Slit2-Robo4 pathway modulates lipopolysaccharide-induced endothelial inflammation and its expression is dysregulated during endotoxemia

Journal of Immunology

Volumn 192, Issue 1, 2014, Pages 385-393

  Zhao, Helong ^a   Anand, Appakkudal R ^b   Ganju, Ramesh K ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b SASTRA UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI LIPOPOLYSACCHARIDE; FOCAL ADHESION KINASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MICRORNA; MICRORNA 218; PROTEIN ROBO4; ROUNDABOUT RECEPTOR; SLIT2 PROTEIN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; LIVER INJURY; MALE; MOLECULAR PATHOLOGY; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84891051959     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302021     Document Type: Article

References (42)

1. Ross, R. 1999. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340: 115-126.
2. Riedemann, N. C., R. F. Guo, and P. A. Ward. 2003. Novel strategies for the treatment of sepsis. Nat. Med. 9: 517-524.
3. Cohen, J. 2002. The immunopathogenesis of sepsis. Nature 420: 885-891.
4. Alexander, C., and E. T. Rietschel. 2001. Bacterial lipopolysaccharides and innate immunity. J. Endotoxin Res. 7: 167-202.
5. Hack, C. E., and S. Zeerleder. 2001. The endothelium in sepsis: source of and a target for inflammation. Crit. Care Med. 29(7, Suppl.)S21-S27.
6. Bierhaus, A., J. Chen, B. Liliensiek, and P. P. Nawroth. 2000. LPS and cytokineactivated endothelium. Semin. Thromb. Hemost. 26: 571-587.
7. Chédotal, A. 2007. Slits and their receptors. Adv. Exp. Med. Biol. 621: 65-80.
8. Fernandis, A. Z., and R. K. Ganju. 2001. Slit: a roadblock for chemotaxis. Sci. STKE 2001: pe1.
9. Nguyen Ba-Charvet, K. T., K. Brose, L. Ma, K. H. Wang, V. Marillat, C. Sotelo, M. Tessier-Lavigne, and A. Chédotal. 2001. Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. J. Neurosci. 21: 4281-4289.
10. Greenberg, J. M., F. Y. Thompson, S. K. Brooks, J. M. Shannon, and A. L. Akeson. 2004. Slit and robo expression in the developing mouse lung. Dev. Dyn. 230: 350-360.
11. Jones, C. A., N. R. London, H. Chen, K. W. Park, D. Sauvaget, R. A. Stockton, J. D. Wythe, W. Suh, F. Larrieu-Lahargue, Y. S. Mukouyama, et al. 2008. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 14: 448-453.
12. Sheldon, H., M. Andre, J. A. Legg, P. Heal, J. M. Herbert, R. Sainson, A. S. Sharma, J. K. Kitajewski, V. L. Heath, and R. Bicknell. 2009. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. FASEB J. 23: 513-522.
13. Zhang, X., J. Yu, P. M. Kuzontkoski, W. Zhu, D. Y. Li, and J. E. Groopman. 2012. Slit2/Robo4 signaling modulates HIV-1 gp120-induced lymphatic hyperpermeability. PLoS Pathog. 8: e1002461.
14. Niclou, S. P., L. Jia, and J. A. Raper. 2000. Slit2 is a repellent for retinal ganglion cell axons. J. Neurosci. 20: 4962-4974.
15. Fish, J. E., J. D.Wythe, T. Xiao, B. G. Bruneau, D. Y. Stainier, D. Srivastava, and S. Woo. 2011. A Slit/miR-218/Robo regulatory loop is required during heart tube formation in zebrafish. Development 138: 1409-1419.
16. Patel, S., Y. W. Huang, A. Reheman, F. G. Pluthero, S. Chaturvedi, I. M. Mukovozov, S. Tole, G. Y. Liu, L. Li, Y. Durocher, et al. 2012. The cell motility modulator Slit2 is a potent inhibitor of platelet function. Circulation 126: 1385-1395.
17. Dallol, A., N. F. Da Silva, P. Viacava, J. D. Minna, I. Bieche, E. R. Maher, and F. Latif. 2002. SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer Res. 62: 5874-5880.
18. Guan, H., G. Zu, Y. Xie, H. Tang, M. Johnson, X. Xu, C. Kevil, W. C. Xiong, C. Elmets, Y. Rao, et al. 2003. Neuronal repellent Slit2 inhibits dendritic cell migration and the development of immune responses. J. Immunol. 171: 6519-6526.
19. Liu, D., J. Hou, X. Hu, X. Wang, Y. Xiao, Y. Mou, and H. De Leon. 2006. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ. Res. 98: 480-489.
20. Jones, C. A., N. Nishiya, N. R. London, W. Zhu, L. K. Sorensen, A. C. Chan, C. J. Lim, H. Chen, Q. Zhang, P. G. Schultz, et al. 2009. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 11: 1325-1331.
21. Ye, B. Q., Z. H. Geng, L. Ma, and J. G. Geng. 2010. Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation. J. Immunol. 185: 6294-6305.
22. Anand, A. R., H. Zhao, T. Nagaraja, L. A. Robinson, and R. K. Ganju. 2013. N-terminal Slit2 inhibits HIV-1 replication by regulating the actin cytoskeleton. Retrovirology 10: 2.
23. Wang, L. J., Y. Zhao, B. Han, Y. G. Ma, J. Zhang, D. M. Yang, J. W. Mao, F. T. Tang, W. D. Li, Y. Yang, et al. 2008. Targeting Slit-Roundabout signaling inhibits tumor angiogenesis in chemical-induced squamous cell carcinogenesis. Cancer Sci. 99: 510-517.
24. London, N. R., W. Zhu, F. A. Bozza, M. C. Smith, D. M. Greif, L. K. Sorensen, L. Chen, Y. Kaminoh, A. C. Chan, S. F. Passi, et al. 2010. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci. Transl. Med. 2: 23ra19.
25. Wang, B., Y. Xiao, B. B. Ding, N. Zhang, Xb. Yuan, L. Gui, K. X. Qian, S. Duan, Z. Chen, Y. Rao, and J. G. Geng. 2003. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 4: 19-29.
26. Narayan, G., C. Goparaju, H. Arias-Pulido, A. M. Kaufmann, A. Schneider, M. Dürst, M. Mansukhani, B. Pothuri, and V. V. Murty. 2006. Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol. Cancer 5: 16.
27. Dong, R., J. Yu, H. Pu, Z. Zhang, and X. Xu. 2012. Frequent SLIT2 promoter methylation in the serum of patients with ovarian cancer. J. Int. Med. Res. 40: 681-686.
28. Dallol, A., E. Forgacs, A. Martinez, Y. Sekido, R. Walker, T. Kishida, P. Rabbitts, E. R. Maher, J. D. Minna, and F. Latif. 2002. Tumour specific promoter region methylation of the human homologue of the Drosophila Roundabout gene DUTT1 (ROBO1) in human cancers. Oncogene 21: 3020-3028.
29. Ning, Y., Q. Sun, Y. Dong, W. Xu, W. Zhang, H. Huang, and Q. Li. 2011. Slit2-N inhibits PDGF-induced migration in rat airway smooth muscle cells: WASP and Arp2/3 involved. Toxicology 283: 32-40.
30. Ambros, V. 2004. The functions of animal microRNAs. Nature 431: 350-355.
31. Calin, G. A., and C. M. Croce. 2006. MicroRNA signatures in human cancers. Nat. Rev. Cancer 6: 857-866.
32. Tili, E., J. J. Michaille, S. Costinean, and C. M. Croce. 2008. MicroRNAs, the immune system and rheumatic disease. Nat. Clin. Pract. Rheumatol. 4: 534-541.
33. Alajez, N. M., M. Lenarduzzi, E. Ito, A. B. Hui, W. Shi, J. Bruce, S. Yue, S. H. Huang, W. Xu, J. Waldron, et al. 2011. MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res. 71: 2381-2391.
34. Small, E. M., L. B. Sutherland, K. N. Rajagopalan, S. Wang, and E. N. Olson. 2010. MicroRNA-218 regulates vascular patterning by modulation of Slit-Robo signaling. Circ. Res. 107: 1336-1344.
35. Prasad, A., Z. Qamri, J. Wu, and R. K. Ganju. 2007. Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells. J. Leukoc. Biol. 82: 465-476.
36. Chen, S., M. Sega, and A. Agarwal. 2004. "Lumen digestion" technique for isolation of aortic endothelial cells from heme oxygenase-1 knockout mice. Biotechniques 37: 84-86, 88-89.
37. Nasser, M. W., Z. Qamri, Y. S. Deol, J. Ravi, C. A. Powell, P. Trikha, R. A. Schwendener, X. F. Bai, K. Shilo, X. Zou, et al. 2012. S100A7 enhances mammary tumorigenesis through upregulation of inflammatory pathways. Cancer Res. 72: 604-615.
38. Anand, A. R., R. Bradley, and R. K. Ganju. 2009. LPS-induced MCP-1 expression in human microvascular endothelial cells is mediated by the tyrosine kinase, Pyk2 via the p38 MAPK/NF-kappaB-dependent pathway. Mol. Immunol. 46: 962-968.
39. Anand, A. R., M. Cucchiarini, E. F. Terwilliger, and R. K. Ganju. 2008. The tyrosine kinase Pyk2 mediates lipopolysaccharide-induced IL-8 expression in human endothelial cells. J. Immunol. 180: 5636-5644.
40. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
41. Guo, S. W., Y. Zheng, Y. Lu, X. Liu, and J. G. Geng. 2012. Slit2 overexpression results in increased microvessel density and lesion size in mice with induced endometriosis. Reprod. Sci. 20: 285-298.
42. Tie, J., Y. Pan, L. Zhao, K. Wu, J. Liu, S. Sun, X. Guo, B. Wang, Y. Gang, Y. Zhang, et al. 2010. MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the Robo1 receptor. PLoS Genet. 6: e1000879.