LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis

Cancer Research

Volumn 73, Issue 6, 2013, Pages 1721-1732

  Cox, Thomas R ^a,b,c   Bird, Demelza ^b,c   Baker, Ann Marie ^b   Barker, Holly E ^b   Ho, Melisa W Y ^d   Lang, Georgina ^b,c   Erler, Janine T ^a,b,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Division of Cancer Biology   (Denmark)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d Inflammation Discovery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; COLLAGEN TYPE 1; FIBRONECTIN; PROTEIN LYSINE 6 OXIDASE; PROTEIN TYROSINE KINASE;

ALVEOLAR BONE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL ACTIVATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; DRUG TARGETING; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROSIS; HOMEOSTASIS; IN VIVO STUDY; IRRADIATION; METASTASIS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; SCORING SYSTEM; TUMOR CELL; TUMOR MICROENVIRONMENT;

BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; COLLAGEN; FIBROSIS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LUNG NEOPLASMS; NEOPLASM METASTASIS; PROTEIN-LYSINE 6-OXIDASE;

EID: 84875445066     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2233     Document Type: Article

References (53)

1. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006;12:895-904.
2. Nguyen DX, Bos PD, Massague J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 2009;9:274-84.
3. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006;127:679-95.
4. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003;3:453-8.
5. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420:860-7.
6. Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 2005;7:17-23.
7. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005;8:241-54.
8. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, Le QT, et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006;440:1222-6.
9. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009; 15:35-44.
10. Cox TR, Erler JT. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 2011;4:165-78.
11. Fidler IJ. The organ microenvironment and cancer metastasis. Differentiation 2002;70:498-505.
12. Bissell MJ, Radisky DC, Rizki A, Weaver VM, Petersen OW. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 2002;70:537-46.
13. Hu M, Polyak K. Microenvironmental regulation of cancer development. Curr Opin Genet Dev 2008;18:27-34.
14. Calvo F, Sahai E. Cell communication networks in cancer invasion. Curr Opin Cell Biol 2011;23:621-9.
15. Tlsty TD, Coussens LM. Tumor stroma and regulation of cancer development. Annu Rev Pathol 2006;1:119-50.
16. Massague J. New concepts in tissue-specific metastases. Clin Adv Hematol Oncol 2003;1:576-7.
17. Cox TR, Gartland A, Erler JT. The pre-metastatic niche: is metastasis random? BoneKEy Rep 2012;1.
18. Erler JT, Weaver VM. Three-dimensional context regulation of metastasis. Clin Exp Metastasis 2009;26:35-49.
19. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007;170:1807-16.
20. Radisky DC, Kenny PA, Bissell MJ. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 2007; 101:830-9.
21. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007;117: 524-9.
22. Keeley EC, Mehrad B, Strieter RM. Fibrocytes: bringing new insights into mechanisms of inflammation and fibrosis. Int J Biochem Cell Biol 2009;42:535-42.
23. Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer 2009;9:108-22.
24. Kagan HM, Li W. Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 2003;88: 660-72.
25. Csiszar K. Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 2001;70:1-32.
26. Phan SH. Fibroblast phenotypes in pulmonary fibrosis. Am J Respir Cell Mol Biol 2003;29 (3 Suppl):S87-92.
27. Crystal RG, Bitterman PB, Mossman B, Schwarz MI, Sheppard D, Almasy L, et al. Future research directions in idiopathic pulmonary fibrosis: summary of a National Heart, Lung, and Blood Institute working group. Am J Respir Crit Care Med 2002;166:236-46.
28. Noble PW. Idiopathic pulmonary fibrosis. New insights into classification and pathogenesis usher in a new era therapeutic approaches. Am J Respir Cell Mol Biol 2003;29 (3 Suppl):S27-31.
29. Egeblad M, Rasch MG, Weaver VM. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 2010;22: 697-706.
30. MaXJ, Dahiya S, Richardson E, Erlander M,Sgroi DC. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res 2009;11:R7.
31. Qiu TH, Chandramouli GV, Hunter KW, Alkharouf NW, Green JE, Liu ET. Global expression profiling identifies signatures of tumor virulence in MMTV-PyMT-transgenic mice: correlation to human disease. Cancer Res 2004;64:5973-81.
32. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003;33:49-54.
33. Calvo A, Catena R, Noble MS, Carbott D, Gil-Bazo I, Gonzalez-Moreno O, et al. Identification of VEGF-regulated genes associated with increased lung metastatic potential: functional involvement of tenascin-C in tumor growth and lung metastasis. Oncogene 2008;27: 5373-84.
34. Jensen BV, Johansen JS, Skovsgaard T, Brandt J, Teisner B. Extracellular matrix building marked by the N-terminal propeptide of procollagen type I reflect aggressiveness of recurrent breast cancer. Int J Cancer 2002;98:582-9.
35. Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010;70:5706-16.
36. Yamazaki Y, Mikami Y, Yuguchi M, Namba Y, Isokawa K. Development of collagen fibres and lysyl oxidase expression in the presumptive dermis of chick limb bud. Anat Histol Embryol 2012;41:68-74.
37. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008;123:2229-38.
38. Llovet JM, Chen Y, Wurmbach E, Roayaie S, Fiel MI, Schwartz M, et al. A molecular signature to discriminate dysplastic nodules from early hepatocellular carcinoma in HCV cirrhosis. Gastroenterology 2006;131:1758-67.
39. Madani I, De Neve W, Mareel M. Does ionizing radiation stimulate cancer invasion and metastasis? Bull Cancer 2008;95:292-300.
40. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988;41:467-70.
41. Zhang HY, Gharaee-Kermani M, Zhang K, Karmiol S, Phan SH. Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 1996;148:527-37.
42. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 2010;16: 1009-17.
43. Friedman SL. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J Biol Chem 2000;275:2247-50.
44. Kapoun AM, Gaspar NJ, Wang Y, Damm D, Liu YW, O'Young G, et al. Transforming growth factor-beta receptor type 1 (TGFbetaRI) kinase activity but not p38 activation is required for TGFbetaRI-induced myofibroblast differentiation and profibrotic gene expression. Mol Pharmacol 2006;70:518-31.
45. Pires IM, Bencokova Z, Milani M, Folkes LK, Li JL, Stratford MR, et al. Effects of acute versus chronic hypoxia on DNA damage responses and genomic instability. Cancer Res 2010;70:925-35.
46. Zibadi S, Vazquez R, Larson DF, Watson RR. T lymphocyte regulation of lysyl oxidase in diet-induced cardiac fibrosis. Cardiovasc Toxicol 2010;10:190-8.
47. Baker AM, Cox TR, Bird D, Lang G, Murray GI, Sun XF, et al. The role of lysyl oxidase in SRC-dependent proliferation and metastasis of colorectal cancer. J Natl Cancer Inst 2011;103:407-24.
48. Nakao A, Fujii M, Matsumura R, Kumano K, Saito Y, Miyazono K, et al. Transient gene transfer and expression of Smad7 prevents bleomycininduced lung fibrosis in mice. J Clin Invest 1999;104:5-11.
49. Kolb M,Margetts PJ,Galt T, SimePJ, Xing Z, SchmidtM, et al. Transient transgene expressionofdecorin in the lungreduces the fibrotic response to bleomycin. Am J Respir Crit Care Med 2001;163:770-7.
50. Ando M, Murakami Y, Kojima F, Endo H, Kitasato H, Hashimoto A, et al. Retrovirally introduced prostaglandin D2 synthase suppresses lung injury induced by bleomycin. Am J Respir Cell Mol Biol 2003;28: 582-91.
51. Kijiyama N, Ueno H, Sugimoto I, Sasaguri Y, Yatera K, Kido M, et al. Intratracheal gene transfer of tissue factor pathway inhibitor attenuates pulmonary fibrosis. Biochem Biophys Res Commun 2006;339: 1113-9.
52. Zhao J, Shi W, Wang YL, Chen H, Bringas P Jr, Datto MB, et al. Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2002;282:L585-93.
53. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci U S A 2011;108: 16369-74.