Neutrophils responsive to endogenous IFN-β regulate tumor angiogenesis and growth in a mouse tumor model

Journal of Clinical Investigation

Volumn 120, Issue 4, 2010, Pages 1151-1164

  Jablonska, Jadwiga ^a   Leschner, Sara ^a   Westphal, Kathrin ^a   Lienenklaus, Stefan ^a   Weiss, Siegfried ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CD11B ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; CYTOKINE; GELATINASE B; INTERFERON; STAT3 PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; BONE MARROW CELL; CANCER INHIBITION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; MELANOMA; METASTASIS; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; RADIOSENSITIVITY; TUMOR MODEL;

ANIMALS; ANTIGENS, CD11B; FEMALE; GENES, MYC; INTERFERON-BETA; KILLER CELLS, NATURAL; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NEUTROPHIL INFILTRATION; NEUTROPHILS; RADIATION TOLERANCE; STAT3 TRANSCRIPTION FACTOR;

EID: 77951187779     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI37223     Document Type: Article

References (69)

1. Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst. 1990; 82(1):4-6.
2. Plate KH, Breier G, Risau W. Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol. 1994;4(3):207-218.
3. Auguste P, Lemiere S, Larrieu-Lahargue F, Bikfalvi A. Molecular mechanisms of tumor vascularization. Crit Rev Oncol Hematol. 2005;54(1):53-61.
4. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1(1):27-31.
5. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57-70.
6. Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005;65(10):3967-3979.
7. Phung TL, et al. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell. 2006;10(2):159-170.
8. Pekarek LA, Starr BA, Toledano AY, Schreiber H. Inhibition of tumor growth by elimination of granulocytes. J Exp Med. 1995;181(1):435-440.
9. Guiducci C, et al. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 2005; 65(8):3437-3446.
10. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A. 2006;103(33):12493-12498.
11. De Palma M, et al. Tumor-targeted interferonalpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell. 2008;14(4):299-311.
12. Li B, et al. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J. 2006;20(9):1495-1497.
13. Nagase H, et al. Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J Leukoc Biol. 2002;71(4):711-717.
14. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol. 2004;14(3):171-179.
15. Salmaggi A, et al. CXCL12 in malignant glial tumors: a possible role in angiogenesis and crosstalk between endothelial and tumoral cells. J Neurooncol. 2004;67(3):305-317.
16. Zlotnik A. Chemokines and cancer. Int J Cancer. 2006;119(9):2026-2029.
17. Tabatabai G, Frank B, Mohle R, Weller M, Wick W. Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain. 2006;129(Pt 9):2426-2435.
18. Samuelsson CV, et al. Transformation of mouse fibroblasts alters the induction pattern of type I IFNs after virus infection. Biochem Biophys Res Commun. 2005;335(2):584-589.
19. Takayanagi H, et al. RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature. 2002;416(6882):744-749.
20. Koerner I, Kochs G, Kalinke U, Weiss S, Staeheli P. Protective role of beta interferon in host defense against influenza A virus. J Virol. 2007;81(4):2025-2030.
21. Decker T, Muller M, Stockinger S. The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol. 2005;5(9):675-687.
22. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol. 2006;6(11):836-848.
23. Deonarain R, et al. Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J Virol. 2000;74(7):3404-3409.
24. Qin XQ, et al. Interferon-beta gene therapy inhibits tumor formation and causes regression of established tumors in immune-deficient mice. Proc Natl Acad Sci U S A. 1998;95(24):14411-14416.
25. Brassard DL, Grace MJ, Bordens RW. Interferon-alpha as an immunotherapeutic protein. J Leukoc Biol. 2002;71(4):565-581.
26. Ferrantini M, et al. Alpha 1-interferon gene transfer into metastatic Friend leukemia cells abrogated tumorigenicity in immunocompetent mice: antitumor therapy by means of interferon-producing cells. Cancer Res. 1993;53(5):1107-1112.
27. Tuting T, et al. Interferon-alpha gene therapy for cancer: retroviral transduction of fibroblasts and particle-mediated transfection of tumor cells are both effective strategies for gene delivery in murine tumor models. Gene Ther. 1997;4(10):1053-1060.
28. Tozer GM, Kanthou C, Baguley BC. Disrupting tumour blood vessels. Nat Rev Cancer. 2005; 5(6):423-435.
29. Hanahan D. A flanking attack on cancer. Nat Med. 1998;4(1):13-14.
30. Takakura N. Role of hematopoietic lineage cells as accessory components in blood vessel formation. Cancer Sci. 2006;97(7):568-574.
31. Getts DR, et al. Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med. 2008;205(10):2319-2337.
32. Toi M, et al. Significance of thymidine phosphorylase as a marker of protumor monocytes in breast cancer. Clin Cancer Res. 1999;5(5):1131-1137.
33. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193(6):727-740.
34. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4(1):71-78.
35. Albini A, Tosetti F, Benelli R, Noonan DM. Tumor inflammatory angiogenesis and its chemoprevention. Cancer Res. 2005;65(23):10637-10641.
36. Yang L, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004;6(4):409-421.
37. Darash-Yahana M, et al. Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J. 2004;18(11):1240-1242.
38. Du R, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13(3):206-220.
39. Grunewald M, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell. 2006;124(1):175-189.
40. Lyden D, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7(11):1194-1201.
41. Jonak GJ, Knight E Jr. Selective reduction of c-myc mRNA in Daudi cells by human beta interferon. Proc Natl Acad Sci U S A. 1984;81(6):1747-1750.
42. Hu X, Bies J, Wolff L. Interferon beta increases c-Myc proteolysis in mouse monocyte/macrophage leukemia cells. Leuk Res. 2005;29(11):1307-1314.
43. Sarkar D, Park ES, Fisher PB. Defining the mechanism by which IFN-beta dowregulates c-myc expression in human melanoma cells: pivotal role for human polynucleotide phosphorylase (hPNPaseold-35). Cell Death Differ. 2006;13(9):1541-1553.
44. Dessauge F, Hilaly S, Baumgartner M, Blumen B, Werling D, Langsley G. c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene. 2005;24(6):1075-1083.
45. Busillo JM, Benovic JL. Regulation of CXCR4 signaling. Biochim Biophys Acta. 2007;1768(4):952-963.
46. Yuan ZL, Guan YJ, Wang L, Wei W, Kane AB, Chin YE. Central role of the threonine residue within the p+1 loop of receptor tyrosine kinase in STAT3 constitutive phosphorylation in metastatic cancer cells. Mol Cell Biol. 2004;24(21):9390-9400.
47. Burger M, et al. Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood. 2005;106(5):1824-1830.
48. Belardelli F, Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol. 2002;23(4):201-208.
49. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 2005;5(10):749-759.
50. Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000;12(2):121-127.
51. Xue ML, et al. A critical role for CCL2 and CCL3 chemokines in the regulation of polymorphonuclear neutrophils recruitment during corneal infection in mice. Immunol Cell Biol. 2007;85(7):525-531.
52. Reichel CA, et al. Ccl2 and Ccl3 mediate neutrophil recruitment via induction of protein synthesis and generation of lipid mediators. Arterioscler Thromb Vasc Biol. 2009;29(11):1787-1793.
53. Reichel CA, et al. Chemokine receptors Ccr1, Ccr2, and Ccr5 mediate neutrophil migration to postischemic tissue. J Leukoc Biol. 2006;79(1):114-122.
54. Maus U, et al. The role of CC chemokine receptor 2 in alveolar monocyte and neutrophil immigration in intact mice. Am J Respir Crit Care Med. 2002; 166(3):268-273.
55. De Keulenaer GW, et al. Convergence of redox-sensitive and mitogen-activated protein kinase signaling pathways in tumor necrosis factor-alpha-mediated monocyte chemoattractant protein-1 induction in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2000;20(2):385-391.
56. Iseki A, et al. Pyrrolidine dithiocarbamate inhibits TNF-alpha-dependent activation of NF-kappaB by increasing intracellular copper level in human aortic smooth muscle cells. Biochem Biophys Res Commun. 2000;276(1):88-92.
57. Asensi V, et al. In vivo interleukin-6 protects neutrophils from apoptosis in osteomyelitis. Infect Immun. 2004;72(7):3823-3828.
58. Walker F, et al. IL6/sIL6R complex contributes to emergency granulopoietic responses in G-CSF- and GM-CSF-deficient mice. Blood. 2008; 111(8):3978-3985.
59. Deonarain R, et al. Critical roles for IFN-beta in lymphoid development, myelopoiesis, and tumor development: links to tumor necrosis factor alpha. Proc Natl Acad Sci U S A. 2003;100(23):13453-13458.
60. Gresser I, Belardelli F. Endogenous type I interferons as a defense against tumors. Cytokine Growth Factor Rev. 2002;13(2):111-118.
61. Jonasch E, Haluska FG. Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities. Oncologist. 2001;6(1):34-55.
62. Wang J, Lin Q, Langston H, Cooper MD. Resident bone marrow macrophages produce type 1 interferons that can selectively inhibit interleukin-7-driven growth of B lineage cells. Immunity. 1995; 3(4):475-484.
63. Heissig B, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002;109(5):625-637.
64. Jung JE, et al. STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J. 2005;19(10):1296-1298.
65. Taniguchi T, Takaoka A. A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol. 2001;2(5):378-386.
66. Denny MF, et al. Interferon-{alpha} promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis. Blood. 2007; 110(8):2907-2915.
67. Asanuma Y, et al. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349(25):2407-2415.
68. Roman MJ, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349(25):2399-2406.
69. Chanprasert S, et al. Thrombopoietin (TPO) induces c-myc expression through a. Cell Signal. 2006; 18(8):1212-1218.