Nitric oxide causes macrophage migration via the HIF-1-stimulated small GTPases Cdc42 and Rac1

Free Radical Biology and Medicine

Volumn 47, Issue 6, 2009, Pages 741-749

  Zhou, Jie ^a   Dehne, Nathalie ^a   Brüne, Bernhard ^a  

^a Institute of Biochemistry I   (Germany)

Author keywords

Actin; Free radicals; Hypoxia; iNOS; Small GTPases

Indexed keywords

ACTIN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEIN CDC42; RAC1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL LINE; CELL MOVEMENT; CYTOSKELETON; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RAC1 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

MUS;

EID: 68349144691     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.06.006     Document Type: Article

References (44)

1. Semenza G.L. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 19 (2004) 176-182
2. Weidemann A., and Johnson R. S. Biology of HIF-1alpha. Cell Death Differ. 15 (2008) 621-627
3. Kaelin Jr. W.G., and Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30 (2008) 393-402
4. Zhou J., Callapina M., Goodall G.J., and Brüne B. Functional integrity of nuclear factor kappaB, phosphatidylinositol 3′-kinase, and mitogen-activated protein kinase signaling allows tumor necrosis factor alpha-evoked Bcl-2 expression to provoke internal ribosome entry site-dependent translation of hypoxia-inducible factor 1alpha. Cancer Res. 64 (2004) 9041-9048
5. Page E.L., Robitaille G.A., Pouyssegur J., and Richard D.E. Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J. Biol. Chem. 277 (2002) 48403-48409
6. Zhou J., and Brüne B. Cytokines and hormones in the regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Cardiovasc. Hematol. Agents Med. Chem. 4 (2006) 189-197
7. Brüne B., and Zhou J. The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr. Med. Chem. 10 (2003) 845-855
8. Semenza G.L. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 71-103
9. Semenza G.L. HIF-1 and human disease: one highly involved factor. Genes Dev. 14 (2000) 1983-1991
10. Moser C., Lang S.A., Mori A., Hellerbrand C., Schlitt H.J., Geissler E.K., Fogler W.E., and Stoeltzing O. ENMD-1198, a novel tubulin-binding agent reduces HIF-1alpha and STAT3 activity in human hepatocellular carcinoma (HCC) cells, and inhibits growth and vascularization in vivo. BMC Cancer 8 (2008) 206-215
11. Sahlgren C., Gustafsson M.V., Jin S., Poellinger L., and Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl. Acad. Sci. USA 105 (2008) 6392-6397
12. Wang X., Li C., Chen Y., Hao Y., Zhou W., Chen C., and Yu Z. Hypoxia enhances CXCR4 expression favoring microglia migration via HIF-1alpha activation. Biochem. Biophys. Res. Commun. 371 (2008) 283-288
13. Osada-Oka M., Ikeda T., Akiba S., and Sato T. Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1alpha-dependent expression of thrombospondin-1. J. Cell. Biochem. 104 (2008) 1918-1926
14. Murdoch C., Giannoudis A., and Lewis C.E. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 104 (2004) 2224-2234
15. Balkwill F., and Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 357 (2001) 539-545
16. Kelly P.M., Davison R.S., Bliss E., and McGee J.O. Macrophages in human breast disease: a quantitative immunohistochemical study. Br. J. Cancer 57 (1988) 174-177
17. Leek R.D., Harris A.L., and Lewis C.E. Cytokine networks in solid human tumors: regulation of angiogenesis. J. Leukocyte Biol. 56 (1994) 423-435
18. Yamashiro S., Takeya M., Nishi T., Kuratsu J., Yoshimura T., Ushio Y., and Takahashi K. Tumor-derived monocyte chemoattractant protein-1 induces intratumoral infiltration of monocyte-derived macrophage subpopulation in transplanted rat tumors. Am. J. Pathol. 145 (1994) 856-867
19. Murdoch C., and Lewis C.E. Macrophage migration and gene expression in response to tumor hypoxia. Int. J. Cancer 117 (2005) 701-708
20. Jones G.E. Cellular signaling in macrophage migration and chemotaxis. J. Leukocyte Biol. 68 (2000) 593-602
21. Allen W.E., Jones G.E., Pollard J.W., and Ridley A.J. Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell. Sci. 110 Pt. 6 (1997) 707-720
22. Magazine H.I., Chang J., Goumon Y., and Stefano G.B. Rebound from nitric oxide inhibition triggers enhanced monocyte activation and chemotaxis. J. Immunol. 165 (2000) 102-107
23. Johann A.M., Barra V., Kuhn A.M., Weigert A., von Knethen A., and Brune B. Apoptotic cells induce arginase II in macrophages, thereby attenuating NO production. FASEB J. 21 (2007) 2704-2712
24. Metzen E., Zhou J., Jelkmann W., Fandrey J., and Brüne B. Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol. Biol. Cell 14 (2003) 3470-3481
25. Kasuno K., Takabuchi S., Fukuda K., Kizaka-Kondoh S., Yodoi J., Adachi T., Semenza G.L., and Hirota K. Nitric oxide induces hypoxia-inducible factor 1 activation that is dependent on MAPK and phosphatidylinositol 3-kinase signaling. J. Biol. Chem. 279 (2004) 2550-2558
26. Li F., Sonveaux P., Rabbani Z.N., Liu S., Yan B., Huang Q., Vujaskovic Z., Dewhirst M.W., and Li C.Y. Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell 26 (2007) 63-74
27. Sumbayev V.V., Budde A., Zhou J., and Brüne B. HIF-1alpha protein as a target for S-nitrosation. FEBS Lett. 535 (2003) 106-112
28. Brennan P.A., and Quintero M. Regulation of hypoxia-inducible factor 1 (HIF-1) by nitric oxide in oral squamous cell carcinoma. Ann. R. Coll. Surg. Engl. 87 (2005) 153-158
29. Peyssonnaux C., Datta V., Cramer T., Doedens A., Theodorakis E.A., Gallo R.L., Hurtado-Ziola N., Nizet V., and Johnson R.S. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 115 (2005) 1806-1815
30. Bosco M.C., Puppo M., Blengio F., Fraone T., Cappello P., Giovarelli M., and Varesio L. Monocytes and dendritic cells in a hypoxic environment: spotlights on chemotaxis and migration. Immunobiology 213 (2008) 733-749
31. Lewis J.S., Landers R.J., Underwood J.C., Harris A.L., and Lewis C.E. Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J. Pathol. 192 (2000) 150-158
32. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., and Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13 (2008) 206-220
33. Cramer T., Yamanishi Y., Clausen B.E., Forster I., Pawlinski R., Mackman N., Haase V.H., Jaenisch R., Corr M., Nizet V., Firestein G.S., Gerber H.P., Ferrara N., and Johnson R.S. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112 (2003) 645-657
34. Bosco M.C., Puppo M., Santangelo C., Anfosso L., Pfeffer U., Fardin P., Battaglia F., and Varesio L. Hypoxia modifies the transcriptome of primary human monocytes: modulation of novel immune-related genes and identification of CC-chemokine ligand 20 as a new hypoxia-inducible gene. J. Immunol. 177 (2006) 1941-1955
35. Belenky S.N., Robbins R.A., and Rubinstein I. Nitric oxide synthase inhibitors attenuate human monocyte chemotaxis in vitro. J. Leukocyte Biol. 53 (1993) 498-503
36. Stefano G.B., Salzet M., Rialas C.M., Mattocks D., Fimiani C., and Bilfinger T.V. Macrophage behavior associated with acute and chronic exposure to HIV GP120, morphine and anandamide: endothelial implications. Int. J. Cardiol. 64 Suppl. 1 (1998) S3-13
37. Magazine H.I., Liu Y., Bilfinger T.V., Fricchione G.L., and Stefano G.B. Morphine-induced conformational changes in human monocytes, granulocytes, and endothelial cells and in invertebrate immunocytes and microglia are mediated by nitric oxide. J. Immunol. 156 (1996) 4845-4850
38. Srivastava K.D., and Magazine H.I. Thrombin receptor activation inhibits monocyte spreading by induction of ET(B) receptor-coupled nitric oxide release. J. Immunol. 161 (1998) 5039-5044
39. Bove P.F., Hristova M., Wesley U.V., Olson N., Lounsbury K.M., and van der Vliet A. Inflammatory levels of nitric oxide inhibit airway epithelial cell migration by inhibition of the kinase ERK1/2 and activation of hypoxia-inducible factor-1 alpha. J. Biol. Chem. 283 (2008) 17919-17928
40. Bove P.F., Wesley U.V., Greul A.K., Hristova M., Dostmann W.R., and van der Vliet A. Nitric oxide promotes airway epithelial wound repair through enhanced activation of MMP-9. Am. J. Respir. Cell Mol. Biol. 36 (2007) 138-146
41. Maa M.C., Chang M.Y., Chen Y.J., Lin C.H., Yu C.J., Yang Y.L., Li J., Chen P.R., Tang C.H., Lei H.Y., and Leu T.H. Requirement of inducible nitric-oxide synthase in lipopolysaccharide-mediated Src induction and macrophage migration. J. Biol. Chem. 283 (2008) 31408-31416
42. Turcotte S., Desrosiers R.R., and Beliveau R. HIF-1alpha mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J. Cell. Sci. 116 (2003) 2247-2260
43. Hirota K., and Semenza G.L. Rac1 activity is required for the activation of hypoxia-inducible factor 1. J. Biol. Chem. 276 (2001) 21166-21172
44. Xue Y., Bi F., Zhang X., Zhang S., Pan Y., Liu N., Shi Y., Yao X., Zheng Y., and Fan D. Role of Rac1 and Cdc42 in hypoxia induced p53 and von Hippel-Lindau suppression and HIF1alpha activation. Int. J. Cancer 118 (2006) 2965-2972