Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment

Nature Medicine

Volumn 16, Issue 9, 2010, Pages 1009-1017

  Barry Hamilton, Vivian ^a   Spangler, Rhyannon ^a   Marshall, Derek ^a   McCauley, Scott ^a   Rodriguez, Hector M ^a   Oyasu, Miho ^a   Mikels, Amanda ^a   Vaysberg, Maria ^a   Ghermazien, Haben ^a   Wai, Carol ^a   Garcia, Carlos A ^a   Velayo, Arleene C ^a   Jorgensen, Brett ^a   Biermann, Donna ^a   Tsai, Daniel ^a   Green, Jennifer ^a   Zaffryar Eilot, Shelly ^b   Holzer, Alison ^a   Ogg, Scott ^a   Thai, Dung ^a   Neufeld, Gera ^b   Van Vlasselaer, Peter ^a   Smith, Victoria ^a   more..

^a Arresto BioSciences   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPIONITRILE; DOCETAXEL; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY AB0023; PROTEIN LYSINE 6 OXIDASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; AB023A; LACTONE; LOXL2 PROTEIN, HUMAN; LOXL2 PROTEIN, MOUSE; OXIDOREDUCTASE; POLYENE; SMALL INTERFERING RNA;

ALLOSTERISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG SAFETY; ENDOTHELIUM CELL; ENZYME INHIBITION; FIBROBLAST; LUNG FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR BIOPSY; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; DRUG EFFECTS; FEMALE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; NEOPLASM METASTASIS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

AMINO ACID OXIDOREDUCTASES; AMINOPROPIONITRILE; ANIMALS; ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; LACTONES; MICE; MICE, NUDE; NEOPLASM METASTASIS; POLYENES; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 77956425361     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2208     Document Type: Article

References (58)

1. Barcellos-Hoff, M.H. & Ravani, S.A. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res. 60, 1254-1260 (2000).
2. Bhowmick, N.A., Neilson, E.G. & Moses, H.L. Stromal fbroblasts in cancer initiation and progression. Nature 432, 332-337 (2004).
3. Coussens, L.M. & Werb, Z. Infammation and cancer. Nature 420, 860-867 (2002).
4. Cunha, G.R., Hayward, S.W., Wang, Y.Z. & Ricke, W.A. Role of the stromal microenvironment in carcinogenesis of the prostate. Int. J. Cancer 107, 1-10 (2003).
5. Jacobs, T.W., Byrne, C., Colditz, G., Connolly, J.L. & Schnitt, S.J. Radial scars in benign breast-biopsy specimens and the risk of breast cancer. N. Engl. J. Med. 340, 430-436 (1999).
6. Olumi, A.F. et al. Carcinoma-associated fbroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 59, 5002-5011 (1999).
7. Orimo, A. et al. Cancer-associated myofbroblasts possess various factors to promote endometrial tumor progression. Clin. Cancer Res. 7, 3097-3105 (2001).
8. Kleeff, J. et al. Pancreatic cancer microenvironment. Int. J. Cancer 121, 699-705 (2007).
9. Cardone, A., Tolino, A., Zarcone, R., Borruto Caracciolo, G. & Tartaglia, E. Prognostic value of desmoplastic reaction and lymphocytic infltration in the management of breast cancer. Panminerva Med. 39, 174-177 (1997).
10. Chu, G.C., Kimmelman, A.C., Hezel, A.F. & DePinho, R.A. Stromal biology of pancreatic cancer. J. Cell. Biochem. 101, 887-907 (2007).
11. Conti, J.A. et al. The desmoplastic reaction surrounding hepatic colorectal adenocarcinoma metastases aids tumor growth and survival via alphav integrin ligation. Clin. Cancer Res. 14, 6405-6413 (2008).
12. Maeshima, A.M. et al. Modifed scar grade: a prognostic indicator in small peripheral lung adenocarcinoma. Cancer 95, 2546-2554 (2002).
13. Sappino, A.P., Skalli, O., Jackson, B., Schurch, W. & Gabbiani, G. Smooth-muscle differentiation in stromal cells of malignant and non-malignant breast tissues. Int. J. Cancer 41, 707-712 (1988).
14. Dong, J. et al. VEGF-null cells require PDGFRα signaling-mediated stromal fbroblast recruitment for tumorigenesis. EMBO J. 23, 2800-2810 (2004).
15. Hinz, B. et al. The myofbroblast: one function, multiple origins. Am. J. Pathol. 170, 1807-1816 (2007).
16. Hlatky, L., Tsionou, C., Hahnfeldt, P. & Coleman, C.N. Mammary fbroblasts may infuence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res. 54, 6083-6086 (1994).
17. Orimo, A. et al. Stromal fbroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335-348 (2005).
18. Butcher, D.T., Alliston, T. & Weaver, V.M. A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122 (2009).
19. Georges, P.C. et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fbrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G1147-G1154 (2007).
20. Levental, K.R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009).
21. Wipff, P.J., Rifkin, D.B., Meister, J.J. & Hinz, B. Myofbroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179, 1311-1323 (2007).
22. Suki, B., Ito, S., Stamenovic, D., Lutchen, K.R. & Ingenito, E.P. Biomechanics of the lung parenchyma: critical roles of collagen and mechanical forces. J. Appl. Physiol. 98, 1892-1899 (2005).
23. Kagan, H.M. & Li, W. Lysyl oxidase: properties, specifcity, and biological roles inside and outside of the cell. J. Cell. Biochem. 88, 660-672 (2003).
24. Payne, S.L., Hendrix, M.J. & Kirschmann, D.A. Paradoxical roles for lysyl oxidases in cancer\a prospect. J. Cell. Biochem. 101, 1338-1354 (2007).
25. Vadasz, Z. et al. Abnormal deposition of collagen around hepatocytes in Wilson's disease is associated with hepatocyte specifc expression of lysyl oxidase and lysyl oxidase like protein-2. J. Hepatol. 43, 499-507 (2005).
26. Erler, J.T. et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440, 1222-1226 (2006).
27. Akiri, G. et al. Lysyl oxidase-related protein-1 promotes tumor fbrosis and tumor progression in vivo. Cancer Res. 63, 1657-1666 (2003).
28. Fong, S.F. et al. Lysyl oxidase-like 2 expression is increased in colon and esophageal tumors and associated with less differentiated colon tumors. Genes Chromosom. Cancer 46, 644-655 (2007).
29. Hollosi, P., Yakushiji, J.K., Fong, K.S., Csiszar, K. & Fong, S.F. Lysyl oxidase-like 2 promotes migration in noninvasive breast cancer cells but not in normal breast epithelial cells. Int. J. Cancer 125, 318-327 (2009).
30. Kirschmann, D.A. et al. A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 62, 4478-4483 (2002).
31. Peng, L. et al. Secreted LOXL2 is a novel therapeutic target that promotes gastric cancer metastasis via the Src/FAK pathway. Carcinogenesis 30, 1660-1669 (2009).
32. Rodriguez, H.M. et al. Modulation of lysyl oxidase-like 2 enzymatic activity by an allosteric antibody inhibitor. J. Biol. Chem. 285, 20964-20974 (2010).
33. Peinado, H. et al. A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J. 24, 3446-3458 (2005).
34. Lelièvre, E. et al. VE-statin/egf7 regulates vascular elastogenesis by interacting with lysyl oxidases. EMBO J. 27, 1658-1670 (2008).
35. Chambers, A.F. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res. 69, 5292-5293 (2009).
36. Yang, F. et al. Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res. 65, 8887-8895 (2005).
37. Gozuacik, D. & Kimchi, A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23, 2891-2906 (2004).
38. Tang, S.S., Trackman, P.C. & Kagan, H.M. Reaction of aortic lysyl oxidase with beta-aminopropionitrile. J. Biol. Chem. 258, 4331-4338 (1983).
39. Trackman, P.C. & Kagan, H.M. Nonpeptidyl amine inhibitors are substrates of lysyl oxidase. J. Biol. Chem. 254, 7831-7836 (1979).
40. Jenkins, D.E., Hornig, Y.S., Oei, Y., Dusich, J. & Purchio, T. Bioluminescent human breast cancer cell lines that permit rapid and sensitive in vivo detection of mammary tumors and multiple metastases in immune defcient mice. Breast Cancer Res. 7, R444-R454 (2005).
41. The French METAVIR Cooperative Study Group. Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. Hepatology 20, 15-20 (1994).
42. Tahashi, Y. et al. Differential regulation of TGF-β signal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 35, 49-61 (2002).
43. Inagaki, Y. et al. Constitutive phosphorylation and nuclear localization of Smad3 are correlated with increased collagen gene transcription in activated hepatic stellate cells. J. Cell. Physiol. 187, 117-123 (2001).
44. Khalil, N. & O'Connor, R. Idiopathic pulmonary fbrosis: current understanding of the pathogenesis and the status of treatment. CMAJ 171, 153-160 (2004).
45. Moeller, A., Ask, K., Warburton, D., Gauldie, J. & Kolb, M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fbrosis? Int. J. Biochem. Cell Biol. 40, 362-382 (2008).
46. Ashcroft, T., Simpson, J.M. & Timbrell, V. Simple method of estimating severity of pulmonary fbrosis on a numerical scale. J. Clin. Pathol. 41, 467-470 (1988).
47. Moeller, A. et al. Circulating fbrocytes are an indicator of poor prognosis in idiopathic pulmonary fbrosis. Am. J. Respir. Crit. Care Med. 179, 588-594 (2009).
48. Park, S.H., Saleh, D., Giaid, A. & Michel, R.P. Increased endothelin-1 in bleomycin-induced pulmonary fbrosis and the effect of an endothelin receptor antagonist. Am. J. Respir. Crit. Care Med. 156, 600-608 (1997).
49. Pulichino, A.M. et al. Identifcation of transforming growth factor beta1-driven genetic programs of acute lung fbrosis. Am. J. Respir. Cell Mol. Biol. 39, 324-336 (2008).
50. Xu, J. et al. Role of the SDF-1/CXCR4 axis in the pathogenesis of lung injury and fbrosis. Am. J. Respir. Cell Mol. Biol. 37, 291-299 (2007).
51. Dornhöfer, N. et al. Connective tissue growth factor-specifc monoclonal antibody therapy inhibits pancreatic tumor growth and metastasis. Cancer Res. 66, 5816-5827 (2006).
52. Guleng, B. et al. Blockade of the stromal cell-derived factor-1/CXCR4 axis attenuates in vivo tumor growth by inhibiting angiogenesis in a vascular endothelial growth factor-independent manner. Cancer Res. 65, 5864-5871 (2005).
53. Bailey, J.M. et al. Sonic hedgehog promotes desmoplasia in pancreatic cancer. Clin. Cancer Res. 14, 5995-6004 (2008).
54. 6 inhibits tumor progression in vivo by a transforming growth factor-β-regulated mechanism. Cancer Res. 68, 561-570 (2008).
55. Ge, R. et al. Inhibition of growth and metastasis of mouse mammary carcinoma by selective inhibitor of transforming growth factor-β type I receptor kinase in vivo. Clin. Cancer Res. 12, 4315-4330 (2006).
56. Nam, J.S. et al. An anti-transforming growth factor β antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res. 68, 3835-3843 (2008).
57. Qiu, W. et al. No evidence of clonal somatic genetic alterations in cancer-associated fbroblasts from human breast and ovarian carcinomas. Nat. Genet. 40, 650-655 (2008).
58. Constandinou, C., Henderson, N. & Iredale, J.P. Modeling liver fbrosis in rodents. Methods Mol. Med. 117, 237-250 (2005).