.
12. Maeyama M, Koga H, Selvendiran K, et al. Switching in discoiddomain receptor expressions in SLUG-induced epithelial-mesenchymal transition. Cancer 2008; 113: 2823-2831.
13. Vogel WF, Abdulhussein R, Ford CE. Sensing extracellular matrix:an update on discoidin domain receptor function. Cell Signal 2006;18: 1108-1116.
14. Zhang Y, Su J, Yu J, et al. An essential role of discoidin domainreceptor 2 (DDR2) in osteoblast differentiation and chondrocytematuration via modulation of Runx2 activation. J Bone Miner Res2011; 26: 604-617.
15. Olaso E, Ikeda K, Eng FJ, et al. DDR2 receptor promotesMMP-2-mediated proliferation and invasion by hepatic stellate cells. J Clin Invest 2001; 108: 1369-1378.
16. Ren T, Zhang J, Liu X, Yao L. Increased expression of discoidindomain receptor 2 (DDR2): a novel independent prognostic markerofworse outcome in breast cancer patients. MedOncol 2013; 30: 397.
17. Su J, Yu J, Ren T, et al. Discoidin domain receptor 2 is associatedwith the increased expression of matrix metalloproteinase-13 insynovial fibroblasts of rheumatoid arthritis. Mol Cell Biochem 2009;330: 141-152.
18. Lester RD, Jo M, Montel V, et al. uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J Cell Biol2007; 178: 425-436.
19. Chen SC, Wang BW, Wang DL, et al. Hypoxia induces discoidindomain receptor-2 expression via the p38 pathway in vascular smoothmuscle cells to increase their migration. Biochem Biophys Res Commun2008; 374: 662-667.
20. Zhang S, Bu X, Zhao H, et al. A host deficiency of discoidin domainreceptor 2 (DDR2) inhibits both tumor angiogenesis and metastasis.J Pathol 2014; 232: 436-448.
21. Walsh LA, Nawshad A, Medici D. Discoidin domain receptor 2 is acritical regulator of epithelial-mesenchymal transition. Matrix Biol2011; 30: 243-247.
22. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nature Rev Cancer 2002; 2: 442-454.
23. Batlle E, Sancho E, Franci C, et al. The transcription factor snail isa repressor of E-cadherin gene expression in epithelial tumour cells.Nature Cell Biol 2000; 2: 84-89.
24. Grunert S, Jechlinger M, Beug H. Diverse cellular and molecularmechanisms contribute to epithelial plasticity and metastasis. Nature Rev Mol Cell Biol 2003; 4: 657-665.
25. Peinado H, Portillo F, Cano A. Transcriptional regulation of cadherinsduring development and carcinogenesis. Int J Dev Biol 2004;48: 365-375.
26. Nieto MA. The snail superfamily of zinc-finger transcription factors.Nature Rev Mol Cell Biol 2002; 3: 155-166.
27. Eger A, Aigner K, Sonderegger S, et al. DeltaEF1 is a transcriptionalrepressor of E-cadherin and regulates epithelial plasticity in breastcancer cells. Oncogene 2005; 24: 2375-2385.
28. Adeyinka A, Nui Y, Cherlet T, et al. Activated mitogen-activatedprotein kinase expression during human breast tumorigenesis andbreast cancer progression. Clin Cancer Res 2002; 8: 1747-1753.
29. Reddy KB, Nabha SM, Atanaskova N. Role of MAP kinase in tumorprogression and invasion. Cancer Metastasis Rev 2003; 22: 395-403.
30. Shyu KG, Chao YM, Wang BW, et al. Regulation of discoidindomain receptor 2 by cyclic mechanical stretch in cultured rat vascularsmooth muscle cells. Hypertension 2005; 46: 614-621.
31. Katanasaka Y, Asai T, Naitou H, et al. Proteomic characterization ofangiogenic endothelial cells stimulated with cancer cell-conditionedmedium. Biol Pharm Bull 2007; 30: 2300-2307.
32. Falanga V, Zhou L, Yufit T. Low oxygen tension stimulates collagensynthesis and COL1A1 transcription through the action of TGF-beta1. J Cell Physiol 2002; 191: 42-50.
33. Horino Y, Takahashi S, Miura T, et al. Prolonged hypoxia acceleratesthe posttranscriptional process of collagen synthesis in cultured fibroblasts. Life Sci 2002; 71: 3031-3045.
34. Eswaramoorthy R, Wang CK, Chen WC, et al. DDR1 regulates thestabilization of cell surface E-cadherin and E-cadherin-mediated cell aggregation. J Cell Physiol 2010; 224: 387-397.
35. Olaso E, Labrador JP, Wang L, et al. Discoidin domain receptor2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem 2002; 277: 3606-3613.
36. Labrador JP, Azcoitia V, Tuckermann J, et al. The collagen receptorDDR2 regulates proliferation and its elimination leads to dwarfism.EMBO Rep 2001; 2: 446-452.
37. Hammerman PS, Sos ML, Ramos AH, et al. Mutations in the DDR2kinase gene identify a novel therapeutic target in squamous cell lungcancer. Cancer Discov 2011; 1: 78-89.
38. Badiola I, Villace P, Basaldua I, et al. Downregulation of discoidindomain receptor 2 in A375 human melanoma cells reduces its experimentalliver metastasis ability. Oncol Rep 2011; 26: 971-978.
39. Zhang K, Corsa CA, Ponik SM, et al. The collagen receptor discoidindomain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nature Cell Biol 2013; 15: 677-687.
40. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1(HIF-1): implications in metastasis and development. Cell Cycle2008; 7: 2090-2096.
41. Lee NO, Park JW, Lee JA, et al. Dual action of a selectivecyclooxygenase-2 inhibitor on vascular endothelial growth factorexpression in human hepatocellular carcinoma cells: novel involvementof discoidin domain receptor 2. J Cancer Res Clin Oncol 2012;138: 73-84.
42. Lundgren K, Nordenskjold B, Landberg G. Hypoxia, Snail andincomplete epithelial-mesenchymal transition in breast cancer. Br J Cancer 2009; 101: 1769-1781.
43. Mottet D, Michel G, Renard P, et al. Role of ERK and calcium inthe hypoxia-induced activation of HIF-1. J Cell Physiol 2003; 194:30-44.
44. Loboda A, Jozkowicz A, Dulak J. HIF-1 and HIF-2 transcription factors-similar but not identical. Molecules Cells 2010; 29: 435-442.
45. De Craene B, Berx G. Regulatory networks defining EMT duringcancer initiation and progression. Nature Rev Cancer 2013; 13:97-110.