Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-β-deficient mouse mammary carcinomas

Cancer Research

Volumn 73, Issue 17, 2013, Pages 5336-5346

  Pickup, Michael W ^a   Laklai, Hanane ^b   Acerbi, Irene ^b   Owens, Philip ^a   Gorska, Agnieszka E ^a   Chytil, Anna ^a   Aakre, Mary ^a   Weaver, Valerie M ^b   Moses, Harold L ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPIONITRILE; COLLAGEN; CYTOKERATIN 14; PROTEIN LYSINE 6 OXIDASE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CONTROLLED STUDY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LUNG METASTASIS; METASTASIS; METASTASIS INHIBITION; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA; TUMOR PROMOTION; TUMOR VOLUME;

ANIMALS; CARCINOGENESIS; COLLAGEN; ENZYME INHIBITORS; FEMALE; FIBROBLASTS; FOCAL ADHESION KINASE 1; HUMANS; IN SITU HYBRIDIZATION; KERATIN-14; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; MICROSCOPY, ATOMIC FORCE; MYELOID CELLS; PHOSPHORYLATION; PROTEIN-LYSINE 6-OXIDASE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84883477750     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-0012     Document Type: Article

References (35)

1. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008;14:518-27. (Pubitemid 351655218)
2. Khamis ZI, Sahab ZJ, Sang QX. Active roles of tumor stroma in breast cancer metastasis. Int J Breast Cancer 2012;2012:574025.
3. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009;139:891 -906.
4. Garamszegi N, Garamszegi SP, Shehadeh LA, Scully SP. Extracellular matrix-induced gene expression in human breast cancer cells. Mol Cancer Res 2009;7:319-29.
5. Boyd NF, Guo H, Martin LJ, Sun L, Stone J, Fishell E, et al. Mammographic density and the risk and detection of breast cancer. New Engl J Med 2007;356:227-36. (Pubitemid 46143226)
6. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, et al. Collagen density promotes mammary tumor initiation and progression. BMC Med 2008;6:11.
7. Taylor MA, Amin JD, Kirschmann DA, Schiemann WP. Lysyl oxidase contributes to mechanotransduction-mediated regulation of transforming growth factor-beta signaling in breast cancer cells. Neoplasia 2011;13:406-18.
8. Forrester E, Chytil A, Bierie B, Aakre M, Gorska AE, Sharif-Afshar AR, et al. Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis. Cancer Res 2005;65:2296-302. (Pubitemid 40490139)
9. Bierie B, Stover DG, Abel TW, Chytil A, Gorska AE, Aakre M, et al. Transforming growth factor-beta regulates mammary carcinoma cell survival and interaction with the adjacent microenvironment. Cancer Res 2008;68:1809-19. (Pubitemid 351416566)
10. Gorden DL, Fingleton B, Crawford HC, Jansen DE, Lepage M, Matrisian LM. Resident stromal cell-derived MMP-9 promotes the growth of colorectal metastases in the liver microenvironment. Int J Cancer 2007;121:495-500. (Pubitemid 46986480)
11. Bullen A, Friedman RS, Krummel MF. Two-photon imaging of the immune system: a custom technology platform for high-speed, multicolor tissue imaging of immune responses. Curr Top Microbiol Immunol 2009;334:1-29.
12. Payne SL, Hendrix MJ, Kirschmann DA. Paradoxical roles for lysyl oxidases in cancer - a prospect. J Cell Biochem 2007;101:1338-54. (Pubitemid 47242767)
13. 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.
14. Wilmarth KR, Froines JR. In vitro and in vivo inhibition of lysyl oxidase by aminopropionitriles. J Toxicol Environ Health 1992;37: 411-23.
15. Bondareva A, Downey CM, Ayres F, Liu W, Boyd SK, Hallgrimsson B, et al. The lysyl oxidase inhibitor, beta-aminopropionitrile, diminishes the metastatic colonization potential of circulating breast cancer cells. PLoS ONE 2009;4:e5620.
16. Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat Rev Cancer 2004;4:448 -56.
17. 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.
18. Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol 2008;26:2568-81.
19. Gatza ML, Kung HN, Blackwell KL, Dewhirst MW, Marks JR, Chi JT. Analysis of tumor environmental response and oncogenic pathway activation identifies distinct basal and luminal features in HER2-related breast tumor subtypes. Breast Cancer Res 2011;13:R62.
20. Cox TR, Bird D, Baker AM, Barker HE, Ho MW, Lang G, et al. LOX-mediated collagen crosslinking is responsible for fibrosis-enhanced metastasis. Cancer Res 2013;73:1721-32.
21. Peyrol S, Raccurt M, Gerard F, Gleyzal C, Grimaud JA, Sommer P. Lysyl oxidase gene expression in the stromal reaction to in situ and invasive ductal breast carcinoma. Am J Pathol 1997;150:497-507. (Pubitemid 27073780)
22. Arora PD, McCulloch CA. Dependence of collagen remodelling on alpha-smooth muscle actin expression by fibroblasts. J Cellular Physiol 1994;159:161-75. (Pubitemid 24234588)
23. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, et al. Abrogation of TGF beta signaling inmammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35. (Pubitemid 350309741)
24. Boak AM, Roy R, Berk J, Taylor L, Polgar P, Goldstein RH, et al. Regulation of lysyl oxidase expression in lung fibroblasts by transforming growth factor-beta 1 and prostaglandin E2. Am J Respir Cell Mol Biol 1994;11:751-5.
25. Choudhary B, Zhou J, Li P, Thomas S, Kaartinen V, Sucov HM. Absence of TGFbeta signaling in embryonic vascular smooth muscle leads to reduced lysyl oxidase expression, impaired elastogenesis, and aneurysm. Genesis 2009;47:115-21.
26. Sethi A, Mao W, Wordinger RJ, Clark AF. Transforming growth factor-beta induces extracellular matrix protein cross-linking lysyl oxidase (LOX) genes in human trabecular meshwork cells. Invest Ophthalmol Vis Sci 2011;52:5240-50.
27. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2002;62:65-74. (Pubitemid 34680517)
28. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012;21: 309-22.
29. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012;196:395-406.
30. Bierie B, Chung CH, Parker JS, Stover DG, Cheng N, Chytil A, et al. Abrogation of TGF-beta signaling enhances chemokine production and correlates with prognosis in human breast cancer. J Clin Invest 2009;119:1571-82.
31. Paiva CE, Serrano SV, Paiva BS, Scapulatempo-Neto C, Soares FA, Rogatto SR, et al. Absence of TGF-betaRII predicts bone and lung metastasis and is associated with poor prognosis in stage III breast tumors. Cancer Biomark 2012;11:209-17.
32. Baker AM, Bird D, Lang G, Cox TR, Erler JT. Lysyl oxidase enzymatic function increases stiffness to drive colorectal cancer progression through FAK. Oncogene 2013;32:1863-8.
33. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial- mesenchymal transition. Mol Biol Cell 2012;23:781-91.
34. Chu IM, Michalowski AM, Hoenerhoff M, Szauter KM, Luger D, Sato M, et al. GATA3 inhibits lysyl oxidase-mediated metastases of human basal triple-negative breast cancer cells. Oncogene 2012;31:2017-27.
35. Nguyen-Ngoc KV, Cheung KJ, Brenot A, Shamir ER, Gray RS, Hines WC, et al. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci U S A 2012;109:E2595-604.