Macrophage Binding to Receptor VCAM-1 Transmits Survival Signals in Breast Cancer Cells that Invade the Lungs

Cancer Cell

Volumn 20, Issue 4, 2011, Pages 538-549

  Chen, Qing ^a   Zhang, Xiang H F ^a   Massagué, Joan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; EZRIN; PROTEIN KINASE B; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL; CELL INFILTRATION; CELL INVASION; CELL SURFACE; CELL SURVIVAL; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN TISSUE; LEUKOCYTE; LUNG METASTASIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 80054725681     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.08.025     Document Type: Article

References (63)

1. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics International 2004, 11:36-42.
2. Alessi D.R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., Hemmings B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 1996, 15:6541-6551.
3. Allinen M., Beroukhim R., Cai L., Brennan C., Lahti-Domenici J., Huang H., Porter D., Hu M., Chin L., Richardson A., et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004, 6:17-32.
4. Anan K., Mitsuyama S., Koga K., Tanabe R., Saimura M., Tanabe Y., Watanabe M., Suehara N., Matsunaga H., Nishihara K., et al. Disparities in the survival improvement of recurrent breast cancer. Breast Cancer 2010, 17:48-55.
5. Aslakson C.J., Miller F.R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992, 52:1399-1405.
6. Barreiro O., Yanez-Mo M., Serrador J.M., Montoya M.C., Vicente-Manzanares M., Tejedor R., Furthmayr H., Sanchez-Madrid F. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol. 2002, 157:1233-1245.
7. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., Massagué J. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
8. Cailleau R., Young R., Olivé M., Reeves W.J. Breast tumor cell lines from pleural effusions. J. Natl. Cancer Inst. 1974, 53:661-674.
9. Cameron M.D., Schmidt E.E., Kerkvliet N., Nadkarni K.V., Morris V.L., Groom A.C., Chambers A.F., MacDonald I.C. Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res. 2000, 60:2541-2546.
10. Cheng J., Huo D.H., Kuang D.M., Yang J., Zheng L., Zhuang S.M. Human macrophages promote the motility and invasiveness of osteopontin-knockdown tumor cells. Cancer Res. 2007, 67:5141-5147.
11. Chuan Y.C., Pang S.T., Cedazo-Minguez A., Norstedt G., Pousette A., Flores-Morales A. Androgen induction of prostate cancer cell invasion is mediated by ezrin. J. Biol. Chem. 2006, 281:29938-29948.
12. Collins B.J., Deak M., Arthur J.S., Armit L.J., Alessi D.R. In vivo role of the PIF-binding docking site of PDK1 defined by knock-in mutation. EMBO J. 2003, 22:4202-4211.
13. Comi G. Treatment of multiple sclerosis: role of natalizumab. Neurol. Sci. 2009, 30(Suppl 2):S155-S158.
14. Cybulsky M.I., Fries J.W., Williams A.J., Sultan P., Eddy R., Byers M., Shows T., Gimbrone M.A., Collins T. Gene structure, chromosomal location, and basis for alternative mRNA splicing of the human VCAM1 gene. Proc. Natl. Acad. Sci. USA 1991, 88:7859-7863.
15. Ding Y.B., Chen G.Y., Xia J.G., Zang X.W., Yang H.Y., Yang L. Association of VCAM-1 overexpression with oncogenesis, tumor angiogenesis and metastasis of gastric carcinoma. World J. Gastroenterol. 2003, 9:1409-1414.
16. Elices M.J., Osborn L., Takada Y., Crouse C., Luhowskyj S., Hemler M.E., Lobb R.R. VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 1990, 60:577-584.
17. Fehon R.G., McClatchey A.I., Bretscher A. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 2010, 11:276-287.
18. Fidler I.J. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 2003, 3:453-458.
19. Gao D., Nolan D.J., Mellick A.S., Bambino K., McDonnell K., Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008, 319:195-198.
20. Gautreau A., Poullet P., Louvard D., Arpin M. Ezrin, a plasma membrane-microfilament linker, signals cell survival through the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. USA 1999, 96:7300-7305.
21. Giraudo E., Inoue M., Hanahan D. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J. Clin. Invest. 2004, 114:623-633.
22. Gocheva V., Wang H.W., Gadea B.B., Shree T., Hunter K.E., Garfall A.L., Berman T., Joyce J.A. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010, 24:241-255.
23. Gupta G.P., Nguyen D.X., Chiang A.C., Bos P.D., Kim J.Y., Nadal C., Gomis R.R., Manova-Todorova K., Massagué J. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007, 446:765-770.
24. Jones D.H., Nakashima T., Sanchez O.H., Kozieradzki I., Komarova S.V., Sarosi I., Morony S., Rubin E., Sarao R., Hojilla C.V., et al. Regulation of cancer cell migration and bone metastasis by RANKL. Nature 2006, 440:692-696.
25. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 2009, 9:239-252.
26. Kalogeris T.J., Kevil C.G., Laroux F.S., Coe L.L., Phifer T.J., Alexander J.S. Differential monocyte adhesion and adhesion molecule expression in venous and arterial endothelial cells. Am. J. Physiol. 1999, 276:L9-L19.
27. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordón-Cardo C., Guise T.A., Massagué J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
28. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
29. Kim M.Y., Oskarsson T., Acharyya S., Nguyen D.X., Zhang X.H., Norton L., Massagué J. Tumor self-seeding by circulating cancer cells. Cell 2009, 139:1315-1326.
30. Krieg J., Hunter T. Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J. Biol. Chem. 1992, 267:19258-19265.
31. Lin E.Y., Li J.F., Gnatovskiy L., Deng Y., Zhu L., Grzesik D.A., Qian H., Xue X.N., Pollard J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006, 66:11238-11246.
32. Lipscomb M.F., Bice D.E., Lyons C.R., Schuyler M.R., Wilkes D. The regulation of pulmonary immunity. Adv. Immunol. 1995, 59:369-455.
33. Luzzi K.J., MacDonald I.C., Schmidt E.E., Kerkvliet N., Morris V.L., Chambers A.F., Groom A.C. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153:865-873.
34. MacDonald I.C., Groom A.C., Chambers A.F. Cancer spread and micrometastasis development: quantitative approaches for in vivo models. Bioessays 2002, 24:885-893.
35. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., Massagué J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524.
36. Minn A.J., Gupta G.P., Padua D., Bos P., Nguyen D.X., Nuyten D., Kreike B., Zhang Y., Wang Y., Ishwaran H., et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc. Natl. Acad. Sci. USA 2007, 104:6740-6745.
37. Müller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
38. Nguyen D.X., Bos P.D., Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 2009, 9:274-284.
39. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43.
40. Osborn L., Hession C., Tizard R., Vassallo C., Luhowskyj S., Chi-Rosso G., Lobb R. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 1989, 59:1203-1211.
41. Padua D., Zhang X.H., Wang Q., Nadal C., Gerald W.L., Gomis R.R., Massagué J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 2008, 133:66-77.
42. Pàez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Viñals F., Inoue M., Bergers G., Hanahan D., Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15:220-231.
43. Perez O.D., Kinoshita S., Hitoshi Y., Payan D.G., Kitamura T., Nolan G.P., Lorens J.B. Activation of the PKB/AKT pathway by ICAM-2. Immunity 2002, 16:51-65.
44. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., He X., Perou C.M. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 2010, 12:R68.
45. Qian B., Deng Y., Im J.H., Muschel R.J., Zou Y., Li J., Lang R.A., Pollard J.W. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 2009, 4:e6562.
46. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
47. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
48. Ricono J.M., Huang M., Barnes L.A., Lau S.K., Weis S.M., Schlaepfer D.D., Hanks S.K., Cheresh D.A. Specific cross-talk between epidermal growth factor receptor and integrin alphavbeta5 promotes carcinoma cell invasion and metastasis. Cancer Res. 2009, 69:1383-1391.
49. Rubin J., Titus L., Nanes M.S. Regulation of complement 5a receptor expression in U937 cells by phorbol ester. J. Leukoc. Biol. 1991, 50:502-508.
50. Ruco L.P., de Laat P.A., Matteucci C., Bernasconi S., Sciacca F.M., van der Kwast T.H., Hoogsteden H.C., Uccini S., Mantovani A., Versnel M.A. Expression of ICAM-1 and VCAM-1 in human malignant mesothelioma. J. Pathol. 1996, 179:266-271.
51. Sangaletti S., Di Carlo E., Gariboldi S., Miotti S., Cappetti B., Parenza M., Rumio C., Brekken R.A., Chiodoni C., Colombo M.P. Macrophage-derived SPARC bridges tumor cell-extracellular matrix interactions toward metastasis. Cancer Res. 2008, 68:9050-9059.
52. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
53. Schmidt K.J., Büning J., Jankowiak C., Lehnert H., Fellermann K. Crohn's targeted therapy: myth or real goal?. Curr. Drug Discov. Technol. 2009, 6:290-298.
54. Shin J., Kim J., Ryu B., Chi S.G., Park H. Caveolin-1 is associated with VCAM-1 dependent adhesion of gastric cancer cells to endothelial cells. Cell. Physiol. Biochem. 2006, 17:211-220.
55. Tavazoie S.F., Alarcón C., Oskarsson T., Padua D., Wang Q., Bos P.D., Gerald W.L., Massagué J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152.
56. van Wetering S., van den Berk N., van Buul J.D., Mul F.P., Lommerse I., Mous R., ten Klooster J.P., Zwaginga J.J., Hordijk P.L. VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leukocyte transmigration. Am. J. Physiol. Cell Physiol. 2003, 285:C343-C352.
57. Vonderheide R.H., Tedder T.F., Springer T.A., Staunton D.E. Residues within a conserved amino acid motif of domains 1 and 4 of VCAM-1 are required for binding to VLA-4. J. Cell Biol. 1994, 125:215-222.
58. Wong C.W., Lee A., Shientag L., Yu J., Dong Y., Kao G., Al-Mehdi A.B., Bernhard E.J., Muschel R.J. Apoptosis: an early event in metastatic inefficiency. Cancer Res. 2001, 61:333-338.
59. Wyckoff J., Wang W., Lin E.Y., Wang Y., Pixley F., Stanley E.R., Graf T., Pollard J.W., Segall J., Condeelis J. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004, 64:7022-7029.
60. Yamamoto T., Sakaguchi N., Hachiya M., Nakayama F., Yamakawa M., Akashi M. Role of catalase in monocytic differentiation of U937 cells by TPA: hydrogen peroxide as a second messenger. Leukemia 2009, 23:761-769.
61. Yin J.J., Selander K., Chirgwin J.M., Dallas M., Grubbs B.G., Wieser R., Massagué J., Mundy G.R., Guise T.A. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 1999, 103:197-206.
62. Zhang X.H., Wang Q., Gerald W., Hudis C.A., Norton L., Smid M., Foekens J.A., Massagué J. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009, 16:67-78.
63. Zoncu R., Efeyan A., Sabatini D.M. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 2011, 12:21-35.