A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships

Blood

Volumn 114, Issue 4, 2009, Pages 901-914

  Pucci, Ferdinando ^a,b,c   Venneri, Mary Anna ^a,b   Biziato, Daniela ^a,b   Nonis, Alessandro ^c   Moi, Davide ^a,b   Sica, Antonio ^d,e   Di Serio, Clelia ^c   Naldini, Luigi ^a,b,c   De Palma, Michele ^a,b  

^a San Raf faele Institute   (Italy)

^b SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; GREEN FLUORESCENT PROTEIN; MICRORNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INVASION; CELL ISOLATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; MACROPHAGE; MONOCYTE; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; ANIMAL EMBRYO; BLOOD CELL; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BLOOD CELLS; CHEMOTAXIS, LEUKOCYTE; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MACROPHAGES; MICE; MICE, TRANSGENIC; MONOCYTES; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTOR, TIE-2;

EID: 67651111095     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-01-200931     Document Type: Article

References (57)

1. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6:24-37. (Pubitemid 43053650)
2. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436-444.
3. Kerbel RS. Tumor angiogenesis. N Engl J Med. 2008;358:2039-2049.
4. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer. 2008;8:618-631.
5. De Palma M, Naldini L. Role of haematopoietic cells and endothelial progenitors in tumour angiogenesis. Biochim Biophys Acta. 2006;1766:159-166. (Pubitemid 44175637)
6. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest. 2007;117:1155-1166. (Pubitemid 46718400)
7. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66:605-612. (Pubitemid 43165918)
8. Geissmann F, Auffray C, Palframan R, et al. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol. 2008;86:398-408. (Pubitemid 351948210)
9. Sunderkotter C, Nikolic T, Dillon MJ, et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol. 2004;172:4410-4417. (Pubitemid 38375256)
10. Pahler JC, Tazzyman S, Erez N, et al. Plasticity in tumor-promoting inflammation: impairment of macrophage recruitment evokes a compensatory neutrophil response. Neoplasia. 2008;10:329-340.
11. Qu C, Edwards EW, Tacke F, et al. Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J Exp Med. 2004;200:1231-1241. (Pubitemid 39552565)
12. Egeblad M, Ewald AJ, Askautrud HA, et al. Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis Model Mech. 2008;1:155-167.
13. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med. 2003;9:789-795. (Pubitemid 36749231)
14. De Palma M, Venneri MA, Galli R, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell. 2005;8:211-226. (Pubitemid 41317592)
15. De Palma M, Murdoch C, Venneri MA, Naldini L, Lewis CE. Tie2-expressing monocytes: regulation of tumor angiogenesis and therapeutic implications. Trends Immunol. 2007;28:545-550. (Pubitemid 350101421)
16. Venneri MA, De Palma M, Ponzoni M, et al. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood. 2007;109:5276-5285. (Pubitemid 46890548)
17. Murdoch C, Tazzyman S, Webster S, Lewis CE. Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. J Immunol. 2007;178:7405-7411. (Pubitemid 46847468)
18. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009;10:165-177.
19. Ovchinnikov DA. Macrophages in the embryo and beyond: much more than just giant phagocytes. Genesis. 2008;46:447-462.
20. Rae F, Woods K, Sasmono T, et al. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter. Dev Biol. 2007;308:232-246. (Pubitemid 47087792)
21. Brown BD, Venneri MA, Zingale A, Sergi Sergi L, Naldini L. Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med. 2006;12:585-591.
22. Yuan JS, Reed A, Chen F, Stewart CN Jr. Statistical analysis of real-time PCR data. BMC Bioinformatics. 2006;7:85. (Pubitemid 43362095)
23. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549-555. (Pubitemid 35223554)
24. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer. 2004;4:11-22.
25. Strieter RM, Belperio JA, Burdick MD, Keane MP. CXC chemokines in angiogenesis relevant to chronic fibroproliferation. Curr Drug Targets Inflamm Allergy. 2005;4:23-26.
26. Lin EY, Jones JG, Li P, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003;163:2113-2126. (Pubitemid 37310040)
27. 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;14:299-311.
28. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004;303:83-86. (Pubitemid 38055775)
29. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol. 2009;9:259-270.
30. Ojalvo LS, King W, Cox D, Pollard JW. High-density gene expression analysis of tumor-associated macrophages from mouse mammary tumors. Am J Pathol. 2009;174:1048-1064.
31. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228. (Pubitemid 29377293)
32. Tepper OM, Capla JM, Galiano RD, et al. Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood. 2005;105:1068-1077.
33. Modarai B, Burnand KG, Sawyer B, Smith A. Endothelial progenitor cells are recruited into resolving venous thrombi. Circulation. 2005;111:2645-2653. (Pubitemid 40740865)
34. Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell. 2008;13:193-205.
35. Du R, Lu KV, Petritsch C, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13:206-220. (Pubitemid 351318372)
36. Shaked Y, Henke E, Roodhart JM, et al. Rapid chemotherapy-induced acute endothelial progenitor cell mobilization: implications for antiangiogenic drugs as chemosensitizing agents. Cancer Cell. 2008;14:263-273.
37. Purhonen S, Palm J, Rossi D, et al. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci U S A. 2008;105:6620-6625. (Pubitemid 351754556)
38. Schledzewski K, Falkowski M, Moldenhauer G, et al. Lymphatic endothelium-specific hyaluronan receptor LYVE-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissue in vivo and in bone marrow cultures in vitro: implications for the assessment of lymphangiogenesis. J Pathol. 2006;209:67-77.
39. Cho CH, Koh YJ, Han J, et al. Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ Res. 2007;100:e47-e57. (Pubitemid 46673270)
40. Chen R, Alvero AB, Silasi DA, Steffensen KD, Mor G. Cancers take their Toll: the function and regulation of Toll-like receptors in cancer cells. Oncogene. 2008;27:225-233.
41. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4:528-539.
42. del Fresno C, Otero K, Gomez-Garcia L, et al. Tumor cells deactivate human monocytes by upregulating IL-1 receptor associated kinase-M expression via CD44 and TLR4. J Immunol. 2005;174:3032-3040. (Pubitemid 40279724)
43. Hiratsuka S, Watanabe A, Sakurai Y, et al. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10:1349-1355.
44. Takakura N. Role of hematopoietic lineage cells as accessory components in blood vessel formation. Cancer Sci. 2006;97:568-574. (Pubitemid 44056603)
45. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438:932-936.
46. Neufeld G, Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer. 2008;8:632-645.
47. Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neoangiogenesis. Trends Immunol. 2007;28:299-307. (Pubitemid 46963141)
48. Liu Y, Wada R, Yamashita T, et al. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest. 2000;106:951-961. (Pubitemid 30800853)
49. Hughes JE, Srinivasan S, Lynch KR, Proia RL, Ferdek P, Hedrick CC. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ Res. 2008;102:950-958. (Pubitemid 351591554)
50. Biswas SK, Gangi L, Paul S, et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood. 2006;107:2112-2122. (Pubitemid 43289397)
51. Passlick B, Flieger D, Ziegler-Heitbrock HW. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood. 1989;74:2527-2534. (Pubitemid 19286475)
52. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953-964.
53. Auffray C, Fogg D, Garfa M, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317:666-670. (Pubitemid 47229966)
54. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047. (Pubitemid 350179569)
55. Varol C, Landsman L, Fogg DK, et al. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med. 2007;204:171-180. (Pubitemid 46148767)
56. Gallina G, Dolcetti L, Serafini P, et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest. 2006;116:2777-2790. (Pubitemid 44511641)
57. Shipley JM, Wesselschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci U S A. 1996;93:3942-3946.