The role of the cell-cell interactions in cancer progression

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 2, 2015, Pages 283-296

  Kamińska, Katarzyna ^a   Szczylik, Cezary ^a   Bielecka, Zofia F ^a,b   Bartnik, Ewa ^c,d   Porta, Camillo ^e   Lian, Fei ^f   Czarnecka, Anna M ^a  

^a MILITARY INSTITUTE OF MEDICINE   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c UNIVERSITY OF WARSAW   (Poland)

^d INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^e FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Cell cell interactions; Stromal cells; Tumour microenvironment

Indexed keywords

ANIMAL; CARCINOGENESIS; CELL COMMUNICATION; DISEASE COURSE; HUMAN; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; CARCINOGENESIS; CELL COMMUNICATION; DISEASE PROGRESSION; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84921671766     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12408     Document Type: Article

References (144)

1. Dennis JE, Charbord P. Origin and differentiation of human and murine stroma. Stem Cells. 2002; 20: 205-14.
2. Bremnes RM, Donnem T, Al-Saad S, et al. The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. Journal of thoracic oncology: official publication of the International Association for the Study of Lung Cancer. 2011; 6: 209-17.
3. Paget SFRCS. The distribution of secondary growths in cancer of the breast. Lancet. 1889; 133: 2.
4. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer. 2001; 1: 46-54.
5. Wiseman BS, Sternlicht MD, Lund LR, et al. Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol. 2003; 162: 1123-33.
6. Bissell MJ, Labarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell. 2005; 7: 17-23.
7. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol. 2012; 196: 395-406.
8. Spano D, Zollo M. Tumor microenvironment: a main actor in the metastasis process. Clin Exp Metastasis. 2012; 29: 381-95.
9. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012; 21: 309-22.
10. Hu M, Polyak K. Molecular characterisation of the tumour microenvironment in breast cancer. Eur J Cancer. 2008; 44: 2760-5.
11. Lin HJ, Zuo T, Lin CH, et al. Breast cancer-associated fibroblasts confer AKT1-mediated epigenetic silencing of Cystatin M in epithelial cells. Cancer Res. 2008; 68: 10257-66.
12. Jern P, Coffin JM. Effects of retroviruses on host genome function. Annu Rev Genet. 2008; 42: 709-32.
13. Anand P, Kunnumakkara AB, Sundaram C, et al. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res. 2008; 25: 2097-116.
14. Rowley DR. What might a stromal response mean to prostate cancer progression? Cancer Metastasis Rev. 1998; 17: 411-9.
15. Tuxhorn JA, Ayala GE, Smith MJ, et al. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res. 2002; 8: 2912-23.
16. Schmitt-Graff A, Desmouliere A, Gabbiani G. Heterogeneity of myofibroblast phenotypic features: an example of fibroblastic cell plasticity. Virchows Arch. 1994; 425: 3-24.
17. Gonda TA, Varro A, Wang TC, et al. Molecular biology of cancer-associated fibroblasts: can these cells be targeted in anti-cancer therapy? Semin Cell Dev Biol. 2010; 21: 2-10.
18. Desmouliere A, Guyot C, Gabbiani G. The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol. 2004; 48: 509-17.
19. Liao D, Luo Y, Markowitz D, et al. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS ONE. 2009; 4: e7965.
20. Orimo A, Gupta PB, Sgroi DC, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005; 121: 335-48.
21. Li H, Fan X, Houghton J. Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem. 2007; 101: 805-15.
22. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-74.
23. Trimboli AJ, Cantemir-Stone CZ, Li F, et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature. 2009; 461: 1084-91.
24. Bronisz A, Godlewski J, Wallace JA, et al. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol. 2012; 14: 159-67.
25. Flaberg E, Markasz L, Petranyi G, et al. High-throughput live-cell imaging reveals differential inhibition of tumor cell proliferation by human fibroblasts. Int J Cancer. 2011; 128: 2793-802.
26. Dor Y, Porat R, Keshet E. Vascular endothelial growth factor and vascular adjustments to perturbations in oxygen homeostasis. Am J Physiol Cell Physiol. 2001; 280: C1367-74.
27. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996; 86: 353-64.
28. Crawford Y, Kasman I, Yu L, et al. PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell. 2009; 15: 21-34.
29. Koshida Y, Kuranami M, Watanabe M. Interaction between stromal fibroblasts and colorectal cancer cells in the expression of vascular endothelial growth factor. J Surg Res. 2006; 134: 270-7.
30. Ohta Y, Shridhar V, Bright RK, et al. VEGF and VEGF type C play an important role in angiogenesis and lymphangiogenesis in human malignant mesothelioma tumours. Br J Cancer. 1999; 81: 54-61.
31. Biselli-Chicote PM, Oliveira AR, Pavarino EC, et al. VEGF gene alternative splicing: pro- and anti-angiogenic isoforms in cancer. J Cancer Res Clin Oncol. 2012; 138: 363-70.
32. Dong J, Grunstein J, Tejada M, et al. VEGF-null cells require PDGFR alpha signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J. 2004; 23: 2800-10.
33. Cristofanilli M, Charnsangavej C, Hortobagyi GN. Angiogenesis modulation in cancer research: novel clinical approaches. Nat Rev Drug Discov. 2002; 1: 415-26.
34. Li X, Tjwa M, Moons L, et al. Revascularization of ischemic tissues by PDGF-CC via effects on endothelial cells and their progenitors. J Clin Investig. 2005; 115: 118-27.
35. Buczek M, Escudier B, Bartnik E, et al. Resistance to tyrosine kinase inhibitors in clear cell renal cell carcinoma: from the patient's bed to molecular mechanisms. Biochim Biophys Acta. 2014; 1845: 31-41.
36. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006; 6: 392-401.
37. Bierie B, Moses HL. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer. 2006; 6: 506-20.
38. Yasushi Shintani AA, Toru K, Tomoyuki N, et al. Cancer-associated fibroblasts induce epithelial-mesenchymal-transition and stemness in non-small-cell lung cancer AACR 103rd Annual Meeting 2012- Mar 31-Apr 4, 2012. Chicago, IL: Cancer Research; 2012.
39. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002; 2: 442-54.
40. Hammers HJ, Verheul HM, Salumbides B, et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol Cancer Ther. 2010; 9: 1525-35.
41. Singer II, Kawka DW, Kazazis DM, et al. In vivo co-distribution of fibronectin and actin fibers in granulation tissue: immunofluorescence and electron microscope studies of the fibronexus at the myofibroblast surface. J Cell Biol. 1984; 98: 2091-106.
42. Ronnov-Jessen L, Petersen OW. Induction of alpha-smooth muscle actin by transforming growth factor-beta 1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab Invest. 1993; 68: 696-707.
43. Desmouliere A, Geinoz A, Gabbiani F, et al. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol. 1993; 122: 103-11.
44. Takeuchi Y, Kodama Y, Matsumoto T. Bone matrix decorin binds transforming growth factor-beta and enhances its bioactivity. J Biol Chem. 1994; 269: 32634-8.
45. Karagiannis GS, Poutahidis T, Erdman SE, et al. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res: MCR, 2012.
46. Giannoni E, Taddei ML, Parri M, et al. EphA2-mediated mesenchymal-amoeboid transition induced by endothelial progenitor cells enhances metastatic spread due to cancer-associated fibroblasts. J Mol Med (Berl). 2013; 91(1): 103-15.
47. O'Connell JT, Sugimoto H, Cooke VG, et al. VEGF-A and Tenascin-C produced by S100A4+ stromal cells are important for metastatic colonization. Proc Natl Acad Sci USA. 2011; 108: 16002-7.
48. McAllister SS, Gifford AM, Greiner AL, et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell. 2008; 133: 994-1005.
49. Peinado H, Lavotshkin S, Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol. 2011; 21: 139-46.
50. Oskarsson T, Massague J. Extracellular matrix players in metastatic niches. EMBO J. 2012; 31: 254-6.
51. Duda DG, Duyverman AM, Kohno M, et al. Malignant cells facilitate lung metastasis by bringing their own soil. Proc Natl Acad Sci USA. 2010; 107: 21677-82.
52. Quante M, Tu SP, Tomita H, et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell. 2011; 19: 257-72.
53. Zhu Y, Zhu M, Lance P. Stromal COX-2 signaling activated by deoxycholic acid mediates proliferation and invasiveness of colorectal epithelial cancer cells. Biochem Biophys Res Commun. 2012; 425: 607-12.
54. Zhu Y, Zhu M, Lance P. IL1beta-mediated Stromal COX-2 signaling mediates proliferation and invasiveness of colonic epithelial cancer cells. Exp Cell Res. 2012; 318: 2520-30.
55. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood. 2006; 107: 1761-7.
56. Erez N, Truitt M, Olson P, et al. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell. 2010; 17: 135-47.
57. Nazareth MR, Broderick L, Simpson-Abelson MR, et al. Characterization of human lung tumor-associated fibroblasts and their ability to modulate the activation of tumor-associated T cells. J Immunol. 2007; 178: 5552-62.
58. Grum-Schwensen B, Klingelhofer J, Grigorian M, et al. Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors. Cancer Res. 2010; 70: 936-47.
59. De Monte L, Reni M, Tassi E, et al. Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med. 2011; 208: 469-78.
60. Tan W, Zhang W, Strasner A, et al. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature. 2011; 470: 548-53.
61. Wong VW, Rustad KC, Akaishi S, et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med. 2012; 18: 148-52.
62. Chao YH, Tsuang YH, Sun JS, et al. Centrifugal force induces human ligamentum flavum fibroblasts inflammation through activation of JNK and p38 pathways. Connect Tissue Res. 2012; 53: 422-9.
63. Kook SH, Jang YS, Lee JC. Involvement of JNK-AP-1 and ERK-NF-kappaB signaling in tension-stimulated expression of type I collagen and MMP-1 in human periodontal ligament fibroblasts. J Appl Physiol. 2011; 111: 1575-83.
64. Fisher CJ Jr, Slotman GJ, Opal SM, et al. Initial evaluation of human recombinant interleukin-1 receptor antagonist in the treatment of sepsis syndrome: a randomized, open-label, placebo-controlled multicenter trial. Crit Care Med. 1994; 22: 12-21.
65. Smedsrod B, Le Couteur D, Ikejima K, et al. Hepatic sinusoidal cells in health and disease: update from the 14th International Symposium. Liver Int. 2009; 29: 490-501.
66. Torres-Rosado A, O'Shea KS, Tsuji A, et al. Hepsin, a putative cell-surface serine protease, is required for mammalian cell growth. Proc Natl Acad Sci USA. 1993; 90: 7181-5.
67. Xing P, Li JG, Jin F, et al. Clinical and biological significance of hepsin overexpression in breast cancer. J Investig Med. 2011; 59: 803-10.
68. Lei K. Hepsin is down-regulated in gastric cancer and predicts a poor prognosis. Chin J Gastroenterol. 2012; 17: 592-8.
69. Hsu YC, Huang HP, Yu IS, et al. Serine protease hepsin regulates hepatocyte size and hemodynamic retention of tumor cells via hepatocyte growth factor signaling. Hepatology. 2012; 56(5): 1913-23.
70. Morrissey C, True LD, Roudier MP, et al. Differential expression of angiogenesis associated genes in prostate cancer bone, liver and lymph node metastases. Clin Exp Metastasis. 2008; 25: 377-88.
71. Klezovitch O, Chevillet J, Mirosevich J, et al. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell. 2004; 6: 185-95.
72. Tabaries S, Dong Z, Annis MG, et al. Claudin-2 is selectively enriched in and promotes the formation of breast cancer liver metastases through engagement of integrin complexes. Oncogene. 2011; 30: 1318-28.
73. Tabaries S, Dupuy F, Dong ZF, et al. Claudin-2 promotes breast cancer liver metastasis by facilitating tumor cell interactions with hepatocytes. Mol Cell Biol. 2012; 32: 2979-91.
74. Muto S, Hata M, Taniguchi J, et al. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA. 2010; 107: 8011-6.
75. Rosenthal R, Milatz S, Krug SM, et al. Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci. 2010; 123: 1913-21.
76. Min BS, Kim NK, Jeong HC, et al. High levels of serum VEGF and TIMP-1 are correlated with colon cancer liver metastasis and intrahepatic recurrence after liver resection. Oncol Lett. 2012; 4: 123-30.
77. Tanindi A, Sahinarslan A, Elbeg S, et al. Relationship between MMP-1, MMP-9, TIMP-1, IL-6 and risk factors, clinical presentation, extent and severity of atherosclerotic coronary artery disease. Open Cardiovasc Med J. 2011; 5: 110-6.
78. Kapsoritakis AN, Kapsoritaki AI, Davidi IP, et al. Imbalance of tissue inhibitors of metalloproteinases (TIMP) - 1 and - 4 serum levels, in patients with inflammatory bowel disease. BMC Gastroenterol. 2008; 8: 55.
79. Dannewitz B, Edrich C, Tomakidi P, et al. Elevated gene expression of MMP-1, MMP-10, and TIMP-1 reveal changes of molecules involved in turn-over of extracellular matrix in cyclosporine-induced gingival overgrowth. Cell Tissue Res. 2006; 325: 513-22.
80. Boeker KH, Haberkorn CI, Michels D, et al. Diagnostic potential of circulating TIMP-1 and MMP-2 as markers of liver fibrosis in patients with chronic hepatitis C. Clin Chim Acta. 2002; 316: 71-81.
81. Sayagues JM, Fontanillo C, Abad MD, et al. Mapping of genetic abnormalities of primary tumours from metastatic CRC by high-resolution SNP arrays. PLoS ONE. 2010; 5: e13752.
82. Munoz-Bellvis L, Fontanillo C, Gonzalez-Gonzalez M, et al. Unique genetic profile of sporadic colorectal cancer liver metastasis versus primary tumors as defined by high-density single-nucleotide polymorphism arrays. Modern Pathol. 2012; 25: 590-601.
83. Mironchik Y, Winnard PT Jr, Vesuna F, et al. Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res. 2005; 65: 10801-9.
84. Malfettone A, Silvestris N, Paradiso A, et al. Overexpression of nuclear NHERF1 in advanced colorectal cancer: association with hypoxic microenvironment and tumor invasive phenotype. Exp Mol Pathol. 2012; 92: 296-303.
85. Wu Y, Brodt P, Sun H, et al. Insulin-like growth factor-I regulates the liver microenvironment in obese mice and promotes liver metastasis. Cancer Res. 2010; 70: 57-67.
86. Boelens MC, van den Berg A, Vogelzang I, et al. Differential expression and distribution of epithelial adhesion molecules in non-small cell lung cancer and normal bronchus. J Clin Pathol. 2007; 60: 608-14.
87. Janik P, Assaf A, Bertram JS. Inhibition of growth of primary and metastatic Lewis lung carcinoma cells by the phosphodiesterase inhibitor isobutylmethylxanthine. Cancer Res. 1980; 40: 1950-4.
88. Terzaghi-Howe M. Inhibition of carcinogen-altered rat tracheal epithelial cell proliferation by normal epithelial cells in vivo. Carcinogenesis. 1987; 8: 145-50.
89. Albright CD, Jones RT, Grimley PM, et al. Intercellular communication in bronchial epithelial cells: review of evidence for a possible role in lung carcinogenesis. Toxicol Pathol. 1990; 18: 324-41.
90. Stahlman MT, Orth DN, Gray ME. Immunocytochemical localization of epidermal growth factor in the developing human respiratory system and in acute and chronic lung disease in the neonate. Lab Invest. 1989; 60: 539-47.
91. Tabassian AR, Nylen ES, Linnoila RI, et al. Stimulation of hamster pulmonary neuroendocrine cells and associated peptides by repeated exposure to cigarette smoke. Am Rev Respir Dis. 1989; 140: 436-40.
92. Yamauchi K, Martinet Y, Basset P, et al. High levels of transforming growth factor-beta are present in the epithelial lining fluid of the normal human lower respiratory tract. Am Rev Respir Dis. 1988; 137: 1360-3.
93. Nylen ES, Linnoila RI, Becker KL. Prenatal cholinergic stimulation of pulmonary neuroendocrine cells by nicotine. Acta Physiol Scand. 1988; 132: 117-8.
94. Han G, Wang XJ. Roles of TGFbeta signaling Smads in squamous cell carcinoma. Cell Biosci. 2011; 1: 41.
95. Maldonado PE, Rose B, Loewenstein WR. Growth factors modulate junctional cell-to-cell communication. J Membr Biol. 1988; 106: 203-10.
96. Wong ST, Winchell LF, McCune BK, et al. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell. 1989; 56: 495-506.
97. Mennerich D, Vogel A, Klaman I, et al. Shift of syndecan-1 expression from epithelial to stromal cells during progression of solid tumours. Eur J Cancer. 2004; 40: 1373-82.
98. Petersen OW, Nielsen HL, Gudjonsson T, et al. Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma. Am J Pathol. 2003; 162: 391-402.
99. Rilla K, Pasonen-Seppanen S, Karna R, et al. HAS3-induced accumulation of hyaluronan in 3D MDCK cultures results in mitotic spindle misorientation and disturbed organization of epithelium. Histochem Cell Biol. 2012; 137: 153-64.
100. Bose N, Masellis AM. Secretory products of breast cancer cells upregulate hyaluronan production in a human osteoblast cell line. Clin Exp Metastasis. 2005; 22: 629-42.
101. Twarock S, Rock K, Sarbia M, et al. Synthesis of hyaluronan in oesophageal cancer cells is uncoupled from the prostaglandin-cAMP pathway. Br J Pharmacol. 2009; 157: 234-43.
102. Pistone Creydt V, Fletcher SJ, Giudice J, et al. Human adipose tissue from normal and tumoral breast regulates the behavior of mammary epithelial cells. Clin Transl Oncol. 2013; 15: 124-31.
103. Giron-Michel J, Azzi S, Khawam K, et al. Interleukin-15 is a major regulator of the cell-microenvironment interactions in human renal cancer. Bull Cancer. 2011; 98: 32-9.
104. Spink BC, Cole RW, Katz BH, et al. Inhibition of MCF-7 breast cancer cell proliferation by MCF-10A breast epithelial cells in coculture. Cell Biol Int. 2006; 30: 227-38.
105. Sen M, Chamorro M, Reifert J, et al. Blockade of Wnt-5A/frizzled 5 signaling inhibits rheumatoid synoviocyte activation. Arthritis Rheum. 2001; 44: 772-81.
106. Kaler P, Augenlicht L, Klampfer L. Activating mutations in beta-catenin in colon cancer cells alter their interaction with macrophages; the role of snail. PLoS ONE. 2012; 7: e45462.
107. Kaler P, Godasi BN, Augenlicht L, et al. The NF-kappaB/AKT-dependent induction of Wnt signaling in colon cancer cells by macrophages and IL-1beta. Cancer Microenviron. 2009; 2: 69-80.
108. Kaler P, Galea V, Augenlicht L, et al. Tumor associated macrophages protect colon cancer cells from TRAIL-induced apoptosis through IL-1beta-dependent stabilization of Snail in tumor cells. PLoS ONE. 2010; 5: e11700.
109. Sasahira T, Sasaki T, Kuniyasu H. Interleukin-15 and transforming growth factor alpha are associated with depletion of tumor-associated macrophages in colon cancer. J Exp Clin Cancer Res. 2005; 24: 69-74.
110. Du Q, Park KS, Guo Z, et al. Regulation of human nitric oxide synthase 2 expression by Wnt beta-catenin signaling. Cancer Res. 2006; 66: 7024-31.
111. Wouda RR, Bansraj MR, de Jong AW, et al. Src family kinases are required for WNT5 signaling through the Derailed/RYK receptor in the Drosophila embryonic central nervous system. Development. 2008; 135: 2277-87.
112. Page TH, Smolinska M, Gillespie J, et al. Tyrosine kinases and inflammatory signalling. Curr Mol Med. 2009; 9: 69-85.
113. Kostourou V, Cartwright JE, Johnstone AP, et al. The role of tumour-derived iNOS in tumour progression and angiogenesis. Br J Cancer. 2011; 104: 83-90.
114. Tyryshkin A, Gorgun FM, Abdel Fattah E, et al. Src kinase-mediated phosphorylation stabilizes inducible nitric-oxide synthase in normal cells and cancer cells. J Biol Chem. 2010; 285: 784-92.
115. Yanagita M, Shimabukuro Y, Nozaki T, et al. IL-15 up-regulates iNOS expression and NO production by gingival epithelial cells. Biochem Biophys Res Commun. 2002; 297: 329-34.
116. Li Q, Wang W, Yamada T, et al. Pleural mesothelioma instigates tumor-associated fibroblasts to promote progression via a malignant cytokine network. Am J Pathol. 2011; 179: 1483-93.
117. Davidson B, Konstantinovsky S, Nielsen S, et al. Altered expression of metastasis-associated and regulatory molecules in effusions from breast cancer patients: a novel model for tumor progression. Clin Cancer Res. 2004; 10: 7335-46.
118. Long H, Zhou B, Jiang FG. Expression of MMP-2 and MMP-9 in retinoblastoma and their significance. Int J Ophthalmol. 2011; 4: 489-91.
119. Sundov Z, Tomic S, Vilovic K, et al. Immunohistochemically detected high expression of matrix metalloproteinase-2 as predictor of poor prognosis in Duke's B colon cancer. Croat Med J. 2008; 49: 636-42.
120. Vasku A, Vasku JB, Necas M, et al. Matrix metalloproteinase-2 promoter genotype as a marker of cutaneous T-cell lymphoma early stage. J Biomed Biotechnol. 2010; 2010: 805907.
121. Rajoria S, Suriano R, George A, et al. Estrogen induced metastatic modulators MMP-2 and MMP-9 are targets of 3, 3′-diindolylmethane in thyroid cancer. PLoS ONE. 2011; 6: e15879.
122. Rojiani MV, Alidina J, Esposito N, et al. Expression of MMP-2 correlates with increased angiogenesis in CNS metastasis of lung carcinoma. Int J Clin Exp Pathol. 2010; 3: 775-81.
123. Du R, Petritsch C, Lu K, et al. Matrix metalloproteinase-2 regulates vascular patterning and growth affecting tumor cell survival and invasion in GBM. Neuro Oncol. 2008; 10: 254-64.
124. Wang LB, Jiang ZN, Fan MY, et al. Changes of histology and expression of MMP-2 and nm23-H1 in primary and metastatic gastric cancer. World J Gastroenterol. 2008; 14: 1612-6.
125. Zhang HY, Zheng XZ, Wang XH, et al. S100A4 mediated cell invasion and metastasis of esophageal squamous cell carcinoma via the regulation of MMP-2 and E-cadherin activity. Mol Biol Rep. 2012; 39: 199-208.
126. Bai FH, Wang NJ, Wang J, et al. Screening and identification of peritoneal metastasis-related genes of gastric adenocarcinoma using a cDNA microarray. Genet Mol Res. 2012; 11: 1682-9.
127. Lee CI, Hsu MY, Chou CH, et al. CTNNB1 (beta-catenin) mutation is rare in brain tumours but involved as a sporadic event in a brain metastasis. Acta Neurochir. 2009; 151: 1107-11.
128. Economidou F, Antoniou KM, Soufla G, et al. Role of VEGF-stromal cell-derived factor-1alpha/CXCL12 axis in pleural effusion of lung cancer. J Recept Signal Transduct Res. 2010; 30: 154-60.
129. Burger JA, Stewart DJ. CXCR4 chemokine receptor antagonists: perspectives in SCLC. Expert Opin Investig Drugs. 2009; 18: 481-90.
130. Kijima T, Maulik G, Ma PC, 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: 6304-11.
131. Lau BW, Kane AB. SDF1/CXCL12 is involved in recruitment of stem-like progenitor cells to orthotopic murine malignant mesothelioma spheroids. Anticancer Res. 2010; 30: 2153-60.
132. Lin CC, Chen LC, Tseng VS, et al. Malignant pleural effusion cells show aberrant glucose metabolism gene expression. Eur Respir J. 2011; 37: 1453-65.
133. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004; 4: 891-9.
134. Cakir E, Yilmaz A, Demirag F, et al. Prognostic significance of micropapillary pattern in lung adenocarcinoma and expression of apoptosis-related markers: caspase-3, bcl-2, and p53. APMIS. 2011; 119: 574-80.
135. Rolny C, Capparuccia L, Casazza A, et al. The tumor suppressor semaphorin 3B triggers a prometastatic program mediated by interleukin 8 and the tumor microenvironment. J Exp Med. 2008; 205: 1155-71.
136. Kubo F, Ueno S, Hiwatashi K, et al. Interleukin 8 in human hepatocellular carcinoma correlates with cancer cell invasion of vessels but not with tumor angiogenesis. Ann Surg Oncol. 2005; 12: 800-7.
137. Padua D, Zhang XH, Wang Q, et al. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell. 2008; 133: 66-77.
138. Minn AJ, Gupta GP, Siegel PM, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005; 436: 518-24.
139. Gupta GP, Nguyen DX, Chiang AC, et al. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature. 2007; 446: 765-70.
140. Gupta GP, Perk J, Acharyya S, et al. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc Natl Acad Sci USA. 2007; 104: 19506-11.
141. Landemaine T, Jackson A, Bellahcene A, et al. A six-gene signature predicting breast cancer lung metastasis. Cancer Res. 2008; 68: 6092-9.
142. Gerber SA, Rybalko VY, Bigelow CE, et al. Preferential attachment of peritoneal tumor metastases to omental immune aggregates and possible role of a unique vascular microenvironment in metastatic survival and growth. Am J Pathol. 2006; 169: 1739-52.
143. Fonsatti E, Maio M. Highlights on endoglin (CD105): from basic findings towards clinical applications in human cancer. J Transl Med. 2004; 2: 18.
144. Samoszuk M, Tan J, Chorn G. Clonogenic growth of human breast cancer cells co-cultured in direct contact with serum-activated fibroblasts. Breast Cancer Res. 2005; 7: R274-83.