A role for miR-155 in enabling tumor-infiltrating innate immune cells to mount effective antitumor responses in mice

Blood

Volumn 122, Issue 2, 2013, Pages 243-252

  Zonari, Erika ^a,b   Pucci, Ferdinando ^a,c   Saini, Massimo ^a,c   Mazzieri, Roberta ^a,c   Politi, Letterio S ^d   Gentner, Bernhard ^a,c   Naldini, Luigi ^a,c  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR6; CHLORDANE; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 13; INTERLEUKIN 6; MICRORNA 155; PROTEIN KINASE B; MICRORNA; MIRN155 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BLOOD CELL COUNT; BONE MARROW CELL; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GRANULOCYTE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNE RESPONSE; INNATE IMMUNITY; MONOCYTE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR VOLUME; UPREGULATION; ANIMAL; BREAST TUMOR; DISEASE MODEL; ENZYME ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ORDER; GENE SILENCING; GENE VECTOR; GENETICS; IMMUNOLOGY; INFLAMMATION; MACROPHAGE; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; BONE MARROW CELLS; BREAST NEOPLASMS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENE ORDER; GENETIC VECTORS; IMMUNITY, INNATE; INFLAMMATION; MACROPHAGES; MICE; MICRORNAS; MYELOID CELLS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TUMOR BURDEN;

EID: 84884478648     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-449306     Document Type: Article

References (50)

1. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309-322.
2. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162-174.
3. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 1996;56(20):4625-4629. (Pubitemid 26338061)
4. Steidl C, Lee T, Shah SP, et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med. 2010;362(10):875-885.
5. Sconocchia G, Zlobec I, Lugli A, et al. Tumor infiltration by FcγRIII (CD16)+ myeloid cells is associated with improved survival in patients with colorectal carcinoma. Int J Cancer. 2011;128(11):2663-2672.
6. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell. 2005;8(3):211-226. (Pubitemid 41317592)
7. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010;141(1):39-51.
8. Venneri MA, De Palma M, Ponzoni M, et al. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood. 2007;109(12):5276-5285. (Pubitemid 46890548)
9. Pucci F, Venneri MA, Biziato D, et al. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood. 2009;114(4):901-914.
10. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-233.
11. Squadrito ML, Pucci F, Magri L, et al. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep. 2012;1(2):141-154.
12. O'Connell RM, Rao DS, Chaudhuri AA, et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med. 2008;205(3):585-594. (Pubitemid 351439306)
13. Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science. 2007;316(5824):608-611. (Pubitemid 46683148)
14. Thai TH, Calado DP, Casola S, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316(5824):604-608. (Pubitemid 46683147)
15. Lu LF, Thai TH, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity. 2009;30(1):80-91.
16. Brown BD, Gentner B, Cantore A, et al. Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat Biotechnol. 2007;25(12):1457-1467. (Pubitemid 350233144)
17. Tili E, Michaille JJ, Cimino A, et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol. 2007;179(8):5082-5089.
18. Gentner B, Schira G, Giustacchini A, Amendola M, Brown BD, Ponzoni M, Naldini L. Stable knockdown of microRNA in vivo by lentiviral vectors. Nat Methods. 2009;6(1):63-66.
19. Amendola M, Passerini L, Pucci F, Gentner B, Bacchetta R, Naldini L. Regulated and multiple miRNA and siRNA delivery into primary cells by a lentiviral platform. Mol Ther. 2009;17(6):1039-1052.
20. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003;163(5):2113-2126. (Pubitemid 37310040)
21. Gentner B, Visigalli I, Hiramatsu H, et al. Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med. 2010;2(58):58ra84.
22. O'Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA. 2007;104(5):1604-1609. (Pubitemid 46214637)
23. Vigorito E, Perks KL, Abreu-Goodger C, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007;27(6):847-859. (Pubitemid 350258623)
24. Androulidaki A, Iliopoulos D, Arranz A, et al. The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity. 2009;31(2):220-231.
25. De Palma M, Mazzieri R, Politi LS, et al. Tumor-targeted interferon-alpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell. 2008;14(4):299-311.
26. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest. 2007;117(5):1155-1166. (Pubitemid 46718400)
27. Yang L, DeBusk LM, Fukuda K, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004;6(4):409-421. (Pubitemid 39361441)
28. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 2011;331(6024):1565-1570.
29. Baran CP, Tridandapani S, Helgason CD, Humphries RK, Krystal G, Marsh CB. The inositol 5′-phosphatase SHIP-1 and the Src kinase Lyn negatively regulate macrophage colonystimulating factor-induced Akt activity. J Biol Chem. 2003;278(40):38628-38636. (Pubitemid 37221760)
30. Mondal S, Subramanian KK, Sakai J, Bajrami B, Luo HR. Phosphoinositide lipid phosphatase SHIP1 and PTEN coordinate to regulate cell migration and adhesion. Mol Biol Cell. 2012;23(7):1219-1230.
31. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA. 2009;106(17):7113-7118.
32. Rajaram MV, Butchar JP, Parsa KV, Cremer TJ, Amer A, Schlesinger LS, Tridandapani S. Akt and SHIP modulate Francisella escape from the phagosome and induction of the Fas-mediated death pathway. PLoS ONE. 2009;4(11):e7919.
33. Chang HC, Han L, Jabeen R, Carotta S, Nutt SL, Kaplan MHPU. PU.1 regulates TCR expression by modulating GATA-3 activity. J Immunol. 2009;183(8):4887-4894.
34. Mihara M, Hashizume M, Yoshida H, Suzuki M, Shiina M. IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clin Sci (Lond). 2012;122(4):143-159.
35. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122(3):787-795.
36. Arranz A, Doxaki C, Vergadi E, et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc Natl Acad Sci USA. 2012;109(24):9517-9522.
37. Cai X, Yin Y, Li N, et al. Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J Mol Cell Biol. 2012;4(5):341-343.
38. Cubillos-Ruiz JR, Baird JR, Tesone AJ, et al. Reprogramming tumor-associated dendritic cells in vivo using miRNA mimetics triggers protective immunity against ovarian cancer. Cancer Res. 2012;72(7):1683-1693.
39. Huffaker TB, Hu R, Runtsch MC, et al. Epistasis between microRNAs 155 and 146a during T cell-mediated antitumor immunity. Cell Rep. 2012;2(6):1697-1709.
40. Hamilton JA. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol. 2008;8(7):533-544. (Pubitemid 351913679)
41. Sethupathy P, Borel C, Gagnebin M, et al. Human microRNA-155 on chromosome 21 differentially interacts with its polymorphic target in the AGTR1 3′ untranslated region: a mechanism for functional single-nucleotide polymorphisms related to phenotypes. Am J Hum Genet. 2007;81(2):405-413. (Pubitemid 47236088)
42. Swirski FK, Nahrendorf M, Etzrodt M, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325(5940):612-616.
43. Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med. 2012;4(3):143-159.
44. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103(7):2257-2261. (Pubitemid 43271657)
45. Yanaihara N, Caplen N, Bowman E, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9(3):189-198. (Pubitemid 43357945)
46. Chen J, Wang BC, Tang JH. Clinical significance of microRNA-155 expression in human breast cancer. J Surg Oncol. 2012;106(3):260-266.
47. Lee DW, Futami M, Carroll M, et al. Loss of SHIP-1 protein expression in high-risk myelodysplastic syndromes is associated with miR-210 and miR-155. Oncogene. 2012;31(37):4085-4094.
48. Gambari R, Fabbri E, Borgatti M, et al. Targeting microRNAs involved in human diseases: a novel approach for modification of gene expression and drug development. Biochem Pharmacol. 2011;82(10):1416-1429.
49. Lovat F, Valeri N, Croce CM. MicroRNAs in the pathogenesis of cancer. Semin Oncol. 2011;38(6):724-733.
50. Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M. microRNAs in cancer management. Lancet Oncol. 2012;13(6):e249-e258.