Home LiteratureArticle Details
PMID: 19563607 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Neutrophils: key mediators of tumour angiogenesis.

International journal of experimental pathology ·Vol. 90 ·No. 3 ·2009-06-00 ·Pages 222-31

Tazzyman S, Lewis CE, Murdoch C

Abstract

It is now well known that most malignant tumours contain a significant amount of leucocytic infiltrates the presence of which has, on many occasions, been linked to poor patient prognosis. These leucocyte populations are recruited to tumours by chemotactic factors released by either viable or necrotic tumour cells, or by cells within the tumour stroma. In recent times, most studies have analysed the role that tumour-associated macrophages (TAM) have on tumour progression. However, there is now increasing evidence to show that neutrophils also actively participate in this process. Whilst there are some data to suggest that neutrophil-derived factors can promote genetic mutations leading to tumourigenesis, or secrete factors that promote tumour cell proliferation; there is now substantial evidence to show that neutrophils, like TAM, significantly affect tumour angiogenesis. In this review, we discuss the likely mechanisms by which neutrophils are recruited into the tumour and then elaborate on how these cells may induce tumour vascularization by the secretion of powerful pro-angiogenic factors. We also discuss possible future chemotherapeutic strategies that are aimed at limiting tumour angiogenesis by inhibiting neutrophil recruitment.

MeSH Terms
Angiogenesis Inhibitors/pharmacology Antineoplastic Agents/pharmacology Humans Neoplasms/blood supply Neovascularization, Pathologic/pathology Neutrophil Infiltration/drug effects Neutrophils/drug effects,physiology
Chemicals
Angiogenesis Inhibitors Antineoplastic Agents
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tazzyman Simon
Tumour Targeting Group, Academic Unit of Pathology, Medical School, University of Sheffield, Sheffield, UK. [email protected]
Lewis Claire E
Murdoch Craig
References (74)
74 references, click to expand
  1. A novel effect of polymorphonuclear leukocytes in the facilitation of angiogenesis.
    Life Sci. 2000 Apr 14;66(21):2113-21 PMID: 10823350
  2. Endothelial cell E- and P-selectin and vascular cell adhesion molecule-1 function as signaling receptors.
    J Cell Biol. 1998 Sep 7;142(5):1381-91 PMID: 9732297
  3. The source of APRIL up-regulation in human solid tumor lesions.
    J Leukoc Biol. 2006 Oct;80(4):697-704 PMID: 16793914
  4. A homolog of the human chemokine receptor CXCR1 is expressed in the mouse.
    Mol Immunol. 2006 Mar;43(7):897-914 PMID: 16084593
  5. IL-8 specifically binds to endothelial but not to smooth muscle cells.
    J Immunol. 1995 Mar 1;154(5):2375-83 PMID: 7868904
  6. Plasticity in tumor-promoting inflammation: impairment of macrophage recruitment evokes a compensatory neutrophil response.
    Neoplasia. 2008 Apr;10(4):329-40 PMID: 18392134
  7. Differential effects of alpha- and beta-defensin on cytokine production by cultured human bronchial epithelial cells.
    Am J Physiol Lung Cell Mol Physiol. 2005 Mar;288(3):L508-13 PMID: 15557089
  8. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis.
    J Biol Chem. 1995 Nov 10;270(45):27348-57 PMID: 7592998
  9. Proliferation and hypoxia in human squamous cell carcinoma of the cervix: first report of combined immunohistochemical assays.
    Int J Radiat Oncol Biol Phys. 1997 Mar 1;37(4):897-905 PMID: 9128967
  10. Pleiotropic effects of CXC chemokines in gastric carcinoma: differences in CXCL8 and CXCL1 expression between diffuse and intestinal types of gastric carcinoma.
    Clin Exp Immunol. 2003 Dec;134(3):508-15 PMID: 14632759
  11. Angiogenic activity of bFGF and VEGF suppressed by proteolytic cleavage by neutrophil elastase.
    Biochem Biophys Res Commun. 2007 Dec 14;364(2):395-401 PMID: 17950695
  12. Neutrophils as a key cellular target for angiostatin: implications for regulation of angiogenesis and inflammation.
    FASEB J. 2002 Feb;16(2):267-9 PMID: 11772950
  13. Role of angiogenesis in tumor growth and metastasis.
    Semin Oncol. 2002 Dec;29(6 Suppl 16):15-8 PMID: 12516034
  14. Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis.
    Fertil Steril. 2000 Jul;74(1):107-12 PMID: 10899506
  15. Human neutrophil defensins induce lung epithelial cell proliferation in vitro.
    J Leukoc Biol. 2002 Jul;72(1):167-74 PMID: 12101277
  16. Proinflammatory mediators stimulate neutrophil-directed angiogenesis.
    Arch Surg. 1999 Dec;134(12):1325-31; discussion 1331-2 PMID: 10593330
  17. Identification of a novel granulocyte chemotactic protein (GCP-2) from human tumor cells. In vitro and in vivo comparison with natural forms of GRO, IP-10, and IL-8.
    J Immunol. 1993 Feb 1;150(3):1000-10 PMID: 8423327
  18. Neutrophil-mediated tumor cell cytotoxicity: role of the peroxidase system.
    J Exp Med. 1975 Jun 1;141(6):1442-7 PMID: 165258
  19. Regulation of myeloid development and function by colony stimulating factors.
    Dev Comp Immunol. 2004 May 3;28(5):509-54 PMID: 15062647
  20. Blockade of the chemokine receptor CXCR2 inhibits pancreatic cancer cell-induced angiogenesis.
    Cancer Lett. 2006 Sep 28;241(2):221-7 PMID: 16458421
  21. Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils.
    J Immunol. 2002 Jun 1;168(11):5798-804 PMID: 12023382
  22. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis.
    Cell. 2000 Oct 27;103(3):481-90 PMID: 11081634
  23. Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice.
    Reproduction. 2004 May;127(5):613-20 PMID: 15129017
  24. GCP-2/CXCL6 synergizes with other endothelial cell-derived chemokines in neutrophil mobilization and is associated with angiogenesis in gastrointestinal tumors.
    Exp Cell Res. 2005 Feb 15;303(2):331-42 PMID: 15652347
  25. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells.
    J Biol Chem. 1994 Apr 29;269(17):12536-40 PMID: 7909803
  26. Oxygenation of human tumors: evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements.
    Cancer Res. 1991 Jun 15;51(12):3316-22 PMID: 2040005
  27. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm.
    Cell. 1994 Jan 28;76(2):301-14 PMID: 7507411
  28. Interleukin-6 induces demargination of intravascular neutrophils and shortens their transit in marrow.
    Am J Physiol Heart Circ Physiol. 2000 Dec;279(6):H2954-60 PMID: 11087252
  29. Proangiogenic role of neutrophil-like inflammatory heterophils during neovascularization induced by growth factors and human tumor cells.
    Blood. 2006 Jan 1;107(1):317-27 PMID: 16174763
  30. Structure and functional expression of a human interleukin-8 receptor.
    Science. 1991 Sep 13;253(5025):1278-80 PMID: 1840701
  31. SAR studies on thiazolo[4,5-d]pyrimidine based CXCR2 antagonists involving a novel tandem displacement reaction.
    Bioorg Med Chem Lett. 2007 May 15;17(10):2731-4 PMID: 17382543
  32. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis.
    Blood. 2004 Jul 15;104(2):565-71 PMID: 15054039
  33. Differential roles of ICAM-1 and E-selectin in polymorphonuclear leukocyte-induced angiogenesis.
    Am J Physiol Cell Physiol. 2002 Apr;282(4):C917-25 PMID: 11880280
  34. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis.
    Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20262-7 PMID: 18077379
  35. Distinct role of macrophages in different tumor microenvironments.
    Cancer Res. 2006 Jan 15;66(2):605-12 PMID: 16423985
  36. Functional capacity of marginated and bone marrow reserve granulocytes.
    Infect Immun. 1987 Oct;55(10):2359-63 PMID: 3653982
  37. Characterization of GRO alpha, beta and gamma expression in human colonic tumours: potential significance of cytokine involvement.
    Surg Oncol. 1992 Aug;1(4):323-9 PMID: 1341267
  38. Cloning of complementary DNA encoding a functional human interleukin-8 receptor.
    Science. 1991 Sep 13;253(5025):1280-3 PMID: 1891716
  39. Homeostatic regulation of blood neutrophil counts.
    J Immunol. 2008 Oct 15;181(8):5183-8 PMID: 18832668
  40. Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice.
    J Clin Invest. 1996 Jun 15;97(12):2792-802 PMID: 8675690
  41. Murine CXCR1 is a functional receptor for GCP-2/CXCL6 and interleukin-8/CXCL8.
    J Biol Chem. 2007 Apr 20;282(16):11658-66 PMID: 17197447
  42. Transcriptional regulation of granulocyte and monocyte development.
    Oncogene. 2002 May 13;21(21):3377-90 PMID: 12032776
  43. Intracellular pool of vascular endothelial growth factor in human neutrophils.
    Blood. 1997 Nov 15;90(10):4153-61 PMID: 9354686
  44. Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo.
    Cancer Res. 2007 Oct 1;67(19):9417-24 PMID: 17909051
  45. Tumor-elicited polymorphonuclear cells, in contrast to "normal" circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5859-63 PMID: 2762301
  46. Neutrophils, nitric oxide synthase, and mutations in the mutatect murine tumor model.
    Am J Pathol. 2000 Feb;156(2):509-18 PMID: 10666380
  47. The intriguing role of polymorphonuclear neutrophils in antitumor reactions.
    Blood. 2001 Jan 15;97(2):339-45 PMID: 11154206
  48. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact.
    Blood. 2000 Oct 15;96(8):2673-81 PMID: 11023497
  49. Upregulation of bronchioloalveolar carcinoma-derived C-X-C chemokines by tumor infiltrating inflammatory cells.
    Inflamm Res. 2004 Jan;53(1):4-12 PMID: 15021975
  50. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12493-8 PMID: 16891410
  51. Purification and identification of 91-kDa neutrophil gelatinase. Release by the activating peptide interleukin-8.
    Eur J Biochem. 1991 Jun 1;198(2):391-8 PMID: 1645657
  52. Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice.
    J Natl Cancer Inst. 2002 Aug 7;94(15):1134-42 PMID: 12165638
  53. Neutrophil-derived proteins: selling cytokines by the pound.
    Adv Immunol. 1999;73:369-509 PMID: 10399011
  54. The association between tumour progression and vascularity in myxofibrosarcoma and myxoid/round cell liposarcoma.
    Virchows Arch. 2001 Jan;438(1):13-22 PMID: 11213831
  55. The CXC chemokines growth-regulated oncogene (GRO) alpha, GRObeta, GROgamma, neutrophil-activating peptide-2, and epithelial cell-derived neutrophil-activating peptide-78 are potent agonists for the type B, but not the type A, human interleukin-8 receptor.
    J Biol Chem. 1996 Aug 23;271(34):20545-50 PMID: 8702798
  56. Matrix metalloproteinases and the development of cancer.
    Chem Biol. 1996 Nov;3(11):895-904 PMID: 8939708
  57. Depletion of CXCR2 inhibits tumor growth and angiogenesis in a murine model of lung cancer.
    J Immunol. 2004 Mar 1;172(5):2853-60 PMID: 14978086
  58. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome.
    Am J Pathol. 1998 Jan;152(1):83-92 PMID: 9422526
  59. Role of tumor-associated macrophages in tumor progression and invasion.
    Cancer Metastasis Rev. 2006 Sep;25(3):315-22 PMID: 16967326
  60. Interleukin-8 as a macrophage-derived mediator of angiogenesis.
    Science. 1992 Dec 11;258(5089):1798-801 PMID: 1281554
  61. Monocyte/macrophage infiltration in tumors: modulators of angiogenesis.
    J Leukoc Biol. 2006 Dec;80(6):1183-96 PMID: 16997855
  62. Multiple mechanisms account for genomic instability and molecular mutation in neoplastic transformation.
    Clin Chem. 1995 May;41(5):644-57 PMID: 7729041
  63. Neutrophils roll on E-selectin.
    J Immunol. 1993 Dec 1;151(11):6338-46 PMID: 7504018
  64. Granulocyte chemotactic protein 2 acts via both IL-8 receptors, CXCR1 and CXCR2.
    Eur J Immunol. 1998 Jan;28(1):164-70 PMID: 9485196
  65. Interleukin-8 and human cancer biology.
    Cytokine Growth Factor Rev. 2001 Dec;12(4):375-91 PMID: 11544106
  66. Colony-stimulating factor-1 antisense treatment suppresses growth of human tumor xenografts in mice.
    Cancer Res. 2002 Sep 15;62(18):5317-24 PMID: 12235002
  67. Tumorigenesis and the angiogenic switch.
    Nat Rev Cancer. 2003 Jun;3(6):401-10 PMID: 12778130
  68. The role of myeloid cells in the promotion of tumour angiogenesis.
    Nat Rev Cancer. 2008 Aug;8(8):618-31 PMID: 18633355
  69. Tumor angiogenesis induced by granulocyte chemotactic protein-2 as a countercurrent principle.
    Am J Pathol. 2001 Oct;159(4):1405-14 PMID: 11583968
  70. Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft.
    J Invest Dermatol. 2007 Aug;127(8):2031-41 PMID: 17460736
  71. Polymorphonuclear neutrophils promote rFGF-2-induced angiogenesis in vivo.
    J Surg Res. 2003 Jan;109(1):37-42 PMID: 12591233
  72. 92 kDa type IV collagenase (MMP-9) is expressed in neutrophils and macrophages but not in malignant epithelial cells in human colon cancer.
    Int J Cancer. 1996 Jan 3;65(1):57-62 PMID: 8543396
  73. Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression.
    Cancer Res. 2005 Oct 1;65(19):8896-904 PMID: 16204061
  74. Tie2-expressing monocytes and tumor angiogenesis: regulation by hypoxia and angiopoietin-2.
    Cancer Res. 2007 Sep 15;67(18):8429-32 PMID: 17875679
Article Info
Journal
International journal of experimental pathology
Abbr.
Int J Exp Pathol
ISSN
1365-2613
Published
2009-06-00
Pages
222-31
Language
English
Region
England
NLM ID
9014042
PMCID
PMC2697547
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]