Neutrophils promote the malignant glioma phenotype through S100A4

Clinical Cancer Research

Volumn 20, Issue 1, 2014, Pages 187-198

  Liang, Ji ^a   Piao, Yuji ^a   Holmes, Lindsay ^a   Fuller, Gregory N ^a   Henry, Verlene ^a   Tiao, Ningyi ^a   De Groot, John F ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; CALVASCULIN; CD31 ANTIGEN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CANCER GROWTH; CANCER RESISTANCE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE IDENTIFICATION; GENE TARGETING; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYME CELL; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; UPREGULATION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASM GRADING; NEUTROPHIL INFILTRATION; PHENOTYPE; S100 PROTEINS; TISSUE ARRAY ANALYSIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84892149953     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-1279     Document Type: Article

References (53)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109.
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
3. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol 2006;1:97-117.
4. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006;9:157-73.
5. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010;17:98-110.
6. Cooper LA, Gutman DA, Long Q, Johnson BA, Cholleti SR, Kurc T, et al. The proneural molecular signature is enriched in oligodendrogliomas and predicts improved survival among diffuse gliomas. PLoS ONE 2010;5:e12548.
7. Piao Y, Liang J, Holmes L, Zurita AJ, Henry V, Heymach JV, et al. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro Oncol 2012;14:1379-92.
8. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012;150:165-78.
9. De Nardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1:54-67.
10. Shree T, Olson OC, Elie BT, Kester JC, Garfall AL, Simpson K, et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 2011;25:2465-79.
11. Van den Eynden GG, Majeed AW, Illemann M, Vermeulen PB, Bird NC, Hoyer-Hansen G, et al. The multifaceted role of the microenvironment in liver metastasis: biology and clinical implications. Cancer Res 2013; 73:2031-43.
12. Fossati G, Ricevuti G, Edwards SW, Walker C, Dalton A, Rossi ML. Neutrophil infiltration into human gliomas. Acta Neuropathol 1999; 98:349-54.
13. Nielsen BS, Timshel S, Kjeldsen L, Sehested M, Pyke C, Borregaard N, et al. 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;65:57-62.
14. Bellocq A, Antoine M, Flahault A, Philippe C, Crestani B, Bernaudin JF, et al. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am J Pathol 1998;152:83-92.
15. Shojaei F, Wu X, Qu X, Kowanetz M, Yu L, Tan M, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci U S A 2009;106:6742-7.
16. Shojaei F, Wu X, Zhong C, Yu L, Liang XH, Yao J, et al. Bv8 regulates myeloid-cell-dependent tumour angiogenesis. Nature 2007;450:825-31.
17. Huang S, Mills L, Mian B, Tellez C, McCarty M, Yang XD, et al. Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol 2002;161:125-34.
18. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 2009;16:183-94.
19. Jablonska J, Leschner S, Westphal K, Lienenklaus S, Weiss S. Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest 2010; 120:1151-64.
20. 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;103:12493-8.
21. Benelli R, Morini M, Carrozzino F, Ferrari N, Minghelli S, Santi L, et al. Neutrophils as a key cellular target for angiostatin: implications for regulation of angiogenesis and inflammation. FASEB J 2002;16:267-9.
22. Liu TJ, Wang M, Breau RL, Henderson Y, El-Naggar AK, Steck KD, et al. Apoptosis induction by E2F-1 via adenoviral-mediated gene transfer results in growth suppression of head and neck squamous cell carcinoma cell lines. Cancer Gene Ther 1999;6:163-71.
23. de Groot J, Liang J, Kong LY, Wei J, Piao Y, Fuller G, et al. Modulating antiangiogenic resistance by inhibiting the signal transducer and activator of transcription 3 pathway in glioblastoma. Oncotarget 2012; 3:1036-48.
24. Hirsch S, Gordon S. Polymorphic expression of a neutrophil differentiation antigen revealed by monoclonal antibody 7/4. Immunogenetics 1983;18:229-39.
25. McDonald JU, Cortini A, Rosas M, Fossati-Jimack L, Ling GS, Lewis KJ, et al. In vivo functional analysis and genetic modification of in vitro-derived mouse neutrophils. FASEB J 2011;25:1972-82.
26. Thiery JP, Sleeman JP. Complex networks orchestrate epithelialmesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-42.
27. Lucio-Eterovic AK, Piao Y, de Groot JF. Mediators of glioblastoma resistance and invasion during antivascular endothelial growth factor therapy. Clin Cancer Res 2009;15:4589-99.
28. Weller M. Novel diagnostic and therapeutic approaches to malignant glioma. Swiss Med Wkly 2011;141:w13210.
29. Gilbert MR, Dignam J, Won M, Blumenthal DT, Vogelbaum MA, Kenneth D, et al. RTOG 0825: Phase III double-blind placebo-controlled trial evaluating bevacizumab (Bev) in patients (Pts) with newly diagnosed glioblastoma (GBM). J Clin Oncol 31: 2013 (suppl; abstr 1).
30. Armstrong TS, Won M, Wefel JS, Gilbert MR, Pugh SL, Brachman D, et al. Comparative impact of treatment on patient reported outcomes (PROs) in patients with glioblastoma (GBM) enrolled in ROTG 0825. J Clin Oncol 31: 2013 (suppl; abstr 2003).
31. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-20.
32. Tazzyman S, Lewis CE, Murdoch C. Neutrophils: key mediators of tumour angiogenesis. Int J Exp Pathol 2009;90:222-31.
33. Gregory AD, Houghton AM. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 2011;71:2411-6.
34. Mentzel T, Brown LF, Dvorak HF, Kuhnen C, Stiller KJ, Katenkamp D, et al. The association between tumour progression and vascularity in myxofibrosarcomaand myxoid/round cell liposarcoma. Virchows Arch 2001;438:13-22.
35. Van Coillie E, Van Aelst I, Wuyts A, Vercauteren R, Devos R, De Wolf-Peeters C, et al. Tumor angiogenesis induced by granulocyte chemotactic protein-2 as a countercurrent principle. Am J Pathol 2001; 159:1405-14.
36. McCourt M, Wang JH, Sookhai S, Redmond HP. Proinflammatory mediators stimulate neutrophil-directed angiogenesis. Arch Surg 1999;134:1325-31.
37. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-90.
38. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-44.
39. Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci U S A 2007;104:20262-7.
40. Heizmann CW, Cox JA. New perspectives on S100 proteins: a multifunctional Ca(2+ )-, Zn(2+ )- and Cu(2+ )-binding protein family. Biometals 1998;11:383-97.
41. Schneider M, Hansen JL, Sheikh SP. S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J Mol Med 2008;86:507-22.
42. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 2002;110:341-50.
43. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinomaassociated fibroblasts. Cancer Res 2007;67:10123-8.
44. Okada H, Danoff TM, Kalluri R, Neilson EG. Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol 1997;273: F563-74.
45. Wang YY, Ye ZY, Zhao ZS, Tao HQ, Chu YQ. High-level expression of S100A4 correlates with lymph node metastasis and poor prognosis in patients with gastric cancer. Ann Surg Oncol 2010;17:89-97.
46. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K, et al. Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 2000;6:4234-42.
47. Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, et al. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int J Oncol 2000; 16:1125-31.
48. Wang HY, Zhang JY, Cui JT, Tan XH, Li WM, Gu J, et al. Expression status of S100A14 and S100A4 correlates with metastatic potential and clinical outcome in colorectal cancer after surgery. Oncolo Rep 2010;23:45-52.
49. Zou M, Al-Baradie RS, Al-Hindi H, Farid NR, Shi Y. S100A4 (Mts1) gene overexpression is associated with invasion and metastasis of papillary thyroid carcinoma. Br J Cancer 2005;93:1277-84.
50. Ismail NI, Kaur G, Hashim H, Hassan MS. S100A4 overexpression proves to be independent marker for breast cancer progression. Cancer Cell Int 2008;8:12.
51. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N, et al. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci U S A 2006;103:14825-30.
52. Iwamoto FM, Hottinger AF, Karimi S, Riedel E, Dantis J, Jahdi M, et al. Longitudinal prospective study of matrix metalloproteinase-9 as a serum marker in gliomas. J Neuro Oncol 2011;105:607-12.
53. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, et al. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003;9:964-8.