Advertisement

The Cooperative Roles of Foxc1 and Foxc2 in Cardiovascular Development

  • Tsutomu Kume
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 665)

Abstract

Foxc1 and Foxc2 are closely related members of the Forkhead/Fox transcription factor family. The two Foxc genes have overlapping expression patterns in mesodermal and neural crest derivatives during development, as well as similar functions of gene regulation. Consistently, mouse mutants for each gene have similar abnormalities in multiple embryonic tissues, including the eye, kidney and cardiovascular system. Analysis of compound Foxc1; Foxc2 mutant embryos reveals that the two Foxc genes have dose-dependent, cooperative roles in development. In particular, recent studies demonstrate that Foxc1 and Foxc2 are essential for arterial cell specification, lymphatic vessel formation, angiogenesis and cardiac outflow tract development. This chapter will summarize and discuss current knowledge about the function of Foxc1 and Foxc2 in cardiovascular development.

Keywords

Neural Crest Lymphatic Endothelial Cell Forkhead Transcription Factor Cardinal Vein Cardiovascular Development 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002; 250:1–23.CrossRefPubMedGoogle Scholar
  2. 2.
    Pierrou S, Hellqvist M, Samuelsson L et al. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J 1994; 13:5002–5012.PubMedGoogle Scholar
  3. 3.
    van Dongen MJ, Cederberg A, Carlsson P et al. Solution structure and dynamics of the DNA-binding domain of the adipocyte-transcription factor FREAC-11. J Mol Biol 2000; 296:351–359.CrossRefPubMedGoogle Scholar
  4. 4.
    Hiemisch H, Monaghan AP, Schutz G et al. Expression of the mouse Fkh1/Mf1 and Mfh1 genes in late gestation embryos is restricted to mesoderm derivatives. Mech Dev 1998; 73:129–132.CrossRefPubMedGoogle Scholar
  5. 5.
    Iida K, Koseki H, Kakinuma H et al. Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 1997; 124:4627–4638.PubMedGoogle Scholar
  6. 6.
    Kume T, Deng K, Hogan BL. Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development 2000; 127:1387–1395.PubMedGoogle Scholar
  7. 7.
    Kume T, Deng KY: Winfrey V et al. The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 1998; 93:985–996.CrossRefPubMedGoogle Scholar
  8. 8.
    Kume T, Jiang H, Topczewska JM et al. The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev 2001; 15:2470–2482.CrossRefPubMedGoogle Scholar
  9. 9.
    Sasaki H, Hogan BL. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 1993; 118:47–59.PubMedGoogle Scholar
  10. 10.
    Seo S, Fujita H, Nakano A et al. The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev Biol 2006; 294:458–470.CrossRefPubMedGoogle Scholar
  11. 11.
    Seo S, Kume T. Forkhead transcription factors, Foxc1 and Foxc2, are required for the morphogenesis of the cardiac outflow tract. Dev Biol 2006; 296:421–436.CrossRefPubMedGoogle Scholar
  12. 12.
    Winnier GE, Hargett L, Hogan BL. The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev 1997; 11:926–940.CrossRefPubMedGoogle Scholar
  13. 13.
    Winnier GE, Kume T, Deng K et al. Roles for the winged helix transcription factors MF1 and MFH1 in cardiovascular development revealed by nonallelic noncomplementation of null alleles. Dev Biol 1999; 213:418–431.CrossRefPubMedGoogle Scholar
  14. 14.
    Gitler AD, Lu MM, Epstein JA. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 2004; 7:107–116.CrossRefPubMedGoogle Scholar
  15. 15.
    Gage PJ, Rhoades W, Prucka SK et al. Fate maps of neural crest and mesoderm in the mammalian eye. Invest Ophthalmol Vis Sci 2005; 46:4200–4208.CrossRefPubMedGoogle Scholar
  16. 16.
    Kidson SH, Kume T, Deng K et al. The forkhead/winged-helix gene, Mf1, is necessary for the normal development of the cornea and formation of the anterior chamber in the mouse eye. Dev Biol 1999; 211:306–322.CrossRefPubMedGoogle Scholar
  17. 17.
    Pohl BS, Knochel W. Of Fox and Frogs: Fox (fork head/winged helix) transcription factors in Xenopus development. Gene 2005; 344:21–32.CrossRefPubMedGoogle Scholar
  18. 18.
    Gruneberg H. Congenital hydrocephalus in the mouse: a case of spurious pleitropism. J. Genetics 1943; 45:1–21.CrossRefGoogle Scholar
  19. 19.
    Hong HK, Lass JH, Chakravarti A. Pleiotropic skeletal and ocular phenotypes of the mouse mutation congenital hydrocephalus (ch/Mf1) arise from a winged helix/forkhead transcriptionfactor gene. Hum Mol Genet 1999; 8:625–637.CrossRefPubMedGoogle Scholar
  20. 20.
    Mattiske D, Kume T, Hogan BL. The mouse forkhead gene Foxc1 is required for primordial germ cell migration and antral follicle development. Dev Biol 2006; 290:447–458.CrossRefPubMedGoogle Scholar
  21. 21.
    Rice R, Rice DP, Olsen BR et al. Progression of calvarial bone development requires Foxc1 regulation of Msx2 and Alx4. Dev Biol 2003; 262:75–87.CrossRefPubMedGoogle Scholar
  22. 22.
    Smith RS, Zabaleta A, Kume T et al. Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development. Hum Mol Genet 2000; 9:1021–1032.CrossRefPubMedGoogle Scholar
  23. 23.
    Jiang X, Iseki S, Maxson RE et al. Tissue origins and interactions in the mammalian skull vault. Dev Biol 2002; 241:106–116.CrossRefPubMedGoogle Scholar
  24. 24.
    Hayashi H, Kume T. Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem Biophys Res Commun 2008; 367:584–589.CrossRefPubMedGoogle Scholar
  25. 25.
    Hayashi H, Kume T. Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS ONE 2008; 3:e2401.CrossRefGoogle Scholar
  26. 26.
    Zarbalis K, Siegenthaler JA, Choe Y et al. Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 2007; 104:14002–14007.CrossRefPubMedGoogle Scholar
  27. 27.
    Takemoto M, He L, Norlin J et al. Large-scale identification of genes implicated in kidney glomerulus development and function. EMBO J 2006; 25:1160–1174.CrossRefPubMedGoogle Scholar
  28. 28.
    Kriederman BM, Myloyde TL, Witte MH et al. FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome. Hum Mol Genet 2003; 12:1179–1185.CrossRefPubMedGoogle Scholar
  29. 29.
    Petrova TV, Karpanen T, Norrmen C et al. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 2004; 10:974–981.CrossRefPubMedGoogle Scholar
  30. 30.
    Hayashi H, Sano H, Seo S et al. The Foxc2 transcription factor regulates angiogenesis via induction of integrin beta 3 expression. J Biol Chem 2008; 283:23791–23800.CrossRefPubMedGoogle Scholar
  31. 31.
    Mears AJ, Jordan T, Mirzayans F et al. Mutations of the forkhead/winged-helix gene, FKHL7, in patients with Axenfeld-Rieger anomaly. Am J Hum Genet 1998; 63:1316–1328.CrossRefPubMedGoogle Scholar
  32. 32.
    Nishimura DY, Swiderski RE, Alward WL et al. The forkhead transcription factor gene FKHL7 is responsible for glaucoma phenotypes which map to 6p25. Nat Genet 1998; 19:140–147.CrossRefPubMedGoogle Scholar
  33. 33.
    Honkanen RA, Nishimura DY, Swiderski RE et al. A family with Axenfeld-Rieger syndrome and Peters Anomaly caused by a point mutation (Phe112Ser) in the FOXC1 gene. Am J Ophthalmol 2003; 135:368–375.CrossRefPubMedGoogle Scholar
  34. 34.
    Fang J, Dagenais SL, Erickson RP et al. Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am J Hum Genet 2000; 67:1382–1388.CrossRefPubMedGoogle Scholar
  35. 35.
    Mellor RH, Brice G, Stanton AW et al. Mutations in FOXC2 are strongly associated with primary valve failure in veins of the lower limb. Circulation 2007; 115:1912–1920.CrossRefPubMedGoogle Scholar
  36. 36.
    Lehmann OJ, Tuft S, Brice G et al. Novel anterior segment phenotypes resulting from forkhead gene alterations: evidence for cross-species conservation of function. Invest Ophthalmol Vis Sci 2003; 44:2627–2633.CrossRefPubMedGoogle Scholar
  37. 37.
    Wilm B, James RG, Schultheiss TM et al. The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate. Dev Biol 2004; 271:176–189.CrossRefPubMedGoogle Scholar
  38. 38.
    Topczewska JM, Topczewski J, Solnica-Krezel L et al. Sequence and expression of zebrafish foxc1a and foxc1b, encoding conserved forkhead/winged helix transcription factors. Mech Dev 2001; 100:343–347.CrossRefPubMedGoogle Scholar
  39. 39.
    Wotton KR, Mazet F, Shimeld SM. Expression of FoxC, FoxF, FoxL1 and FoxQ1 genes in the dogfish Scyliorhinus canicula defines ancient and derived roles for Fox genes in vertebrate development. Dev Dyn 2008; 237:1590–1603.CrossRefPubMedGoogle Scholar
  40. 40.
    Wotton KR, Shimeld SM. Comparative genomics of vertebrate Fox cluster loci. BMC Genomics 2006; 7:271.CrossRefPubMedGoogle Scholar
  41. 41.
    Topczewska JM, Topczewski J, Shostak A et al. The winged helix transcription factor Foxc1a is essential for somitogenesis in zebrafish. Genes Dev 2001; 15:2483–2493.CrossRefPubMedGoogle Scholar
  42. 42.
    Hong CC, Kume T, Peterson RT. Role of crosstalk between phosphatidylinositol 3-kinase and extracellular signal-regulated kinase/mitogen-activated protein kinase pathways in artery-vein specification. Circ Res 2008; 103:573–579.CrossRefPubMedGoogle Scholar
  43. 43.
    Red-Horse K, Crawford Y, Shojaei F et al. Endothelium-microenvironment interactions in the developing embryo and in the adult. Dev Cell 2007; 12:181–194.CrossRefPubMedGoogle Scholar
  44. 44.
    You LR, Lin FJ, Lee CT et al. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 2005; 435:98–104.CrossRefPubMedGoogle Scholar
  45. 45.
    Duarte A, Hirashima M, Benedito R et al. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 2004; 18:2474–2478.CrossRefPubMedGoogle Scholar
  46. 46.
    Kokubo H, Miyagawa-Tomita S, Nakazawa M et al. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev Biol 2005; 278:301–309.CrossRefPubMedGoogle Scholar
  47. 47.
    Krebs LT, Shutter JR, Tanigaki K et al. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 2004; 18:2469–2473.CrossRefPubMedGoogle Scholar
  48. 48.
    Lawson ND, Scheer N, Pham VN et al. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 2001; 128:3675–3683.PubMedGoogle Scholar
  49. 49.
    Zhong TP, Childs S, Leu JP et al. Gridlock signalling pathway fashions the first embryonic artery. Nature 2001; 414:216–220.CrossRefPubMedGoogle Scholar
  50. 50.
    Liu ZJ, Shirakawa T, Li Y et al. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol 2003; 23:14–25.CrossRefPubMedGoogle Scholar
  51. 51.
    Hong CC, Peterson QP, Hong JY et al. Artery/Vein Specification Is Governed by Opposing Phosphatidylinositol-3 Kinase and MAP Kinase/ERK Signaling. Curr Biol 2006; 16:1366–1372.CrossRefPubMedGoogle Scholar
  52. 52.
    Mukouyama YS, Gerber HP, Ferrara N et al. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 2005; 132:941–952.CrossRefPubMedGoogle Scholar
  53. 53.
    Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007; 8:464–478.CrossRefPubMedGoogle Scholar
  54. 54.
    Francois M, Caprini A, Hosking B et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008; 456:643–647.CrossRefPubMedGoogle Scholar
  55. 55.
    Srinivasan RS, Dillard ME, Lagutin OV et al. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 2007; 21:2422–2432.CrossRefPubMedGoogle Scholar
  56. 56.
    Karkkainen MJ, Haiko P, Sainio K et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 2004; 5:74–80.CrossRefPubMedGoogle Scholar
  57. 57.
    Xue Y, Cao R, Nilsson D et al. FOXC2 controls Ang-2 expression and modulates angiogenesis, vascular patterning, remodeling and functions in adipose tissue. Proc Natl Acad Sci USA 2008; 105:10167–10172.CrossRefPubMedGoogle Scholar
  58. 58.
    Avraamides CJ, Garmy-Susini B, Varner JA. Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 2008; 8:604–617.CrossRefPubMedGoogle Scholar
  59. 59.
    Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signalingpathway: a molecularhub modulating neo-angiogenesis. Trends Immunol 2007; 28:299–307.CrossRefPubMedGoogle Scholar
  60. 60.
    Kume T. Foxc2 transcription factor: a newly described regulator of angiogenesis. Trends Cardiovasc Med 2008; 18:224–228.CrossRefPubMedGoogle Scholar
  61. 61.
    Mani SA, Yang J, Brooks M et al. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci USA 2007; 104:10069–10074.CrossRefPubMedGoogle Scholar
  62. 62.
    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; 7:327–331.CrossRefPubMedGoogle Scholar
  63. 63.
    Buckingham M, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet 2005; 6:826–835.CrossRefPubMedGoogle Scholar
  64. 64.
    Black BL. Transcriptional pathways in second heart field development. Semin Cell Dev Biol 2007; 18:67–76.CrossRefPubMedGoogle Scholar
  65. 65.
    Dunwoodie SL. Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation. Semin Cell Dev Biol 2007; 18:54–66.CrossRefPubMedGoogle Scholar
  66. 66.
    Xu H, Baldini A. Genetic pathways to mammalian heart development: Recent progress from manipulation of the mouse genome. Semin Cell Dev Biol 2007; 18:77–83.CrossRefPubMedGoogle Scholar
  67. 67.
    Meilhac SM, Esner M, Kelly RG et al. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell 2004; 6:685–698.CrossRefPubMedGoogle Scholar
  68. 68.
    Prall OW, Menon MK, Solloway MJ et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell. 2007; 128:947–959.CrossRefPubMedGoogle Scholar
  69. 69.
    Dodou E, Verzi MP, Anderson JP et at. Mef2c is a direct transcriptional target of ISLI and GATA factors in the anterior heart field during mouse embryonic development. Development 2004; 131:3931–3942.CrossRefPubMedGoogle Scholar
  70. 70.
    von Both I, Silvestri C, Erdemir T et al. Foxh1 is essential for development of the anterior heart field. Dev Cell 2004; 7:331–345.CrossRefGoogle Scholar
  71. 71.
    Takeuchi JK, Mileikovskaia M, Koshiba-Takeuchi K et al. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Development 2005; 132:2463–2474.CrossRefPubMedGoogle Scholar
  72. 72.
    Cai CL, Liang X, Shi Y et al. IsH identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 2003; 5:877–889.CrossRefPubMedGoogle Scholar
  73. 73.
    Xu H, Morishima M, Wylie JN et al. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 2004; 131:3217–3227.CrossRefPubMedGoogle Scholar
  74. 74.
    Maeda J, Yamagishi H, McAnally J et al. Tbx1 is regulated by forkhead proteins in the secondary heart field. Dev Dyn 2006; 235:701–710.CrossRefPubMedGoogle Scholar
  75. 75.
    Hu T, Yamagishi H, Maeda J et al. Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development 2004; 131:5491–5502.CrossRefPubMedGoogle Scholar
  76. 76.
    Yamagishi H, Maeda J, Hu T et al. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev 2003; 17:269–281.CrossRefPubMedGoogle Scholar
  77. 77.
    Hutson MR, Kirby ML. Model systems for the study of heart development and disease Cardiac neural crest and conotruncal malformations. Semin Cell Dev Biol 2007; 18:101–110.CrossRefPubMedGoogle Scholar
  78. 78.
    Hutson MR, Kirby ML. Neural crest and cardiovascular development: a 20-year perspective. Birth Defects Res Part C Embryo Today 2003; 69:2–13.CrossRefGoogle Scholar
  79. 79.
    Yelbuz TM, Waldo KL, Kumiski DH et al. Shortened outflow tract leads to altered cardiac looping after neural crest ablation. Circulation 2002; 106:504–510.CrossRefPubMedGoogle Scholar
  80. 80.
    Farrell MJ, Burch JL, Wallis K et al. FGF-8 in the ventral pharynx alters development of myocardial calcium transients after neural crest ablation. J Clin Invest 2001; 107:1509–1517.CrossRefPubMedGoogle Scholar
  81. 81.
    Hutson MR, Zhang P, Stadt HA et al. Cardiac arterial pole alignment is sensitive to FGF8 signaling in the pharynx. Dev Biol 2006; 295:486–497.CrossRefPubMedGoogle Scholar
  82. 82.
    Waldo KL, Hutson MR, Stadt HA et al. Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev Biol 2005; 281:66–77.CrossRefPubMedGoogle Scholar
  83. 83.
    Park EJ, Watanabe Y, Smyth G et al. An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 2008; 135:3599–3610.CrossRefPubMedGoogle Scholar
  84. 84.
    Olivey HE, Compton LA, Barnett JV. Coronary vessel development: the epicardium delivers. Trends Cardiovasc Med 2004; 14:247–251.PubMedGoogle Scholar
  85. 85.
    Reese DE, Mikawa T, Bader DM. Development of the coronary vessel system. Circ Res 2002; 91:761–768.CrossRefPubMedGoogle Scholar
  86. 86.
    Cai CL, Martin JC, Sun Y et al. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008; 454:104–108.CrossRefPubMedGoogle Scholar
  87. 87.
    Zhou B, Ma Q, Rajagopal S et al. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008; 454:109–113.CrossRefPubMedGoogle Scholar
  88. 88.
    Wessels A, Perez-Pomares JM. The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells. Anat Rec A Discov Mol Cell Evol Biol 2004; 276:43–57.CrossRefPubMedGoogle Scholar
  89. 89.
    Tevosian SG, Deconinck AE, Tanaka M et al. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 2000; 101:729–739.CrossRefPubMedGoogle Scholar
  90. 90.
    Olivey HE, Mundell NA, Austin AF et al. Transforming growth factor-beta stimulates epithelial-mesenchymal transformation in the proepicardium. Dev Dyn 2006; 235:50–59.CrossRefPubMedGoogle Scholar
  91. 91.
    Furuyama T, Kitayama K, Shimoda Y et al. Abnormal angiogenesis in Foxo1 (Fkhr-deficient mice. J Biol Chem 2004; 279:34741–34749.CrossRefPubMedGoogle Scholar
  92. 92.
    Hosaka T, Biggs WH 3rd, Tieu D et al. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 2004; 101:2975–2980.CrossRefPubMedGoogle Scholar
  93. 93.
    De Val S, Chi NC, Meadows SM et al. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 2008; 135:1053–1064.CrossRefPubMedGoogle Scholar
  94. 94.
    Chien KR, Domian IJ, Parker KK. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 2008; 322:1494–1497.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer+Business Media 2009

Authors and Affiliations

  1. 1.Division of Cardiovascular Medicine, Department of MedicineVanderbilt University Medical CenterNashvilleUSA

Personalised recommendations