Stromal estrogen receptor-α promotes tumor growth by normalizing an increased angiogenesis

Cancer Research

Volumn 72, Issue 12, 2012, Pages 3010-3019

  Péqueux, Christel ^a,d   Raymond Letron, Isabelle ^b   Blacher, Silvia ^d   Boudou, Frédéric ^a   Adlanmerini, Marine ^a   Fouque, Marie José ^a   Rochaix, Philippe ^c   Noël, Agnès ^d   Foidart, Jean Michel ^d   Krust, Andrée ^e   Chambon, Pierre ^e   Brouchet, Laurent ^a   Arnal, Jean François ^a   Lenfant, Françoise ^a  

^a University Hospital of Toulouse   (France)

^b ENVT   (France)

^c INSTITUT CLAUDIUS REGAUD   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; ESTROGEN RECEPTOR ALPHA; FIBROBLAST GROWTH FACTOR 2; THROMBOCYTE FACTOR 4; THROMBOSPONDIN 1; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ADAPTIVE IMMUNITY; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; IMMUNOBLOTTING; IMMUNOCOMPETENCE; IMMUNOCYTOCHEMISTRY; MICROENVIRONMENT; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OVARIECTOMY; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR VOLUME; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; MELANOMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84862539695     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3768     Document Type: Article

References (50)

1. Nilsson S, Gustafsson JA. Estrogen receptors: therapies targeted to receptor subtypes. Clin Pharmacol Ther 2011;89:44-55.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
3. Winuthayanon W, Hewitt SC, Orvis GD, Behringer RR, Korach KS. Uterine epithelial estrogen receptor alpha is dispensable for proliferation but essential for complete biological and biochemical responses. Proc Natl Acad Sci U S A 2010;107:19272-7.
4. Losordo DW, Isner JM. Estrogen and angiogenesis: A review. Arterioscler Thromb Vasc Biol 2001;21:6-12. (Pubitemid 32061922)
5. Arnal JF, Fontaine C, Billon-Gales A, Favre J, Laurell H, Lenfant F, et al. Estrogen receptors and endothelium. Arterioscler Thromb Vasc Biol 2010;30:1506-12.
6. Simpson ER, Misso M, Hewitt KN, Hill RA, Boon WC, Jones ME, et al. Estrogen-the good, the bad, and the unexpected. Endocr Rev 2005;26:322-30.
7. Riant E, Waget A, Cogo H, Arnal JF, Burcelin R, Gourdy P. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 2009;150:2109-17.
8. Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, Katzenellenbogen BS. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol Endocrinol 2008;22:2116-27.
9. Systemic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy. 133 randomised trials involving 31,000 recurrences and 24,000 deaths among 75,000 women. Early Breast Cancer Trialists' Collaborative Group. Lancet 1992;339:1-15.
10. Chappuis PO, Nethercot V, Foulkes WD. Clinico-pathological characteristics of BRCA1-and BRCA2-related breast cancer. Semin Surg Oncol 2000;18:287-95. (Pubitemid 30253021)
11. Putti TC, El-Rehim DM, Rakha EA, Paish CE, Lee AH, Pinder SE, et al. Estrogen receptor-negative breast carcinomas: a review of morphology and immunophenotypical analysis. Mod Pathol 2005;18:26-35. (Pubitemid 40128091)
12. Swain SM. Tamoxifen for patients with estrogen receptor-negative breast cancer. J Clin Oncol 2001;19:93S-7S. (Pubitemid 32880089)
13. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010;363:1938-48.
14. Gupta PB, Proia D, Cingoz O, Weremowicz J, Naber SP, Weinberg RA, et al. Systemic stromal effects of estrogen promote the growth of estrogen receptor-negative cancers. Cancer Res 2007;67:2062-71. (Pubitemid 46424224)
15. Friedl A, Jordan VC. Oestradiol stimulates growth of oestrogen receptor-negative MDA-MB-231 breast cancer cells in immunodeficient mice by reducing cell loss. Eur J Cancer 1994;30A:1559-64. (Pubitemid 24343022)
16. Johns A, Freay AD, Fraser W, Korach KS, Rubanyi GM. Disruption of estrogen receptor gene prevents 17 beta estradiol-induced angiogenesis in transgenic mice. Endocrinology 1996;137:4511-3. (Pubitemid 26321904)
17. Hartman J, Lindberg K, Morani A, Inzunza J, Strom A, Gustafsson JA. Estrogen receptor beta inhibits angiogenesis and growth of T47D breast cancer xenografts. Cancer Res 2006;66:11207-13. (Pubitemid 46009948)
18. Arnal JF, Lenfant F, Flouriot G, Tremollieres F, Laurell H, Fontaine C, et al. From in vivo gene targeting of estrogen receptors to optimisation of their modulation in menopause. Br J Pharmacol 2012;165:57-66.
19. Mantovani A, Romero P, Palucka AK, Marincola FM. Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 2008;371:771-83.
20. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
21. Douin-Echinard V, Bornes S, Rochaix P, Tilkin AF, Peron JM, Bonnet J, et al. The expression of CD70 and CD80 by gene-modified tumor cells induces an antitumor response depending on the MHC status. Cancer Gene Ther 2000;7:1543-56. (Pubitemid 32098765)
22. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000;127:4277-91.
23. Billon-Gales A, Fontaine C, Douin-Echinard V, Delpy L, Berges H, Calippe B, et al. Endothelial estrogen receptor-alpha plays a crucial role in the atheroprotective action of 17beta-estradiol in low-density lipoprotein receptor-deficient mice. Circulation 2009;120:2567-76.
24. Laurell H, Iacovoni JS, Abot A, Svec D, Maoret JJ, Arnal JF, et al. Correction of RT-qPCR data for genomic DNA-derived signals with ValidPrime. Nucleic Acids Res 2012;40:e51.
25. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011;473:298-307.
26. Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009;136:839-51.
27. Thurston G, Noguera-Troise I, Yancopoulos GD. The Delta paradox: DLL4 blockade leads to more tumour vessels but less tumour growth. Nat Rev Cancer 2007;7:327-31. (Pubitemid 46652486)
28. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 2001;230:230-42. (Pubitemid 32171420)
29. Jain RK, Duda DG. Role of bone marrow-derived cells in tumor angiogenesis and treatment. Cancer Cell 2003;3:515-6. (Pubitemid 36808644)
30. El-Haibi CP, Karnoub AE. Mesenchymal stem cells in the pathogenesis and therapy of breast cancer. J Mammary Gland Biol Neoplasia 2010;15:399-409.
31. Maret A, Coudert JD, Garidou L, Foucras G, Gourdy P, Krust A, et al. Estradiol enhances primary antigen-specific CD4 T cell responses and Th1 development in vivo. Essential role of estrogen receptor alpha expression in hematopoietic cells. Eur J Immunol 2003;33:512-21. (Pubitemid 36267617)
32. Gourdy P, Araujo LM, Zhu R, Garmy-Susini B, Diem S, Laurell H, et al. Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-gamma production by invariant natural killer T cells. Blood 2005;105:2415-20. (Pubitemid 40387040)
33. Calippe B, Douin-Echinard V, Laffargue M, Laurell H, Rana-Poussine V, Pipy B, et al. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 2008;180:7980-8.
34. Tammela T, Zarkada G, Nurmi H, Jakobsson L, Heinolainen K, Tvorogov D, et al. VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat Cell Biol 2011;13:1202-13.
35. Lorquet S, Berndt S, Blacher S, Gengoux E, Peulen O, Maquoi E, et al. Soluble forms of VEGF receptor-1 and-2 promote vascular maturation via mural cell recruitment. FASEB J 2010;24:3782-95.
36. Hyder SM, Liang Y, Wu J. Estrogen regulation of thrombospondin-1 in human breast cancer cells. Int J Cancer 2009;125:1045-53.
37. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 2011;10:417-27.
38. Wilson WR, Hay MP. Targeting hypoxia in cancer therapy. Nat Rev Cancer 2011;11:393-410.
39. De Bock K, Mazzone M, Carmeliet P. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol 2011;8:393-404.
40. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62. (Pubitemid 40093472)
41. Hede K. Lung cancer may be different for men and women, but researchers ponder what to do? J Natl Cancer Inst 2007;99:1830-2.
42. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, 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;8:211-26. (Pubitemid 41317592)
43. 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;9:789-95. (Pubitemid 36749231)
44. Staton CA, Valluru M, Hoh L, Reed MW, Brown NJ. Angiopoietin-1, angiopoietin-2 and Tie-2 receptor expression in human dermal wound repair and scarring. Br J Dermatol 2010;163:920-7.
45. Lewis CE, De Palma M, Naldini L. Tie2-expressing monocytes and tumor angiogenesis: regulation by hypoxia and angiopoietin-2. Cancer Res 2007;67:8429-32. (Pubitemid 47437413)
46. Duda DG, Cohen KS, Kozin SV, Perentes JY, Fukumura D, Scadden DT, et al. Evidence for incorporation of bone marrow-derived endothelial cells into perfused blood vessels in tumors. Blood 2006;107:2774-6.
47. Gothert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, et al. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 2004;104:1769-77. (Pubitemid 39202286)
48. Cid MC, Schnaper HW, Kleinman HK. Estrogens and the vascular endothelium. Ann N Y Acad Sci 2002;966:143-57. (Pubitemid 34729170)
49. Rubanyi GM, Johns A, Kauser K. Effect of estrogen on endothelial function and angiogenesis. Vascul Pharmacol 2002;38:89-98. (Pubitemid 36398281)
50. Toutain CE, Filipe C, Billon A, Fontaine C, Brouchet L, Guery JC, et al. Estrogen receptor alpha expression in both endothelium and hematopoietic cells is required for the accelerative effect of estradiol on reendothelialization. Arterioscler Thromb Vasc Biol 2009;29:1543-50.