Slit2N and Robo4 regulate lymphangiogenesis through the VEGF-C/VEGFR-3 pathway

Cell Communication and Signaling

Volumn 12, Issue 1, 2014, Pages

  Yu, Jinlong ^a,d   Zhang, Xuefeng ^a   Kuzontkoski, Paula M ^a   Jiang, Shuxian ^a   Zhu, Weiquan ^b   Li, Dean Y ^b,c   Groopman, Jerome E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c SICHUAN PROVINCIAL PEOPLE'S HOSPITAL   (China)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Akt; Lymphangiogenesis; Migration; PI3K; Proliferation; Robo4; Slit2; VEGF C; VEGFR 3

Indexed keywords

CELL PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; ROBO4 PROTEIN; SLIT2N PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3; CELL SURFACE RECEPTOR; NERVE PROTEIN; PEPTIDE FRAGMENT; ROBO4 PROTEIN, HUMAN; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN; VEGFR3 PROTEIN, HUMAN;

ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERNALIZATION; INTRACELLULAR SIGNALING; LUNG ALVEOLUS CELL; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; LYMPHOID CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; UPREGULATION; CELL LINE; CELL MOTION; CYTOLOGY; DRUG EFFECT; GENETICS; LYMPH VESSEL; METABOLISM;

CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CELL SURFACE; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84899644860     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-12-25     Document Type: Article

References (84)

1. Current views on the function of the lymphatic vasculature in health and disease. Wang Y, Oliver G, Genes Dev 2010 24 2115 2126 10.1101/gad.1955910 20889712
2. VEGF-mediated signal transduction in lymphatic endothelial cells. Bahram F, Claesson-Welsh L, Pathophysiology: the official journal of the International Society for Pathophysiology/ISP 2010 17 253 261
3. Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways. Salameh A, Galvagni F, Bardelli M, Bussolino F, Oliviero S, Blood 2005 106 3423 3431 10.1182/blood-2005-04-1388 16076871 (Pubitemid 41609177)
4. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K, EMBO J 1996 15 290 298 8617204 (Pubitemid 26029207)
5. Expression of vascular endothelial growth factor (VEGF) family members in breast cancer. Kurebayashi J, Otsuki T, Kunisue H, Mikami Y, Tanaka K, Yamamoto S, Sonoo H, Jpn J Canc Res 1999 90 977 981 10.1111/j.1349-7006.1999.tb00844.x (Pubitemid 29500437)
6. Vascular endothelial growth factors VEGF-B and VEGF-C are expressed in human tumors. Salven P, Lymboussaki A, Heikkila P, Jaaskela-Saari H, Enholm B, Aase K, von Euler G, Eriksson U, Alitalo K, Joensuu H, Am J Pathol 1998 153 103 108 10.1016/S0002-9440(10)65550-2 9665470 (Pubitemid 28317512)
7. Lymphangiogenesis and lymphatic metastasis in breast cancer. Ran S, Volk L, Hall K, Flister MJ, Pathophysiology: the official journal of the International Society for Pathophysiology/ISP 2010 17 229 251
8. Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Niki T, Iba S, Tokunou M, Yamada T, Matsuno Y, Hirohashi S, Clin Canc Res: an official journal of the American Association for Cancer Research 2000 6 2431 2439 (Pubitemid 30399212)
9. Increased vascular endothelial growth factor and vascular endothelial growth factor-c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. Ohta Y, Nozawa H, Tanaka Y, Oda M, Watanabe Y, J Thorac Cardiovasc Surg 2000 119 804 813 10.1016/S0022-5223(00)70017-1 10733773 (Pubitemid 30395479)
10. VEGFc and VEGFR3 expression in human thyroid pathologies. Shushanov S, Bronstein M, Adelaide J, Jussila L, Tchipysheva T, Jacquemier J, Stavrovskaya A, Birnbaum D, Karamysheva A, Int J Canc Journal international du cancer 2000 86 47 52 10.1002/(SICI)1097-0215(20000401)86:1<47::AID-IJC7>3.0.CO;2-R (Pubitemid 30133985)
11. Expression of angiogenesis stimulators and inhibitors in human thyroid tumors and correlation with clinical pathological features. Bunone G, Vigneri P, Mariani L, Buto S, Collini P, Pilotti S, Pierotti MA, Bongarzone I, Am J Pathol 1999 155 1967 1976 10.1016/S0002-9440(10)65515-0 10595926
12. Vascular endothelial growth factor-C gene expression in papillary and follicular thyroid carcinomas. Fellmer PT, Sato K, Tanaka R, Okamoto T, Kato Y, Kobayashi M, Shibuya M, Obara T, Surgery 1999 126 1056 1061 discussion 1061-1052 10.1067/msy.2099.101432 10598188
13. Role of vascular endothelial growth factor C expression in the development of lymph node metastasis in gastric cancer. Yonemura Y, Endo Y, Fujita H, Fushida S, Ninomiya I, Bandou E, Taniguchi K, Miwa K, Ohoyama S, Sugiyama K, Sasaki T, Clin Cancer Res 1999 5 1823 1829 10430087 (Pubitemid 29334464)
14. Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Akagi K, Ikeda Y, Miyazaki M, Abe T, Kinoshita J, Maehara Y, Sugimachi K, Br J Cancer 2000 83 887 891 10.1054/bjoc.2000.1396 10970690
15. Vegf, Vegf-B, Vegf-C and their receptors KDR, FLT-1 and FLT-4 during the neoplastic progression of human colonic mucosa. Andre T, Kotelevets L, Vaillant JC, Coudray AM, Weber L, Prevot S, Parc R, Gespach C, Chastre E, Int J Canc Journal International du Cancer 2000 86 174 181 10.1002/(SICI)1097- 0215(20000415)86:2<174::AID-IJC5>3.0.CO;2-E (Pubitemid 30180811)
16. Vascular endothelial growth factor-C expression in human prostatic carcinoma and its relationship to lymph node metastasis. Tsurusaki T, Kanda S, Sakai H, Kanetake H, Saito Y, Alitalo K, Koji T, Br J Cancer 1999 80 309 313 10.1038/sj.bjc.6690356 10390013 (Pubitemid 29210123)
17. Vascular endothelial growth factor-C promotes the growth and invasion of gallbladder cancer via an autocrine mechanism. Chen Y, Jiang L, She F, Tang N, Wang X, Li X, Han S, Zhu J, Mol Cell Biochem 2010 345 77 89 10.1007/s11010-010- 0562-y 20734221
18. Tumor lymphangiogenesis as a potential therapeutic target. Duong T, Koopman P, Francois M, J Oncol 2012 2012 204946 22481918
19. Lymphangiogenesis and cancer metastasis. Mumprecht V, Detmar M, J Cell Mol Med 2009 13 1405 1416 10.1111/j.1582-4934.2009.00834.x 19583813
20. Expressions of COX-2 and VEGF-C in gastric cancer: correlations with lymphangiogenesis and prognostic implications. Gou HF, Chen XC, Zhu J, Jiang M, Yang Y, Cao D, Hou M, J E Clin Canc Res: CR 2011 30 14 10.1186/1756-9966-30-14
21. The effect of the expression of vascular endothelial growth factor (VEGF)-C and VEGF receptor-3 on the clinical outcome in patients with gastric carcinoma. Han FH, Li HM, Zheng DH, He YL, Zhan WH, Eur J Surg Oncol 2010 36 1172 1179 10.1016/j.ejso.2010.09.002 20888167
22. Clinical significance of vascular endothelial growth factors C and D and chemokine receptor CCR7 in gastric cancer. Deguchi K, Ichikawa D, Soga K, Watanabe K, Kosuga T, Takeshita H, Konishi H, Morimura R, Tsujiura M, Komatsu S, Shiozaki A, Okamoto K, Fujiwara H, Otsuji E, Anticancer Res 2010 30 2361 2366 20651394
23. Vascular endothelial growth factor C (VEGF-C) in esophageal cancer correlates with lymph node metastasis and poor patient prognosis. Tanaka T, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Katada T, Shiozaki M, Naganawa Y, Fujii Y, Takeyama H, J Exp Clin Cancer Res 2010 29 83 10.1186/1756-9966-29-83 20584281
24. HER2/neu expression correlates with vascular endothelial growth factor-C and lymphangiogenesis in lymph node-positive breast cancer. Schoppmann SF, Tamandl D, Roberts L, Jomrich G, Schoppmann A, Zwrtek R, Dubsky P, Gnant M, Jakesz R, Birner P, Ann Oncol 2010 21 955 960 10.1093/annonc/mdp532 19940005
25. Expression of vascular endothelial growth factors C and D correlates with lymphangiogenesis and lymph node metastasis in lung adenocarcinoma. Bo C, Xiaopeng D, Chuanliang P, Xiaogang Z, Thorac Cardiovasc Surg 2009 57 291 294 10.1055/s-0029-1185625 19629892
26. Lymphangiogenesis and cancer metastasis. Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K, Nat Rev Cancer 2002 2 573 583 10.1038/nrc863 12154350 (Pubitemid 37328924)
27. Unique patterns of metastases in common and rare types of malignancy. Leong SP, Nakakura EK, Pollock R, Choti MA, Morton DL, Henner WD, Lal A, Pillai R, Clark OH, Cady B, J Surg Oncol 2011 103 607 614 10.1002/jso.21841 21480255
28. Tumor and lymph node lymphangiogenesis-impact on cancer metastasis. Tobler NE, Detmar M, J Leukoc Biol 2006 80 691 696 10.1189/jlb.1105653 16793912 (Pubitemid 44835883)
29. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, Takahashi T, Alitalo K, J Natl Cancer Inst 2002 94 819 825 10.1093/jnci/94.11.819 12048269 (Pubitemid 34705053)
30. Differential in vivo and in vitro expression of vascular endothelial growth factor (VEGF)-C and VEGF-D in tumors and its relationship to lymphatic metastasis in immunocompetent rats. Krishnan J, Kirkin V, Steffen A, Hegen M, Weih D, Tomarev S, Wilting J, Sleeman JP, Cancer Res 2003 63 713 722 12566318 (Pubitemid 36158152)
31. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Lin J, Lalani AS, Harding TC, Gonzalez M, Wu WW, Luan B, Tu GH, Koprivnikar K, VanRoey MJ, He Y, Alitalo K, Jooss K, Cancer Res 2005 65 6901 6909 10.1158/0008-5472.CAN-05- 0408 16061674 (Pubitemid 41060729)
32. Down-regulation of vascular endothelial cell growth factor-C expression using small interfering RNA vectors in mammary tumors inhibits tumor lymphangiogenesis and spontaneous metastasis and enhances survival. Chen Z, Varney ML, Backora MW, Cowan K, Solheim JC, Talmadge JE, Singh RK, Cancer Res 2005 65 9004 9011 10.1158/0008-5472.CAN-05-0885 16204074 (Pubitemid 41377392)
33. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, Yla-Herttuala S, Harding T, Jooss K, Takahashi T, Alitalo K, Cancer Res 2005 65 4739 4746 10.1158/0008-5472.CAN-04-4576 15930292 (Pubitemid 40740810)
34. Suppression of prostate cancer nodal and systemic metastasis by blockade of the lymphangiogenic axis. Burton JB, Priceman SJ, Sung JL, Brakenhielm E, An DS, Pytowski B, Alitalo K, Wu L, Cancer Res 2008 68 7828 7837 10.1158/0008-5472.CAN-08-1488 18829538
35. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Roberts N, Kloos B, Cassella M, Podgrabinska S, Persaud K, Wu Y, Pytowski B, Skobe M, Cancer Res 2006 66 2650 2657 10.1158/0008-5472.CAN-05-1843 16510584
36. Targeting lymphangiogenesis to prevent tumour metastasis. Achen MG, Mann GB, Stacker SA, Br J Cancer 2006 94 1355 1360 10.1038/sj.bjc.6603120 16641900 (Pubitemid 43772266)
37. Interaction of tumor cells and lymphatic vessels in cancer progression. Alitalo A, Detmar M, Oncogene 2012 31 4499 4508 10.1038/onc.2011.602 22179834
38. The human cutaneous squamous cell carcinoma microenvironment is characterized by increased lymphatic density and enhanced expression of macrophage-derived VEGF-C. Moussai D, Mitsui H, Pettersen JS, Pierson KC, Shah KR, Suarez-Farinas M, Cardinale IR, Bluth MJ, Krueger JG, Carucci JA, J Investig Dermatol 2011 131 229 236 10.1038/jid.2010.266 20827282
39. Soluble vascular endothelial growth factor receptor-3 suppresses lymphangiogenesis and lymphatic metastasis in bladder cancer. Yang H, Kim C, Kim MJ, Schwendener RA, Alitalo K, Heston W, Kim I, Kim WJ, Koh GY, Mol Cancer 2011 10 36 10.1186/1476-4598-10-36 21481239
40. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D, Breitman M, Alitalo K, Proc Natl Acad Sci U S A 1995 92 3566 3570 10.1073/pnas.92.8.3566 7724599
41. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M, Blood 2007 109 1010 1017 17032920 (Pubitemid 46220646)
42. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T, Cell 1999 96 795 806 10.1016/S0092-8674(00)80590-5 10102268 (Pubitemid 29165083)
43. Structural insights into the Slit-Robo complex. Morlot C, Thielens NM, Ravelli RB, Hemrika W, Romijn RA, Gros P, Cusack S, McCarthy AA, Proc Natl Acad Sci U S A 2007 104 14923 14928 10.1073/pnas.0705310104 17848514 (Pubitemid 47619569)
44. Identification and characterization of roundabout orthologs in zebrafish. Challa AK, Beattie CE, Seeger MA, Mech Dev 2001 101 249 253 10.1016/S0925-4773(00)00570-0 11231085 (Pubitemid 32186336)
45. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R, Genomics 2002 79 547 552 10.1006/geno.2002.6745 11944987 (Pubitemid 34274296)
46. Structural insight into Slit-Robo signalling. Hohenester E, Biochem Soc Trans 2008 36 251 256 10.1042/BST0360251 18363568 (Pubitemid 351570597)
47. Cloning and expression of three zebrafish roundabout homologs suggest roles in axon guidance and cell migration. Lee JS, Ray R, Chien CB, Dev Dyn 2001 221 216 230 10.1002/dvdy.1136 11376489 (Pubitemid 32476570)
48. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Park KW, Morrison CM, Sorensen LK, Jones CA, Rao Y, Chien CB, Wu JY, Urness LD, Li DY, Dev Biol 2003 261 251 267 10.1016/S0012-1606(03)00258-6 12941633 (Pubitemid 36993830)
49. Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. Nguyen Ba-Charvet KT, Brose K, Ma L, Wang KH, Marillat V, Sotelo C, Tessier-Lavigne M, Chedotal A, J Neurosci 2001 21 4281 4289 11404413 (Pubitemid 32538553)
50. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS, Henzel W, Tessier-Lavigne M, Cell 1999 96 771 784 10.1016/S0092-8674(00)80588-7 10102266 (Pubitemid 29165081)
51. Moving away from the midline: new developments for Slit and Robo. Ypsilanti AR, Zagar Y, Chedotal A, Development 2010 137 1939 1952 10.1242/dev.044511 20501589
52. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Jones CA, Nishiya N, London NR, Zhu W, Sorensen LK, Chan AC, Lim CJ, Chen H, Zhang Q, Schultz PG, Hayallah AM, Thomas KR, Famulok M, Zhang K, Ginsberg MH, Li DY, Nat Cell Biol 2009 11 1325 1331 10.1038/ncb1976 19855388
53. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Jones CA, London NR, Chen H, Park KW, Sauvaget D, Stockton RA, Wythe JD, Suh W, Larrieu-Lahargue F, Mukouyama YS, Lindblom P, Seth P, Frias A, Nishiya N, Ginsberg MH, Gerhardt H, Zhang K, Li DY, Nat Med 2008 14 448 453 10.1038/nm1742 18345009 (Pubitemid 351499393)
54. Robo4 counteracts VEGF signaling. Acevedo LM, Weis SM, Cheresh DA, Nat Med 2008 14 372 373 10.1038/nm0408-372 18391935 (Pubitemid 351499382)
55. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Wang B, Xiao Y, Ding BB, Zhang N, Yuan X, Gui L, Qian KX, Duan S, Chen Z, Rao Y, Geng JG, Cancer Cell 2003 4 19 29 10.1016/S1535-6108(03)00164-8 12892710 (Pubitemid 36904158)
56. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Yang XM, Han HX, Sui F, Dai YM, Chen M, Geng JG, Biochem Biophys Res Commun 2010 396 571 577 10.1016/j.bbrc.2010.04.152 20438712
57. MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the Robo1 receptor. Tie J, Pan Y, Zhao L, Wu K, Liu J, Sun S, Guo X, Wang B, Gang Y, Zhang Y, Li Q, Qiao T, Zhao Q, Nie Y, Fan D, PLoS Genet 2010 6 1000879 10.1371/journal.pgen.1000879 20300657
58. The fungicide ciclopirox inhibits lymphatic endothelial cell tube formation by suppressing VEGFR-3-mediated ERK signaling pathway. Luo Y, Zhou H, Liu L, Shen T, Chen W, Xu B, Han X, Zhang F, Scott RS, Alexander JS, Alam A, Huang S, Oncogene 2011 30 2098 2107 10.1038/onc.2010.590 21217783
59. Vascular endothelial growth factor receptor-3 directly interacts with phosphatidylinositol 3-kinase to regulate lymphangiogenesis. Coso S, Zeng Y, Opeskin K, Williams ED, PLoS One 2012 7 39558 10.1371/journal.pone.0039558 22745786
60. Effective suppression of vascular network formation by combination of antibodies blocking VEGFR ligand binding and receptor dimerization. Tvorogov D, Anisimov A, Zheng W, Leppanen VM, Tammela T, Laurinavicius S, Holnthoner W, Helotera H, Holopainen T, Jeltsch M, Kalkkinen N, Lankinen H, Ojala PM, Alitalo K, Cancer Cell 2010 18 630 640 10.1016/j.ccr.2010.11.001 21130043
61. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. Karpanen T, Heckman CA, Keskitalo S, Jeltsch M, Ollila H, Neufeld G, Tamagnone L, Alitalo K, FASEB J 2006 20 1462 1472 10.1096/fj.05-5646com 16816121 (Pubitemid 44943854)
62. Blocking neuropilin-2 function inhibits tumor cell metastasis. Caunt M, Mak J, Liang WC, Stawicki S, Pan Q, Tong RK, Kowalski J, Ho C, Reslan HB, Ross J, Berry L, Kasman I, Zlot C, Cheng Z, Le Couter J, Filvaroff EH, Plowman G, Peale F, French D, Carano R, Koch AW, Wu Y, Watts RJ, Tessier-Lavigne M, Bagri A, Cancer Cell 2008 13 331 342 10.1016/j.ccr.2008.01.029 18394556 (Pubitemid 351446192)
63. Signal transduction by vascular endothelial growth factor receptors. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L, Biochem J 2011 437 169 183 10.1042/BJ20110301 21711246
64. Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. Dixelius J, Makinen T, Wirzenius M, Karkkainen MJ, Wernstedt C, Alitalo K, Claesson-Welsh L, J Biol Chem 2003 278 40973 40979 10.1074/jbc.M304499200 12881528 (Pubitemid 37280919)
65. Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. Zhang X, Groopman JE, Wang JF, J Cell Physiol 2005 202 205 214 10.1002/jcp.20106 15389531 (Pubitemid 39603377)
66. Magic roundabout, a tumor endothelial marker: expression and signaling. Seth P, Lin Y, Hanai J, Shivalingappa V, Duyao MP, Sukhatme VP, Biochem Biophys Res Commun 2005 332 533 541 10.1016/j.bbrc.2005.03.250 15894287 (Pubitemid 40725009)
67. Molecular regulation of angiogenesis and lymphangiogenesis. Adams RH, Alitalo K, Nat Rev Mol Cell Biol 2007 8 464 478 10.1038/nrm2183 17522591 (Pubitemid 46823443)
68. Angiocrine factors modulate tumor proliferation and motility through EphA2 repression of Slit2 tumor suppressor function in endothelium. Brantley-Sieders DM, Dunaway CM, Rao M, Short S, Hwang Y, Gao Y, Li D, Jiang A, Shyr Y, Wu JY, Chen J, Cancer Res 2011 71 976 987 10.1158/0008-5472.CAN-10-3396 21148069
69. Slit-2 facilitates interaction of P-cadherin with Robo-3 and inhibits cell migration in an oral squamous cell carcinoma cell line. Bauer K, Dowejko A, Bosserhoff AK, Reichert TE, Bauer R, Carcinogenesis 2011 32 935 943 10.1093/carcin/bgr059 21459757
70. Slit-2 induces a tumor-suppressive effect by regulating beta-catenin in breast cancer cells. Prasad A, Paruchuri V, Preet A, Latif F, Ganju RK, J Biol Chem 2008 283 26624 26633 10.1074/jbc.M800679200 18611862
71. SLIT2 attenuation during lung cancer progression deregulates beta-catenin and E-cadherin and associates with poor prognosis. Tseng RC, Lee SH, Hsu HS, Chen BH, Tsai WC, Tzao C, Wang YC, Cancer Res 2010 70 543 551 10.1158/0008-5472.CAN-09-2084 20068157
72. Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Yiin JJ, Hu B, Jarzynka MJ, Feng H, Liu KW, Wu JY, Ma HI, Cheng SY, Neuro Oncol 2009 11 779 789 10.1215/15228517-2009-017 20008733
73. SLITs suppress tumor growth in vivo by silencing Sdf1/Cxcr4 within breast epithelium. Marlow R, Strickland P, Lee JS, Wu X, Pebenito M, Binnewies M, Le EK, Moran A, Macias H, Cardiff RD, Sukumar S, Hinck L, Cancer Res 2008 68 7819 7827 10.1158/0008-5472.CAN-08-1357 18829537
74. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E, J Cell Biol 2006 174 593 604 10.1083/jcb.200602080 16893970 (Pubitemid 44231870)
75. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Le Roy C, Wrana JL, Nat Rev Mol Cell Biol 2005 6 112 126 10.1038/nrm1571 15687999 (Pubitemid 40215807)
76. Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Sawamiphak S, Seidel S, Essmann CL, Wilkinson GA, Pitulescu ME, Acker T, Acker-Palmer A, Nature 2010 465 487 491 10.1038/nature08995 20445540
77. Slit2N/Robo1 inhibit HIV-gp120-induced migration and podosome formation in immature dendritic cells by sequestering LSP1 and WASp. Prasad A, Kuzontkoski PM, Shrivastava A, Zhu W, Li DY, Groopman JE, PLoS One 2012 7 48854 10.1371/journal.pone.0048854 23119100
78. Slit2-N inhibits PDGF-induced migration in rat airway smooth muscle cells: WASP and Arp2/3 involved. Ning Y, Sun Q, Dong Y, Xu W, Zhang W, Huang H, Li Q, Toxicology 2011 283 32 40 10.1016/j.tox.2011.01.026 21315131
79. Robo4-dependent Slit signaling stabilizes the vasculature during pathologic angiogenesis and cytokine storm. London NR, Li DY, Curr Opin Hematol 2011 18 186 190 10.1097/MOH.0b013e328345a4b9 21423011
80. ARF proteins: roles in membrane traffic and beyond. D'Souza-Schorey C, Chavrier P, Nat Rev Mol Cell Biol 2006 7 347 358 10.1038/nrm1910 16633337
81. N-terminal Slit2 inhibits HIV-1 replication by regulating the actin cytoskeleton. Anand AR, Zhao H, Nagaraja T, Robinson LA, Ganju RK, Retrovirology 2013 10 2 10.1186/1742-4690-10-2 23294842
82. Slit2/Robo4 signaling modulates HIV-1 gp120-induced lymphatic hyperpermeability. Zhang X, Yu J, Kuzontkoski PM, Zhu W, Li DY, Groopman JE, PLoS Pathog 2012 8 1002461 10.1371/journal.ppat.1002461 22241990
83. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. Suchting S, Heal P, Tahtis K, Stewart LM, Bicknell R, FASEB J 2005 19 121 123 15486058 (Pubitemid 40069938)
84. Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. Wang JF, Zhang XF, Groopman JE, J Biol Chem 2001 276 41950 41957 10.1074/jbc.M101370200 11553610 (Pubitemid 37371095)