The supernatant of apoptotic cells causes transcriptional activation of hypoxia-inducible factor-1α in macrophages via sphingosine-1-phosphate and transforming growth factor-β

Blood

Volumn 114, Issue 10, 2009, Pages 2140-2148

  Herr, Barbara ^a   Zhou, Jie ^a   Werno, Christian ^a   Menrad, Heidi ^a   Namgaladze, Dmitry ^a   Weigert, Andreas ^a   Dehne, Nathalie ^a   Brüne, Bernhard ^a  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CD31 ANTIGEN; CYCLOSPORIN A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; NEUTRALIZING ANTIBODY; SPHINGOSINE 1 PHOSPHATE; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; CYCLOSPORIN; DRUG DERIVATIVE; HIF1A PROTEIN, HUMAN; HIF1A PROTEIN, MOUSE; IMMUNOSUPPRESSIVE AGENT; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; TRANSCRIPTION FACTOR NFAT; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; EMBRYO; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR CELL; UPREGULATION; ANIMAL; BIOSYNTHESIS; CULTURE MEDIUM; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; LEUKEMIA CELL LINE; METABOLISM; MOUSE MUTANT; NEOPLASM; PATHOLOGY;

ANIMALS; ANTIGENS, CD31; APOPTOSIS; CALCINEURIN; CULTURE MEDIA, CONDITIONED; CYCLOSPORINE; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOSUPPRESSIVE AGENTS; JURKAT CELLS; LYSOPHOSPHOLIPIDS; MACROPHAGES; MICE; MICE, KNOCKOUT; NEOPLASMS; NFATC TRANSCRIPTION FACTORS; RNA, MESSENGER; SPHINGOSINE; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70349246856     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-01-201889     Document Type: Article

References (49)

1. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605-612. (Pubitemid 43165918)
2. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677-686. (Pubitemid 39457982)
3. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8:958-969.
4. ChenW, Frank ME, JinW,Wahl SM. TGF-β released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity. 2001;14:715-725.
5. Tomimori Y, Ikawa Y, Oyaizu N. Ultraviolet-irradiated apoptotic lymphocytes produce interleukin-10 by themselves. Immunol Lett. 2000;71:49-54. (Pubitemid 30068611)
6. Reiter I, Krammer B, Schwamberger G. Cutting edge: differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J Immunol. 1999;163:1730-1732. (Pubitemid 29382166)
7. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol. 2002;2:965-975. (Pubitemid 37323217)
8. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-β, PGE2, and PAF. J Clin Invest. 1998;101:890-898. (Pubitemid 28096086)
9. Weigert A, Johann AM, von Knethen A, Schmidt H, Geisslinger G, Brune B. Apoptotic cells promote macrophage survival by releasing the antiapoptotic mediator sphingosine-1-phosphate. Blood. 2006;108:1635-1642. (Pubitemid 44316132)
10. Freire-de-Lima CG, Xiao YQ, Gardai SJ, Bratton DL, Schiemann WP, Henson PM. Apoptotic cells, through transforming growth factor-β, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem. 2006;281: 38376-38384.
11. Mantovani A, Allavena P, Sica A. Tumorassociated macrophages as a prototypic type II polarized phagocyte population: role in tumor progression. Eur J Cancer. 2004;40:1660-1667. (Pubitemid 38902900)
12. Johann AM, Barra V, Kuhn AM, Weigert A, von Knethen A, Brune B. Apoptotic cells induce arginase II in macrophages, thereby attenuating NO production. FASEB J. 2007;21:2704-2712. (Pubitemid 47372738)
13. Weigert A, Tzieply N, von Knethen A, et al. Tumor cell apoptosis polarizes macrophages role of sphingosine-1-phosphate. Mol Biol Cell. 2007;18: 3810-3819. (Pubitemid 47519475)
14. Hughes JE, Srinivasan S, Lynch KR, Proia RL, Ferdek P, Hedrick CC. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res. 2008;102:950-958. (Pubitemid 351591554)
15. Gude DR, Alvarez SE, Paugh SW, et al. Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a "come-and-getme" signal. FASEB J. 2008;22:2629-2638.
16. Taha TA, Argraves KM, Obeid LM. Sphingosine- 1-phosphate receptors: receptor specificity versus functional redundancy. Biochim Biophys Acta. 2004;1682:48-55. (Pubitemid 38670534)
17. von Wenckstern H, Zimmermann K, Kleuser B. The role of the lysophospholipid sphingosine 1-phosphate in immune cell biology. Arch Immunol Ther Exp. 2006;54:239-251. (Pubitemid 44231830)
18. Lee MJ, Thangada S, Claffey KP, et al. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1- phosphate. Cell. 1999;99:301-312. (Pubitemid 29519909)
19. Liu Y, Wada R, Yamashita T, et al. Edg-1, the G protein-coupled receptor for sphingosine-1- phosphate, is essential for vascular maturation. J Clin Invest. 2000;106:951-961. (Pubitemid 30800853)
20. Rankin EB, Giaccia AJ. The role of hypoxiainducible factors in tumorigenesis. Cell Death Differ. 2008;15:678-685.
21. Semenza GL. Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life. 2008;60:591-597.
22. Frede S, Stockmann C, Freitag P, Fandrey J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-κB. Biochem J. 2006;396:517-527. (Pubitemid 44228166)
23. Walczak-Drzewiecka A, Ratajewski M, Wagner W, Dastych J. HIF-1α is up-regulated in activated mast cells by a process that involves calcineurin and NFAT. J Immunol. 2008;181:1665-1672.
24. Niu G, Briggs J, Deng J, et al. Signal transducer and activator of transcription 3 is required for hypoxia-inducible factor-1α RNA expression in both tumor cells and tumor-associated myeloid cells. Mol Cancer Res. 2008;6:1099-1105.
25. Zhou J, Kohl R, Herr B, Frank R, Brune B. Calpain mediates a von Hippel-Lindau protein-independent destruction of hypoxia-inducible factor-1α. Mol Biol Cell. 2006;17:1549-1558. (Pubitemid 44011575)
26. Jennewein C, Kuhn AM, Schmidt MV, et al. Sumoylation of peroxisome proliferator-activated receptor γ by apoptotic cells prevents lipopoly-saccharide- induced NCoR removal from κB binding sites mediating transrepression of proinflammatory cytokines. J Immunol. 2008;181:5646-5652.
27. Robertson E, Bradley A, Kuehn M, Evans M. Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature. 1986;323:445-448. (Pubitemid 16026271)
28. Keller G, Kennedy M, Papayannopoulou T, Wiles MV. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol. 1993;13:473-486. (Pubitemid 23006925)
29. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645-657. (Pubitemid 36331777)
30. Johann AM, Weigert A, Eberhardt W, et al. Apoptotic cell-derived sphingosine-1-phosphate promotes HuR-dependent cyclooxygenase-2 mRNA stabilization and protein expression. J Immunol. 2008;180:1239-1248.
31. Yang J, Rothermel B, Vega RB, et al. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ Res. 2000;87:E61-E68.
32. Gray MJ, Zhang J, Ellis LM, et al. HIF-1α, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene. 2005;24:3110-3120. (Pubitemid 40695080)
33. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther. 2009;121: 29-40.
34. Hannig M, Figulla HR, Sauer H, Wartenberg M. Control of leukocyte differentiation from embryonic stem cells upon vasculogenesis and confrontation with tumor tissue. J Cell Mol Med. Pre-published on July 9, 2008, as DOI 10.1111/j.1582-4934.2008.00424.x.
35. Xin C, Ren S, Kleuser B, et al. Sphingosine 1-phosphate cross-activates the Smad signaling cascade and mimics transforming growth factor- β-induced cell responses. J Biol Chem. 2004; 279:35255-35262. (Pubitemid 39100522)
36. Ross S, Hill CS. How the Smads regulate transcription. Int J Biochem Cell Biol. 2008;40:383-408.
37. Lin EY, Li JF, Gnatovskiy L, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006;66:11238-11246. (Pubitemid 46009952)
38. Weis N,Weigert A, von Knethen A, Brune B. Heme oxygenase-1 contributes to an alternative macrophage activation profile induced by apoptotic cell supernatants. Mol Biol Cell. 2009;20:1280-1288.
39. Jakobsson L, Domogatskaya A, Tryggvason K, Edgar D, Claesson-Welsh L. Laminin deposition is dispensable for vasculogenesis but regulates blood vessel diameter independent of flow. FASEB J. 2008;22:1530-1539. (Pubitemid 351656793)
40. Zamboni DS, Rabinovitch M. Phagocytosis of apoptotic cells increases the susceptibility of macrophages to infection with Coxiella burnetii phase II through down-modulation of nitric oxide production. Infect Immun. 2004;72:2075-2080. (Pubitemid 38419920)
41. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell. 2005;7:211-217. (Pubitemid 40568680)
42. Visentin B, Vekich JA, Sibbald BJ, et al. Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell. 2006;9:225-238. (Pubitemid 43357948)
43. Serrati S, Margheri F, Pucci M, et al. TGFβ1 antagonistic peptides inhibit TGFβ1-dependent angiogenesis. Biochem Pharmacol. 2009;77:813-825.
44. Enholm B, Paavonen K, Ristimaki A, et al. Comparison of VEGF, VEGF-B, VEGF-C, and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene. 1997;14:2475-2483. (Pubitemid 27268166)
45. David KC, Scott RH, Nixon GF. Advanced glycation endproducts induce a proliferative response in vascular smooth muscle cells via altered calcium signaling. Biochem Pharmacol. 2008;76: 1110-1120.
46. Liu Q, Busby JC, Molkentin JD. Interaction between TAK1-TAB1-TAB2 and RCAN1-calcineurin defines a signalling nodal control point. Nat Cell Biol. 2009;11:154-161.
47. Lu H, Huan C. Transcription factor NFAT, its role in cancer development, and as a potential target for chemoprevention. Curr Cancer Drug Targets. 2007;7:343-353. (Pubitemid 46849239)
48. De Ponti C, Carini R, Alchera E, et al. Adenosine A2a receptor-mediated, normoxic induction of HIF-1 through PKC and PI-3K-dependent pathways in macrophages. J Leukocyte Biol. 2007;82: 392-402. (Pubitemid 47230651)
49. Zhong H, Willard M, Simons J. NS398 reduces hypoxia-inducible factor (HIF)-1α and HIF-1 activity: multiple-level effects involving cyclooxygenase- 2 dependent and independent mechanisms. Int J Cancer. 2004;112:585-595. (Pubitemid 39425938)