Role of ROBO4 signalling in developmental and pathological angiogenesis

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Yadav, Suresh Singh ^a   Narayan, Gopeshwar ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GLUTATHIONE TRANSFERASE; MOLECULAR SCAFFOLD; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN CDC42; PROTEIN TYROSINE KINASE; ROUNDABOUT RECEPTOR; ROUNDABOUT RECEPTOR 1; ROUNDABOUT RECEPTOR 2; ROUNDABOUT RECEPTOR 3; ROUNDABOUT RECEPTOR 4; SLIT PROTEIN; SLIT2 PROTEIN; SLIT3 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; WISKOTT ALDRICH SYNDROME PROTEIN; CELL SURFACE RECEPTOR; LIGAND;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; AUTOPHOSPHORYLATION; BLOOD VESSEL PERMEABILITY; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; ENDOTHELIUM CELL; INTRACELLULAR SIGNALING; MIGRATION; NONHUMAN; OVERALL SURVIVAL; PROTEIN INTERACTION; RETINA BLOOD VESSEL; REVIEW; TUMOR GROWTH; TUMOR VASCULARIZATION; ANIMAL; BLOOD VESSEL; CHEMISTRY; HUMAN; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); SIGNAL TRANSDUCTION;

ANIMALS; BLOOD VESSELS; HUMANS; LIGANDS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84896872807     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/683025     Document Type: Review

References (69)

1. Carmeliet P., Blood vessels and nerves: common signals, pathways and diseases. Nature Reviews Genetics 2003 4 9 710 720 2-s2.0-0041378074 10.1038/nrg1158
2. Bicknell R., Harris A. L., Novel angiogenic signaling pathways and vascular targets. Annual Review of Pharmacology and Toxicology 2004 44 219 238 2-s2.0-1342287074 10.1146/annurev.pharmtox.44.101802.121650
3. Soker S., Takashima S., Miao H. Q., 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 6 735 745 2-s2.0-0032549799 10.1016/S0092-8674(00)81402-6
4. Klagsbrun M., Takashima S., Mamluk R., The role of neuropilin in vascular and tumor biology. Advances in Experimental Medicine and Biology 2002 515 33 48 2-s2.0-0036933684
5. Wang H. U., Chen Z.-F., Anderson D. J., Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998 93 5 741 753 2-s2.0-0032577446 10.1016/S0092-8674(00)81436-1
6. Gerety S. S., Wang H. U., Chen Z.-F., Anderson D. J., Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Molecular Cell 1999 4 3 403 414 2-s2.0-0033197535 10.1016/S1097-2765(00)80342-1
7. Krebs L. T., Xue Y., Norton C. R., Shutter J. R., Maguire M., Sundberg J. P., Gallahan D., Closson V., Kitajewski J., Callahan R., Smith G. H., Stark K. L., Gridley T., Notch signaling is essential for vascular morphogenesis in mice. Genes and Development 2000 14 11 1343 1352 2-s2.0-0034212710
8. Shutter J. R., Scully S., Fan W., Richards W. G., Kitajewski J., Deblandre G. A., Kintner C. R., Stark K. L., D114, a novel Notch ligand expressed in arterial endothelium. Genes and Development 2000 14 11 1313 1318 2-s2.0-0034195220
9. Funahashi Y., Shawber C. J., Sharma A., Kanamaru E., Choi Y. K., Kitajewski J., Notch modulates VEGF action in endothelial cells by inducing Matrix Metalloprotease activity. Vascular Cell 2011 3 1, article 2 2-s2.0-79955598040 10.1186/2045-824X-3-2
10. 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 4 547 552 2-s2.0-0036209165 10.1006/geno.2002.6745
11. 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. Developmental Biology 2003 261 1 251 267 2-s2.0-0042663890 10.1016/S0012-1606(03)00258-6
12. Wang B., Xiao Y., Ding B.-B., Zhang N., Yuan X.-B., 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 1 19 29 2-s2.0-10744224816 10.1016/S1535-6108(03)00164-8
13. Carmeliet P., Tessier-Lavigne M., Common mechanisms of nerve and blood vessel wiring. Nature 2005 436 7048 193 200 2-s2.0-22444447946 10.1038/nature03875
14. 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 6 795 806 2-s2.0-0033582914
15. Li H.-S., Chen J.-H., Wu W., Fagaly T., Zhou L., Yuan W., Dupuis S., Jiang Z.-H., Nash W., Gick C., Ornitz D. M., Wu J. Y., Rao Y., Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 1999 96 6 807 818 2-s2.0-0033582927
16. 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 5517 737 740 2-s2.0-0035957670 10.1126/science. 1058766
17. Grieshammer U., Ma L., Plump A. S., Wang F., Tessier-Lavigne M., Martin G. R., SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Developmental Cell 2004 6 5 709 717 2-s2.0-2342629171 10.1016/S1534- 5807(04)00108-X
18. Fish J. E., Wythe J. D., Xiao T., Bruneau B. G., Stainier D. Y. R., Srivastava D., Woo S., A Slit/miR-218/Robo regulatory loop is required during heart tube formation in zebrafish. Development 2011 138 7 1409 1419 2-s2.0-79955155124 10.1242/dev.060046
19. Wu J. Y., Feng L., Park H.-T., Havlioglu N., Wen L., Tang H., Bacon K. B., Jiang Z.-H., Zhang X.-C., Rao Y., The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001 410 6831 948 952 2-s2.0-0035912244 10.1038/35073616
20. Zhao Y., Su Y., Ye L., Slit-Robo: a potential way to treat periodontitis. Medical Hypotheses 2012 79 2 186 188
21. Yuen D. A., Robinson L. A., Slit2-Robo signaling: a novel regulator of vascular injury. Current Opinion in Nephrology and Hypertension 2013 22 4 445 451
22. Samant G. V., Schupp M. O., Francois M., Moleri S., Kothinti R. K., Chun C. Z., Sinha I., Sellars S., Leigh N., Pramanik K., Horswill M. A., Remadevi I., Li K., Wilkinson G. A., Tabatabai N. M., Beltrame M., Koopman P., Ramchandran R., Sox factors transcriptionally regulate ROBO4 gene expression in developing vasculature in zebrafish. The Journal of Biological Chemistry 2011 286 35 30740 30747 2-s2.0-80052229773 10.1074/jbc.M111.220665
23. Yuan W., Zhou L., Chen J.-H., Wu J. Y., Rao Y., Ornitz D. M., The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Developmental Biology 1999 212 2 290 306 2-s2.0-0033566579 10.1006/dbio.1999.9371
24. Holmes G. P., Negus K., Burridge L., Raman S., Algar E., Yamada T., Little M. H., Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mechanisms of Development 1998 79 1-2 57 72 2-s2.0-0032416836 10.1016/S0925-4773(98)00174-9
25. Latil A., Chêne L., Cochant-Priollet B., Mangin P., Fournier G., Berthon P., Cussenot O., Quantification of expression of netrins, slits and their receptors in human prostate tumors. International Journal of Cancer 2003 103 3 306 315 2-s2.0-0037454779 10.1002/ijc.10821
26. Boles K. S., Schmieder A. H., Koch A. W., Carano R. A. D., Wu Y., Caruthers S. D., Tong R. K., Stawicki S., Hu G., Scott M. J., Zhang H., Reynolds B. A., Wickline S. A., Lanza G. M., MR angiogenesis imaging with Robo4- vs. α V β 3-targeted nanoparticles in a B16/F10 mouse melanoma model. The FASEB Journal 2010 24 11 4262 4270 2-s2.0-78649855174 10.1096/fj.10-157933
27. Kaur S., Castellone M. D., Bedell V. M., Konar M., Gutkind J. S., Ramchandran R., Robo4 signaling in endothelial cells implies attraction guidance mechanisms. The Journal of Biological Chemistry 2006 281 16 11347 11356 2-s2.0-33744952643 10.1074/jbc.M508853200
28. Howitt J. A., Clout N. J., Hohenester E., Binding site for Robo receptors revealed by dissection of the leucine-rich region of Slit. The EMBO Journal 2004 23 22 4406 4412 2-s2.0-10044233924 10.1038/sj.emboj.7600446
29. 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 Robol and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. The FASEB Journal 2009 23 2 513 522 2-s2.0-59649086084 10.1096/fj.07-098269
30. 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 19 4300 4309 2-s2.0-77950546322 10.1182/blood-2008-12-193326
31. Seth P., Lin Y., Hanai J.-I., Shivalingappa V., Duyao M. P., Sukhatme V. P., Magic roundabout, a tumor endothelial marker: expression and signaling. Biochemical and Biophysical Research Communications 2005 332 2 533 541 2-s2.0-19444367337 10.1016/j.bbrc.2005.03.250
32. 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 Biology 2008 9, article 61 2-s2.0-58149397961 10.1186/1471-2121-9-61
33. Ballard M. S., Hinck L. A., Roundabout way to cancer. Advances in Cancer Research 2012 114 187 235
34. Song H.-J., Ming G.-L., Poo M.-M., cAMP-induced switching in turning direction of nerve growth cones. Nature 1997 388 6639 275 279 2-s2.0-0030877318 10.1038/40864
35. Marlow R., Binnewies M., Sorensen L. K., Monica S. D., Strickland P., Camilla Forsberg E., Li D. Y., Hinck L., Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proceedings of the National Academy of Sciences of the United States of America 2010 107 23 10520 10525 2-s2.0-77953803209 10.1073/pnas.1001896107
36. Autiero M., de Smet F., Claes F., Carmeliet P., Role of neural guidance signals in blood vessel navigation. Cardiovascular Research 2005 65 3 629 638 2-s2.0-12344332651 10.1016/j.cardiores.2004.09.013
37. Kidd T., Brose K., Mitchell K. J., Fetter R. D., Tessier-Lavigne M., Goodman C. S., Tear G., Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 1998 92 2 205 215 2-s2.0-0032559219 10.1016/S0092-8674(00)80915-0
38. Prasad A., Qamri Z., Wu J., Ganju R. K., Pivotal Advance: Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells. Journal of Leukocyte Biology 2007 82 3 465 476 2-s2.0-34548407427 10.1189/jlb.1106678
39. 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 Science 2008 29 3 510 517 2-s2.0-38949206522 10.1111/j.1349-7006.2007.00721.x
40. 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 29 4611 4616 2-s2.0-0043170818 10.1038/sj.onc.1206687
41. Narayan G., Goparaju C., Arias-Pulido H., Kaufmann A. M., Schneider A., Dürst M., Mansukhani M., Pothuri B., Murty V. V., Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Molecular Cancer 2006 5, article 16 2-s2.0-33745493625 10.1186/1476-4598-5-16
42. Okada Y., Yano K., Jin E., Funahashi N., Kitayama M., Doi T., Spokes K., Beeler D. L., Shih S.-C., Okada H., Danilov T. A., Maynard E., Minami T., Oettgen P., Aird W. C., A three-kilobase fragment of the human Robo4 promoter directs cell type-specific expression in endothelium. Circulation Research 2007 100 12 1712 1722 2-s2.0-34250868931 10.1161/01.RES.0000269779.10644.dc
43. Pircher A., Fiegla M., Untergassera G., Favorable prognosis of operable non-small cell lung cancer (NSCLC) patients harboring an increased expression of tumor endothelial markers (TEMs). Lung Cancer 2013 81 2 252 258 10.1016/j.lungcan.2013.04.014
44. 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., Frias A., Nishiya N., Ginsberg M. H., Gerhardt H., Zhang K., Li D. Y., Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nature Medicine 2008 14 4 448 453 2-s2.0-41849131420 10.1038/nm1742
45. Gavard J., Gutkind J. S., VEGF controls endothelial-cell permeability promoting β -arrestin-dependent endocytosis VE-cadherin. Nature Cell Biology 2006 8 11 1223 1234 2-s2.0-33750529948 10.1038/ncb1486
46. Garrett T. A., van Buul J. D., Burridge K., VEGF-induced Rac1 activation in endothelial cells is regulated by the guanine nucleotide exchange factor Vav2. Experimental Cell Research 2007 313 15 3285 3297 2-s2.0-34548028024 10.1016/j.yexcr.2007.05.027
47. 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., Famulok M., Zhang K., Ginsberg M. H., Li D. Y., Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nature Cell Biology 2009 11 11 1325 1331 2-s2.0-70449529782 10.1038/ncb1976
48. Koch A. W., Mathivet T., Larrivée B., Tong R. K., Kowalski J., Pibouin-Fragner L., Bouvrée K., Stawicki S., Nicholes K., Rathore N., Scales S. J., Luis E., del Toro R., Freitas C., Bréant C., Michaud A., Corvol P., Thomas J.-L., Wu Y., Peale F., Watts R. J., Tessier-Lavigne M., Bagri A., Eichmann A., Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Developmental Cell 2011 20 1 33 46 2-s2.0-78651433171 10.1016/j.devcel.2010.12.001
49. Suchting S., Heal P., Tahtis K., Stewart L. M., Bicknell R., Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. The FASEB Journal 2005 19 1 121 123 2-s2.0-11244262363 10.1096/fj.04-1991fje
50. Paul J. D., Coulombe K. L., Toth P. T., SLIT3-ROBO4 activation promotes vascular network formation in human engineered tissue and angiogenesis in vivo. Journal of Molecular and Cellular Cardiology 2013 64 124 131 10.1016/j.yjmcc.2013.09.005
51. Liu J., Zhang L., Wang D., Shen H., Jiang M., Mei P., Hayden P. S., Sedor J. R., Hu H., Congenital diaphragmatic hernia, kidney agenesis and cardiac defects associated with Slit3-deficiency in mice. Mechanisms of Development 2003 120 9 1059 1070 2-s2.0-0141783992 10.1016/S0925-4773(03)00161-8
52. Hivert B., Liu Z., Chuang C.-Y., Doherty P., Sundaresan V., Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Molecular and Cellular Neuroscience 2002 21 4 534 545 2-s2.0-0036939517 10.1006/mcne.2002. 1193
53. Yoshikawa M., Mukai Y., Okada Y., Yoshioka Y., Tsunoda S.-I., Tsutsumi Y., Okada N., Aird W. C., Doi T., Nakagawa S., Ligand-independent assembly of purified soluble magic roundabout (Robo4), a tumor-specific endothelial marker. Protein Expression and Purification 2008 61 1 78 82 2-s2.0-47749104480 10.1016/j.pep.2008.05.006
54. London N. R., Zhu W., Bozza F. A., Smith M. C. P., Greif D. M., Sorensen L. K., Chen L., Kaminoh Y., Chan A. C., Passi S. F., Day C. W., Barnard D. L., Zimmerman G. A., Krasnow M. A., Li D. Y., Targeting Robo4-dependent slit signaling to survive the cytokine storm in sepsis and influenza. Science Translational Medicine 2010 2 23 2-s2.0-77951836880 10.1126/scitranslmed.3000678
55. Tang X., Jang S.-W., Okada M., Chan C.-B., Feng Y., Liu Y., Luo S.-W., Hong Y., Rama N., Xiong W.-C., Mehlen P., Ye K., Netrin-1 mediates neuronal survival through PIKE-L interaction with the dependence receptor UNC5B. Nature Cell Biology 2008 10 6 698 706 2-s2.0-44649197812 10.1038/ncb1732
56. Guijarro-Muñoz I., Cuesta A. M., Alvarez-Cienfuegos A., Geng J. G., Alvarez-Vallina L., Sanz L., The axonal repellent Slit2 inhibits pericyte migration: potential implications in angiogenesis. Experimental Cell Research 2012 318 4 371 378 2-s2.0-84856108037 10.1016/j.yexcr.2011.12.005
57. 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. Proceedings of the National Academy of Sciences of the United States of America 2005 102 18 6373 6378 2-s2.0-20944450769 10.1073/pnas.0408318102
58. 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-Oncology 2009 11 6 779 789 2-s2.0-73249126948 10.1215/15228517-2008-017
59. Turcotte S., Desrosiers R. R., Béliveau R., HIF-1 α mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. Journal of Cell Science 2003 116 11 2247 2260 2-s2.0-0038348531 10.1242/jcs.00427
60. Liao W. X., Laurent L. C., Agent S., Hodges J., Chen D. B., Human placental expression of SLIT/ROBO signaling cues: effects of preeclampsia and hypoxia. Biology of Reproduction 2012 86 4 111 10.1095/biolreprod.110.088138
61. 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., Rao Y., Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001 107 2 209 221 2-s2.0-17944380009 10.1016/S0092-8674(01)00530-X
62. 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. Proceedings of the National Academy of Sciences of the United States of America 2005 102 12 4613 4618 2-s2.0-15444380880 10.1073/pnas.0409325102
63. Lundström A., Gallio M., Englund C., Steneberg P., Hemphälä J., Aspenström 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 and Development 2004 18 17 2161 2171 2-s2.0-4444379134 10.1101/gad.310204
64. Tole S., Mukovozov I. M., Huang Y.-W., Magalhaes M. A. O., 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. Journal of Leukocyte Biology 2009 86 6 1403 1415 2-s2.0-73149088851 10.1189/jlb.0609391
65. Martinez-Quiles N., Rohatgi R., Antón I. M., Medina M., Saville S. P., Miki H., Yamaguchi H., Takenawa T., Hartwig J. H., Geha R. S., Ramesh N., WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nature Cell Biology 2001 3 5 484 491 2-s2.0-0035003138 10.1038/35074551
66. Kessels M. M., Qualmann B., Syndapin oligomers interconnect the machineries for endocytic vesicle formation and actin polymerization. The Journal of Biological Chemistry 2006 281 19 13285 13299 2-s2.0-33745000739 10.1074/jbc.M510226200
67. Krugmann S., Jordens I., Gevaert K., Driessens M., Vandekerckhove J., Hall A., Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Current Biology 2001 11 21 1645 1655 2-s2.0-0035975963 10.1016/S0960-9822(01)00506-1
68. 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. The Journal of Biological Chemistry 2006 281 51 39693 39698 2-s2.0-33846024764 10.1074/jbc.M609384200
69. 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. The Journal of Biological Chemistry 2008 283 23 16226 16234 2-s2.0-47049089676 10.1074/jbc.M800688200