The lysyl oxidase inhibitor, β-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Bondavera, Alla ^a,c   Downey, Charlene M ^a,c   Ayres, Fabio ^b,c   Liu, Wei ^b,c   Boyd, Steven K ^b,c   Hallgrimsson, Benedikt ^b,c   Jirik, Frank R ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPIONITRILE; LUCIFERASE; PROTEIN LYSINE 6 OXIDASE; ANTINEOPLASTIC AGENT;

ADRENAL METASTASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BLADDER METASTASIS; BONE METASTASIS; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER INVASION; CELL MOTILITY; CONTROLLED STUDY; DISEASE FREE SURVIVAL; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HEART METASTASIS; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; METASTASIS INHIBITION; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOLYSIS; OVARY METASTASIS; OVERALL SURVIVAL; PANCREAS CANCER; PERITONEUM METASTASIS; PROTEIN EXPRESSION; STOMACH CANCER; TREATMENT OUTCOME; TUMOR VOLUME; ANIMAL; BREAST TUMOR; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; METASTASIS; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR EMBOLISM;

MUS;

AMINOPROPIONITRILE; ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; PROTEIN-LYSINE 6-OXIDASE; X-RAY MICROTOMOGRAPHY;

EID: 66049119129     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005620     Document Type: Article

References (59)

1. Gonzalez-Angulo AM, Morales-Vasquez F, Hortobagyi GN (2007) Overview of resistance to systemic therapy in patients with breast cancer. Adv Exp Med Biol 608: 1-22.
2. Manders K, van de Poll-Franse LV, Creemers GJ, Vreugdenhil G, van der Sangen MJ, et al. (2006) Clinical management of women with metastatic breast cancer: a descriptive study according to age group. BMC Cancer 6: 179.
3. Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2: 563-572.
4. Lu X, Kang Y (2007) Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 12: 153-162.
5. Duffy MJ, McGowan PM, Gallagher WM (2008) Cancer invasion and metastasis: changing views. J Pathol 214: 283-293.
6. Gupta GP, Massague J (2006) Cancer metastasis: building a framework. Cell 127: 679-695.
7. Wu M, Wu ZF, Merajver SD (2007) Rho proteins and cell-matrix interactions in cancer. Cells Tissues Organs 185: 100-103.
8. Casey T, Bond J, Tighe S, Hunter T, Lintault L, et al. (2008) Molecular signatures suggest a major role for stromal cells in development of invasive breast cancer. Breast Cancer Res Treat.
9. Crawford NP, Walker RC, Lukes L, Officewala JS, Williams RW, et al. (2008) The Diasporin Pathway: a tumor progression-related transcriptional network that predicts breast cancer survival. Clin Exp Metastasis 25: 357-369.
10. Kagan HM, Li W (2003) Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 88: 660-672.
11. Mello ML, Contente S, Vidal BC, Planding W, Schenck U (1995) Modulation of ras transformation affecting chromatin supraorganization as assessed by image analysis. Exp Cell Res 220: 374-382.
12. Di Donato A, Lacal JC, Di Duca M, Giampuzzi M, Ghiggeri G, et al. (1997) Micro-injection of recombinant lysyl oxidase blocks oncogenic p21-Ha-Ras and progesterone effects on Xenopus laevis oocyte maturation. FEBS Lett 419: 63-68.
13. Giampuzzi M, Botti G, Di Duca M, Arata L, Ghiggeri G, et al. (2000) Lysyl oxidase activates the transcription activity of human collagene III promoter. Possible involvement of Ku antigen. J Biol Chem 275: 36341-36349.
14. Maki JM, Rasanen J, Tikkanen H, Sormunen R, Makikallio K, et al. (2002) Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice. Circulation 106: 2503-2509.
15. Denko NC, Fontana LA, Hudson KM, Sutphin PD, Raychaudhuri S, et al. (2003) Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 22: 5907-5914.
16. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, et al. (2006) Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440: 1222-1226.
17. Postovit LM, Abbott DE, Payne SL, Wheaton WW, Margaryan NV, et al. (2008) Hypoxia/reoxygenation: a dynamic regulator of lysyl oxidase-facilitated breast cancer migration. J Cell Biochem 103: 1369-1378.
18. Li W, Liu G, Chou IN, Kagan HM (2000) Hydrogen peroxide-mediated, lysyl oxidase-dependent chemotaxis of vascular smooth muscle cells. J Cell Biochem 78: 550-557.
19. Giampuzzi M, Oleggini R, Di Donato A (2003) Altered adhesion features and signal transduction in NRK-49F cells transformed by down-regulation of lysyl oxidase. Biochim Biophys Acta 1647: 239-244.
20. Payne SL, Fogelgren B, Hess AR, Seftor EA, Wiley EL, et al. (2005) Lysyl oxidase regulates breast cancer cell migration and adhesion through a hydrogen peroxide-mediated mechanism. Cancer Res 65: 11429-11436.
21. Payne SL, Hendrix MJ, Kirschmann DA (2007) Paradoxical roles for lysyl oxidases in cancer-a prospect. J Cell Biochem 101: 1338-1354.
22. Kirschmann DA, Seftor EA, Nieva DR, Mariano EA, Hendrix MJ (1999) Differentially expressed genes associated with the metastatic phenotype in breast cancer. Breast Cancer Res Treat 55: 127-136.
23. Nagaraja GM, Othman M, Fox BP, Alsaber R, Pellegrino CM, et al. (2006) Gene expression signatures and biomarkers of noninvasive and invasive breast cancer cells: comprehensive profiles by representational difference analysis, microarrays and proteomics. Oncogene 25: 2328-2338.
24. Kirschmann DA, Seftor EA, Fong SF, Nieva DR, Sullivan CM, et al. (2002) A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res 62: 4478-4483.
25. Peinado H, Del Carmen Iglesias-de la Cruz M, Olmeda D, Csiszar K, Fong KS, et al. (2005) A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. Embo J 24: 3446-3458.
26. Minn AJ, Kang Y, Serganova I, Gupta GP, Giri DD, et al. (2005) Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest 115: 44-55.
27. Jenkins DE, Hornig YS, Oei Y, Dusich J, Purchio T (2005) Bioluminescent human breast cancer cell lines that permit rapid and sensitive in vivo detection of mammary tumors and multiple metastases in immune deficient mice. Breast Cancer Res 7: R444-454.
28. Lee KC, Hamstra DA, Bhojani MS, Khan AP, Ross BD, et al. (2007) Noninvasive molecular imaging sheds light on the synergy between 5-fluorouracil and TRAIL/Apo2L for cancer therapy. Clin Cancer Res 13: 1839-1846.
29. Drake JM, Gabriel CL, Henry MD (2005) Assessing tumor growth and distribution in a model of prostate cancer metastasis using bioluminescence imaging. Clin Exp Metastasis 22: 674-684.
30. Schluter K, Gassmann P, Enns A, Korb T, Hemping-Bovenkerk A, et al. (2006) Organ-specific metastatic tumor cell adhesion and extravasation of colon carcinoma cells with different metastatic potential. Am J Pathol 169: 1064-1073.
31. Yamauchi K, Yang M, Jiang P, Xu M, Yamamoto N, et al. (2006) Development of real-time subcellular dynamic multicolor imaging of cancer-cell trafficking in live mice with a variable-magnification whole-mouse imaging system. Cancer Res 66: 4208-4214.
32. Morris VL, Schmidt EE, MacDonald IC, Groom AC, Chambers AF (1997) Sequential steps in hematogenous metastasis of cancer cells studied by in vivo videomicroscopy. Invasion Metastasis 17: 281-296.
33. Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, et al. (1998) Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol 153: 865-873.
34. Braun S, Vogl FD, Naume B, Janni W, Osborne MP, et al. (2005) A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 353: 793-802.
35. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, et al. (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537-549.
36. Amer MH (1982) Chemotherapy and pattern of metastases in breast cancer patients. J Surg Oncol 19: 101-105.
37. Lee YT (1983) Breast carcinoma: pattern of metastasis at autopsy. J Surg Oncol 23: 175-180.
38. Kozlow W, Guise TA (2005) Breast cancer metastasis to bone: mechanisms of osteolysis and implications for therapy. J Mammary Gland Biol Neoplasia 10: 169-180.
39. Jenkins DE, Oei Y, Hornig YS, Yu SF, Dusich J, et al. (2003) Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clin Exp Metastasis 20: 733-744.
40. Cowey S, Szafran AA, Kappes J, Zinn KR, Siegal GP, et al. (2007) Breast cancer metastasis to bone: evaluation of bioluminescent imaging and microSPECT/CT for detecting bone metastasis in immunodeficient mice. Clin Exp Metastasis 24: 389-401.
41. Phadke PA, Mercer RR, Harms JF, Jia Y, Frost AR, et al. (2006) Kinetics of metastatic breast cancer cell trafficking in bone. Clin Cancer Res 12: 1431-1440.
42. Naumov GN, Wilson SM, MacDonald IC, Schmidt EE, Morris VL, et al. (1999) Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J Cell Sci 112(Pt 12): 1835-1842.
43. Weis S, Cui J, Barnes L, Cheresh D (2004) Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol 167: 223-229.
44. Miles FL, Pruitt FL, van Golen KL, Cooper CR (2008) Stepping out of the flow: capillary extravasation in cancer metastasis. Clin Exp Metastasis 25: 305-324.
45. Hornstra IK, Birge S, Starcher B, Bailey AJ, Mecham RP, et al. (2003) Lysyl oxidase is required for vascular and diaphragmatic development in mice. J Biol Chem 278: 14387-14393.
46. Levene CI, Heale G, Robins SP (1989) Collagen cross-link synthesis in cultured vascular endothelium. Br J Exp Pathol 70: 621-626.
47. Rodriguez C, Martinez-Gonzalez J, Raposo B, Alcudia JF, Guadall A, et al. (2008) Regulation of lysyl oxidase in vascular cells: lysyl oxidase as a new player in cardiovascular diseases. Cardiovasc Res 79: 7-13.
48. Payne SL, Hendrix MJ, Kirschmann DA (2006) Lysyl oxidase regulates actin filament formation through the p130(Cas)/Crk/DOCK180 signaling complex. J Cell Biochem 98: 827-837.
49. Usatyuk PV, Natarajan V (2005) Regulation of reactive oxygen species-induced endothelial cell-cell and cell-matrix contacts by focal adhesion kinase and adherens junction proteins. Am J Physiol Lung Cell Mol Physiol 289: L999-1010.
50. Ben Mahdi MH, Andrieu V, Pasquier C (2000) Focal adhesion kinase regulation by oxidative stress in different cell types. IUBMB Life 50: 291-299.
51. Carbajal JM, Schaeffer RC Jr (1998) H2O2 and genistein differentially modulate protein tyrosine phosphorylation, endothelial morphology, and monolayer barrier function. Biochem Biophys Res Commun 249: 461-466.
52. Chiarugi P, Pani G, Giannoni E, Taddei L, Colavitti R, et al. (2003) Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J Cell Biol 161: 933-944.
53. Kevil CG, Okayama N, Alexander JS (2001) H(2)O(2)-mediated permeability II: importance of tyrosine phosphatase and kinase activity. Am J Physiol Cell Physiol 281: C1940-1947.
54. Earley S, Plopper GE (2008) Phosphorylation of focal adhesion kinase promotes extravasation of breast cancer cells. Biochem Biophys Res Commun 366: 476-482.
55. Choy A, McCulloch P (1996) Induction of tumour cell shedding into effluent venous blood breast cancer surgery. Br J Cancer 73: 79-82.
56. Galan M, Vinolas N, Colomer D, Soler G, Munoz M, et al. (2002) Detection of occult breast cancer cells by amplification of CK19 mRNA by reverse transcriptase-polymerase chain reaction: role of surgical manipulation. Anticancer Res 22: 2877-2884.
57. Erler JT, Giaccia AJ (2006) Lysyl oxidase mediates hypoxic control of metastasis. Cancer Res 66: 10238-10241.
58. Li X, Wang J, An Z, Yang M, Baranov E, et al. (2002) Optically imageable metastatic model of human breast cancer. Clin Exp Metastasis 19: 347-350.
59. Lazarus HM, Cruikshank WW, Narasimhan N, Kagan HM, Center DM (1995) Induction of human monocyte motility by lysyl oxidase. Matrix Biol 14: 727-731.