TGFβ 1-endo180-dependent collagen deposition is dysregulated at the tumour-stromal interface in bone metastasis

Journal of Pathology

Volumn 226, Issue 5, 2012, Pages 775-783

  Caley, Matthew P ^a   Kogianni, Giolanta ^a   Adamarek, Adam ^a   Gronau, Julian H ^a   Rodriguez Teja, Mercedes ^a   Fonseca, Ana Violeta ^a   Mauri, Francesco ^b   Sandison, Ann ^c   Rhim, Johng S ^d   Palmieri, Carlo ^a   Cobb, Justin P ^a   Waxman, Jonathan ^a   Sturge, Justin ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

^d University of the Health Sciences   (United States)

Author keywords

Bone; Collagen; Endo180; Metastasis; Metastatic; Osteoblast; Osteolytic; Prostate cancer

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN BINDING PROTEIN; COLLAGEN RECEPTOR; COLLAGEN TYPE 1; ENDO180 COLLAGEN RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; BONE BIOPSY; BONE METASTASIS; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTERNALIZATION; OSTEOBLAST; PRIORITY JOURNAL; PROSTATE TUMOR; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR MICROENVIRONMENT; UPREGULATION;

AUTOCRINE COMMUNICATION; BIOPSY; BONE NEOPLASMS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; COLLAGEN TYPE I; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MANNOSE-BINDING LECTINS; MEMBRANE GLYCOPROTEINS; OSTEOBLASTS; PARACRINE COMMUNICATION; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, MITOGEN; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1; TUMOR MICROENVIRONMENT;

EID: 84857993919     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.3958     Document Type: Article

References (39)

1. Henriksen K, Neutzsky-Wulff AV, Bonewald LF, et al. Local communication on and within bone controls bone remodeling. Bone 2009; 44: 1026-1033.
2. Clines GA, Guise TA. Molecular mechanisms and treatment of bone metastasis. Expert Rev Mol Med 2008; 10: e7.
3. Sturge J, Caley MP, Waxman J. Bone metastasis in prostate cancer: emerging therapeutic strategies. Nature Rev Clin Oncol 2011; 8: 357-368.
4. Thomas EK, Nakamura M, Wienke D, et al. Endo180 binds to the C-terminal region of type I collagen. J Biol Chem 2005; 280: 22596-22605. (Pubitemid 40853163)
5. Jurgensen HJ, Madsen DH, Ingvarsen S, et al. A novel functional role of collagen glycosylation: interaction with the endocytic receptor uPARAP/Endo180. J Biol Chem 2011; 286: 32736-32748.
6. Wagenaar-Miller RA, Engelholm LH, Gavard J, et al. Complementary roles of intracellular and pericellular collagen degradation pathways in vivo. Mol Cell Biol 2007; 27: 6309-6322. (Pubitemid 47435739)
7. Fasquelle C, Sartelet A, Li W, et al. Balancing selection of a frame-shift mutation in the MRC2 gene accounts for the outbreak of the Crooked Tail Syndrome in Belgian Blue Cattle. PLoS Genet 2009; 5: e1000666.
8. Huijbers IJ, Iravani M, Popov S, et al. A role for fibrillar collagen deposition and the collagen internalization receptor Endo180 in glioma invasion. PLoS One 2010; 5: e9808.
9. Wienke D, Davies GC, Johnson DA, et al. The collagen receptor Endo180 (CD280) is expressed on basal-like breast tumor cells and promotes tumor growth in vivo. Cancer Res 2007; 67: 10230-10240. (Pubitemid 350070796)
10. Juarez P, Guise TA. TGF-beta in cancer and bone: implications for treatment of bone metastases. Bone 2011; 48: 23-29.
11. East L, McCarthy A, Wienke D, et al. A targeted deletion in the endocytic receptor gene Endo180 results in a defect in collagen uptake. EMBO Rep 2003; 4: 710-716. (Pubitemid 36974757)
12. Engelholm LH, List K, Netzel-Arnett S, et al. uPARAP/Endo180 is essential for cellular uptake of collagen and promotes fibroblast collagen adhesion. J Cell Biol 2003; 160: 1009-1015. (Pubitemid 36443870)
13. Wienke D, MacFadyen JR, Isacke CM. Identification and characterization of the endocytic transmembrane glycoprotein Endo180 as a novel collagen receptor. Mol Biol Cell 2003; 14: 3592-3604. (Pubitemid 37151611)
14. Madsen DH, Ingvarsen S, Jurgensen HJ, et al. The non-phagocytic route of collagen uptake: a distinct degradation pathway. J Biol Chem 2011; 286: 26996-27010.
15. Sturge J, Wienke D, Isacke CM. Endosomes generate localized Rho-ROCK-MLC2-based contractile signals via Endo180 to promote adhesion disassembly. J Cell Biol 2006; 175: 337-347. (Pubitemid 44631427)
16. Wu K, Yuan J, Lasky LA. Characterization of a novel member of the macrophage mannose receptor type C lectin family. J Biol Chem 1996; 271: 21323-21330. (Pubitemid 26292993)
17. Howard MJ, Chambers MG, Mason RM, et al. Distribution of Endo180 receptor and ligand in developing articular cartilage. Osteoarthritis Cartilage 2004; 12: 74-82. (Pubitemid 38111553)
18. Engelholm LH, Nielsen BS, Netzel-Arnett S, et al. The urokinase plasminogen activator receptor-associated protein/Endo180 is coexpressed with its interaction partners urokinase plasminogen activator receptor and matrix metalloprotease-13 during osteogenesis. Lab Invest 2001; 81: 1403-1414. (Pubitemid 32980163)
19. Kogianni G, Walker MM, Waxman J, et al. Endo180 expression with cofunctional partners MT1-MMP and uPAR-uPA is correlated with prostate cancer progression. Eur J Cancer 2009; 45: 685-693.
20. Yasunaga Y, Nakamura K, Ko D, et al. A novel human cancer culture model for the study of prostate cancer. Oncogene 2001; 20: 8036-8041. (Pubitemid 34001565)
21. Gu Y, Kim KH, Ko D, et al. A telomerase-immortalized primary human prostate cancer clonal cell line with neoplastic phenotypes. Int J Oncol 2004; 25: 1057-1064.
22. Gu Y, Li H, Miki J, et al. Phenotypic characterization of telomerase-immortalized primary non-malignant and malignant tumor-derived human prostate epithelial cell lines. Exp Cell Res 2006; 312: 831-843.
23. Reichert JC, Quent VM, Burke LJ, et al. Mineralized human primary osteoblast matrices as a model system to analyse interactions of prostate cancer cells with the bone microenvironment. Biomaterials 2010; 31: 7928-7936.
24. Nemeth JA, Harb JF, Barroso U Jr, et al. Severe combined immunodeficient-hu model of human prostate cancer metastasis to human bone. Cancer Res 1999; 59: 1987-1993. (Pubitemid 29186176)
25. Akech J, Wixted JJ, Bedard K, et al. Runx2 association with progression of prostate cancer in patients: mechanisms mediating bone osteolysis and osteoblastic metastatic lesions. Oncogene 2009; 29: 811-821.
26. Lee Y, Schwarz E, Davies M, et al. Differences in the cytokine profiles associated with prostate cancer cell induced osteoblastic and osteolytic lesions in bone. J Orthop Res 2003; 21: 62-72. (Pubitemid 36157621)
27. Wu HC, Hsieh JT, Gleave ME, et al. Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int J Cancer 1994; 57: 406-412. (Pubitemid 24168617)
28. Wilding G, Zugmeier G, Knabbe C, et al. Differential effects of transforming growth factor beta on human prostate cancer cells in vitro. Mol Cell Endocrinol 1989; 62: 79-87. (Pubitemid 19070496)
29. Kim IY, Ahn HJ, Zelner DJ, et al. Genetic change in transforming growth factor beta (TGF-beta) receptor type I gene correlates with insensitivity to TGF-beta 1 in human prostate cancer cells. Cancer Res 1996; 56: 44-48. (Pubitemid 26010383)
30. Kim IY, Zelner DJ, Sensibar JA, et al. Modulation of sensitivity to transforming growth factor-beta 1 (TGF-beta 1) and the level of type II TGF-beta receptor in LNCaP cells by dihydrotestosterone. Exp Cell Res 1996; 222: 103-110.
31. Tang Y, Wu X, Lei W, et al. TGF-β1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nature Med 2009; 15: 757-765.
32. Centrella M, McCarthy TL, Canalis E. Transforming growth factor beta is a bifunctional regulator of replication and collagen synthesis in osteoblast-enriched cell cultures from fetal rat bone. J Biol Chem 1987; 262: 2869-2874.
33. D'Souza RN, Niederreither K, de Crombrugghe B. Osteoblast-specific expression of the alpha 2(I) collagen promoter in transgenic mice: correlation with the distribution of TGF-beta 1. J Bone Miner Res 1993; 8: 1127-1136. (Pubitemid 23261107)
34. Horner A, Kemp P, Summers C, et al. Expression and distribution of transforming growth factor-beta isoforms and their signaling receptors in growing human bone. Bone 1998; 23: 95-102. (Pubitemid 28379869)
35. Kang Y, Siegel PM, Shu W, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003; 3: 537-549. (Pubitemid 36808649)
36. Kang Y, He W, Tulley S, et al. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc Natl Acad Sci U S A 2005; 102: 13909-13914. (Pubitemid 41377677)
37. Korpal M, Yan J, Lu X, et al. Imaging transforming growth factor-beta signaling dynamics and therapeutic response in breast cancer bone metastasis. Nature Med 2009; 15: 960-966.
38. Coulson-Thomas VJ, Gesteira TF, Coulson-Thomas YM, et al. Fibroblast and prostate tumor cell cross-talk: fibroblast differentiation, TGF-β, and extracellular matrix down-regulation. Exp Cell Res 2010; 316: 3207-3226.
39. Ye Q, Xing Q, Ren Y, et al. Endo180 and MT1-MMP are involved in the phagocytosis of collagen scaffolds by macrophages and is regulated by interferon-gamma. Eur Cell Mater 2010; 20: 197-209.