Interleukin-27 re-educates intratumoral myeloid cells and down-regulates stemness genes in non-small cell lung cancer

Oncotarget

Volumn 6, Issue 6, 2015, Pages 3694-3708

  Airoldi, Irma ^a   Tupone, Maria Grazia ^b   Esposito, Silvia ^b   Russo, Marco V ^b   Barbarito, Giulia ^a   Cipollone, Giuseppe ^b,c   Di Carlo, Emma ^b  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c Ospedale 'SS Annunziata'   (Italy)

Author keywords

Cytokines; Immunotherapy; Inflammation; Lung cancer; Tumor microenvironment

Indexed keywords

CXCL3 CHEMOKINE; INTERLEUKIN 27; INTERLEUKIN 27 ALPHA RECEPTOR; INTERLEUKIN RECEPTOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; CYTOKINE; RECOMBINANT PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KLF4 GENE; MAJOR CLINICAL STUDY; MALE; MOUSE; NESTIN GENE; NON SMALL CELL LUNG CANCER; NONHUMAN; NOTCH1 GENE; OCT4A GENE; SHH GENE; SNAI1 GENE; SNAI2 GENE; SOX2 GENE; ZEB1 GENE; ANIMAL; BONE MARROW CELL; CANCER STEM CELL; CARCINOMA, NON-SMALL-CELL LUNG; DRUG EFFECTS; DRUG SCREENING; GENETICS; IMMUNOTHERAPY; LUNG NEOPLASMS; METABOLISM; MIDDLE AGED; NONOBESE DIABETIC MOUSE; NUDE MOUSE; PATHOLOGY; PROCEDURES; SCID MOUSE;

AGED; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; CYTOKINES; DOWN-REGULATION; FEMALE; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-27; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; MIDDLE AGED; MYELOID CELLS; NEOPLASTIC STEM CELLS; RECOMBINANT PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924268722     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2797     Document Type: Article

References (50)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer 2013; Available from http://globocan.iarc.fr.
3. Lortet-Tieulent J, Soerjomataram I, Ferlay J, Rutherford M, Weiderpass E, Bray F. International trends in lung cancer incidence by histological subtype: adenocarcinoma stabilizing in men but still increasing in women. Lung Cancer. 2014; 84:13-22.
4. Majem M, Pallarès C. An update on molecularly targeted therapies in second-and third-line treatment in non-small cell lung cancer: focus on EGFR inhibitors and anti-angiogenic agents. Clin Transl Oncol. 2013; 15:343-357.
5. Cardarella S, Johnson BE. The impact of genomic changes on treatment of lung cancer. Am J Respir Crit Care Med. 2013; 188:770-775.
6. Vignali DA, Kuchroo VK. IL-12 family cytokines: immunological playmakers. Nat Immunol. 2012; 13:722-728.
7. Bosmann M, Ward PA. Modulation of inflammation by interleukin-27. J Leukoc Biol. 2013; 94:1159-1165.
8. Zorzoli A, Di Carlo E, Cocco C, Ognio E, Ribatti D, Ferretti E, Dufour C, Locatelli F, Montagna D, Airoldi I. Interleukin-27 inhibits the growth of pediatric acute myeloid leukemia in NOD/SCID/Il2rg-/-mice. Clin Cancer Res. 2012; 18:1630-1640.
9. Murugaiyan G, Saha B. IL-27 in tumor immunity and immunotherapy. Trends Mol Med. 2013; 19:108-116.
10. Di Carlo E, Sorrentino C, Zorzoli A, Di Meo S, Tupone MG, Ognio E, Mincione G, Airoldi I. The antitumor potential of Interleukin-27 in prostate cancer. Oncotarget. 2014; 5:10332-10341.
11. Ho MY, Leu SJ, Sun GH, Tao MH, Tang SJ, Sun KH. IL-27 directly restrains lung tumorigenicity by suppressing cyclooxygenase-2-mediated activities. J Immunol. 2009; 183:6217-6226.
12. Kachroo P, Lee MH, Zhang L, Baratelli F, Lee G, Srivastava MK, Wang G, Walser TC, Krysan K, Sharma S, Dubinett SM, Lee JM. IL-27 inhibits epithelial-mesenchymal transition and angiogenic factor production in a STAT1-dominant pathway in human non-small cell lung cancer. J Exp Clin Cancer Res. 2013; 32:97.
13. Zhang J, Tian H, Li C, Cheng L, Zhang S, Zhang X, Wang R, Xu F, Dai L, Shi G, Chen X, Li Y, Du T, et al. Antitumor effects obtained by autologous Lewis lung cancer cell vaccine engineered to secrete mouse interleukin 27 by means of cationic liposome. Mol Immunol. 2013; 55:264-274.
14. Strieter RM, Polverini PJ, Kunkel SL, Arenberg DA, Burdick MD, Kasper J, Dzuiba J, Van Damme J, Walz A, Marriott D, Chan SY, Roczniak S, Shanafelt AB. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J Biol Chem. 1995; 270:27348-27357.
15. Geiser T, Dewald B, Ehrengruber MU, Clark-Lewis I, Baggiolini M. The interleukin-8-related chemotactic cytokines GRO alpha, GRO beta, and GRO gamma activate human neutrophil and basophil leukocytes. J Biol Chem. 1993; 268:15419-15424.
16. Baggiolini M, Dewald B, Moser B. Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol. 1994; 55:97-179.
17. Koch AE, Kunkel SL, Harlow LA, Mazarakis DD, Haines GK, Burdick MD, Pope RM, Strieter RM. Macrophage inflammatory protein-1 alpha. A novel chemotactic cytokine for macrophages in rheumatoid arthritis. J Clin Invest. 1994; 93:921-928.
18. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM. Nestin expression-a property of multi-lineage progenitor cells? Cell Mol Life Sci. 2004; 61:2510-2522.
19. Narita K, Matsuda Y, Seike M, Naito Z, Gemma A, Ishiwata T. Nestin regulates proliferation, migration, invasion and stemness of lung adenocarcinoma. Int J Oncol. 2014; 44:1118-1130.
20. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009; 119:1420-1428.
21. Sánchez-Tilló E, Liu Y, de Barrios O, Siles L, Fanlo L, Cuatrecasas M, Darling DS, Dean DC, Castells A, Postigo A. EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci. 2012; 69:3429-3456.
22. Grotegut S, von Schweinitz D, Christofori G, Lehembre F. Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J. 2006; 25:3534-3545.
23. Leroy P, Mostov KE. Slug is required for cell survival during partial epithelial-mesenchymal transition of HGF-induced tubulogenesis. Mol Biol Cell. 2007; 18:1943-1952.
24. Xu S, Neamati N. gp130: a promising drug target for cancer therapy. Expert Opin Ther Targets. 2013; 17:1303-1328.
25. Haura EB, Livingston S, Coppola D. Autocrine interleukin-6/interleukin-6 receptor stimulation in non-small-cell lung cancer. Clin Lung Cancer. 2006; 7:273-275.
26. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, Lebecque S, Fridman WH, Cadranel J. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol. 2008; 26:4410-4417.
27. Sautès-Fridman C, Cherfils-Vicini J, Damotte D, Fisson S, Fridman WH, Cremer I, Dieu-Nosjean MC. Tumor microenvironment is multifaceted. Cancer Metastasis Rev. 2011; 30:13-25.
28. McCarthy F, Roshani R, Steele J, Hagemann T. Current clinical immunotherapy targets in advanced nonsmall cell lung cancer (NSCLC). J Leukoc Biol. 2013; 94:1201-1206.
29. Chambers SE, O'Neill CL, O'Doherty TM, Medina RJ, Stitt AW. The role of immune-related myeloid cells in angiogenesis. Immunobiology. 2013; 218:1370-1375.
30. Galdiero MR, Bonavita E, Barajon I, Garlanda C, Mantovani A, Jaillon S. Tumor associated macrophages and neutrophils in cancer. Immunobiology. 2013; 218:1402-1410.
31. Tecchio C, Scapini P, Pizzolo G, Cassatella MA. On the cytokines produced by human neutrophils in tumors. Semin Cancer Biol. 2013; 23:159-170.
32. Di Carlo E, Forni G, Lollini P, Colombo MP, Modesti A, Musiani P. The intriguing role of polymorphonuclear neutrophils in antitumor reactions. Blood. 2001; 97:339-345.
33. de Fraipont F, Nicholson AC, Feige JJ, Van Meir EG. Thrombospondins and tumor angiogenesis. Trends Mol Med. 2001; 7:401-407.
34. Dejana E, Vestweber D. The role of VE-cadherin in vascular morphogenesis and permeability control. Prog Mol Biol Transl Sci. 2013; 116:119-144.
35. Ishikawa F, Miyazono K, Hellman U, Drexler H, Wernstedt C, Hagiwara K, Usuki K, Takaku F, Risau W, Heldin CH. Identification of angiogenic activity and the cloning and expression of platelet-derived endothelial cell growth factor. Nature. 1989; 338:557-562.
36. Wirtz S, Tubbe I, Galle PR, Schild HJ, Birkenbach M, Blumberg RS, Neurath MF. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J Exp Med. 2006; 203:1875-1881.
37. Pflanz S, Hibbert L, Mattson J, Rosales R, Vaisberg E, Bazan JF, Phillips JH, McClanahan TK, de Waal Malefyt R, Kastelein RA. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J Immunol. 2004; 172:2225-2231.
38. Rinchai D, Khaenam P, Kewcharoenwong C, Buddhisa S, Pankla R, Chaussabel D, Bancroft GJ, Lertmemongkolchai G. Production of interleukin-27 by human neutrophils regulates their function during bacterial infection. Eur J Immunol. 2012; 42:3280-3290.
39. Radisky DC, LaBarge MA. Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell. 2008; 2:511-512.
40. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010; 140:62-73.
41. Hayashida T, Jinno H, Kitagawa Y, Kitajima M. Cooperation of cancer stem cell properties and epithelial-mesenchymal transition in the establishment of breast cancer metastasis. J Oncol. 2011;2011:591427. doi: 10.1155/2011/591427.
42. Chambers I, Tomlinson SR. The transcriptional foundation of pluripotency. Development. 2009; 136:2311-2322.
43. Merchant AA, Matsui W. Targeting Hedgehog-a cancer stem cell pathway. Clin Cancer Res. 2010; 16:3130-3140.
44. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer. 2011; 11:268-277.
45. Dibra D, Cutrera J, Xia X, Li S. WSX1 expression in tumors induces immune tolerance via suppression of effector immune cells. PLoS One. 2011; 6:e19072.
46. Sobin LH, Gospodarowicz MK, Wittekind CH. TNM classification of malignant tumors, 7th edition. 2009; Hoboken, NJ: Wiley-Blackwell. ISBN: 978-1-4443-3241-4.
47. Kerr KM. Pulmonary preinvasive neoplasia. J Clin Pathol. 2001; 54:257-271.
48. Wistuba II, Gazdar AF. Lung cancer preneoplasia. Annu Rev Pathol. 2006; 1:331-348.
49. Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC. Pathology and genetics of tumours of the lung, pleura, thymus and heart, 3rd ed. World Health Organization international classification of tumors. 2004; Geneva: WHO Press.
50. Sjöö F, Hassan Z, Abedi-Valugerdi M, Griskevicius L, Nilsson C, Remberger M, Aschan J, Concha H, Gaughan U, Hassan M. Myeloablative and immunosuppressive properties of treosulfan in mice. Exp Hematol. 2006; 34:115-121.