Stroma-derived fibrinogen-like protein 2 activates cancer-associated fibroblasts to promote tumor growth in lung cancer

International Journal of Biological Sciences

Volumn 13, Issue 6, 2017, Pages 804-814

  Zhu, Ying ^a,b   Zhang, Longhui ^a,b   Zha, Haoran ^a,b   Yang, Fei ^a   Hu, Chunyan ^a,b   Chen, Lin ^c   Guo, Bo ^a   Zhu, Bo ^a,b  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Chongqing Key Laboratory of Neurology   (China)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Cancer associated fibroblast; Fgl2; Lung cancer; Myeloid derived suppressor cell

Indexed keywords

FGL2 PROTEIN, HUMAN; FIBRINOGEN; STROMAL CELL DERIVED FACTOR 1;

ANIMAL; APOPTOSIS; CANCER ASSOCIATED FIBROBLAST; CELL LINE; FEMALE; FLOW CYTOMETRY; GENETICS; KNOCKOUT MOUSE; LEWIS CARCINOMA; LUNG TUMOR; MALE; METABOLISM; MOUSE; MYELOID-DERIVED SUPPRESSOR CELL; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CANCER-ASSOCIATED FIBROBLASTS; CARCINOMA, LEWIS LUNG; CELL LINE; CHEMOKINE CXCL12; FEMALE; FIBRINOGEN; FLOW CYTOMETRY; LUNG NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; MYELOID-DERIVED SUPPRESSOR CELLS; TUMOR MICROENVIRONMENT;

EID: 85020465136     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.19398     Document Type: Article

References (45)

1. Turley SJ, Cremasco V, Astarita JL. Immunological hallmarks of stromal cells in the tumour microenvironment. Nature reviews Immunology. 2015; 15: 669-82.
2. Brock A, Krause S, Ingber DE. Control of cancer formation by intrinsic genetic noise and microenvironmental cues. Nature reviews Cancer. 2015; 15: 499-509.
3. Liu J, Tan Y, Zhang J, et al. C5aR, TNF-alpha, and FGL2 contribute to coagulation and complement activation in virus-induced fulminant hepatitis. Journal of hepatology. 2015; 62: 354-62.
4. Liu Y, Xu S, Xiao F, et al. The FGL2/fibroleukin prothrombinase is involved in alveolar macrophage activation in COPD through the MAPK pathway. Biochemical and biophysical research communications. 2010; 396: 555-61.
5. Clark DA, Foerster K, Fung L, et al. The fgl2 prothrombinase/fibroleukin gene is required for lipopolysaccharide-triggered abortions and for normal mouse reproduction. Molecular human reproduction. 2004; 10: 99-108.
6. Ghanekar A, Mendicino M, Liu H, et al. Endothelial induction of fgl2 contributes to thrombosis during acute vascular xenograft rejection. Journal of immunology. 2004; 172: 5693-701.
7. Joller N, Lozano E, Burkett PR, et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity. 2014; 40: 569-81.
8. Chan CW, Kay LS, Khadaroo RG, et al. Soluble fibrinogen-like protein 2/fibroleukin exhibits immunosuppressive properties: suppressing T cell proliferation and inhibiting maturation of bone marrow-derived dendritic cells. Journal of immunology. 2003; 170: 4036-44.
9. Liu H, Shalev I, Manuel J, et al. The FGL2-FcgammaRIIB pathway: a novel mechanism leading to immunosuppression. European journal of immunology. 2008; 38: 3114-26.
10. Yuwaraj S, Ding J, Liu M, et al. Genomic characterization, localization, and functional expression of FGL2, the human gene encoding fibroleukin: a novel human procoagulant. Genomics. 2001; 71: 330-8.
11. Su K, Chen F, Yan WM, et al. Fibrinogen-like protein 2/fibroleukin prothrombinase contributes to tumor hypercoagulability via IL-2 and IFN-gamma. World journal of gastroenterology. 2008; 14: 5980-9.
12. Liu Y, Xu L, Zeng Q, et al. Downregulation of FGL2/prothrombinase delays HCCLM6 xenograft tumour growth and decreases tumour angiogenesis. Liver international: official journal of the International Association for the Study of the Liver. 2012; 32: 1585-95.
13. Yan J, Kong LY, Hu J, et al. FGL2 as a Multimodality Regulator of Tumor-Mediated Immune Suppression and Therapeutic Target in Gliomas. Journal of the National Cancer Institute. 2015; 107.
14. Hu J, Yan J, Rao G, et al. The Duality of Fgl2 - Secreted Immune Checkpoint Regulator Versus Membrane-Associated Procoagulant: Therapeutic Potential and Implications. International reviews of immunology. 2014.
15. Sharon Y, Alon L, Glanz S, et al. Isolation of normal and cancer-associated fibroblasts from fresh tissues by Fluorescence Activated Cell Sorting (FACS). Journal of visualized experiments: JoVE. 2013: e4425.
16. Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science signaling. 2013; 6: pl1.
17. Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer discovery. 2012; 2: 401-4.
18. Qin WZ, Li QL, Chen WF, et al. Overexpression of fibrinogen-like protein 2 induces epithelial-to-mesenchymal transition and promotes tumor progression in colorectal carcinoma. Medical oncology. 2014; 31: 181.
19. Woo EY, Chu CS, Goletz TJ, et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer research. 2001; 61: 4766-72.
20. Sawant A, Schafer CC, Jin TH, et al. Enhancement of antitumor immunity in lung cancer by targeting myeloid-derived suppressor cell pathways. Cancer research. 2013; 73: 6609-20.
21. Dai F, Liu L, Che G, et al. The number and microlocalization of tumor-associated immune cells are associated with patient's survival time in non-small cell lung cancer. BMC cancer. 2010; 10: 220.
22. Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nature reviews Immunology. 2005; 5: 641-54.
23. Rodriguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunological reviews. 2008; 222: 180-91.
24. Yang L, Huang J, Ren X, et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer cell. 2008; 13: 23-35.
25. Liu Y, Lai L, Chen Q, et al. MicroRNA-494 is required for the accumulation and functions of tumor-expanded myeloid-derived suppressor cells via targeting of PTEN. Journal of immunology. 2012; 188: 5500-10.
26. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-74.
27. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer cell. 2012; 21: 309-22.
28. Erez N, Truitt M, Olson P, et al. Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-kappaB-Dependent Manner. Cancer cell. 2010; 17: 135-47.
29. Olumi AF, Grossfeld GD, Hayward SW, et al. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer research. 1999; 59: 5002-11.
30. Singh S, Ross SR, Acena M, et al. Stroma is critical for preventing or permitting immunological destruction of antigenic cancer cells. The Journal of experimental medicine. 1992; 175: 139-46.
31. Iijima J, Konno K, Itano N. Inflammatory alterations of the extracellular matrix in the tumor microenvironment. Cancers. 2011; 3: 3189-205.
32. Liao D, Luo Y, Markowitz D, et al. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PloS one. 2009; 4: e7965.
33. Polanska UM, Orimo A. Carcinoma-associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells. Journal of cellular physiology. 2013; 228: 1651-7.
34. Ohlund D, Elyada E, Tuveson D. Fibroblast heterogeneity in the cancer wound. The Journal of experimental medicine. 2014; 211: 1503-23.
35. Madar S, Goldstein I, Rotter V. 'Cancer associated fibroblasts'--more than meets the eye. Trends in molecular medicine. 2013; 19: 447-53.
36. Shalev I, Wong KM, Foerster K, et al. The novel CD4+CD25+ regulatory T cell effector molecule fibrinogen-like protein 2 contributes to the outcome of murine fulminant viral hepatitis. Hepatology. 2009; 49: 387-97.
37. Sun Y, Xi D, Ding W, et al. Soluble FGL2, a novel effector molecule of activated hepatic stellate cells, regulates T-cell function in cirrhotic patients with hepatocellular carcinoma. Hepatology international. 2014; 8: 567-75.
38. Gascard P, Tlsty TD. Carcinoma-associated fibroblasts: orchestrating the composition of malignancy. Genes & development. 2016; 30: 1002-19.
39. Foerster K, Helmy A, Zhu Y, et al. The novel immunoregulatory molecule FGL2: a potential biomarker for severity of chronic hepatitis C virus infection. Journal of hepatology. 2010; 53: 608-15.
40. Pickup M, Novitskiy S, Moses HL. The roles of TGFbeta in the tumour microenvironment. Nature reviews Cancer. 2013; 13: 788-99.
41. Moskovits N, Kalinkovich A, Bar J, et al. p53 Attenuates cancer cell migration and invasion through repression of SDF-1/CXCL12 expression in stromal fibroblasts. Cancer research. 2006; 66: 10671-6.
42. Obermajer N, Muthuswamy R, Odunsi K, et al. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer research. 2011; 71: 7463-70.
43. Domanska UM, Timmer-Bosscha H, Nagengast WB, et al. CXCR4 inhibition with AMD3100 sensitizes prostate cancer to docetaxel chemotherapy. Neoplasia. 2012; 14: 709-18.
44. Li X, Ma Q, Xu Q, et al. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of Hedgehog pathway. Cancer letters. 2012; 322: 169-76.
45. Feig C, Jones JO, Kraman M, et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110: 20212-7.