Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation

Journal of Immunology

Volumn 185, Issue 10, 2010, Pages 6294-6305

  Ye, Bu Qing ^a   Geng, Zhen H ^b   Ma, Li ^b   Geng, Jian Guo ^b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EOSINOPHIL CHEMOTACTIC FACTOR; EOTAXIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; RECOMBINANT PROTEIN; ROBO1 PROTEIN; ROUNDABOUT RECEPTOR; SLIT ROBO GTPASE ACTIVATING PROTEIN 1; SLIT2 PROTEIN; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHUS MUCOSA; CELL INFILTRATION; CLARA CELL; CONTROLLED STUDY; ENZYME ACTIVATION; EOSINOPHIL; HUMAN; HUMAN CELL; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; BRONCHI; CHEMOTAXIS, LEUKOCYTE; EOSINOPHILS; FLUORESCENT ANTIBODY TECHNIQUE; GTPASE-ACTIVATING PROTEINS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEUTROPHILS; PNEUMONIA; PULMONARY ALVEOLI; RECEPTORS, IMMUNOLOGIC; RESPIRATORY HYPERSENSITIVITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 78650672144     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001648     Document Type: Article

References (57)

1. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301-314.
2. Wong, K., H. T. Park, J. Y. Wu, and Y. Rao. 2002. Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr. Opin. Genet. Dev. 12:583-591.
3. Laudanna, C., J. Y. Kim, G. Constantin, and E. Butcher. 2002. Rapid leukocyte integrin activation by chemokines. Immunol. Rev. 186:37-46.
4. Furie, B., and B. C. Furie. 1995. The molecular basis of platelet and endothelial cell interaction with neutrophils and monocytes: role of P-selectin and the P-selectin ligand, PSGL-1. Thromb. Haemost. 74:224-227.
5. Malech, H. L., R. K. Root, and J. I. Gallin. 1977. Structural analysis of human neutrophil migration. Centriole, microtubule, and microfilament orientation and function during chemotaxis. J. Cell Biol. 75:666-693.
6. Mishra, R. K., J. E. Scaife, Z. Harb, B. C. Gray, R. Djukanovic, and G. Dent. 2005. Differential dependence of eosinophil chemotactic responses on phosphoinositide 3-kinase (PI3K). Allergy 60:1204-1207.
7. Sallusto, F., and M. Baggiolini. 2008. Chemokines and leukocyte traffic. Nat. Immunol. 9:949-952.
8. Kidd, T., K. Brose, K. J. Mitchell, R. D. Fetter, M. Tessier-Lavigne, C. S. Goodman, and G. Tear. 1998. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92:205-215.
9. Brose, K., K. S. Bland, K. H. Wang, D. Arnott, W. Henzel, C. S. Goodman, M. Tessier-Lavigne, and T. Kidd. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795-806.
10. Li, H. S., J. H. Chen, W. Wu, T. Fagaly, L. Zhou, W. Yuan, S. Dupuis, Z. H. Jiang, W. Nash, C. Gick, et al. 1999. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96:807-818.
11. Wu, W., K. Wong, J. Chen, Z. Jiang, S. Dupuis, J. Y. Wu, and Y. Rao. 1999. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400:331-336.
12. Wu, J. Y., L. Feng, H. T. Park, N. Havlioglu, L. Wen, H. Tang, K. B. Bacon, Jiang Zh, Zhang Xc, and Y. Rao. 2001. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 410:948-952.
13. Kanellis, J., G. E. Garcia, P. Li, G. Parra, C. B. Wilson, Y. Rao, S. Han, C. W. Smith, R. J. Johnson, J. Y. Wu, and L. Feng. 2004. Modulation of inflammation by slit protein in vivo in experimental crescentic glomerulonephritis. Am. J. Pathol. 165:341-352.
14. 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.
15. 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.
16. Altay, T., B. McLaughlin, J. Y. Wu, T. S. Park, and J. M. Gidday. 2007. Slit modulates cerebrovascular inflammation and mediates neuroprotection against global cerebral ischemia. Exp. Neurol. 207:186-194.
17. Tole, S., I. M. Mukovozov, Y. W. Huang, M. A. O. Magalhaes, M. Yan, M. R. Crow, G. Y. Liu, C. X. Sun, Y. Durocher, M. Glogauer, and L. A. Robinson. 2009. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J. Leukoc. Biol. 86:1403-1415.
18. Wang, B., Y. Xiao, B.-B. Ding, N. Zhang, X.-B. 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.
19. 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.
20. Urbich, C., L. Rössig, D. Kaluza, M. Potente, J. N. Boeckel, A. Knau, F. Diehl, J.-G. Geng, W. K. Hofmann, A. M. Zeiher, and S. Dimmeler. 2009. HDAC5 is a repressor of angiogenesis and determines the angiogenic gene expression pattern of endothelial cells. Blood 113:5669-5679.
21. Zhang, B., U. M. Dietrich, J.-G. Geng, R. Bicknell, J. D. Esko, and L. Wang. 2009. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood 114:4300-4309.
22. Schmid, B. C., G. A. Rezniczek, G. Fabjani, T. Yoneda, S. Leodolter, and R. Zeillinger. 2007. The neuronal guidance cue Slit2 induces targeted migration and may play a role in brain metastasis of breast cancer cells. Breast Cancer Res. Treat. 106:333-342.
23. Mertsch, S., N. Schmitz, A. Jeibmann, J.-G. Geng, W. Paulus, and V. Senner. 2008. Slit2 involvement in glioma cell migration is mediated by Robo1 receptor. J. Neurooncol. 87:1-7.
24. Yuasa-Kawada, J., M. Kinoshita-Kawada, Y. Rao, and J. Y. Wu. 2009. Deubiquitinating enzyme USP33/VDU1 is required for Slit signaling in inhibiting breast cancer cell migration. Proc. Natl. Acad. Sci. USA 106:14530-14535.
25. Bashaw, G. J., T. Kidd, D. Murray, T. Pawson, and C. S. Goodman. 2000. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101:703-715.
26. Fritz, J. L., and M. F. A. Van Berkum. 2000. Calmodulin and son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS. Development 127:1991-2000.
27. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
28. Wong, K., X. R. Ren, Y. Z. Huang, Y. Xie, G. Liu, H. Saito, H. Tang, L. Wen, S. M. Brady-Kalnay, L. Mei, et al. 2001. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107:209-221.
29. Kölsch, V., P. G. Charest, and R. A. Firtel. 2008. The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121:551-559.
30. Ly, N. P., K. Komatsuzaki, I. P. Fraser, A. A. Tseng, P. Prodhan, K. J. Moore, and T. B. Kinane. 2005. Netrin-1 inhibits leukocyte migration in vitro and in vivo. Proc. Natl. Acad. Sci. USA 102:14729-14734.
31. Hjorthaug, H. S., and H. C. Aasheim. 2007. Ephrin-A1 stimulates migration of CD8+CCR7+ T lymphocytes. Eur. J. Immunol. 37:2326-2336.
32. Lee, N. A., M. P. McGarry, K. A. Larson, M. A. Horton, A. B. Kristensen, and J. J. Lee. 1997. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J. Immunol. 158:1332-1344.
33. Yang, X.-M., H.-X. Han, F. Sui, Y.-M. Dai, M. Chen, and J.-G. Geng. 2010. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem. Biophys. Res. Commun. 396:571-577.
34. Wang, H.-B., J.-T. Wang, L. Zhang, Z. H. Geng, W.-L. Xu, T. Xu, Y. Huo, X. Zhu, E. F. Plow, M. Chen, and J.-G. Geng. 2007. P-selectin primes leukocyte integrin activation during inflammation. Nat. Immunol. 8:882-892.
35. Nguyen-Ba-Charvet, K. T., and A. Chédotal. 2002. Role of Slit proteins in the vertebrate brain. J. Physiol. Paris 96:91-98.
36. Baumann, M. A., and C. C. Paul. 1998. The AML14 and AML14.3D10 cell lines: a long-overdue model for the study of eosinophils and more. Stem Cells 16:16-24.
37. Boxio, R., C. Bossenmeyer-Pourié, N. Steinckwich, C. Dournon, and O. Nüsse. 2004. Mouse bone marrow contains large numbers of functionally competent neutrophils. J. Leukoc. Biol. 75:604-611.
38. Reynolds, S. D., and A. M. Malkinson. 2010. Clara cell: progenitor for the bronchiolar epithelium. Int. J. Biochem. Cell Biol. 42:1-4.
39. Terakawa, M., Y. Tomimori, M. Goto, and Y. Fukuda. 2006. Mast cell chymase induces expression of chemokines for neutrophils in eosinophilic EoL-1 cells and mouse peritonitis eosinophils. Eur. J. Pharmacol. 538:175-181.
40. Li, X., Y. Chen, Y. Liu, J. Gao, F. Gao, M. Bartlam, J. Y. Wu, and Z. Rao. 2006. Structural basis of Robo proline-rich motif recognition by the srGAP1 Src homology 3 domain in the Slit-Robo signaling pathway. J. Biol. Chem. 281:28430-28437.
41. Heit, B., L. X. Liu, P. Colarusso, K. D. Puri, and P. Kubes. 2008. PI3K accelerates, but is not required for, neutrophil chemotaxis to fMLP. J. Cell Sci. 121:205-214.
42. Ebihara, S., H. Kurachi, and Y. Watanabe. 2007. A simple preparation method for mouse eosinophils and their responses to anti-allergic drugs. Inflamm. Res. 56:112-117.
43. 62 of p50. J. Immunol. 173:4207-4217.
44. Arndt, P. G., S. K. Young, J. G. Lieber, M. B. Fessler, J. A. Nick, and G. S. Worthen. 2005. Inhibition of c-Jun. N-terminal kinase limits lipopolysaccharide-induced pulmonary neutrophil influx. Am. J. Respir. Crit. Care Med. 171:978-986.
45. Wang, Z. L., X. H. Wu, L. F. Song, Y. S. Wang, X. H. Hu, Y. F. Luo, Z. Z. Chen, J. Ke, X. D. Peng, C. M. He, et al. 2009. Phosphoinositide 3-kinase γ inhibitor ameliorates concanavalin A-induced hepatic injury in mice. Biochem. Biophys. Res. Commun. 386:569-574.
46. Oez, S., E. Platzer, and K. Welte. 1990. Aquantitative colorimetric methodtoevaluate the functional state of human polymorphonuclear leukocytes. Blut 60:97-102.
47. Anselmo, M. A., S. Dalvin, P. Prodhan, K. Komatsuzaki, J. T. Aidlen, J. J. Schnitzer, J. Y. Wu, and T. B. Kinane. 2003. Slit and robo: expression patterns in lung development. Gene Expr. Patterns 3:13-19.
48. 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.
49. Plump, A. S., L. Erskine, C. Sabatier, K. Brose, C. J. Epstein, C. S. Goodman, C. A. Mason, and M. Tessier-Lavigne. 2002. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33:219-232.
50. Sawamoto, K., H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, et al. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629-632.
51. Hu, H. 2001. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 4:695-701.
52. Borchers, M. T., T. Ansay, R. DeSalle, B. L. Daugherty, H. Shen, M. Metzger, N. A. Lee, and J. J. Lee. 2002. In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J. Leukoc. Biol. 71:1033-1041.
53. Dent, L. A., G. H. Munro, K. P. Piper, C. J. Sanderson, D. A. Finlay, R. K. Dempster, L. P. Bignold, D. G. Harkin, and P. Hagan. 1997. Eosinophilic interleukin 5 (IL-5) transgenic mice: eosinophil activity and impaired clearance of Schistosoma mansoni. Parasite Immunol. 19:291-300.
54. McKinley, L., J. Kim, G. L. Bolgos, J. Siddiqui, and D. G. Remick. 2005. CXC chemokines modulate IgE secretion and pulmonary inflammation in a model of allergic asthma. Cytokine 32:178-185.
55. Monteseirín, J. 2009. Neutrophils and asthma. J. Investig. Allergol. Clin. Immunol. 19:340-354.
56. John, A. E., Y. M. Zhu, C. E. Brightling, L. Pang, and A. J. Knox. 2009. Human airway smooth muscle cells from asthmatic individuals have CXCL8 hypersecretion due to increased NF-κ B p65, C/EBP β, and RNA polymerase II binding to the CXCL8 promoter. J. Immunol. 183:4682-4692.
57. Coward, W. R., H. Sagara, S. J. Wilson, S. T. Holgate, and M. K. Church. 2004. Allergen activates peripheral blood eosinophil nuclear factor-kappaB to generate granulocyte macrophage-colony stimulating factor, tumour necrosis factor-a and interleukin-8. Clin. Exp. Allergy 34:1071-1078.