Tumor-Associated macrophages (TAMs) form an interconnected cellular supportive network in anaplastic thyroid carcinoma

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Caillou, Bernard ^a   Talbot, Monique ^b   Weyemi, Urbain ^b   Pioche Durieu, Catherine ^b   Ghuzlan, Abir ^a   Bidart, Jean Michel ^a   Chouaib, Salem ^c   Schlumberger, Martin ^a   Dupuy, Corinne ^b  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b CNRS   (France)

^c Unite Inst Natl de la S et de la Rech Med U753 Immunol des Tumeurs Humaines   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD68 ANTIGEN; CONNEXIN 43; GLUCOSE TRANSPORTER 1; PROTEIN P22; PROTEIN P22PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; CD3 ANTIGEN; CYBA PROTEIN, HUMAN; KI 67 ANTIGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SLC2A1 PROTEIN, HUMAN; TUMOR PROTEIN;

ADULT; AGED; ANAPLASTIC THYROID CARCINOMA; ARTICLE; BLOOD VESSEL; CANCER CELL; CANCER SURVIVAL; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PROTEIN EXPRESSION; STROMA; THYROID CARCINOMA; TUMOR ASSOCIATED LEUKOCYTE; CELL FRACTIONATION; CELL JUNCTION; CELL SHAPE; COMPUTER ASSISTED TOMOGRAPHY; MACROPHAGE; METABOLISM; MIDDLE AGED; PATHOLOGY; POSITRON EMISSION TOMOGRAPHY; RADIOGRAPHY; SCINTISCANNING; STAINING; THYROID TUMOR; TUMOR CELL LINE; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; ANTIGENS, CD3; BLOOD VESSELS; CELL LINE, TUMOR; CELL SHAPE; CONNEXIN 43; GAP JUNCTIONS; GLUCOSE TRANSPORTER TYPE 1; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MACROPHAGES; MIDDLE AGED; NADPH OXIDASE; NEOPLASM PROTEINS; POSITRON-EMISSION TOMOGRAPHY; STAINING AND LABELING; SUBCELLULAR FRACTIONS; THYROID NEOPLASMS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 79960644632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022567     Document Type: Article

References (69)

1. Cornett WR, Sharma AK, Day TA, Richardson MS, Hoda RS, et al. (2007) Anaplastic thyroid carcinoma: an overview. Curr Oncol Rep 9: 152-158.
2. Are C, Shaha AR, (2006) Anaplastic thyroid carcinoma: biology, pathogenesis, prognostic factors, and treatment approaches. Ann Surg Oncol 13: 453-464.
3. Ain KB, (1998) Anaplastic thyroid carcinoma: behavior, biology, and therapeutic approaches. Thyroid 8: 715-726.
4. Ordonez NG, El-Naggar AK, Hickey RC, Samaan NA, (1991) Anaplastic thyroid carcinoma. Immunocytochemical study of 32 cases. Am J Clin Pathol 96: 15-24.
5. Ryder M, Ghossein RA, Ricarte-Filho JC, Knauf JA, Fagin JA, (2008) Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocr Relat Cancer 15: 1069-1074.
6. Mantovani A, Bottazzi B, Colotta F, Sozzani S, Ruco L, (1992) The origin and function of tumor-associated macrophages. Immunol Today 13: 265-270.
7. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A, (2006) Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev 25: 315-322.
8. Gordon S, (2003) Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
9. Pollard JW, (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4: 71-78.
10. Mosser DM, (2003) The many faces of macrophage activation. J Leukoc Biol 73: 209-212.
11. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A, (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23: 549-555.
12. Bedard K, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313.
13. Fabriek BO, Dijkstra CD, van den Berg TK, (2005) The macrophage scavenger receptor CD163. Immunobiology 210: 153-160.
14. Schaer DJ, Boretti FS, Schoedon G, Schaffner A, (2002) Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br J Haematol 119: 239-243.
15. Kunisch E, Fuhrmann R, Roth A, Winter R, Lungershausen W, et al. (2004) Macrophage specificity of three anti-CD68 monoclonal antibodies (KP1, EBM11, and PGM1) widely used for immunohistochemistry and flow cytometry. Ann Rheum Dis 63: 774-784.
16. Beranek JT, (2005) CD68 is not a macrophage-specific antigen. Ann Rheum Dis 64: 342-343.
17. Oviedo-Orta E, Howard EW, (2004) Gap junctions and connexin-mediated communication in the immune system. Biochim Biophys Acta 1662: 102-112.
18. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC, (2003) Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 83: 1359-1400.
19. Dbouk HA, Mroue RM, El-Sabban ME, Talhouk RS, (2009) Connexins: a myriad of functions extending beyond assembly of gap junction channels. Cell Commun Signal 7: 4.
20. Goldberg GS, Valiunas V, Brink PR, (2004) Selective permeability of gap junction channels. Biochim Biophys Acta 1662: 96-101.
21. Simek J, Churko J, Shao Q, Laird DW, (2009) Cx43 has distinct mobility within plasma-membrane domains, indicative of progressive formation of gap-junction plaques. J Cell Sci 122: 554-562.
22. Evans WH, De VE, Leybaert L, (2006) The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 397: 1-14.
23. Fu Y, Maianu L, Melbert BR, Garvey WT, (2004) Facilitative glucose transporter gene expression in human lymphocytes, monocytes, and macrophages: a role for GLUT isoforms 1, 3, and 5 in the immune response and foam cell formation. Blood Cells Mol Dis 32: 182-190.
24. Fina L, Molgaard HV, Robertson D, Bradley NJ, Monaghan P, et al. (1990) Expression of the CD34 gene in vascular endothelial cells. Blood 75: 2417-2426.
25. Hinz B, (2007) Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127: 526-537.
26. Frank SJ, Samelson LE, Klausner RD, (1990) The structure and signalling functions of the invariant T cell receptor components. Semin Immunol 2: 89-97.
27. Scholzen T, Gerdes J, (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182: 311-322.
28. Poisson T, Deandreis D, Leboulleux S, Bidault F, Bonniaud G, et al. (2010) 18F-fluorodeoxyglucose positron emission tomography and computed tomography in anaplastic thyroid cancer. Eur J Nucl Med Mol Imaging 37: 2277-2285.
29. Lewis CE, Pollard JW, (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66: 605-612.
30. Mosser DM, Edwards JP, (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969.
31. Condeelis J, Pollard JW, (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266.
32. Barabasi AL, Oltvai ZN, (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113 10.1038/nrg1272 [doi];nrg1272 [pii].
33. Jeong H, Tombor B, Albert R, Oltvai ZN, Barabasi AL, (2000) The large-scale organization of metabolic networks. Nature 407: 651-654.
34. Albert R, Jeong H, Barabasi AL, (2000) Error and attack tolerance of complex networks. Nature 406: 378-382.
35. Brown JM, Giaccia AJ, (1998) The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res 58: 1408-1416.
36. Pries AR, Hopfner M, le NF, Dewhirst MW, Secomb TW, (2010) The shunt problem: control of functional shunting in normal and tumour vasculature. Nat Rev Cancer 10: 587-593.
37. Pries AR, Cornelissen AJ, Sloot AA, Hinkeldey M, Dreher MR, et al. (2009) Structural adaptation and heterogeneity of normal and tumor microvascular networks. PLoS Comput Biol 5: e1000394.
38. Awwad HK, el NM, Mocktar N, Barsoum M, (1986) Intercapillary distance measurement as an indicator of hypoxia in carcinoma of the cervix uteri. Int J Radiat Oncol Biol Phys 12: 1329-1333.
39. Hlatky L, Hahnfeldt P, Folkman J, (2002) Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 94: 883-893.
40. Dome B, Hendrix MJ, Paku S, Tovari J, Timar J, (2007) Alternative vascularization mechanisms in cancer: Pathology and therapeutic implications. Am J Pathol 170: 1-15.
41. Scavelli C, Nico B, Cirulli T, Ria R, Di PG, et al. (2008) Vasculogenic mimicry by bone marrow macrophages in patients with multiple myeloma. Oncogene 27: 663-674.
42. Schmeisser A, Garlichs CD, Zhang H, Eskafi S, Graffy C, et al. (2001) Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc Res 49: 671-680.
43. Anghelina M, Moldovan L, Zabuawala T, Ostrowski MC, Moldovan NI, (2006) A subpopulation of peritoneal macrophages form capillarylike lumens and branching patterns in vitro. J Cell Mol Med 10: 708-715.
44. Havemann K, Pujol BF, Adamkiewicz J, (2003) In vitro transformation of monocytes and dendritic cells into endothelial like cells. Adv Exp Med Biol 522: 47-57.
45. Anghelina M, Schmeisser A, Krishnan P, Moldovan L, Strasser RH, et al. (2002) Migration of monocytes/macrophages in vitro and in vivo is accompanied by MMP12-dependent tunnel formation and by neovascularization. Cold Spring Harb Symp Quant Biol 67: 209-215.
46. Glod J, Kobiler D, Noel M, Koneru R, Lehrer S, et al. (2006) Monocytes form a vascular barrier and participate in vessel repair after brain injury. Blood 107: 940-946.
47. Schmeisser A, Graffy C, Daniel WG, Strasser RH, (2003) Phenotypic overlap between monocytes and vascular endothelial cells. Adv Exp Med Biol 522: 59-74.
48. Li B, Vincent A, Cates J, Brantley-Sieders DM, Polk DB, Young PP, (2009) Low levels of tumor necrosis factor alpha increase tumor growth by inducing an endothelial phenotype of monocytes recruited to the tumor site. Cancer Res 69: 338-348.
49. Brown RS, Leung JY, Fisher SJ, Frey KA, Ethier SP, et al. (1996) Intratumoral distribution of tritiated-FDG in breast carcinoma: correlation between Glut-1 expression and FDG uptake. J Nucl Med 37: 1042-1047.
50. Bustos R, Sobrino F, (1989) Control of fructose 2,6-bisphosphate levels in rat macrophages by glucose and phorbol ester. FEBS Lett 251: 143-146.
51. Brindle K, (2008) New approaches for imaging tumour responses to treatment. Nat Rev Cancer 8: 94-107.
52. Bogsrud TV, Karantanis D, Nathan MA, Mullan BP, Wiseman GA, et al. (2008) 18F-FDG PET in the management of patients with anaplastic thyroid carcinoma. Thyroid 18: 713-719.
53. Kubota R, Yamada S, Kubota K, Ishiwata K, Tamahashi N, et al. (1992) Intratumoral distribution of fluorine-18-fluorodeoxyglucose in vivo: high accumulation in macrophages and granulation tissues studied by microautoradiography. J Nucl Med 33: 1972-1980.
54. Shinkai K, Mukai M, Akedo H, (1986) Superoxide radical potentiates invasive capacity of rat ascites hepatoma cells in vitro. Cancer Lett 32: 7-13.
55. Mukai M, Shinkai K, Tateishi R, Mori Y, Akedo H, (1987) Macrophage potentiation of invasive capacity of rat ascites hepatoma cells. Cancer Res 47: 2167-2171.
56. Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, et al. (2009) Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182: 5693-5701.
57. Kono K, Salazar-Onfray F, Petersson M, Hansson J, Masucci G, et al. (1996) Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing zeta molecules and inhibits tumor-specific T cell-and natural killer cell-mediated cytotoxicity. Eur J Immunol 26: 1308-1313.
58. Yamaguchi H, Pixley F, Condeelis J, (2006) Invadopodia and podosomes in tumor invasion. Eur J Cell Biol 85: 213-218 S0171-9335(05)00174-3.
59. Weaver AM, (2009) Regulation of cancer invasion by reactive oxygen species and Tks family scaffold proteins. Sci Signal 2: e56.
60. Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, et al. (2009) Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2: ra53.
61. Mander PK, Jekabsone A, Brown GC, (2006) Microglia proliferation is regulated by hydrogen peroxide from NADPH oxidase. J Immunol 176: 1046-1052.
62. Groeger G, Quiney C, Cotter TG, (2009) Hydrogen peroxide as a cell survival signaling molecule. Antioxid Redox Signal pp. 10.1089.
63. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, et al. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84.
64. Szatrowski TP, Nathan CF, (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798.
65. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK, (2008) Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res 68: 1777-1785.
66. Giardina SF, Mikami M, Goubaeva F, Yang J, (2007) Connexin 43 confers resistance to hydrogen peroxide-mediated apoptosis. Biochem Biophys Res Commun 362: 747-752.
67. Stout RD, Watkins SK, Suttles J, (2009) Functional plasticity of macrophages: in situ reprogramming of tumor-associated macrophages. J Leukoc Biol 86 (5): 1105-9.
68. Guiducci C, Vicari AP, Sangaletti S, Trinchieri G, Colombo MP, (2005) Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res 65: 3437-3446.
69. Buhtoiarov IN, Lum H, Berke G, Paulnock DM, Sondel PM, et al. (2005) CD40 ligation activates murine macrophages via an IFN-gamma-dependent mechanism resulting in tumor cell destruction in vitro. J Immunol 174: 6013-6022.