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PMID: 20080943 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion.

Genes & development ·Vol. 24 ·No. 3 ·2010-02-01 ·Pages 241-55

Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, Berman T, Joyce JA

Abstract

Innate immune cells can constitute a substantial proportion of the cells within the tumor microenvironment and have been associated with tumor malignancy in patients and animal models of cancer; however, the mechanisms by which they modulate cancer progression are incompletely understood. Here, we show that high levels of cathepsin protease activity are induced in the majority of macrophages in the microenvironment of pancreatic islet cancers, mammary tumors, and lung metastases during malignant progression. We further show that tumor-associated macrophage (TAM)-supplied cathepsins B and S are critical for promoting pancreatic tumor growth, angiogenesis, and invasion in vivo, and markedly enhance the invasiveness of cancer cells in culture. Finally, we demonstrate that interleukin-4 (IL-4) is responsible for inducing cathepsin activity in macrophages in vitro and in vivo. Together, these data establish IL-4 as an important regulator, and cathepsin proteases as critical mediators, of the cancer-promoting functions of TAMs.

MeSH Terms
Animals Biomarkers, Tumor/metabolism Cathepsins/metabolism Cell Line, Tumor Female Interleukin-4/metabolism Lung Neoplasms/pathology Macrophages/enzymology,metabolism Mammary Neoplasms, Experimental Mice Mice, Transgenic Neoplasm Invasiveness Neoplasms/enzymology,pathology Neovascularization, Pathologic/enzymology,pathology Pancreatic Neoplasms/pathology
Chemicals
Biomarkers, Tumor Interleukin-4 Cathepsins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Gocheva Vasilena
Cancer Biology and Genetics Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10021, USA.
Wang Hao-Wei
Gadea Bedrick B
Shree Tanaya
Hunter Karen E
Garfall Alfred L
Berman Tara
Joyce Johanna A
References (48)
48 references, click to expand
  1. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis.
    Genes Dev. 2006 Mar 1;20(5):543-56 PMID: 16481467
  2. Emerging roles of cysteine cathepsins in disease and their potential as drug targets.
    Curr Pharm Des. 2007;13(4):387-403 PMID: 17311556
  3. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages.
    Cancer Cell. 2009 Aug 4;16(2):91-102 PMID: 19647220
  4. Monocytes/macrophages in kidney allograft intimal arteritis: no association with markers of humoral rejection or with inferior outcome.
    Nephrol Dial Transplant. 2009 Jun;24(6):1979-86 PMID: 19223275
  5. Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors.
    J Biol Chem. 2006 Mar 3;281(9):6020-9 PMID: 16365041
  6. Cysteine cathepsins: multifunctional enzymes in cancer.
    Nat Rev Cancer. 2006 Oct;6(10):764-75 PMID: 16990854
  7. Phase II trial of recombinant human interleukin-4 in patients with disseminated malignant melanoma: a Southwest Oncology Group study.
    J Immunother. 1998 Nov;21(6):440-6 PMID: 9807739
  8. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases.
    Am J Pathol. 2003 Nov;163(5):2113-26 PMID: 14578209
  9. Comparative localization of cathepsin B protein and activity in colorectal cancer.
    J Histochem Cytochem. 2000 Oct;48(10):1421-30 PMID: 10990495
  10. Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis.
    Cancer Cell. 2002 May;1(4):339-53 PMID: 12086849
  11. Degradation of laminin by human tumor cathepsin B.
    Clin Exp Metastasis. 1989 Jul-Aug;7(4):461-8 PMID: 2785014
  12. The role of myeloid cells in the promotion of tumour angiogenesis.
    Nat Rev Cancer. 2008 Aug;8(8):618-31 PMID: 18633355
  13. Chemical approaches for functionally probing the proteome.
    Mol Cell Proteomics. 2002 Jan;1(1):60-8 PMID: 12096141
  14. Tumor stroma and regulation of cancer development.
    Annu Rev Pathol. 2006;1:119-50 PMID: 18039110
  15. Cysteine cathepsin proteases as pharmacological targets in cancer.
    Trends Pharmacol Sci. 2008 Jan;29(1):22-8 PMID: 18037508
  16. Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer.
    Cancer Res. 2006 May 15;66(10):5242-50 PMID: 16707449
  17. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):9037-41 PMID: 2848253
  18. Endogenous interleukin-4 promotes tumor development by increasing tumor cell resistance to apoptosis.
    Cancer Res. 2008 Nov 1;68(21):8687-94 PMID: 18974110
  19. Phase II trial of recombinant human interleukin-4 in patients with advanced renal cell carcinoma: a southwest oncology group study.
    J Immunother. 2002 Jul-Aug;25(4):352-8 PMID: 12142558
  20. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis.
    Cancer Cell. 2004 May;5(5):443-53 PMID: 15144952
  21. Interleukin-4 enhances proliferation of human pancreatic cancer cells: evidence for autocrine and paracrine actions.
    Br J Cancer. 2005 Mar 14;92(5):921-8 PMID: 15714203
  22. Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling.
    FASEB J. 2000 Oct;14(13):2075-86 PMID: 11023992
  23. Anti-interleukin-4 therapy.
    Immunol Allergy Clin North Am. 2004 Nov;24(4):599-614, vi PMID: 15474861
  24. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke.
    Nat Med. 2009 Feb;15(2):192-9 PMID: 19169263
  25. Localization of nuclear cathepsin L and its association with disease progression and poor outcome in colorectal cancer.
    Int J Cancer. 2009 Jul 1;125(1):54-61 PMID: 19291794
  26. Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis.
    J Clin Invest. 2000 Sep;106(6):773-81 PMID: 10995788
  27. Alternative activation of macrophages: an immunologic functional perspective.
    Annu Rev Immunol. 2009;27:451-83 PMID: 19105661
  28. Recombinant human interleukin 4 has antiproliferative activity on human tumor cell lines derived from epithelial and nonepithelial histologies.
    Cancer Res. 1995 May 15;55(10):2173-6 PMID: 7743520
  29. The duplicitous effects of interleukin 4 on tumour immunity: how can the same cytokine improve or impair control of tumour growth?
    Tissue Antigens. 2007 Apr;69(4):293-8 PMID: 17389011
  30. Elevations in cathepsin B protein content and enzyme activity occur independently of glycosylation during colorectal tumor progression.
    J Biol Chem. 1997 Nov 14;272(46):29190-9 PMID: 9360997
  31. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop.
    Cancer Res. 2005 Jun 15;65(12):5278-83 PMID: 15958574
  32. Microenvironmental regulation of metastasis.
    Nat Rev Cancer. 2009 Apr;9(4):239-52 PMID: 19279573
  33. Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4.
    Cell Death Differ. 2008 Apr;15(4):762-72 PMID: 18202702
  34. Cancer-related inflammation.
    Nature. 2008 Jul 24;454(7203):436-44 PMID: 18650914
  35. Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumour tissues.
    Biochem J. 1992 Feb 15;282 ( Pt 1):273-8 PMID: 1540143
  36. Differential expression of cytokine transcripts in human epithelial ovarian carcinoma by solid tumour specimens, peritoneal exudate cells containing tumour, tumour-infiltrating lymphocyte (TIL)-derived T cell lines and established tumour cell lines.
    Clin Exp Immunol. 1998 May;112(2):172-80 PMID: 9649178
  37. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo.
    Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8627-32 PMID: 10411926
  38. Generation and analysis of interleukin-4 deficient mice.
    Science. 1991 Nov 1;254(5032):707-10 PMID: 1948049
  39. Increased levels of macrophage-secreted cathepsin S during prostate cancer progression in TRAMP mice and patients.
    Cancer Genomics Proteomics. 2009 May-Jun;6(3):149-59 PMID: 19487544
  40. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease.
    Mol Cell Biol. 1992 Mar;12(3):954-61 PMID: 1312220
  41. 'Green mice' as a source of ubiquitous green cells.
    FEBS Lett. 1997 May 5;407(3):313-9 PMID: 9175875
  42. Cathepsin S required for normal MHC class II peptide loading and germinal center development.
    Immunity. 1999 Feb;10(2):197-206 PMID: 10072072
  43. Automated data acquisition by confocal laser scanning microscopy and image analysis of triple stained immunofluorescent leukocytes in tissue.
    J Immunol Methods. 2000 Apr 3;237(1-2):39-50 PMID: 10725450
  44. Heritable formation of pancreatic beta-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes.
    Nature. 1985 May 9-15;315(6015):115-22 PMID: 2986015
  45. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  46. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors.
    Cancer Res. 2004 Oct 1;64(19):7022-9 PMID: 15466195
  47. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival.
    Nat Cell Biol. 2005 Sep;7(9):870-9 PMID: 16113679
  48. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4.
    Cell Stem Cell. 2007 Oct 11;1(4):389-402 PMID: 18371377
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
1549-5477
Published
2010-02-01
Epub
2010-00-15
Pages
241-55
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC2811826
Subset
IM
Grants
NCI NIH HHS · R01 CA125162 · United States
Howard Hughes Medical Institute · United States
NCI NIH HHS · T32 CA009615 · United States
NCI NIH HHS · R01-CA125162 · United States
NIGMS NIH HHS · T32 GM007739 · United States
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