Guidance molecules in lung cancer

Cell Adhesion and Migration

Volumn 4, Issue 1, 2010, Pages 130-145

  Nasarre, Patrick ^a   Potiron, Vincent ^a   Drabkin, Harry ^a   Roche, Joëlle ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITÉ DE POITIERS   (France)

Author keywords

DCC; Ephrin; Lung cancer; Netrin; Neuropilin; Notch; Robo; Semaphorin; Slit; UNC5

Indexed keywords

CASPASE 3; CELL CYCLE PROTEIN; EPHRIN; EPHRIN RECEPTOR; NETRIN; NOTCH RECEPTOR; PLEXIN; SEMAPHORIN; SLIT PROTEIN;

CELL MIGRATION; CELL STRUCTURE; GENE EXPRESSION; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; LUNG DEVELOPMENT; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION;

EID: 77449122270     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.4.1.10882     Document Type: Review

References (166)

1. Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science 1996; 274:1123-33.
2. Hinck L. The versatile roles of "axon guidance" cues in tissue morphogenesis. Dev Cell 2004; 7:783-93.
3. Suchting S, Bicknell R, Eichmann A. Neuronal clues to vascular guidance. Exp Cell Res 2006; 312:668-75.
4. Chedotal A, Kerjan G, Moreau-Fauvarque C. The brain within the tumor: new roles for axon guidance molecules in cancers. Cell Death Differ 2005; 12:1044-56.
5. Klagsbrun M, Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 2005; 16:535-48.
6. Potiron VA, Roche J, Drabkin HA. Semaphorins and their receptors in lung cancer. Cancer Lett 2009; 273:1-14.
7. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998; 92:735-45.
8. Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol 1999; 146:233-42.
9. Favier B, Alam A, Barron P, Bonnin J, Laboudie P, Fons P, et al. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 2006; 108:1243-50.
10. Karpanen T, Heckman CA, Keskitalo S, Jeltsch M, Ollila H, Neufeld G, et al. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. Faseb J 2006; 20:1462-72.
11. Uniewicz KA, Fernig DG. Neuropilins: a versatile partner of extracellular molecules that regulate development and disease. Front Biosci 2008; 13:4339-60.
12. Kruger RP, Aurandt J, Guan KL. Semaphorins command cells to move. Nat Rev Mol Cell Biol 2005; 6:789-800.
13. Swiercz JM, Worzfeld T, Offermanns S. ErbB-2 and met reciprocally regulate cellular signaling via plexin-B1. J Biol Chem 2008; 283:1893-901.
14. Puschel AW. GTPases in semaphorin signaling. Adv Exp Med Biol 2007; 600:12-23.
15. Klostermann A, Lutz B, Gertler F, Behl C. The orthologous human and murine semaphorin 6A-1 proteins (SEMA6A-1/Sema6A-1) bind to the enabled/vasodilator-stimulated phosphoprotein-like protein (EVL) via a novel carboxyl-terminal zyxin-like domain. J Biol Chem 2000; 275:39647-53.
16. Toyofuku T, Zhang H, Kumanogoh A, Takegahara N, Yabuki M, Harada K, et al. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat Cell Biol 2004; 6:1204-11.
17. Surawska H, Ma PC, Salgia R. The role of ephrins and Eph receptors in cancer. Cytokine Growth Factor Rev 2004; 15:419-33.
18. Zhang J, Hughes S. Role of the ephrin and Eph receptor tyrosine kinase families in angiogenesis and development of the cardiovascular system. J Pathol 2006; 208:453-61.
19. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008; 133:38-52.
20. Arvanitis D, Davy A. Eph/ephrin signaling: networks. Genes Dev 2008; 22:416-29.
21. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999; 97:927-41.
22. Arakawa H. Netrin-1 and its receptors in tumorigenesis. Nat Rev Cancer 2004; 4:978-87.
23. Bernet A, Fitamant J. Netrin-1 and its receptors in tumour growth promotion. Expert Opin Ther Targets 2008; 12:995-1007.
24. Nikolopoulos SN, Giancotti FG. Netrin-integrin signaling in epithelial morphogenesis, axon guidance and vascular patterning. Cell Cycle 2005; 4:131-5.
25. Yebra M, Montgomery AM, Diaferia GR, Kaido T, Silletti S, Perez B, et al. Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev Cell 2003; 5:695-707.
26. Hagedorn EJ, Yashiro H, Ziel JW, Ihara S, Wang Z, Sherwood DR. Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. Dev Cell 2009; 17:187-98.
27. Mehlen P, Rabizadeh S, Snipas SJ, Assa-Munt N, Salvesen GS, Bredesen DE. The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis. Nature 1998; 395:801-4.
28. Mille F, Llambi F, Guix C, Delloye-Bourgeois C, Guenebeaud C, Castro-Obregon S, et al. Interfering with multimerization of netrin-1 receptors triggers tumor cell death. Cell Death Differ 2009; 16:1344-51.
29. Tanikawa C, Matsuda K, Fukuda S, Nakamura Y, Arakawa H. p53RDL1 regulates p53-dependent apoptosis. Nat Cell Biol 2003; 5:216-23.
30. Schon MP, Schon M. To die or not to die, that's the question-and the answer may depend on netrin-1. J Natl Cancer Inst 2009; 101:217-9.
31. Taniguchi Y, Kim SH, Sisodia SS. Presenilin-dependent "gamma-secretase" processing of deleted in colorectal cancer (DCC). J Biol Chem 2003; 278:30425-8.
32. Legg JA, Herbert JM, Clissold P, Bicknell R. Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 2008; 11:13-21.
33. Suchting S, Heal P, Tahtis K, Stewart LM, Bicknell R. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. Faseb J 2005; 19:121-3.
34. Wang B, Xiao Y, Ding BB, Zhang N, Yuan X, Gui L, et al. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 2003; 4:19-29.
35. Wang LJ, Zhao Y, Han B, Ma YG, Zhang J, Yang DM, et al. Targeting Slit-Roundabout signaling inhibits tumor angiogenesis in chemical-induced squamous cell carcinogenesis. Cancer Sci 2008; 99:510-7.
36. Kaur S, Castellone MD, Bedell VM, Konar M, Gutkind JS, Ramchandran R. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. J Biol Chem 2006; 281:11347-56.
37. Jones CA, London NR, Chen H, Park KW, Sauvaget D, Stockton RA, et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med 2008; 14:448-53.
38. Stella MC, Trusolino L, Comoglio PM. The Slit/Robo system suppresses hepatocyte growth factor-dependent invasion and morphogenesis. Mol Biol Cell 2009; 20:642-57.
39. Wu JY, Feng L, Park HT, Havlioglu N, Wen L, Tang H, et al. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001; 410:948-52.
40. Stein E, Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001; 291:1928-38.
41. Forcet C, Ye X, Granger L, Corset V, Shin H, Bredesen DE, et al. The dependence receptor DCC (deleted in colorectal cancer) defines an alternative mechanism for caspase activation. Proc Natl Acad Sci USA 2001; 98:3416-21.
42. Giniger E, Jan LY, Jan YN. Specifying the path of the intersegmental nerve of the Drosophila embryo: a role for Delta and Notch. Development 1993; 117:431-40.
43. De Bellard ME, Ching W, Gossler A, Bronner-Fraser M. Disruption of segmental neural crest migration and ephrin expression in delta-1 null mice. Dev Biol 2002; 249:121-30.
44. Ferrari-Toninelli G, Bonini SA, Bettinsoli P, Uberti D, Memo M. Microtubule stabilizing effect of notch activation in primary cortical neurons. Neuroscience 2008; 154:946-52.
45. Fuss B, Josten F, Feix M, Hoch M. Cell movements controlled by the Notch signalling cascade during foregut development in Drosophila. Development 2004; 131:1587-95.
46. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, Radtke F, et al. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 2008; 60:273-84.
47. Thurston G, Noguera-Troise I, Yancopoulos GD. The Delta paradox: DLL4 blockade leads to more tumour vessels but less tumour growth. Nat Rev Cancer 2007; 7:327-31.
48. Bray S. Notch signalling in Drosophila: three ways to use a pathway. Semin Cell Dev Biol 1998; 9:591-7.
49. Ito T, Kagoshima M, Sasaki Y, Li C, Udaka N, Kitsukawa T, et al. Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mech Dev 2000; 97:35-45.
50. Kagoshima M, Ito T. Diverse gene expression and function of semaphorins in developing lung: positive and negative regulatory roles of semaphorins in lung branching morphogenesis. Genes Cells 2001; 6:559-71.
51. Brambilla E, Constantin B, Drabkin H, Roche J. Semaphorin SEMA3F localization in malignant human lung and cell lines: A suggested role in cell adhesion and cell migration. Am J Pathol 2000; 156:939-50.
52. Wilkinson GA, Schittny JC, Reinhardt DP, Klein R. Role for ephrinB2 in postnatal lung alveolar development and elastic matrix integrity. Dev Dyn 2008; 237:2220-34.
53. Wohlfahrt JG, Karagiannidis C, Kunzmann S, Epstein MM, Kempf W, Blaser K, et al. Ephrin-A1 suppresses Th2 cell activation and provides a regulatory link to lung epithelial cells. J Immunol 2004; 172:843-50.
54. Aasheim HC, Pedeutour F, Grosgeorge J, Logtenberg T. Cloning, chromosal mapping and tissue expression of the gene encoding the human Eph-family kinase ligand ephrin-A2. Biochem Biophys Res Commun 1998; 252:378-82.
55. Fox GM, Holst PL, Chute HT, Lindberg RA, Janssen AM, Basu R, et al. cDNA cloning and tissue distribution of five human EPH-like receptor protein-tyrosine kinases. Oncogene 1995; 10:897-905.
56. Beckmann MP, Cerretti DP, Baum P, Vanden Bos T, James L, Farrah T, et al. Molecular characterization of a family of ligands for eph-related tyrosine kinase receptors. EMBO J 1994; 13:3757-62.
57. Bohme B, Holtrich U, Wolf G, Luzius H, Grzeschik KH, Strebhardt K, et al. PCR mediated detection of a new human receptor-tyrosine-kinase, HEK 2. Oncogene 1993; 8:2857-62.
58. Cerretti DP, Vanden Bos T, Nelson N, Kozlosky CJ, Reddy P, Maraskovsky E, et al. Isolation of LERK-5: a ligand of the eph-related receptor tyrosine kinases. Mol Immunol 1995; 32:1197-205.
59. Fletcher FA, Carpenter MK, Shilling H, Baum P, Ziegler SF, Gimpel S, et al. LERK-2, a binding protein for the receptor-tyrosine kinase ELK, is evolutionarily conserved and expressed in a developmentally regulated pattern. Oncogene 1994; 9:3241-7.
60. Hafner C, Schmitz G, Meyer S, Bataille F, Hau P, Langmann T, et al. Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin Chem 2004; 50:490-9.
61. Favre CJ, Mancuso M, Maas K, McLean JW, Baluk P, McDonald DM. Expression of genes involved in vascular development and angiogenesis in endothelial cells of adult lung. Am J Physiol Heart Circ Physiol 2003; 285:1917-38.
62. Gale NW, Baluk P, Pan L, Kwan M, Holash J, DeChiara TM, et al. Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev Biol 2001; 230:151-60.
63. Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998; 93:741-53.
64. Schwarz MA, Caldwell L, Cafasso D, Zheng H. Emerging pulmonary vasculature lacks fate specification. Am J Physiol Lung Cell Mol Physiol 2009; 296:71-81.
65. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 2006; 124:161-73.
66. Erber R, Eichelsbacher U, Powajbo V, Korn T, Djonov V, Lin J, et al. EphB4 controls blood vascular morphogenesis during postnatal angiogenesis. EMBO J 2006; 25:628-41.
67. Larson J, Schomberg S, Schroeder W, Carpenter TC. Endothelial EphA receptor stimulation increases lung vascular permeability. Am J Physiol Lung Cell Mol Physiol 2008; 295:431-9.
68. Eichmann A, Makinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 2005; 19:1013-21.
69. Dalvin S, Anselmo MA, Prodhan P, Komatsuzaki K, Schnitzer JJ, Kinane TB. Expression of Netrin-1 and its two receptors DCC and UNC5H2 in the developing mouse lung. Gene Expr Patterns 2003; 3:279-83.
70. Liu Y, Stein E, Oliver T, Li Y, Brunken WJ, Koch M, et al. Novel role for Netrins in regulating epithelial behavior during lung branching morphogenesis. Curr Biol 2004; 14:897-905.
71. Xian J, Clark KJ, Fordham R, Pannell R, Rabbitts TH, Rabbitts PH. Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene. Proc Natl Acad Sci USA 2001; 98:15062-6.
72. Greenberg JM, Thompson FY, Brooks SK, Shannon JM, Akeson AL. Slit and robo expression in the developing mouse lung. Dev Dyn 2004; 230:350-60.
73. Anselmo MA, Dalvin S, Prodhan P, Komatsuzaki K, Aidlen JT, Schnitzer JJ, et al. Slit and robo: expression patterns in lung development. Gene Expr Patterns 2003; 3:13-9.
74. Clark K, Hammond E, Rabbitts P. Temporal and spatial expression of two isoforms of the Dutt1/Robo1 gene in mouse development. FEBS Lett 2002; 523:12-6.
75. Guseh JS, Bores SA, Stanger BZ, Zhou Q, Anderson WJ, Melton DA, et al. Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Development 2009; 136:1751-9.
76. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, Sudo T, et al. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 2000; 127:3913-21.
77. Post LC, Ternet M, Hogan BL. Notch/Delta expression in the developing mouse lung. Mech Dev 2000; 98:95-8.
78. Shan L, Aster JC, Sklar J, Sunday ME. Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am J Physiol Lung Cell Mol Physiol 2007; 292:500-9.
79. Tsao PN, Vasconcelos M, Izvolsky KI, Qian J, Lu J, Cardoso WV. Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 2009; 136:2297-307.
80. Tsao PN, Chen F, Izvolsky KI, Walker J, Kukuruzinska MA, Lu J, et al. Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J Biol Chem 2008; 283:29532-44.
81. Borges M, Linnoila RI, van de Velde HJ, Chen H, Nelkin BD, Mabry M, et al. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 1997; 386:852-5.
82. Leimeister C, Schumacher N, Steidl C, Gessler M. Analysis of HeyL expression in wild-type and Notch pathway mutant mouse embryos. Mech Dev 2000; 98:175-8.
83. Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, et al. Characterization of the human and mouse HEY1, HEY2 and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 2000; 66:195-203.
84. de Pontual L, Nepote V, Attie-Bitach T, Al Halabiah H, Trang H, Elghouzzi V, et al. Noradrenergic neuronal development is impaired by mutation of the proneural HASH-1 gene in congenital central hypoventilation syndrome (Ondine's curse). Hum Mol Genet 2003; 12:3173-80.
85. Huang MT, Dai YS, Chou YB, Juan YH, Wang CC, Chiang BL. Regulatory T cells negatively regulate neovasculature of airway remodeling via DLL4-notch signaling. J Immunol 2009; 183:4745-54.
86. Raymond T, Schaller M, Hogaboam CM, Lukacs NW, Rochford R, Kunkel SL. Toll-like receptors, Notch ligands and cytokines drive the chronicity of lung inflammation. Proc Am Thorac Soc 2007; 4:635-41.
87. Tilley AE, Harvey BG, Heguy A, Hackett NR, Wang R, O'Connor TP, et al. Downregulation of the notch pathway in human airway epithelium in association with smoking and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2009; 179:457-66.
88. Bagri A, Tessier-Lavigne M, Watts RJ. Neuropilins in tumor biology. Clin Cancer Res 2009; 15:1860-4.
89. Capparuccia L, Tamagnone L. Semaphorin signaling in cancer cells and in cells of the tumor microenvironment: two sides of a coin. J Cell Sci 2009; 122:1723-36.
90. Geretti E, Shimizu A, Klagsbrun M. Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 2008; 11:31-9.
91. Neufeld G, Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer 2008; 8:632-45.
92. Roche J, Boldog F, Robinson M, Robinson L, Varella-Garcia M, Swanton M, et al. Distinct 3p21.3 deletions in lung cancer and identification of a new human semaphorin. Oncogene 1996; 12:1289-97.
93. Sekido Y, Bader S, Latif F, Chen JY, Duh FM, Wei MH, et al. Human semaphorins A(V) and IV reside in the 3p21.3 small cell lung cancer deletion region and demonstrate distinct expression patterns. Proc Natl Acad Sci USA 1996; 93:4120-5.
94. Xiang RH, Hensel CH, Garcia DK, Carlson HC, Kok K, Daly MC, et al. Isolation of the human semaphorin III/F gene (SEMA3F) at chromosome 3p21, a region deleted in lung cancer. Genomics 1996; 32:39-48.
95. Clarhaut J, Gemmill RM, Potiron VA, Ait-Si-Ali S, Imbert J, Drabkin HA, et al. ZEB-1, a repressor of the semaphorin 3F tumor suppressor gene in lung cancer cells. Neoplasia 2009; 11:157-66.
96. Lantuejoul S, Constantin B, Drabkin H, Brambilla C, Roche J, Brambilla E. Expression of VEGF, semaphorin SEMA3F, and their common receptors neuropilins NP1 and NP2 in preinvasive bronchial lesions, lung tumours, and cell lines. J Pathol 2003; 200:336-47.
97. Castro-Rivera E, Ran S, Brekken RA, Minna JD. Semaphorin 3B inhibits the phosphatidylinositol 3-kinase/Akt pathway through neuropilin-1 in lung and breast cancer cells. Cancer Res 2008; 68:8295-303.
98. Koyama N, Zhang J, Huqun, Miyazawa H, Tanaka T, Su X, et al. Identification of IGFBP-6 as an effector of the tumor suppressor activity of SEMA3B. Oncogene 2008; 27:6581-9.
99. Rolny C, Capparuccia L, Casazza A, Mazzone M, Vallario A, Cignetti 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.
100. Pan SH, Chao YC, Chen HY, Hung PF, Lin PY, Lin CW, et al. Long form collapsin response mediator protein-1 (LCRMP-1) expression is associated with clinical outcome and lymph node metastasis in non-small cell lung cancer patients. Lung Cancer 2009; ahead of print.
101. Lugli A, Spichtin H, Maurer R, Mirlacher M, Kiefer J, Huusko P, et al. EphB2 expression across 138 human tumor types in a tissue microarray: high levels of expression in gastrointestinal cancers. Clin Cancer Res 2005; 11:6450-8.
102. Yu J, Bulk E, Ji P, Hascher A, Koschmieder S, Berdel WE, et al. The kinase defective EPHB6 receptor tyrosine kinase activates MAP kinase signaling in lung adenocarcinoma. Int J Oncol 2009; 35:175-9.
103. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, et al. Predicting drug susceptibility of nonsmall cell lung cancers based on genetic lesions. J Clin Invest 2009; 119:1727-40.
104. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008; 455:1069-75.
105. Nasreen N, Mohammed KA, Lai Y, Antony VB. Receptor EphA2 activation with ephrinA1 suppresses growth of malignant mesothelioma (MM). Cancer Lett 2007; 258:215-22.
106. Ogawa K, Pasqualini R, Lindberg RA, Kain R, Freeman AL, Pasquale EB. The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 2000; 19:6043-52.
107. Fearon ER, Cho KR, Nigro JM, Kern SE, Simons JW, Ruppert JM, et al. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 1990; 247:49-56.
108. Shin SK, Nagasaka T, Jung BH, Matsubara N, Kim WH, Carethers JM, et al. Epigenetic and genetic alterations in Netrin-1 receptors UNC5C and DCC in human colon cancer. Gastroenterology 2007; 133:1849-57.
109. Delloye-Bourgeois C, Brambilla E, Coissieux MM, Guenebeaud C, Pedeux R, Firlej V, et al. Interference with netrin-1 and tumor cell death in non-small cell lung cancer. J Natl Cancer Inst 2009; 101:237-47.
110. Fitamant J, Guenebeaud C, Coissieux MM, Guix C, Treilleux I, Scoazec JY, et al. Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer. Proc Natl Acad Sci USA 2008; 105:4850-5.
111. Rodrigues S, De Wever O, Bruyneel E, Rooney RJ, Gespach C. Opposing roles of netrin-1 and the dependence receptor DCC in cancer cell invasion, tumor growth and metastasis. Oncogene 2007; 26:5615-25.
112. Link BC, Reichelt U, Schreiber M, Kaifi JT, Wachowiak R, Bogoevski D, et al. Prognostic implications of netrin-1 expression and its receptors in patients with adenocarcinoma of the pancreas. Ann Surg Oncol 2007; 14:2591-9.
113. Castets M, Coissieux MM, Delloye-Bourgeois C, Bernard L, Delcros JG, Bernet A, et al. Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis. Dev Cell 2009; 16:614-20.
114. Park KW, Crouse D, Lee M, Karnik SK, Sorensen LK, Murphy KJ, et al. The axonal attractant Netrin-1 is an angiogenic factor. Proc Natl Acad Sci USA 2004; 101:16210-5.
115. Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004; 432:179-86.
116. Wilson BD, Ii M, Park KW, Suli A, Sorensen LK, Larrieu-Lahargue F, et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006; 313:640-4.
117. Llambi F, Lourenco FC, Gozuacik D, Guix C, Pays L, Del Rio G, et al. The dependence receptor UNC5H2 mediates apoptosis through DAP-kinase. EMBO J 2005; 24:1192-201.
118. Inbal B, Cohen O, Polak-Charcon S, Kopolovic J, Vadai E, Eisenbach L, et al. DAP kinase links the control of apoptosis to metastasis. Nature 1997; 390:180-4.
119. Yanagawa N, Tamura G, Oizumi H, Kanauchi N, Endoh M, Sadahiro M, et al. Promoter hypermethylation of RASSF1A and RUNX3 genes as an independent prognostic prediction marker in surgically resected nonsmall cell lung cancers. Lung Cancer 2007; 58:131-8.
120. Abdollahi A, Schwager C, Kleeff J, Esposito I, Domhan S, Peschke P, et al. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci USA 2007; 104:12890-5.
121. Dallol A, Forgacs E, Martinez A, Sekido Y, Walker R, Kishida T, et al. Tumour specific promoter region methylation of the human homologue of the Drosophila Roundabout gene DUTT1 (ROBO1) in human cancers. Oncogene 2002; 21:3020-8.
122. Sundaresan V, Chung G, Heppell-Parton A, Xiong J, Grundy C, Roberts I, et al. Homozygous deletions at 3p12 in breast and lung cancer. Oncogene 1998; 17:1723-9.
123. Georgas K, Burridge L, Smith K, Holmes GP, Chenevix-Trench G, Ioannou PA, et al. Assignment of the human slit homologue SLIT2 to human chromosome band 4p15.2. Cytogenet Cell Genet 1999; 86:246-7.
124. Shivapurkar N, Virmani AK, Wistuba II, Milchgrub S, Mackay B, Minna JD, et al. Deletions of chromosome 4 at multiple sites are frequent in malignant mesothelioma and small cell lung carcinoma. Clin Cancer Res 1999; 5:17-23.
125. Girard L, Zochbauer-Muller S, Virmani AK, Gazdar AF, Minna JD. Genome-wide allelotyping of lung cancer identifies new regions of allelic loss, differences between small cell lung cancer and non-small cell lung cancer, and loci clustering. Cancer Res 2000; 60:4894-906.
126. Dallol A, Da Silva NF, Viacava P, Minna JD, Bieche I, Maher ER, et al. SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer Res 2002; 62:5874-80.
127. Gorn M, Anige M, Burkholder I, Muller B, Scheffler A, Edler L, et al. Serum levels of Magic Roundabout protein in patients with advanced non-small cell lung cancer (NSCLC). Lung Cancer 2005; 49:71-6.
128. Zheng Q, Qin H, Zhang H, Li J, Hou L, Wang H, et al. Notch signaling inhibits growth of the human lung adenocarcinoma cell line A549. Oncol Rep 2007; 17:847-52.
129. Chen Y, De Marco MA, Graziani I, Gazdar AF, Strack PR, Miele L, et al. Oxygen concentration determines the biological effects of NOTCH-1 signaling in adenocarcinoma of the lung. Cancer Res 2007; 67:7954-9.
130. Garnis C, Campbell J, Davies JJ, Macaulay C, Lam S, Lam WL. Involvement of multiple developmental genes on chromosome 1p in lung tumorigenesis. Hum Mol Genet 2005; 14:475-82.
131. Dang TP, Gazdar AF, Virmani AK, Sepetavec T, Hande KR, Minna JD, et al. Chromosome 19 translocation, overexpression of Notch3, and human lung cancer. J Natl Cancer Inst 2000; 92:1355-7.
132. Haruki N, Kawaguchi KS, Eichenberger S, Massion PP, Olson S, Gonzalez A, et al. Dominant-negative Notch3 receptor inhibits mitogen-activated protein kinase pathway and the growth of human lung cancers. Cancer Res 2005; 65:3555-61.
133. Konishi J, Kawaguchi KS, Vo H, Haruki N, Gonzalez A, Carbone DP, et al. Gamma-secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res 2007; 67:8051-7.
134. Sriuranpong V, Borges MW, Ravi RK, Arnold DR, Nelkin BD, Baylin SB, et al. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res 2001; 61:3200-5.
135. Sriuranpong V, Borges MW, Strock CL, Nakakura EK, Watkins DN, Blaumueller CM, et al. Notch signaling induces rapid degradation of achaete-scute homolog 1. Mol Cell Biol 2002; 22:3129-39.
136. Nie L, Xu M, Vladimirova A, Sun XH. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J 2003; 22:5780-92.
137. Greenblatt DY, Vaccaro AM, Jaskula-Sztul R, Ning L, Haymart M, Kunnimalaiyaan M, et al. Valproic acid activates notch-1 signaling and regulates the neuroendocrine phenotype in carcinoid cancer cells. Oncologist 2007; 12:942-51.
138. Choi K, Ahn YH, Gibbons DL, Tran HT, Creighton CJ, Girard L, et al. Distinct biological roles for the notch ligands Jagged-1 and Jagged-2. J Biol Chem 2009; 284:17766-74.
139. Geretti E, Klagsbrun M. Neuropilins: novel targets for anti-angiogenesis therapies. Cell Adh Migr 2007; 1:56-61.
140. Binetruy-Tournaire R, Demangel C, Malavaud B, Vassy R, Rouyre S, Kraemer M, et al. Identification of a peptide blocking vascular endothelial growth factor (VEGF)-mediated angiogenesis. EMBO J 2000; 19:1525-33.
141. Narazaki M, Segarra M, Tosato G. Sulfated polysaccharides identified as inducers of neuropilin-1 internalization and functional inhibition of VEGF165 and semaphorin3A. Blood 2008; 111:4126-36.
142. Roth L, Nasarre C, Dirrig-Grosch S, Aunis D, Cremel G, Hubert P, et al. Transmembrane domain interactions control biological functions of neuropilin-1. Mol Biol Cell 2008; 19:646-54.
143. Caunt M, Mak J, Liang WC, Stawicki S, Pan Q, Tong RK, et al. Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 2008; 13:331-42.
144. Pan Q, Chanthery Y, Liang WC, Stawicki S, Mak J, Rathore N, et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007; 11:53-67.
145. Balakrishnan A, Penachioni JY, Lamba S, Bleeker FE, Zanon C, Rodolfo M, et al. Molecular profiling of the "plexinome" in melanoma and pancreatic cancer. Hum Mutat 2009; 30:1167-74.
146. Wong OG, Nitkunan T, Oinuma I, Zhou C, Blanc V, Brown RS, et al. Plexin-B1 mutations in prostate cancer. Proc Natl Acad Sci USA 2007; 104:19040-5.
147. Kaneko S, Iwanami A, Nakamura M, Kishino A, Kikuchi K, Shibata S, et al. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat Med 2006; 12:1380-9.
148. Montolio M, Messeguer J, Masip I, Guijarro P, Gavin R, Antonio Del Rio J, et al. A semaphorin 3A inhibitor blocks axonal chemorepulsion and enhances axon regeneration. Chem Biol 2009; 16:691-701.
149. Nguyen QD, Rodrigues S, Rodrigue CM, Rivat C, Grijelmo C, Bruyneel E, et al. Inhibition of vascular endothelial growth factor (VEGF)-165 and semaphorin 3A-mediated cellular invasion and tumor growth by the VEGF signaling inhibitor ZD4190 in human colon cancer cells and xenografts. Mol Cancer Ther 2006; 5:2070-7.
150. Brantley-Sieders DM, Zhuang G, Hicks D, Fang WB, Hwang Y, Cates JM, et al. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J Clin Invest 2008; 118:64-78.
151. Ireton RC, Chen J. EphA2 receptor tyrosine kinase as a promising target for cancer therapeutics. Curr Cancer Drug Targets 2005; 5:149-57.
152. Noberini R, Koolpe M, Peddibhotla S, Dahl R, Su Y, Cosford ND, et al. Small molecules can selectively inhibit ephrin binding to the EphA4 and EphA2 receptors. J Biol Chem 2008; 283:29461-72.
153. Jackson D, Gooya J, Mao S, Kinneer K, Xu L, Camara M, et al. A human antibody-drug conjugate targeting EphA2 inhibits tumor growth in vivo. Cancer Res 2008; 68:9367-74.
154. Wykosky J, Debinski W. The EphA2 receptor and ephrinA1 ligand in solid tumors: function and therapeutic targeting. Mol Cancer Res 2008; 6:1795-806.
155. Chaudhari A, Mahfouz M, Fialho AM, Yamada T, Granja AT, Zhu Y, et al. Cupredoxin-cancer interrelationship: azurin binding with EphB2, interference in EphB2 tyrosine phosphorylation, and inhibition of cancer growth. Biochemistry 2007; 46:1799-810.
156. Martiny-Baron G, Korff T, Schaffner F, Esser N, Eggstein S, Marme D, et al. Inhibition of tumor growth and angiogenesis by soluble EphB4. Neoplasia 2004; 6:248-57.
157. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15:232-9.
158. Kamba T, McDonald DM. Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br J Cancer 2007; 96:1788-95.
159. Huminiecki L, Bicknell R. In silico cloning of novel endothelial-specific genes. Genome Res 2000; 10:1796-806.
160. Neri D, Bicknell R. Tumour vascular targeting. Nat Rev Cancer 2005; 5:436-46.
161. Greenberg JI, Shields DJ, Barillas SG, Acevedo LM, Murphy E, Huang J, et al. A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 2008; 456:809-13.
162. 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; 15:220-31.
163. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI, et al. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 2008; 456:814-8.
164. Round J, Stein E. Netrin signaling leading to directed growth cone steering. Curr Opin Neurobiol 2007; 17:15-21.
165. Nichols JT, Miyamoto A, Weinmaster G. Notch signaling-constantly on the move. Traffic 2007; 8:959-69.
166. Maeda Y, Dave V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev 2007; 87:219-44.