Tumour-processed osteopontin and lactadherin drive the protumorigenic reprogramming of microglia and glioma progression

Oncogene

Volumn 35, Issue 50, 2016, Pages 6366-6377

  Ellert Miklaszewska, A ^a   Wisniewski, P ^a   Kijewska, M ^a   Gajdanowicz, P ^a   Pszczolkowska, D ^a   Przanowski, P ^a   Dabrowski, M ^a   Maleszewska, M ^a   Kaminska, B ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; FOCAL ADHESION KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTEGRIN; INTERFERON REGULATORY FACTOR 7; LACTADHERIN; LAMININ; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MATRILYSIN; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN; PROTEIN KINASE B; SHORT HAIRPIN RNA; SMAD7 PROTEIN; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; STROMELYSIN; STROMELYSIN 2; THROMBIN; MATRIX METALLOPROTEINASE; MEMBRANE ANTIGEN; MFGE8 PROTEIN, RAT; MILK PROTEIN; SPP1 PROTEIN, RAT;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CANCER GROWTH; CONTROLLED STUDY; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; MACROPHAGE; MICROGLIA; PHAGOCYTOSIS; PILOCYTIC ASTROCYTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SECRETION; SIGNAL TRANSDUCTION; ANIMAL; BRAIN NEOPLASMS; MALE; NUCLEAR REPROGRAMMING; PHYSIOLOGY; PROTEOMICS; RAT; TUMOR CELL LINE; WISTAR RAT;

ANIMALS; ANTIGENS, SURFACE; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELLULAR REPROGRAMMING; GLIOMA; HUMANS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASES; MICROGLIA; MILK PROTEINS; OSTEOPONTIN; PROTEOMICS; RATS; RATS, WISTAR;

EID: 84962087225     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.55     Document Type: Article

References (41)

1. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010; 22: 231-237.
2. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41: 49-61.
3. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014; 41: 14-20.
4. Heusinkveld M, de Vos van Steenwijk PJ, Goedemans R, Ramwadhdoebe TH, Gorter A, Welters MJ et al. M2 macrophages induced by prostaglandin E2 and IL-6 from cervical carcinoma are switched to activated M1 macrophages by CD4+ Th1 cells. J Immunol 2011; 187: 1157-1165.
5. Roca H, Varsos ZS, Sud S, Craig MJ, Ying C, Pienta KJ. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem 2009; 284: 34342-34354.
6. Solinas G, Schiarea S, Liguori M, Fabbri M, Pesce S, Zammataro L et al. Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J Immunol 2010; 185: 642-652.
7. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y et al. Carcinomaproduced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009; 457: 102-106.
8. Badie B, Schartner JM. Flow cytometric characterization of tumorassociated macrophages in experimental gliomas. Neurosurgery 2000; 46: 957-961; discussion 961-952.
9. Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol 2008; 216: 15-24.
10. Wei J, Gabrusiewicz K, Heimberger A. The controversial role of microglia in malignant gliomas. Clin Dev Immunol 2013; 2013: 285246.
11. Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K et al. Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proc Natl Acad Sci USA 2009; 106: 12530-12535.
12. Sliwa M, Markovic D, Gabrusiewicz K, Synowitz M, Glass R, Zawadzka M et al. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain 2007; 130: 476-489.
13. Gabrusiewicz K, Ellert-Miklaszewska A, Lipko M, Sielska M, Frankowska M, Kaminska B. Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One 2011; 6: e23902.
14. Hussain SF, Heimberger AB. Immunotherapy for human glioma: innovative approaches and recent results. Expert Rev Anticancer Ther 2005; 5: 777-790.
15. Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro-Oncology 2006; 8: 261-279.
16. Hussain SF, Yang D, Suki D, Grimm E, Heimberger AB. Innate immune functions of microglia isolated from human glioma patients. J Transl Med 2006; 4: 15.
17. Sielska M, Przanowski P, Wylot B, Gabrusiewicz K, Maleszewska M, Kijewska M et al. Distinct roles of CSF family cytokines in macrophage infiltration and activation in glioma progression and injury response. J Pathol 2013; 230: 310-321.
18. Wei J, Barr J, Kong LY, Wang Y, Wu A, Sharma AK et al. Glioma-associated cancerinitiating cells induce immunosuppression. Clin Cancer Res 2010; 16: 461-473.
19. Wesolowska A, Kwiatkowska A, Slomnicki L, Dembinski M, Master A, Sliwa M et al. Microglia-derived TGF-beta as an important regulator of glioblastoma invasion-an inhibition of TGF-beta-dependent effects by shRNA against human TGF-beta type II receptor. Oncogene 2008; 27: 918-930.
20. Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J Immunol 2012; 189: 444-453.
21. Ellert-Miklaszewska A, Dabrowski M, Lipko M, Sliwa M, Maleszewska M, Kaminska B. Molecular definition of the pro-tumorigenic phenotype of glioma-activated microglia. Glia 2013; 61: 1178-1190.
22. Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S et al. Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol 2003; 54: 388-392.
23. Okada M, Saio M, Kito Y, Ohe N, Yano H, Yoshimura S et al. Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int J Oncol 2009; 34: 1621-1627.
24. Held-Feindt J, Hattermann K, Muerkoster SS, Wedderkopp H, Knerlich-Lukoschus F, Ungefroren H et al. CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs). Exp Cell Res 2010; 316: 1553-1566.
25. Ku MC, Wolf SA, Respondek D, Matyash V, Pohlmann A, Waiczies S et al. GDNF mediates glioblastoma-induced microglia attraction but not astrogliosis. Acta Neuropathol 2013; 125: 609-620.
26. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF et al. CSF-1 R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013; 19: 1264-1272.
27. Raymond A, Ensslin MA, Shur BD. SED1/MFG-E8: a bi-motif protein that orchestrates diverse cellular interactions. J Cell Biochem 2009; 106: 957-966.
28. Yamaguchi Y, Shao Z, Sharif S, Du XY, Myles T, Merchant M et al. Thrombincleaved fragments of osteopontin are overexpressed in malignant glial tumors and provide a molecular niche with survival advantage. J Biol Chem 2013; 288: 3097-3111.
29. Shao Z, Morser J, Leung LL. Thrombin cleavage of osteopontin disrupts a pro-chemotactic sequence for dendritic cells, which is compensated by the release of its pro-chemotactic C-terminal fragment. J Biol Chem 2014; 289: 27146-27158.
30. Agnihotri R, Crawford HC, Haro H, Matrisian LM, Havrda MC, Liaw L. Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J Biol Chem 2001; 276: 28261-28267.
31. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 2013; 121: e57-e69.
32. Anborgh PH, Mutrie JC, Tuck AB, Chambers AF. Role of the metastasis-promoting protein osteopontin in the tumour microenvironment. J Cell Mol Med 2010; 14: 2037-2044.
33. Silvestre JS, Thery C, Hamard G, Boddaert J, Aguilar B, Delcayre A et al. Lactadherin promotes VEGF-dependent neovascularization. Nat Med 2005; 11: 499-506.
34. Pello OM, De Pizzol M, Mirolo M, Soucek L, Zammataro L, Amabile A et al. Role of c-Myc in alternative activation of human macrophages and tumor-associated macrophage biology. Blood 2011; 119: 411-421.
35. Denhardt DT, Noda M, O'Regan AW, Pavlin D, Berman JS. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 2001; 107: 1055-1061.
36. Smith LL, Cheung HK, Ling LE, Chen J, Sheppard D, Pytela R et al. Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by alpha9beta1 integrin. J Biol Chem 1996; 271: 28485-28491.
37. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002; 417: 182-187.
38. Grassinger J, Haylock DN, Storan MJ, Haines GO, Williams B, Whitty GA et al. Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha9beta1 and alpha4beta1 integrins. Blood 2009; 114: 49-59.
39. Cook AC, Tuck AB, McCarthy S, Turner JG, Irby RB, Bloom GC et al. Osteopontin induces multiple changes in gene expression that reflect the six 'hallmarks of cancer' in a model of breast cancer progression. Mol Carcinogen 2005; 43: 225-236.
40. Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J et al. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol 2015; 17: 170-182.
41. Przanowski P, Dabrowski M, Ellert-Miklaszewska A, Kloss M, Mieczkowski J, Kaza B et al. The signal transducers Stat1 and Stat3 and their novel target Jmjd3 drive the expression of inflammatory genes in microglia. J Mol Med (Berl) 2014; 92: 239-254.