The role of the tumor-microenvironment in lung cancer-metastasis and its relationship to potential therapeutic targets

Cancer Treatment Reviews

Volumn 40, Issue 4, 2014, Pages 558-566

  Wood, Steven L ^a   Pernemalm, Maria ^a,b   Crosbie, Philip A ^a   Whetton, Anthony D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Chemotaxis; Lung cancer; Metastasis; Metastatic niche; Micro environment; Organ tropism

Indexed keywords

ADRENAL METASTASIS; ADVANCED CANCER; ANGIOGENESIS; AUTOCRINE EFFECT; BONE METASTASIS; BRAIN METASTASIS; CANCER MORTALITY; CANCER SURVIVAL; CELL INTERACTION; CHEMOTAXIS; DRUG TARGETING; EXTRACELLULAR MATRIX; GROWTH; HUMAN; INTRACELLULAR SPACE; LIVER METASTASIS; LUNG CANCER; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; METASTASIS; MICROMETASTASIS; NONHUMAN; OVERALL SURVIVAL; OXYGENATION; PARACRINE SIGNALING; PRIMARY TUMOR; QUALITY OF LIFE; REVIEW; RNA SEQUENCE; SURVIVAL RATE; SURVIVAL TIME; TROPISM; TUMOR MICROENVIRONMENT; VASCULARIZATION;

CHEMOTAXIS; LUNG CANCER; METASTASIS; METASTATIC NICHE; MICRO-ENVIRONMENT; ORGAN-TROPISM;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL COMMUNICATION; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84896737116     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2013.10.001     Document Type: Review

References (127)

1. Langer C.J., Besse B., Gualberto A., Brambilla E., Soria J.C. The evolving role of histology in the management of advanced non-small-cell lung cancer. J Clin Oncol 2010, 28:5311-5320.
2. Thomsen M., Dahl M., Lange P., Vestbo J., Nordestgaard B.G. Inflammatory biomarkers and comorbidities in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012, 186:982-988.
3. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
4. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
5. Azzali G. The modality of transendothelial passage of lymphocytes and tumor cells in the absorbing lymphatic vessel. Eur J Histochem 2007, 51(Suppl 1):73-77.
6. Gupta G.P., Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
7. Chunhacha P., Chanvorachote P. Roles of caveolin-1 on anoikis resistance in non small cell lung cancer. Int J Physiol Pathophysiol Pharmacol 2012, 4:149-155.
8. Al-Mehdi A.B., Tozawa K., Fisher A.B., Shientag L., Lee A., Muschel R.J. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 2000, 6:100-102.
9. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2002, 2:563-572.
10. Gupta G.P., Nguyen D.X., Chiang A.C., Bos P.D., Kim J.Y., Nadal C., et al. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007, 446:765-770.
11. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009, 9:285-293.
12. Erler J.T., Bennewith K.L., Cox T.R., 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.
13. Zhang X.H., Wang Q., Gerald W., Hudis C.A., Norton L., Smid M., et al. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009, 16:67-78.
14. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordon-Cardo C., et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
15. Nguyen D.X., Bos P.D., Massague J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 2009, 9:274-284.
16. Friedl P., Locker J., Sahai E., Segall J.E. Classifying collective cancer cell invasion. Nat Cell Biol 2012, 14:777-783.
17. Tischler V., Pfeifer M., Hausladen S., Schirmer U., Bonde A.K., Kristiansen G., et al. L1CAM protein expression is associated with poor prognosis in non-small cell lung cancer. Mol Cancer 2011, 10:127.
18. Pan S.H., Chao Y.C., Hung P.F., Chen H.Y., Yang S.C., Chang Y.L., et al. The ability of LCRMP-1 to promote cancer invasion by enhancing filopodia formation is antagonized by CRMP-1. J Clin Invest 2011, 121:3189-3205.
19. Haraguchi M., Okubo T., Miyashita Y., Miyamoto Y., Hayashi M., Crotti T.N., et al. Snail regulates cell-matrix adhesion by regulation of the expression of integrins and basement membrane proteins. J Biol Chem 2008, 283:23514-23523.
20. Hung J.J., Yang M.H., Hsu H.S., Hsu W.H., Liu J.S., Wu K.J. Prognostic significance of hypoxia-inducible factor-1alpha, TWIST1 and snail expression in resectable non-small cell lung cancer. Thorax 2009, 64:1082-1089.
21. O'Flaherty J.D., Barr M., Fennell D., Richard D., Reynolds J., O'Leary J., et al. The cancer stem-cell hypothesis: its emerging role in lung cancer biology and its relevance for future therapy. J Thorac Oncol 2012, 7:1880-1890.
22. El-Nikhely N., Larzabal L., Seeger W., Calvo A., Savai R. Tumor-stromal interactions in lung cancer: novel candidate targets for therapeutic intervention. Expert Opin Investig Drugs 2012, 21:1107-1122.
23. Ramaswamy S., Ross K.N., Lander E.S., Golub T.R. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003, 33:49-54.
24. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009, 9:239-252.
25. Grivennikov S.I., Karin M. Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 2010, 20:65-71.
26. Wang W., Li Q., Yamada T., Matsumoto K., Matsumoto I., Oda M., et al. Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clin Cancer Res 2009, 15:6630-6638.
27. Cekanova M., Masi T., Plummer H.K., Majidi M., Fedorocko P., Schuller H.M. Pulmonary fibroblasts stimulate the proliferation of cell lines from human lung adenocarcinomas. Anticancer Drugs 2006, 17:771-781.
28. Trimis G., Chatzistamou I., Politi K., Kiaris H., Papavassiliou A.G. Expression of p21waf1/Cip1 in stromal fibroblasts of primary breast tumors. Hum Mol Genet 2008, 17:3596-3600.
29. Chatzistamou I., Dioufa N., Trimis G., Sklavounou A., Kittas C., Kiaris H., et al. P21/waf1 and smooth-muscle actin alpha expression in stromal fibroblasts of oral cancers. Anal Cell Pathol (Amst) 2010, 33:19-26.
30. Bar J., Feniger-Barish R., Lukashchuk N., Shaham H., Moskovits N., Goldfinger N., et al. Cancer cells suppress p53 in adjacent fibroblasts. Oncogene 2009, 28:933-936.
31. Neaud V., Faouzi S., Guirouilh J., Le Bail B., Balabaud C., Bioulac-Sage P., et al. Human hepatic myofibroblasts increase invasiveness of hepatocellular carcinoma cells: evidence for a role of hepatocyte growth factor. Hepatology 1997, 26:1458-1466.
32. Quante M., Tu S.P., Tomita H., Gonda T., Wang S.S., Takashi S., et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19:257-272.
33. Chaudhry S.I., Hooper S., Nye E., Williamson P., Harrington K., Sahai E. Autocrine IL-1beta-TRAF6 signalling promotes squamous cell carcinoma invasion through paracrine TNFalpha signalling to carcinoma-associated fibroblasts. Oncogene 2013, 32:747-758.
34. An J., Enomoto A., Weng L., Kato T., Iwakoshi A., Ushida K., et al. Significance of cancer-associated fibroblasts in the regulation of gene expression in the leading cells of invasive lung cancer. J Cancer Res Clin Oncol 2013, 139:379-388.
35. Wald O., Izhar U., Amir G., Kirshberg S., Shlomai Z., Zamir G., et al. Interaction between neoplastic cells and cancer-associated fibroblasts through the CXCL12/CXCR4 axis: role in non-small cell lung cancer tumor proliferation. J Thorac Cardiovasc Surg 2011, 141:1503-1512.
36. Calvo F., Ege N., Grande-Garcia A., Hooper S., Jenkins R.P., Chaudhry S.I., et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 2013, 15:637-646.
37. Honda E., Yoshida K., Munakata H. Transforming growth factor-beta upregulates the expression of integrin and related proteins in MRC-5 human myofibroblasts. Tohoku J Exp Med 2010, 220:319-327.
38. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230.
39. Lawson M.H., Cummings N.M., Rassl D.M., Vowler S.L., Wickens M., Howat W.J., et al. Bcl-2 and beta1-integrin predict survival in a tissue microarray of small cell lung cancer. Br J Cancer 2010, 103:1710-1715.
40. Kinoshita T., Ishii G., Hiraoka N., Hirayama S., Yamauchi C., Aokage K., et al. Forkhead box P3 regulatory T cells coexisting with cancer associated fibroblasts are correlated with a poor outcome in lung adenocarcinoma. Cancer Sci 2013, 104:409-415.
41. Bergfeld S.A., DeClerck Y.A. Bone marrow-derived mesenchymal stem cells and the tumor microenvironment. Cancer Metastasis Rev 2010, 29:249-261.
42. Son B.R., Marquez-Curtis L.A., Kucia M., Wysoczynski M., Turner A.R., Ratajczak J., et al. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 2006, 24:1254-1264.
43. De Miguel M.P., Fuentes-Julian S., Blazquez-Martinez A., Pascual C.Y., Aller M.A., Arias J., et al. Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr Mol Med 2012, 12:574-591.
44. Noel D., Djouad F., Bouffi C., Mrugala D., Jorgensen C. Multipotent mesenchymal stromal cells and immune tolerance. Leuk Lymphoma 2007, 48:1283-1289.
45. Gottschling S., Granzow M., Kuner R., Jauch A., Herpel E., Xu E.C., et al. Mesenchymal stem cells in non-small cell lung cancer-different from others? Insights from comparative molecular and functional analyses. Lung Cancer 2013, 80:19-29.
46. Liu L., Ge D., Ma L., Mei J., Liu S., Zhang Q., et al. Interleukin-17 and prostaglandin E2 are involved in formation of an M2 macrophage-dominant microenvironment in lung cancer. J Thorac Oncol 2012, 7:1091-1100.
47. Wang R., Zhang J., Chen S., Lu M., Luo X., Yao S., et al. Tumor-associated macrophages provide a suitable microenvironment for non-small lung cancer invasion and progression. Lung Cancer 2011, 74:188-196.
48. Ma J., Liu L., Che G., Yu N., Dai F., You Z. The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer 2010, 10:112.
49. Chow G., Tauler J., Mulshine J.L. Cytokines and growth factors stimulate hyaluronan production: role of hyaluronan in epithelial to mesenchymal-like transition in non-small cell lung cancer. J Biomed Biotechnol 2010, 2010:485468.
50. Wei L., Song X.R., Sun J.J., Wang X.W., Xie L., Lv L.Y. Lysyl oxidase may play a critical role in hypoxia-induced NSCLC cells invasion and migration. Cancer Biother Radiopharm 2012, 27:672-677.
51. Wilgus M.L., Borczuk A.C., Stoopler M., Ginsburg M., Gorenstein L., Sonett J.R., et al. Lysyl oxidase: a lung adenocarcinoma biomarker of invasion and survival. Cancer 2011, 117:2186-2191.
52. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
53. Sauter W., Rosenberger A., Beckmann L., Kropp S., Mittelstrass K., Timofeeva M., et al. Matrix metalloproteinase 1 (MMP1) is associated with early-onset lung cancer. Cancer Epidemiol Biomarkers Prev 2008, 17:1127-1135.
54. Gonzalez-Arriaga P., Pascual T., Garcia-Alvarez A., Fernandez-Somoano A., Lopez-Cima M.F., Tardon A. Genetic polymorphisms in MMP 2, 9 and 3 genes modify lung cancer risk and survival. BMC Cancer 2012, 12:121.
55. Hida Y., Hamada J. Differential expressions of matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs and their endogenous inhibitors among histologic subtypes of lung cancers. Anticancer Agents Med Chem 2012, 12:744-752.
56. Cohen B.H., Diamond E.L., Graves C.G., Kreiss P., Levy D.A., Menkes H.A., et al. A common familial component in lung cancer and chronic obstructive pulmonary disease. Lancet 1977, 2:523-526.
57. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
58. Hernandez L., Magalhaes M.A., Coniglio S.J., Condeelis J.S., Segall J.E. Opposing roles of CXCR4 and CXCR7 in breast cancer metastasis. Breast Cancer Res 2011, 13:R128.
59. Costello C.M., McCullagh B., Howell K., Sands M., Belperio J.A., Keane M.P., et al. A role for the CXCL12 receptor, CXCR7, in the pathogenesis of human pulmonary vascular disease. Eur Respir J 2012, 39:1415-1424.
60. Iwakiri S., Mino N., Takahashi T., Sonobe M., Nagai S., Okubo K., et al. Higher expression of chemokine receptor CXCR7 is linked to early and metastatic recurrence in pathological stage I nonsmall cell lung cancer. Cancer 2009, 115:2580-2593.
61. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 2006, 203:2201-2213.
62. Gridley T. Notch signaling during vascular development. Proc Natl Acad Sci USA 2001, 98:5377-5378.
63. Ye Y.Z., Zhang Z.H., Fan X.Y., Xu X.L., Chen M.L., Chang B.W., et al. Notch3 overexpression associates with poor prognosis in human non-small-cell lung cancer. Med Oncol 2013, 30:595.
64. Riethdorf S., Wikman H., Pantel K. Review: biological relevance of disseminated tumor cells in cancer patients. Int J Cancer 2008, 123:1991-2006.
65. Pantel K., Izbicki J.R., Angstwurm M., Braun S., Passlick B., Karg O., et al. Immunocytological detection of bone marrow micrometastasis in operable non-small cell lung cancer. Cancer Res 1993, 53:1027-1031.
66. Grabinski N., Bartkowiak K., Grupp K., Brandt B., Pantel K., Jucker M. Distinct functional roles of Akt isoforms for proliferation, survival, migration and EGF-mediated signalling in lung cancer derived disseminated tumor cells. Cell Signal 2011, 23:1952-1960.
67. Krebs M.G., Hou J.M., Sloane R., Lancashire L., Priest L., Nonaka D., et al. Analysis of circulating tumor cells in patients with non-small cell lung cancer using epithelial marker-dependent and -independent approaches. J Thorac Oncol 2012, 7:306-315.
68. Wendel M., Bazhenova L., Boshuizen R., Kolatkar A., Honnatti M., Cho E.H., et al. Fluid biopsy for circulating tumor cell identification in patients with early-and late-stage non-small cell lung cancer: a glimpse into lung cancer biology. Phys Biol 2012, 9:016005.
69. Punnoose E.A., Atwal S.K., Spoerke J.M., Savage H., Pandita A., Yeh R.F., et al. Molecular biomarker analyses using circulating tumor cells. PLoS One 2010, 5:e12517.
70. Das M., Riess J.W., Frankel P., Schwartz E., Bennis R., Hsieh H.B., et al. ERCC1 expression in circulating tumor cells (CTCs) using a novel detection platform correlates with progression-free survival (PFS) in patients with metastatic non-small-cell lung cancer (NSCLC) receiving platinum chemotherapy. Lung Cancer 2012, 77:421-426.
71. Kopp H.G., Placke T., Salih H.R. Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res 2009, 69:7775-7783.
72. St Hill C.A. Interactions between endothelial selectins and cancer cells regulate metastasis. Front Biosci 2011, 16:3233-3251.
73. Richter U., Schroder C., Wicklein D., Lange T., Geleff S., Dippel V., et al. Adhesion of small cell lung cancer cells to E- and P-selectin under physiological flow conditions: implications for metastasis formation. Histochem Cell Biol 2011, 135:499-512.
74. Kim Y.N., Koo K.H., Sung J.Y., Yun U.J., Kim H. Anoikis resistance: an essential prerequisite for tumor metastasis. Int J Cell Biol 2012, 2012:306879.
75. Kuang B.H., Wen X.Z., Ding Y., Peng R.Q., Cai P.Q., Zhang M.Q., et al. The prognostic value of platelet endothelial cell adhesion molecule-1 in non-small-cell lung cancer patients. Med Oncol 2013, 30:536.
76. Uekita T., Fujii S., Miyazawa Y., Hashiguchi A., Abe H., Sakamoto M., et al. Suppression of autophagy by CUB domain-containing protein 1 signaling is essential for anchorage-independent survival of lung cancer cells. Cancer Sci 2013.
77. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 1989, 8:98-101.
78. Galaup A., Cazes A., Le Jan S., Philippe J., Connault E., Le Coz E., et al. Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc Natl Acad Sci USA 2006, 103:18721-18726.
79. Lee B.C., Lee T.H., Avraham S., Avraham H.K. Involvement of the chemokine receptor CXCR4 and its ligand stromal cell-derived factor 1alpha in breast cancer cell migration through human brain microvascular endothelial cells. Mol Cancer Res 2004, 2:327-338.
80. Bauer K., Mierke C., Behrens J. Expression profiling reveals genes associated with transendothelial migration of tumor cells: a functional role for alphavbeta3 integrin. Int J Cancer 2007, 121:1910-1918.
81. Ulisse S., Baldini E., Sorrenti S., D'Armiento M. The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets 2009, 9:32-71.
82. Schmitt M., Harbeck N., Thomssen C., Wilhelm O., Magdolen V., Reuning U., et al. Clinical impact of the plasminogen activation system in tumor invasion and metastasis: prognostic relevance and target for therapy. Thromb Haemost 1997, 78:285-296.
83. Madani I., De Neve W., Mareel M. Does ionizing radiation stimulate cancer invasion and metastasis?. Bull Cancer 2008, 95:292-300.
84. Erler J.T., Weaver V.M. Three-dimensional context regulation of metastasis. Clin Exp Metastasis 2009, 26:35-49.
85. Psaila B., Lyden D., Roberts I. Megakaryocytes, malignancy and bone marrow vascular niches. J Thromb Haemost 2012, 10:177-188.
86. Matthews M.J., Kanhouwa S., Pickren J., Robinette D. Frequency of residual and metastatic tumor in patients undergoing curative surgical resection for lung cancer. Cancer Chemother Rep 3 1973, 4:63-67.
87. Quint L.E., Tummala S., Brisson L.J., Francis I.R., Krupnick A.S., Kazerooni E.A., et al. Distribution of distant metastases from newly diagnosed non-small cell lung cancer. Ann Thorac Surg 1996, 62:246-250.
88. Sorensen J.B., Hansen H.H., Hansen M., Dombernowsky P. Brain metastases in adenocarcinoma of the lung: frequency, risk groups, and prognosis. J Clin Oncol 1988, 6:1474-1480.
89. Gavrilovic I.T., Posner J.B. Brain metastases: epidemiology and pathophysiology. J Neurooncol 2005, 75:5-14.
90. Belperio J.A., Phillips R.J., Burdick M.D., Lutz M., Keane M., Strieter R. The SDF-1/CXCL 12/CXCR4 biological axis in non-small cell lung cancer metastases. Chest 2004, 125:156S.
91. Kijima T., Maulik G., Ma P.C., Tibaldi E.V., Turner R.E., Rollins B., et al. Regulation of cellular proliferation, cytoskeletal function, and signal transduction through CXCR4 and c-Kit in small cell lung cancer cells. Cancer Res 2002, 62:6304-6311.
92. Gil M., Seshadri M., Komorowski M.P., Abrams S.I., Kozbor D. Targeting CXCL12/CXCR4 signaling with oncolytic virotherapy disrupts tumor vasculature and inhibits breast cancer metastases. Proc Natl Acad Sci USA 2013, 110:E1291-E1300.
93. Debnath B., Xu S., Grande F., Garofalo A., Neamati N. Small molecule inhibitors of CXCR4. Theranostics 2013, 3:47-75.
94. Nolte S.M., Venugopal C., McFarlane N., Morozova O., Hallett R.M., O'Farrell E., et al. A cancer stem cell model for studying brain metastases from primary lung cancer. J Natl Cancer Inst 2013, 107:1801-1811.
95. Castellvi J., Garcia A., Rojo F., Ruiz-Marcellan C., Gil A., Baselga J., et al. Phosphorylated 4E binding protein 1: a hallmark of cell signaling that correlates with survival in ovarian cancer. Cancer 2006, 107:1801-1811.
96. Rojo F., Najera L., Lirola J., Jimenez J., Guzman M., Sabadell M.D., et al. 4E-binding protein 1, a cell signaling hallmark in breast cancer that correlates with pathologic grade and prognosis. Clin Cancer Res 2007, 13:81-89.
97. Improta G., Zupa A., Fillmore H., Deng J., Aieta M., Musto P., et al. Protein pathway activation mapping of brain metastasis from lung and breast cancers reveals organ type specific drug target activation. J Proteome Res 2011, 10:3089-3097.
98. Tsuya A., Kurata T., Tamura K., Fukuoka M. Skeletal metastases in non-small cell lung cancer: a retrospective study. Lung Cancer 2007, 57:229-232.
99. Sekine I., Nokihara H., Yamamoto N., Kunitoh H., Ohe Y., Tamura T. Risk factors for skeletal-related events in patients with non-small cell lung cancer treated by chemotherapy. Lung Cancer 2009, 65:219-222.
100. Peng X., Guo W., Ren T., Lou X., Zhang S., Lu Q., et al. Differential regulation of the RANKL/RANK/OPG system is associated with bone metastasis in human non-small cell lung cancer. PLoS One 2013, 8(3):e58361.
101. Peters S., Meylan E. Targeting receptor activator of nuclear factor-kappa B as a new therapy for bone metastasis in non-small cell lung cancer. Curr Opin Oncol 2013, 25:137-144.
102. Zhu C.Q., Ding K., Strumpf D., Weir B.A., Meyerson M., Pennell N., et al. Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small-cell lung cancer. J Clin Oncol 2010, 28:4417-4424.
103. Hai J., Zhu C.Q., Bandarchi B., Wang Y.H., Navab R., Shepherd F.A., et al. L1 cell adhesion molecule promotes tumorigenicity and metastatic potential in non-small cell lung cancer. Clin Cancer Res 2012, 18:1914-1924.
104. Salvatierra A., Baamonde C., Llamas J.M., Cruz F., Lopez-Pujol J. Extrathoracic staging of bronchogenic carcinoma. Chest 1990, 97:1052-1058.
105. Brodt P., Fallavollita L., Khatib A.M., Samani A.A., Zhang D. Cooperative regulation of the invasive and metastatic phenotypes by different domains of the type I insulin-like growth factor receptor beta subunit. J Biol Chem 2001, 276:33608-33615.
106. Burnier J.V., Wang N., Michel R.P., Hassanain M., Li S., Lu Y., et al. Type IV collagen-initiated signals provide survival and growth cues required for liver metastasis. Oncogene 2011, 30:3766-3783.
107. Yoshimura K., Meckel K.F., Laird L.S., Chia C.Y., Park J.J., Olino K.L., et al. Integrin alpha2 mediates selective metastasis to the liver. Cancer Res 2009, 69:7320-7328.
108. Sato S., Hanibuchi M., Kuramoto T., Yamamori N., Goto H., Ogawa H., et al. Macrophage stimulating protein promotes liver metastases of small cell lung cancer cells by affecting the organ microenvironment. Clin Exp Metastasis 2013, 30:333-344.
109. Abrams H.L., Spiro R., Goldstein N. Metastases in carcinoma; analysis of 1000 autopsied cases. Cancer 1950, 3:74-85.
110. Mercier O., Fadel E., de Perrot M., Mussot S., Stella F., Chapelier A., et al. Surgical treatment of solitary adrenal metastasis from non-small cell lung cancer. J Thorac Cardiovasc Surg 2005, 130:136-140.
111. Meyer K.K. Direct lymphatic connections from the lower lobes of the lung to the abdomen. J Thorac Surg 1958, 35:726-733.
112. Raynaud C.M., Mercier O., Dartevelle P., Commo F., Olaussen K.A., de Montpreville V., et al. Expression of chemokine receptor CCR6 as a molecular determinant of adrenal metastatic relapse in patients with primary lung cancer. Clin Lung Cancer 2010, 11:187-191.
113. Starner T.D., Barker C.K., Jia H.P., Kang Y., McCray P.B. CCL20 is an inducible product of human airway epithelia with innate immune properties. Am J Respir Cell Mol Biol 2003, 29:627-633.
114. Bozzetti C., Tiseo M., Lagrasta C., Nizzoli R., Guazzi A., Leonardi F., et al. Comparison between epidermal growth factor receptor (EGFR) gene expression in primary non-small cell lung cancer (NSCLC) and in fine-needle aspirates from distant metastatic sites. J Thorac Oncol 2008, 3:18-22.
115. Raynaud C.M., Mercier O., Commo F., Dartevelle P., Gomez-Roca C., de Montpreville V., et al. Telomere length, telomeric proteins and DNA damage repair proteins are differentially expressed between primary lung tumors and their adrenal metastases. Lung Cancer 2009, 65:144-149.
116. Steeg P.S. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006, 12:895-904.
117. Ettinger D.S., Akerley W., Bepler G., Blum M.G., Chang A., Cheney R.T., et al. Non-small cell lung cancer. J Natl Compr Canc Netw 2010, 8:740-801.
118. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15:220-231.
119. Azam F., Mehta S., Harris A.L. Mechanisms of resistance to antiangiogenesis therapy. Eur J Cancer 2010, 46:1323-1332.
120. Weilbaecher K.N., Guise T.A., McCauley L.K. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011, 11:411-425.
121. Bartolotti M., Franceschi E., Brandes A.A. EGF receptor tyrosine kinase inhibitors in the treatment of brain metastases from non-small-cell lung cancer. Expert Rev Anticancer Ther 2012, 12:1429-1435.
122. Porta R., Sanchez-Torres J.M., Paz-Ares L., Massuti B., Reguart N., Mayo C., et al. Brain metastases from lung cancer responding to erlotinib: the importance of EGFR mutation. Eur Respir J 2011, 37:624-631.
123. Sandler A., Gray R., Perry M.C., Brahmer J., Schiller J.H., Dowlati A., et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006, 355:2542-2550.
124. Jubb A.M., Cesario A., Ferguson M., Congedo M.T., Gatter K.C., Lococo F., et al. Vascular phenotypes in primary non-small cell lung carcinomas and matched brain metastases. Br J Cancer 2011, 104:1877-1881.
125. Socinski M.A., Langer C.J., Huang J.E., Kolb M.M., Compton P., Wang L., et al. Safety of bevacizumab in patients with non-small-cell lung cancer and brain metastases. J Clin Oncol 2009, 27:5255-5261.
126. Mehlen P., Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006, 6:449-458.
127. Schiller J.H., Harrington D., Belani C.P., Langer C., Sandler A., Krook J., et al. Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 2002, 346:92-98.