Home LiteratureArticle Details
PMID: 15520864 Published · ppublish English Journal Article

Mast cell-derived angiopoietin-1 plays a critical role in the growth of plasma cell tumors.

The Journal of clinical investigation ·Vol. 114 ·No. 9 ·2004-11-00 ·Pages 1317-25

Nakayama T, Yao L, Tosato G

Abstract

Multiple myeloma in humans is frequently associated with mast cell infiltration and neovascularization, which correlate directly with disease severity, but the mechanisms underlying this relationship remain unclear. Here, we report that primary murine mast cells express angiopoietin-1 (Ang-1) and low levels of VEGF-A but not Ang-2 and that 2 established murine plasmacytoma cell lines express high levels of VEGF-A but little or no Ang-1 or Ang-2. An in vivo angiogenesis assay using extracellular matrix components shows that mast cells and plasmacytoma cells, together, promote marked neovascularization composed of dilated vessels, which is prevented by neutralization of VEGF-A and Ang-1 but is only partially reduced by neutralization of either VEGF-A or Ang-1. Mast cells within extracellular matrix components express Ang-1, and recombinant Ang-1 together with plasmacytoma cells promotes extracellular matrix neovascularization similar to that induced by mast cells. A transplantation assay shows that primary mast cells accelerate tumor growth by established plasmacytoma cell lines and that neutralization of Ang-1 alone or with VEGF-A reduces significantly the growth of plasmacytomas containing mast cells. These results demonstrate that mast cell-derived Ang-1 promotes the growth of plasmacytomas by stimulating neovascularization and provide further evidence supporting a causal relationship between inflammation and tumor growth.

MeSH Terms
Angiopoietin-1/metabolism,physiology Angiopoietin-2/biosynthesis Animals Cell Proliferation Cells, Cultured Collagen/pharmacology Cytokines/metabolism Drug Combinations Extracellular Matrix Female Immunohistochemistry Inflammation Laminin/pharmacology Mast Cells/metabolism Mice Mice, Inbred BALB C Multiple Myeloma/pathology Neovascularization, Pathologic Plasmacytoma/metabolism Proteoglycans/pharmacology RNA/metabolism Recombinant Proteins/chemistry Reverse Transcriptase Polymerase Chain Reaction Time Factors Vascular Endothelial Growth Factor A/biosynthesis
Chemicals
Angiopoietin-1 Angiopoietin-2 Cytokines Drug Combinations Laminin Proteoglycans Recombinant Proteins Vascular Endothelial Growth Factor A matrigel RNA Collagen
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Nakayama Takayuki
Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland 20892, USA.
Yao Lei
Tosato Giovanna
References (59)
59 references, click to expand
  1. Immunohistochemical detection of T-cell subsets and other leukocytes in paraffin-embedded rat and mouse tissues with monoclonal antibodies.
    J Histochem Cytochem. 1995 Mar;43(3):313-20 PMID: 7868861
  2. Risk factors for hepatocellular carcinoma among patients with chronic liver disease.
    N Engl J Med. 1993 Jun 24;328(25):1797-801 PMID: 7684822
  3. Bone marrow angiogenesis and mast cell density increase simultaneously with progression of human multiple myeloma.
    Br J Cancer. 1999 Feb;79(3-4):451-5 PMID: 10027312
  4. Nonsteroidal anti-inflammatory drugs and cancer prevention.
    Annu Rev Med. 2000;51:511-23 PMID: 10774479
  5. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation.
    Nature. 1995 Jul 6;376(6535):70-4 PMID: 7596437
  6. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line.
    J Exp Med. 1989 Apr 1;169(4):1485-90 PMID: 2926331
  7. Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors.
    Cancer Res. 2003 Jun 15;63(12):3370-7 PMID: 12810673
  8. Analysis of Ia antigen expression in macrophages derived from bone marrow cells cultured in granulocyte-macrophage colony-stimulating factor or macrophage colony-stimulating factor.
    J Immunol. 1988 Apr 15;140(8):2652-60 PMID: 3128601
  9. Differences in the peritoneal response to pristane in BALB/cAnPt and BALB/cJ mice.
    Curr Top Microbiol Immunol. 1985;122:242-53 PMID: 2412763
  10. Mast cells and tumor angiogenesis.
    Int J Cancer. 1976 Nov 15;18(5):703-9 PMID: 62725
  11. Multiple myeloma biology: lessons from the 5TMM models.
    Immunol Rev. 2003 Aug;194:196-206 PMID: 12846816
  12. Proangiogenic properties of human myeloma cells: production of angiopoietin-1 and its potential relationship to myeloma-induced angiogenesis.
    Blood. 2003 Jul 15;102(2):638-45 PMID: 12649156
  13. Generation of a novel stem cell factor-dependent mast cell progenitor.
    J Immunol. 1998 Nov 15;161(10):5143-6 PMID: 9820483
  14. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  15. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning.
    Cell. 1996 Dec 27;87(7):1161-9 PMID: 8980223
  16. Inflammation and cancer.
    Nature. 2002 Dec 19-26;420(6917):860-7 PMID: 12490959
  17. Chemokines and the arrest of lymphocytes rolling under flow conditions.
    Science. 1998 Jan 16;279(5349):381-4 PMID: 9430588
  18. Inhibition of plasmacytoma development in BALB/c mice by indomethacin.
    J Exp Med. 1985 May 1;161(5):996-1012 PMID: 3989472
  19. Enhanced expression of Tie2, its ligand angiopoietin-1, vascular endothelial growth factor, and CD31 in human non-small cell lung carcinomas.
    Clin Cancer Res. 1999 Sep;5(9):2506-10 PMID: 10499626
  20. LAT is essential for Fc(epsilon)RI-mediated mast cell activation.
    Immunity. 2000 May;12(5):525-35 PMID: 10843385
  21. Bone marrow angiogenesis in patients with active multiple myeloma.
    Semin Oncol. 2001 Dec;28(6):543-50 PMID: 11740807
  22. The role of mast cells in tumour angiogenesis.
    Br J Haematol. 2001 Dec;115(3):514-21 PMID: 11736931
  23. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells.
    J Exp Med. 2001 May 7;193(9):1005-14 PMID: 11342585
  24. The biology of interleukin-6.
    Blood. 1989 Jul;74(1):1-10 PMID: 2473791
  25. Vasostatin, a calreticulin fragment, inhibits angiogenesis and suppresses tumor growth.
    J Exp Med. 1998 Dec 21;188(12):2349-56 PMID: 9858521
  26. Inhibition of tumor angiogenesis using a soluble receptor establishes a role for Tie2 in pathologic vascular growth.
    J Clin Invest. 1997 Oct 15;100(8):2072-8 PMID: 9329972
  27. The biology of VEGF and its receptors.
    Nat Med. 2003 Jun;9(6):669-76 PMID: 12778165
  28. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF.
    Science. 1999 Jun 18;284(5422):1994-8 PMID: 10373119
  29. Structural characteristics of CD40 ligand that determine biological function.
    Semin Immunol. 1994 Oct;6(5):267-78 PMID: 7532457
  30. Preventive and therapeutic vaccines against Helicobacter pylori: current status and future challenges.
    Curr Pharm Des. 2000 Oct;6(15):1557-73 PMID: 10974152
  31. New functions for the matrix metalloproteinases in cancer progression.
    Nat Rev Cancer. 2002 Mar;2(3):161-74 PMID: 11990853
  32. Colony-stimulating factor-1 impairs both proliferation and differentiation signals of erythropoietin during the commitment of bipotential NFS-60 cell line to the monocytic lineage.
    Exp Hematol. 1999 May;27(5):797-805 PMID: 10340394
  33. Interleukin-15 prevents mouse mast cell apoptosis through STAT6-mediated Bcl-xL expression.
    J Biol Chem. 2001 Jul 13;276(28):26107-13 PMID: 11369758
  34. Identifying intercellular signaling genes expressed in malignant plasma cells by using complementary DNA arrays.
    Blood. 2001 Aug 1;98(3):771-80 PMID: 11468178
  35. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis.
    Genes Dev. 1999 Jun 1;13(11):1382-97 PMID: 10364156
  36. Inflammation and cancer: back to Virchow?
    Lancet. 2001 Feb 17;357(9255):539-45 PMID: 11229684
  37. Mast cells and angiogenesis.
    APMIS. 2002 May;110(5):355-71 PMID: 12076253
  38. Angiopoietin-1 protects the adult vasculature against plasma leakage.
    Nat Med. 2000 Apr;6(4):460-3 PMID: 10742156
  39. Generation of plasmacytomas with the chromosomal translocation t(12;15) in interleukin 6 transgenic mice.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):232-5 PMID: 1729694
  40. Expression of Tie1, Tie2, and angiopoietins 1, 2, and 4 in Kaposi's sarcoma and cutaneous angiosarcoma.
    Am J Pathol. 2000 Jun;156(6):2179-83 PMID: 10854238
  41. Neoplastic development in plasma cells.
    Immunol Rev. 2003 Aug;194:177-95 PMID: 12846815
  42. Interpreting the molecular biology and clinical behavior of multiple myeloma in the context of global gene expression profiling.
    Immunol Rev. 2003 Aug;194:140-63 PMID: 12846813
  43. Prostaglandin E2 selectively enhances the IgE-mediated production of IL-6 and granulocyte-macrophage colony-stimulating factor by mast cells through an EP1/EP3-dependent mechanism.
    J Immunol. 2000 Dec 1;165(11):6545-52 PMID: 11086097
  44. Mast cell accumulation at sites of murine tumor implantation: implications for angiogenesis and tumor metastasis.
    Invasion Metastasis. 1994-1995;14(1-6):395-408 PMID: 7544776
  45. Angiopoietins have distinct modular domains essential for receptor binding, dimerization and superclustering.
    Nat Struct Biol. 2003 Jan;10(1):38-44 PMID: 12469114
  46. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis.
    Cell. 1996 Dec 27;87(7):1171-80 PMID: 8980224
  47. Mast-cell-deficient W/Wv mice exhibit a decreased rate of tumor angiogenesis.
    Int J Cancer. 1988 Jul 15;42(1):48-52 PMID: 2455691
  48. The diverse roles of mast cells.
    J Exp Med. 2001 Jul 2;194(1):F1-5 PMID: 11435478
  49. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis.
    Cell. 2000 Oct 27;103(3):481-90 PMID: 11081634
  50. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1.
    Science. 1999 Dec 24;286(5449):2511-4 PMID: 10617467
  51. Thrombin induces the release of angiopoietin-1 from platelets.
    Thromb Haemost. 2001 Feb;85(2):204-6 PMID: 11246533
  52. Angiogenesis in health and disease.
    Nat Med. 2003 Jun;9(6):653-60 PMID: 12778163
  53. Mast cell-mediated stimulation of angiogenesis: cooperative interaction between A2B and A3 adenosine receptors.
    Circ Res. 2003 Mar 21;92(5):485-92 PMID: 12600879
  54. Chemokine receptor CCR2 is expressed by human multiple myeloma cells and mediates migration to bone marrow stromal cell-produced monocyte chemotactic proteins MCP-1, -2 and -3.
    Br J Cancer. 2003 Mar 24;88(6):855-62 PMID: 12644822
  55. Induction of plasma-cell neoplasms in strain BALB/c mice with mineral oil and mineral oil adjuvants.
    Nature. 1962 Mar 17;193:1086-7 PMID: 14488296
  56. The enigmatic role of angiopoietin-1 in tumor angiogenesis.
    Cell Res. 2003 Oct;13(5):309-17 PMID: 14672554
  57. A macrophage-derived factor required by plasmacytomas for survival and proliferation in vitro.
    Science. 1986 Aug 1;233(4763):566-9 PMID: 3726549
  58. Expressions of vascular endothelial growth factor and angiopoietin-2 in myeloma cells.
    Haematologica. 2003 Jan;88(1):113-5 PMID: 12551836
  59. Precancer and cancer in extensive ulcerative colitis: findings among 401 patients over 22 years.
    Gut. 1990 Jul;31(7):800-6 PMID: 2370015
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2004-11-00
Pages
1317-25
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC524229
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: product@genelibs.com