A Roundabout Way to Cancer

Advances in Cancer Research

Volumn 114, Issue , 2012, Pages 187-235

  Ballard, Mimmi S ^a   Hinck, Lindsay ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon guidance molecules; Cancer; Robo; Slit; Tumor; Tumor angiogenesis

Indexed keywords

ROUNDABOUT RECEPTOR; SLIT PROTEIN;

ANGIOGENESIS; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

EID: 84860826598     PISSN: 0065230X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386503-8.00005-3     Document Type: Chapter

References (158)

1. Abdollahi A., Schwager C., Kleeff J., Esposito I., Domhan S., Peschke P., Hauser K., Hahnfeldt P., Hlatky L., Debus J., Peters J.M., Friess H., et al. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc. Natl. Acad. Sci. USA 2007, 104:12890-12895.
2. Alajez N.M., Lenarduzzi M., Ito E., Hui A.B., Shi W., Bruce J., Yue S., Huang S.H., Xu W., Waldron J., O'Sullivan B., Liu F.F. MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res. 2011, 71:2381-2391.
3. Allington T.M., Schiemann W.P. The Cain and Abl of epithelial-mesenchymal transition and transforming growth factor-beta in mammary epithelial cells. Cells Tissues Organs 2011, 193:98-113.
4. Altay T., McLaughlin B., Wu J.Y., Park T.S., Gidday J.M. Slit modulates cerebrovascular inflammation and mediates neuroprotection against global cerebral ischemia. Exp. Neurol. 2007, 207:186-194.
5. Angeloni D., ter Elst A., Wei M.H., van der Veen A.Y., Braga E.A., Klimov E.A., Timmer T., Korobeinikova L., Lerman M.I., Buys C.H. Analysis of a new homozygous deletion in the tumor suppressor region at 3p12.3 reveals two novel intronic noncoding RNA genes. Genes Chromosomes Cancer 2006, 45:676-691.
6. Avci M.E., Konu O., Yagci T. Quantification of SLIT-ROBO transcripts in hepatocellular carcinoma reveals two groups of genes with coordinate expression. BMC Cancer 2008, 8:392.
7. Bashaw G.J., Kidd T., Murray D., Pawson T., Goodman C.S. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 2000, 101:703-715.
8. Bauer K., Dowejko A., Bosserhoff A.K., Reichert T.E., Bauer R. Slit-2 facilitates interaction of P-cadherin with Robo-3 and inhibits cell migration in an oral squamous cell carcinoma cell line. Carcinogenesis 2011, 32:935-943.
9. Bear J.E., Gertler F.B. Ena/VASP: towards resolving a pointed controversy at the barbed end. J. Cell Sci. 2009, 122:1947-1953.
10. Bedell V.M., Yeo S.Y., Park K.W., Chung J., Seth P., Shivalingappa V., Zhao J., Obara T., Sukhatme V.P., Drummond I.A., Li D.Y., Ramchandran R. Roundabout4 is essential for angiogenesis in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:6373-6378.
11. Blanco D., Vicent S., Elizegi E., Pino I., Fraga M.F., Esteller M., Saffiotti U., Lecanda F., Montuenga L.M. Altered expression of adhesion molecules and epithelial-mesenchymal transition in silica-induced rat lung carcinogenesis. Lab. Invest. 2004, 84:999-1012.
12. Brantley-Sieders D.M., Dunaway C.M., Rao M., Short S., Hwang Y., Gao Y., Li D., Jiang A., Shyr Y., Wu J.Y., Chen J. Angiocrine factors modulate tumor proliferation and motility through EphA2 repression of Slit2 tumor suppressor function in endothelium. Cancer Res. 2011, 71:976-987.
13. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999, 96:795-806.
14. Challa A.K., Beattie C.E., Seeger M.A. Identification and characterization of roundabout orthologs in zebrafish. Mech. Dev. 2001, 101:249-253.
15. Chanana B., Steigemann P., Jackle H., Vorbruggen G. Reception of Slit requires only the chondroitin-sulphate-modified extracellular domain of Syndecan at the target cell surface. Proc. Natl. Acad. Sci. USA 2009, 106:11984-11988.
16. Chen J.H., Wen L., Dupuis S., Wu J.Y., Rao Y. The N-terminal leucine-rich regions in Slit are sufficient to repel olfactory bulb axons and subventricular zone neurons. J. Neurosci. 2001, 21:1548-1556.
17. Christgen M., Bruchhardt H., Hadamitzky C., Rudolph C., Steinemann D., Gadzicki D., Hasemeier B., Romermann D., Focken T., Krech T., Ballmaier M., Schlegelberger B., et al. Comprehensive genetic and functional characterization of IPH-926: a novel CDH1-null tumour cell line from human lobular breast cancer. J. Pathol. 2009, 217:620-632.
18. Clark K., Hammond E., Rabbitts P. Temporal and spatial expression of two isoforms of the Dutt1/Robo1 gene in mouse development. FEBS Lett. 2002, 523:12-16.
19. Coleman H.A., Labrador J.P., Chance R.K., Bashaw G.J. The Adam family metalloprotease Kuzbanian regulates the cleavage of the roundabout receptor to control axon repulsion at the midline. Development 2010, 137:2417-2426.
20. Dallol A., Da Silva N.F., Viacava P., Minna J.D., Bieche I., Maher E.R., Latif F. 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, 62:5874-5880.
21. Dallol A., Forgacs E., Martinez A., Sekido Y., Walker R., Kishida T., Rabbitts P., Maher E.R., Minna J.D., Latif F. Tumour specific promoter region methylation of the human homologue of the Drosophila Roundabout gene DUTT1 (ROBO1) in human cancers. Oncogene 2002, 21:3020-3028.
22. Dallol A., Krex D., Hesson L., Eng C., Maher E.R., Latif F. Frequent epigenetic inactivation of the SLIT2 gene in gliomas. Oncogene 2003, 22:4611-4616.
23. Dallol A., Morton D., Maher E.R., Latif F. SLIT2 axon guidance molecule is frequently inactivated in colorectal cancer and suppresses growth of colorectal carcinoma cells. Cancer Res. 2003, 63:1054-1058.
24. Dallol A., Dickinson R.E., Latif F. Epigenetic Disruption of the SLIT-ROBO Interactions in Human Cancer 2005, Springer, New York, NY.
25. Delloye-Bourgeois C., Fitamant J., Paradisi A., Cappellen D., Douc-Rasy S., Raquin M.A., Stupack D., Nakagawara A., Rousseau R., Combaret V., Puisieux A., Valteau-Couanet D., et al. Netrin-1 acts as a survival factor for aggressive neuroblastoma. J. Exp. Med. 2009, 206:833-847.
26. Dickinson R.E., Dallol A., Bieche I., Krex D., Morton D., Maher E.R., Latif F. Epigenetic inactivation of SLIT3 and SLIT1 genes in human cancers. Br. J. Cancer 2004, 91:2071-2078.
27. Dickson B.J., Gilestro G.F. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 2006, 22:651-675.
28. Doi T., Hajduk P., Puri P. Upregulation of Slit-2 and Slit-3 gene expressions in the nitrofen-induced hypoplastic lung. J. Pediatr. Surg. 2009, 44:2092-2095.
29. Dunaway C.M., Hwang Y., Lindsley C.W., Cook R.S., Wu J.Y., Boothby M., Chen J., Brantley-Sieders D.M. Cooperative signaling between Slit2 and Ephrin-A1 regulates a balance between angiogenesis and angiostasis. Mol. Cell. Biol. 2011, 31:404-416.
30. Dunwell T.L., Dickinson R.E., Stankovic T., Dallol A., Weston V., Austen B., Catchpoole D., Maher E.R., Latif F. Frequent epigenetic inactivation of the SLIT2 gene in chronic and acute lymphocytic leukemia. Epigenetics 2009, 4:265-269.
31. Evans T.A., Bashaw G.J. Functional diversity of Robo receptor immunoglobulin domains promotes distinct axon guidance decisions. Curr. Biol. 2010, 20:567-572.
32. Fan X., Labrador J.P., Hing H., Bashaw G.J. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 2003, 40:113-127.
33. Fitamant J., Guenebeaud C., Coissieux M.M., Guix C., Treilleux I., Scoazec J.Y., Bachelot T., Bernet A., Mehlen P. Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer. Proc. Natl. Acad. Sci. USA 2008, 105:4850-4855.
34. Fukuhara N., Howitt J.A., Hussain S.A., Hohenester E. Structural and functional analysis of slit and heparin binding to immunoglobulin-like domains 1 and 2 of Drosophila Robo. J. Biol. Chem. 2008, 283:16226-16234.
35. Fulda S., Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006, 25:4798-4811.
36. Furne C., Rama N., Corset V., Chedotal A., Mehlen P. Netrin-1 is a survival factor during commissural neuron navigation. Proc. Natl. Acad. Sci. USA 2008, 105:14465-14470.
37. Gertler F., Condeelis J. Metastasis: tumor cells becoming MENAcing. Trends Cell Biol. 2011, 21:81-90.
38. Ghosh S., Ghosh A., Maiti G.P., Alam N., Roy A., Roychoudhury S., Panda C.K. Alterations of ROBO1/DUTT1 and ROBO2 loci in early dysplastic lesions of head and neck: clinical and prognostic implications. Hum. Genet. 2009, 125:189-198.
39. Gorn M., Anige M., Burkholder I., Muller B., Scheffler A., Edler L., Boeters I., Panse J., Schuch G., Hossfeld D.K., Laack E. Serum levels of Magic Roundabout protein in patients with advanced non-small cell lung cancer (NSCLC). Lung Cancer 2005, 49:71-76.
40. Greenberg J.M., Thompson F.Y., Brooks S.K., Shannon J.M., Akeson A.L. Slit and robo expression in the developing mouse lung. Dev. Dyn. 2004, 230:350-360.
41. Grone J., Doebler O., Loddenkemper C., Hotz B., Buhr H.J., Bhargava S. Robo1/Robo4: differential expression of angiogenic markers in colorectal cancer. Oncol. Rep. 2006, 15:1437-1443.
42. Guan H., Zu G., Xie Y., Tang H., Johnson M., Xu X., Kevil C., Xiong W.C., Elmets C., Rao Y., Wu J.Y., Xu H. Neuronal repellent Slit2 inhibits dendritic cell migration and the development of immune responses. J. Immunol. 2003, 171:6519-6526.
43. Hall A. The cytoskeleton and cancer. Cancer Metastasis Rev. 2009, 28:5-14.
44. Han X., Zhang M.C. Potential anti-angiogenic role of Slit2 in corneal neovascularization. Exp. Eye Res. 2010, 90:742-749.
45. Hinck L. The versatile roles of " axon guidance" cues in tissue morphogenesis. Dev. Cell 2004, 7:783-793.
46. Hohenester E. Structural insight into Slit-Robo signalling. Biochem. Soc. Trans. 2008, 36:251-256.
47. Hohenester E., Hussain S., Howitt J.A. Interaction of the guidance molecule Slit with cellular receptors. Biochem. Soc. Trans. 2006, 34:418-421.
48. Howitt J.A., Clout N.J., Hohenester E. Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit. EMBO J. 2004, 23:4406-4412.
49. Hu H. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 2001, 4:695-701.
50. Hu H., Li M., Labrador J.P., McEwen J., Lai E.C., Goodman C.S., Bashaw G.J. Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc. Natl. Acad. Sci. USA 2005, 102:4613-4618.
51. Huang L., Xu Y., Yu W., Li X., Liqun C., He X., Peiying H. Robo1: a potential role in ocular angiogenesis. Curr. Eye Res. 2009, 34:1019-1029.
52. Huang L., Yu W., Li X., Niu L., Li K., Li J. Robo1/robo4: different expression patterns in retinal development. Exp. Eye Res. 2009, 88:583-588.
53. Huang L., Yu W., Li X., Xu Y., Niu L., He X., Dong J., Yan Z. Expression of Robo4 in the fibrovascular membranes from patients with proliferative diabetic retinopathy and its role in RF/6A and RPE cells. Mol. Vis. 2009, 15:1057-1069.
54. Huminiecki L., Bicknell R. In silico cloning of novel endothelial-specific genes. Genome Res. 2000, 10:1796-1806.
55. Huminiecki L., Gorn M., Suchting S., Poulsom R., Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 2002, 79:547-552.
56. Hussain S.A., Piper M., Fukuhara N., Strochlic L., Cho G., Howitt J.A., Ahmed Y., Powell A.K., Turnbull J.E., Holt C.E., Hohenester E. A molecular mechanism for the heparan sulfate dependence of slit-robo signaling. J. Biol. Chem. 2006, 281:39693-39698.
57. Inatani M., Irie F., Plump A.S., Tessier-Lavigne M., Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 2003, 302:1044-1046.
58. Ito H., Funahashi S., Yamauchi N., Shibahara J., Midorikawa Y., Kawai S., Kinoshita Y., Watanabe A., Hippo Y., Ohtomo T., Iwanari H., Nakajima A., et al. Identification of ROBO1 as a novel hepatocellular carcinoma antigen and a potential therapeutic and diagnostic target. Clin. Cancer Res. 2006, 12:3257-3264.
59. Jin J., You H., Yu B., Deng Y., Tang N., Yao G., Shu H., Yang S., Qin W. Epigenetic inactivation of SLIT2 in human hepatocellular carcinomas. Biochem. Biophys. Res. Commun. 2009, 379:86-91.
60. Johnson D.W., Berg J.N., Baldwin M.A., Gallione C.J., Marondel I., Yoon S.J., Stenzel T.T., Speer M., Pericak-Vance M.A., Diamond A., Guttmacher A.E., Jackson C.E., et al. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 1996, 13:189-195.
61. Johnson K.G., Ghose A., Epstein E., Lincecum J., O'Connor M.B., Van Vactor D. Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr. Biol. 2004, 14:499-504.
62. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., Larrieu-Lahargue F., Mukouyama Y.S., Lindblom P., Seth P., et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 2008, 14:448-453.
63. Jones C.A., Nishiya N., London N.R., Zhu W., Sorensen L.K., Chan A.C., Lim C.J., Chen H., Zhang Q., Schultz P.G., Hayallah A.M., Thomas K.R., et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 2009, 11:1325-1331.
64. Kanellis J., Garcia G.E., Li P., Parra G., Wilson C.B., Rao Y., Han S., Smith C.W., Johnson R.J., Wu J.Y., Feng L. Modulation of inflammation by slit protein in vivo in experimental crescentic glomerulonephritis. Am. J. Pathol. 2004, 165:341-352.
65. Kastenhuber E., Kern U., Bonkowsky J.L., Chien C.B., Driever W., Schweitzer J. Netrin-DCC, Robo-Slit, and heparan sulfate proteoglycans coordinate lateral positioning of longitudinal dopaminergic diencephalospinal axons. J. Neurosci. 2009, 29:8914-8926.
66. Kaur S., Castellone M.D., Bedell V.M., Konar M., Gutkind J.S., Ramchandran R. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. J. Biol. Chem. 2006, 281:11347-11356.
67. Kaur S., Samant G.V., Pramanik K., Loscombe P.W., Pendrak M.L., Roberts D.D., Ramchandran R. Silencing of directional migration in roundabout4 knockdown endothelial cells. BMC Cell Biol. 2008, 9:61.
68. Kerbel R.S. Tumor angiogenesis. N. Engl. J. Med. 2008, 358:2039-2049.
69. Khusial P.R., Vadla B., Krishnan H., Ramlall T.F., Shen Y., Ichikawa H., Geng J.G., Goldberg G.S. Src activates Abl to augment Robo1 expression in order to promote tumor cell migration. Oncotarget 2010, 1:198-209.
70. Kidd T., Bland K.S., Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 1999, 96:785-794.
71. Koch A.W., Mathivet T., Larrivee B., Tong R.K., Kowalski J., Pibouin-Fragner L., Bouvree K., Stawicki S., Nicholes K., Rathore N., Scales S.J., Luis E., et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev. Cell 2011, 20:33-46.
72. Kramer S.G., Kidd T., Simpson J.H., Goodman C.S. Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 2001, 292:737-740.
73. Latil A., Bieche I., Chene L., Laurendeau I., Berthon P., Cussenot O., Vidaud M. Gene expression profiling in clinically localized prostate cancer: a four-gene expression model predicts clinical behavior. Clin. Cancer Res. 2003, 9:5477-5485.
74. Lee J.S., Ray R., Chien C.B. Cloning and expression of three zebrafish roundabout homologs suggest roles in axon guidance and cell migration. Dev. Dyn. 2001, 221:216-230.
75. Lee J.S., von der Hardt S., Rusch M.A., Stringer S.E., Stickney H.L., Talbot W.S., Geisler R., Nusslein-Volhard C., Selleck S.B., Chien C.B., Roehl H. Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer). Neuron 2004, 44:947-960.
76. Legg J.A., Herbert J.M., Clissold P., Bicknell R. Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 2008, 11:13-21.
77. Leonardo E.D., Hinck L., Masu M., Keino-Masu K., Ackerman S.L., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838.
78. Liang Y., Annan R.S., Carr S.A., Popp S., Mevissen M., Margolis R.K., Margolis R.U. Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J. Biol. Chem. 1999, 274:17885-17892.
79. Liu Z., Patel K., Schmidt H., Andrews W., Pini A., Sundaresan V. Extracellular Ig domains 1 and 2 of Robo are important for ligand (Slit) binding. Mol. Cell. Neurosci. 2004, 26:232-240.
80. Liu D., Hou J., Hu X., Wang X., Xiao Y., Mou Y., De Leon H. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ. Res. 2006, 98:480-489.
81. London N.R., Li D.Y. Robo4-dependent Slit signaling stabilizes the vasculature during pathologic angiogenesis and cytokine storm. Curr. Opin. Hematol. 2011, 18:186-190.
82. London N.R., Zhu W., Bozza F.A., Smith M.C., Greif D.M., Sorensen L.K., Chen L., Kaminoh Y., Chan A.C., Passi S.F., Day C.W., Barnard D.L., et al. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci. Transl. Med. 2010, 2:23ra19.
83. Lundstrom A., Gallio M., Englund C., Steneberg P., Hemphala J., Aspenstrom P., Keleman K., Falileeva L., Dickson B.J., Samakovlis C. Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 2004, 18:2161-2171.
84. Ma X.J., Wang Z., Ryan P.D., Isakoff S.J., Barmettler A., Fuller A., Muir B., Mohapatra G., Salunga R., Tuggle J.T., Tran Y., Tran D., et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004, 5:607-616.
85. Macias H., Moran A., Samara Y., Moreno M., Compton J.E., Harburg G., Strickland P., Hinck L. SLIT/ROBO1 signaling suppresses mammary branching morphogenesis by limiting basal cell number. Dev. Cell 2011, 20:827-840.
86. Marlow R., Strickland P., Lee J.S., Wu X., Pebenito M., Binnewies M., Le E.K., Moran A., Macias H., Cardiff R.D., Sukumar S., Hinck L. SLITs suppress tumor growth in vivo by silencing Sdf1/Cxcr4 within breast epithelium. Cancer Res. 2008, 68:7819-7827.
87. Marlow R., Binnewies M., Sorensen L.K., Monica S.D., Strickland P., Forsberg E.C., Li D.Y., Hinck L. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proc. Natl. Acad. Sci. USA 2010, 107:10520-10525.
88. Medioni C., Bertrand N., Mesbah K., Hudry B., Dupays L., Wolstein O., Washkowitz A.J., Papaioannou V.E., Mohun T.J., Harvey R.P., Zaffran S. Expression of Slit and Robo genes in the developing mouse heart. Dev. Dyn. 2010, 239:3303-3311.
89. Mertsch S., Schmitz N., Jeibmann A., Geng J.G., Paulus W., Senner V. Slit2 involvement in glioma cell migration is mediated by Robo1 receptor. J. Neurooncol 2008, 87:1-7.
90. Moore M.A. The role of chemoattraction in cancer metastases. Bioessays 2001, 23:674-676.
91. Moore S.W., Tessier-Lavigne M., Kennedy T.E. Netrins and their receptors. Adv. Exp. Med. Biol. 2007, 621:17-31.
92. Morlot C., Hemrika W., Romijn R.A., Gros P., Cusack S., McCarthy A.A. Production of Slit2 LRR domains in mammalian cells for structural studies and the structure of human Slit2 domain 3. Acta Crystallogr. D Biol. Crystallogr. 2007, 63:961-968.
93. Morlot C., Thielens N.M., Ravelli R.B., Hemrika W., Romijn R.A., Gros P., Cusack S., McCarthy A.A. Structural insights into the Slit-Robo complex. Proc. Natl. Acad. Sci. USA 2007, 104:14923-14928.
94. Mulik S., Sharma S., Suryawanshi A., Veiga-Parga T., Reddy P.B., Rajasagi N.K., Rouse B.T. Activation of endothelial roundabout receptor 4 reduces the severity of virus-induced keratitis. J. Immunol. 2011, 186:7195-7204.
95. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., Barrera J.L., Mohar A., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
96. Mura M., Swain R.K., Zhuang X., Vorschmitt H., Reynolds G., Durant S., Beesley J.F., Herbert J.M., Sheldon H., Andre M., Sanderson S., Glen K., et al. Identification and angiogenic role of the novel tumor endothelial marker CLEC14A. Oncogene 2011, 31:293-305.
97. Narayan G., Goparaju C., Arias-Pulido H., Kaufmann A.M., Schneider A., Durst M., Mansukhani M., Pothuri B., Murty V.V. Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol. Cancer 2006, 5:16.
98. Nguyen Ba-Charvet K.T., Brose K., Ma L., Wang K.H., Marillat V., Sotelo C., Tessier-Lavigne M., Chedotal A. Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. J. Neurosci. 2001, 21:4281-4289.
99. Ning Y., Sun Q., Dong Y., Xu W., Zhang W., Huang H., Li Q. Slit2-N inhibits PDGF-induced migration in rat airway smooth muscle cells: WASP and Arp2/3 involved. Toxicology 2011, 283:32-40.
100. Ogata-Iwao M., Inatani M., Iwao K., Takihara Y., Nakaishi-Fukuchi Y., Irie F., Sato S., Furukawa T., Yamaguchi Y., Tanihara H. Heparan sulfate regulates intraretinal axon pathfinding by retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2011, 52:6671-6679.
101. Park K.W., Morrison C.M., Sorensen L.K., Jones C.A., Rao Y., Chien C.B., Wu J.Y., Urness L.D., Li D.Y. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev. Biol. 2003, 261:251-267.
102. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., Olivi A., McLendon R., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
103. Piper M., Georgas K., Yamada T., Little M. Expression of the vertebrate Slit gene family and their putative receptors, the Robo genes, in the developing murine kidney. Mech. Dev. 2000, 94:213-217.
104. Piper M., Anderson R., Dwivedy A., Weinl C., van Horck F., Leung K.M., Cogill E., Holt C. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 2006, 49:215-228.
105. Plump A.S., Erskine L., Sabatier C., Brose K., Epstein C.J., Goodman C.S., Mason C.A., Tessier-Lavigne M. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 2002, 33:219-232.
106. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
107. Prasad A., Fernandis A.Z., Rao Y., Ganju R.K. Slit protein-mediated inhibition of CXCR4-induced chemotactic and chemoinvasive signaling pathways in breast cancer cells. J. Biol. Chem. 2004, 279:9115-9124.
108. Prasad A., Qamri Z., Wu J., Ganju R.K. Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells. J. Leukoc. Biol. 2007, 82:465-476.
109. Prasad A., Paruchuri V., Preet A., Latif F., Ganju R.K. Slit-2 induces a tumor-suppressive effect by regulating beta-catenin in breast cancer cells. J. Biol. Chem. 2008, 283:26624-26633.
110. Qiu H., Zhu J., Yu J., Pu H., Dong R. SLIT2 is epigenetically silenced in ovarian cancers and suppresses growth when activated. Asian Pac. J. Cancer Prev. 2011, 12:791-795.
111. Rhee J., Mahfooz N.S., Arregui C., Lilien J., Balsamo J., VanBerkum M.F. Activation of the repulsive receptor Roundabout inhibits N-cadherin-mediated cell adhesion. Nat. Cell Biol. 2002, 4:798-805.
112. Rhee J., Buchan T., Zukerberg L., Lilien J., Balsamo J. Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat. Cell Biol. 2007, 9:883-892.
113. Rhiner C., Gysi S., Frohli E., Hengartner M.O., Hajnal A. Syndecan regulates cell migration and axon guidance in C. elegans. Development 2005, 132:4621-4633.
114. Richardson A.L., Wang Z.C., De Nicolo A., Lu X., Brown M., Miron A., Liao X., Iglehart J.D., Livingston D.M., Ganesan S. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006, 9:121-132.
115. Ronca F., Andersen J.S., Paech V., Margolis R.U. Characterization of Slit protein interactions with glypican-1. J. Biol. Chem. 2001, 276:29141-29147.
116. Salvucci O., Bouchard A., Baccarelli A., Deschenes J., Sauter G., Simon R., Bianchi R., Basik M. The role of CXCR4 receptor expression in breast cancer: a large tissue microarray study. Breast Cancer Res. Treat. 2006, 97:275-283.
117. Santiago-Martinez E., Soplop N.H., Patel R., Kramer S.G. Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J. Cell Biol. 2008, 182:241-248.
118. Schmid B.C., Rezniczek G.A., Fabjani G., Yoneda T., Leodolter S., Zeillinger R. The neuronal guidance cue Slit2 induces targeted migration and may play a role in brain metastasis of breast cancer cells. Breast Cancer Res. Treat. 2007, 106:333-342.
119. Schulz J.G., Ceulemans H., Caussinus E., Baietti M.F., Affolter M., Hassan B.A., David G. Drosophila syndecan regulates tracheal cell migration by stabilizing Robo levels. EMBO Rep. 2011, 12:1039-1046.
120. Seki M., Watanabe A., Enomoto S., Kawamura T., Ito H., Kodama T., Hamakubo T., Aburatani H. Human ROBO1 is cleaved by metalloproteinases and gamma-secretase and migrates to the nucleus in cancer cells. FEBS Lett. 2010, 584:2909-2915.
121. Seth P., Lin Y., Hanai J., Shivalingappa V., Duyao M.P., Sukhatme V.P. Magic roundabout, a tumor endothelial marker: expression and signaling. Biochem. Biophys. Res. Commun. 2005, 332:533-541.
122. Sharma G., Mirza S., Prasad C.P., Srivastava A., Gupta S.D., Ralhan R. Promoter hypermethylation of p16INK4A, p14ARF, CyclinD2 and Slit2 in serum and tumor DNA from breast cancer patients. Life Sci. 2007, 80:1873-1881.
123. Sheldon H., Andre M., Legg J.A., Heal P., Herbert J.M., Sainson R., Sharma A.S., Kitajewski J.K., Heath V.L., Bicknell R. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. FASEB J. 2009, 23:513-522.
124. Shiau C.E., Bronner-Fraser M. N-cadherin acts in concert with Slit1-Robo2 signaling in regulating aggregation of placode-derived cranial sensory neurons. Development 2009, 136:4155-4164.
125. Shivapurkar N., Sood S., Wistuba I.I., Virmani A.K., Maitra A., Milchgrub S., Minna J.D., Gazdar A.F. Multiple regions of chromosome 4 demonstrating allelic losses in breast carcinomas. Cancer Res. 1999, 59:3576-3580.
126. Shivapurkar N., Virmani A.K., Wistuba I.I., Milchgrub S., Mackay B., Minna J.D., Gazdar A.F. Deletions of chromosome 4 at multiple sites are frequent in malignant mesothelioma and small cell lung carcinoma. Clin. Cancer Res. 1999, 5:17-23.
127. Singh R.K., Indra D., Mitra S., Mondal R.K., Basu P.S., Roy A., Roychowdhury S., Panda C.K. Deletions in chromosome 4 differentially associated with the development of cervical cancer: evidence of slit2 as a candidate tumor suppressor gene. Hum. Genet. 2007, 122:71-81.
128. Smart A.D., Course M.M., Rawson J., Selleck S., Van Vactor D., Johnson K.G. Heparan sulfate proteoglycan specificity during axon pathway formation in the Drosophila embryo. Dev. Neurobiol. 2011, 71:608-618.
129. Spitzweck B., Brankatschk M., Dickson B.J. Distinct protein domains and expression patterns confer divergent axon guidance functions for Drosophila Robo receptors. Cell 2010, 140:409-420.
130. Steigemann P., Molitor A., Fellert S., Jackle H., Vorbruggen G. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 2004, 14:225-230.
131. Stein E., Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001, 291:1928-1938.
132. Stella M.C., Trusolino L., Comoglio P.M. The Slit/Robo system suppresses hepatocyte growth factor-dependent invasion and morphogenesis. Mol. Biol. Cell 2009, 20:642-657.
133. Strickland P., Shin G.C., Plump A., Tessier-Lavigne M., Hinck L. Slit2 and netrin 1 act synergistically as adhesive cues to generate tubular bi-layers during ductal morphogenesis. Development 2006, 133:823-832.
134. Suchting S., Heal P., Tahtis K., Stewart L.M., Bicknell R. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. FASEB J. 2005, 19:121-123.
135. Suryawanshi A., Mulik S., Sharma S., Reddy P.B., Sehrawat S., Rouse B.T. Ocular neovascularization caused by herpes simplex virus type 1 infection results from breakdown of binding between vascular endothelial growth factor A and its soluble receptor. J. Immunol. 2011, 186:3653-3665.
136. Tie J., Pan Y., Zhao L., Wu K., Liu J., Sun S., Guo X., Wang B., Gang Y., Zhang Y., Li Q., Qiao T., et al. MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the Robo1 receptor. PLoS Genet. 2010, 6:e1000879.
137. Tole S., Mukovozov I.M., Huang Y.W., Magalhaes M.A., Yan M., Crow M.R., Liu G.Y., Sun C.X., Durocher Y., Glogauer M., Robinson L.A. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J. Leukoc. Biol. 2009, 86:1403-1415.
138. Tseng R.C., Lee S.H., Hsu H.S., Chen B.H., Tsai W.C., Tzao C., Wang Y.C. SLIT2 attenuation during lung cancer progression deregulates beta-catenin and E-cadherin and associates with poor prognosis. Cancer Res. 2010, 70:543-551.
139. Urness L.D., Sorensen L.K., Li D.Y. Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 2000, 26:328-331.
140. Verissimo A.R., Herbert J.M., Heath V.L., Legg J.A., Sheldon H., Andre M., Swain R.K., Bicknell R. Functionally defining the endothelial transcriptome, from Robo4 to ECSCR. Biochem. Soc. Trans. 2009, 37:1214-1217.
141. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., Tessier-Lavigne M. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 1999, 96:771-784.
142. Wang B., Xiao Y., Ding B.B., Zhang N., Yuan X., Gui L., Qian K.X., Duan S., Chen Z., Rao Y., Geng J.G. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 2003, 4:19-29.
143. Wang L.J., Zhao Y., Han B., Ma Y.G., Zhang J., Yang D.M., Mao J.W., Tang F.T., Li W.D., Yang Y., Wang R., Geng J.G. Targeting Slit-Roundabout signaling inhibits tumor angiogenesis in chemical-induced squamous cell carcinogenesis. Cancer Sci. 2008, 99:510-517.
144. Werbowetski-Ogilvie T.E., Seyed Sadr M., Jabado N., Angers-Loustau A., Agar N.Y., Wu J., Bjerkvig R., Antel J.P., Faury D., Rao Y., Del Maestro R.F. Inhibition of medulloblastoma cell invasion by Slit. Oncogene 2006, 25:5103-5112.
145. Wong K., Ren X.R., Huang Y.Z., Xie Y., Liu G., Saito H., Tang H., Wen L., Brady-Kalnay S.M., Mei L., Wu J.Y., Xiong W.C., et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001, 107:209-221.
146. Wu J.Y., Feng L., Park H.T., Havlioglu N., Wen L., Tang H., Bacon K.B., Jiang Z., Zhang X., Rao Y. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001, 410:948-952.
147. Xian J., Clark K.J., Fordham R., Pannell R., Rabbitts T.H., Rabbitts P.H. Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene. Proc. Natl. Acad. Sci. USA 2001, 98:15062-15066.
148. Xu Y., Li W.L., Fu L., Gu F., Ma Y.J. Slit2/Robo1 signaling in glioma migration and invasion. Neurosci. Bull. 2010, 26:474-478.
149. Yang L., Bashaw G.J. Son of sevenless directly links the Robo receptor to rac activation to control axon repulsion at the midline. Neuron 2006, 52:595-607.
150. Yang X.M., Han H.X., Sui F., Dai Y.M., Chen M., Geng J.G. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem. Biophys. Res. Commun. 2010, 396:571-577.
151. Ye B.Q., Geng Z.H., Ma L., Geng J.G. Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation. J. Immunol. 2010, 185:6294-6305.
152. Yiin J.J., Hu B., Jarzynka M.J., Feng H., Liu K.W., Wu J.Y., Ma H.I., Cheng S.Y. Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Neuro Oncol. 2009, 11:779-789.
153. Yu J., Cao Q., Wu L., Dallol A., Li J., Chen G., Grasso C., Cao X., Lonigro R.J., Varambally S., Mehra R., Palanisamy N., et al. The neuronal repellent SLIT2 is a target for repression by EZH2 in prostate cancer. Oncogene 2010, 29:5370-5380.
154. Yuasa-Kawada J., Kinoshita-Kawada M., Rao Y., Wu J.Y. Deubiquitinating enzyme USP33/VDU1 is required for Slit signaling in inhibiting breast cancer cell migration. Proc. Natl. Acad. Sci. USA 2009, 106:14530-14535.
155. Zhang F., Ronca F., Linhardt R.J., Margolis R.U. Structural determinants of heparan sulfate interactions with Slit proteins. Biochem. Biophys. Res. Commun. 2004, 317:352-357.
156. Zhang B., Dietrich U.M., Geng J.G., Bicknell R., Esko J.D., Wang L. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood 2009, 114:4300-4309.
157. Zheng W., Geng A.Q., Li P.F., Wang Y., Yuan X.B. Robo4 regulates the radial migration of newborn neurons in developing neocortex. Cereb. Cortex 2011, [Epub ahead of print].
158. Zhou W.J., Geng Z.H., Chi S., Zhang W., Niu X.F., Lan S.J., Ma L., Yang X., Wang L.J., Ding Y.Q., Geng J.G. Slit-Robo signaling induces malignant transformation through Hakai-mediated E-cadherin degradation during colorectal epithelial cell carcinogenesis. Cell Res. 2011, 21:609-626.