Forkhead box transcription factor FoxC1 preserves corneal transparency by regulating vascular growth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 6, 2012, Pages 2015-2020

  Seo, Seungwoon ^a   Singh, Hardeep P ^b   Lacal, Pedro M ^c   Sasman, Amy ^a   Fatima, Anees ^a   Liu, Ting ^a   Schultz, Kathryn M ^a   Losordo, Douglas W ^a   Lehmann, Ordan J ^b   Kume, Tsutomu ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Avascularity; Soluble form of VEGF receptor 1; VEGF bioavailablility

Indexed keywords

CD31 ANTIGEN; COLLAGEN TYPE 1; FIBROBLAST GROWTH FACTOR 2; GELATINASE B; MATRIX METALLOPROTEINASE 19; STROMELYSIN; TRANSCRIPTION FACTOR FOXC1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR EYE SEGMENT; ARTICLE; CONTROLLED STUDY; CORNEA INJURY; CORNEA LIMBUS; CORNEA OPACITY; EMBRYO; ENVIRONMENTAL EXPOSURE; EXTRACELLULAR MATRIX; GENE MUTATION; GROWTH REGULATION; HAPLOINSUFFICIENCY; HOMOZYGOSITY; LYMPHANGIOGENESIS; MOUSE; MUTATIONAL ANALYSIS; NEURAL CREST; NONHUMAN; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIEGER SYNDROME; SIGNAL TRANSDUCTION; VASCULARIZATION;

ALKALIES; ANIMALS; ANTERIOR EYE SEGMENT; BLOOD VESSELS; BURNS; CORNEA; CORNEAL STROMA; EYE ABNORMALITIES; FORKHEAD TRANSCRIPTION FACTORS; HAPLOINSUFFICIENCY; HETEROZYGOTE; LYMPHANGIOGENESIS; MATRIX METALLOPROTEINASES; MICE; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; NEURAL CREST; PHENOTYPE; PUPIL; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MURINAE; MUS;

EID: 84857126252     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109540109     Document Type: Article

References (55)

1. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298-307.
2. Regenfuss B, Bock F, Parthasarathy A, Cursiefen C (2008) Corneal (lymph)angiogenesis - from bedside to bench and back: A tribute to Judah Folkman. Lymphat Res Biol 6:191-201.
3. Sassa Y, Hata Y (2010) Antiangiogenic drugs in the management of ocular diseases: Focus on antivascular endothelial growth factor. Clin Ophthalmol 4:275-283.
4. Tolentino MJ (2009) Current molecular understanding and future treatment strategies for pathologic ocular neovascularization. Curr Mol Med 9:973-981.
5. Azar DT (2006) Corneal angiogenic privilege: Angiogenic and antiangiogenic factors in corneal avascularity, vasculogenesis, and wound healing (an American Ophthalmological Society thesis). Trans Am Ophthalmol Soc 104:264-302.
6. Chang JH, Gabison EE, Kato T, Azar DT (2001) Corneal neovascularization. Curr Opin Ophthalmol 12:242-249. (Pubitemid 32751680)
7. Qazi Y, Wong G, Monson B, Stringham J, Ambati BK (2010) Corneal transparency: Genesis, maintenance and dysfunction. Brain Res Bull 81:198-210.
8. De Bock K, Cauwenberghs S, Carmeliet P (2011) Vessel abnormalization: Another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr Opin Genet Dev 21:73-79.
9. Ambati BK, et al. (2006) Corneal avascularity is due to soluble VEGF receptor-1. Nature 443:993-997. (Pubitemid 44646176)
10. Crawford Y, Ferrara N (2009) VEGF inhibition: Insights from preclinical and clinical studies. Cell Tissue Res 335:261-269.
11. Benayoun BA, Caburet S, Veitia RA (2011) Forkhead transcription factors: Key players in health and disease. Trends Genet 27:224-232.
12. Carlsson P, Mahlapuu M (2002) Forkhead transcription factors: Key players in development and metabolism. Dev Biol 250:1-23.
13. Hannenhalli S, Kaestner KH (2009) The evolution of Fox genes and their role in development and disease. Nat Rev Genet 10:233-240.
14. Lehmann OJ, Sowden JC, Carlsson P, Jordan T, Bhattacharya SS (2003) Fox's in development and disease. Trends Genet 19:339-344. (Pubitemid 36694617)
15. Kume T (2009) The cooperative roles of Foxc1 and Foxc2 in cardiovascular development. Adv Exp Med Biol 665:63-77.
16. Papanicolaou KN, Izumiya Y, Walsh K (2008) Forkhead transcription factors and cardiovascular biology. Circ Res 102:16-31.
17. Koçak-Midillioglu I, Karadeniz N, Yalvaç I, Koçak-Altintas AG, Duman S (2003) Eight-year follow-up of Axenfeld-Rieger syndrome with Turner syndrome. Eur J Ophthalmol 13:580-583. (Pubitemid 38208844)
18. Shields MB, Buckley E, Klintworth GK, Thresher R (1985) Axenfeld-Rieger syndrome: A spectrum of developmental disorders. Surv Ophthalmol 29:387-409. (Pubitemid 15040348)
19. Aldinger KA, et al. (2009) FOXC1 is required for normal cerebellar development and is a major contributor to chromosome 6p25.3 Dandy-Walker malformation. Nat Genet 41:1037-1042.
20. Matt N, et al. (2005) Retinoic acid-dependent eye morphogenesis is orchestrated by neural crest cells. Development 132:4789-4800. (Pubitemid 41685288)
21. Siegenthaler JA, et al. (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597-609.
22. Alward WL (2000) Axenfeld-Rieger syndrome in the age of molecular genetics. Am J Ophthalmol 130:107-115.
23. Lehmann OJ, et al. (2000) Chromosomal duplication involving the forkhead transcription factor gene FOXC1 causes iris hypoplasia and glaucoma. Am J Hum Genet 67:1129-1135.
24. Mears AJ, et al. (1998) Mutations of the forkhead/winged-helix gene, FKHL7, in patients with Axenfeld-Rieger anomaly. Am J Hum Genet 63:1316-1328. (Pubitemid 30418529)
25. Nishimura DY, et al. (1998) The forkhead transcription factor gene FKHL7 is responsible for glaucoma phenotypes which map to 6p25. Nat Genet 19:140-147. (Pubitemid 28248794)
26. Tümer Z, Bach-Holm D (2009) Axenfeld-Rieger syndrome and spectrum of PITX2 and FOXC1 mutations. Eur J Hum Genet 17:1527-1539.
27. Smith RS, et al. (2000) Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development. Hum Mol Genet 9:1021-1032. (Pubitemid 30216007)
28. Kidson SH, Kume T, Deng K, Winfrey V, Hogan BL (1999) 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 211:306-322. (Pubitemid 29343284)
29. Kume T, et al. (1998) The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93:985-996. (Pubitemid 28280792)
30. Gage PJ, Rhoades W, Prucka SK, Hjalt T (2005) Fate maps of neural crest and mesoderm in the mammalian eye. Invest Ophthalmol Vis Sci 46:4200-4208. (Pubitemid 44264623)
31. Chanda B, et al. (2008) A novel mechanistic spectrum underlies glaucoma-associated chromosome 6p25 copy number variation. Hum Mol Genet 17:3446-3458.
32. Gage PJ, Zacharias AL (2009) Signaling "cross-talk" is integrated by transcription factors in the development of the anterior segment in the eye. Dev Dyn 238:2149-2162.
33. Hayashi H, Kume T (2008) Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS ONE 3:e2401.
34. Hayashi H, Kume T (2008) Forkhead transcription factors regulate expression of the chemokine receptor CXCR4 in endothelial cells and CXCL12-induced cell migration. Biochem Biophys Res Commun 367:584-589.
35. Kume T, Jiang H, Topczewska JM, Hogan BL (2001) The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev 15:2470-2482. (Pubitemid 32899749)
36. Seo S, et al. (2006) The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev Biol 294:458-470. (Pubitemid 43884821)
37. Ellenberg D, et al. (2010) Novel aspects of corneal angiogenic and lymphangiogenic privilege. Prog Retin Eye Res 29:208-248.
38. Nakao S, et al. (2010) Lymphangiogenesis and angiogenesis: Concurrence and/or dependence? Studies in inbred mouse strains. FASEB J 24:504-513.
39. Nakao S, et al. (2011) Blood vessel endothelial VEGFR-2 delays lymphangiogenesis: An endogenous trapping mechanism links lymph- and angiogenesis. Blood 117:1081-1090.
40. Chappell JC, Taylor SM, Ferrara N, Bautch VL (2009) Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell 17:377-386.
41. Storz P, Döppler H, Copland JA, Simpson KJ, Toker A (2009) FOXO3a promotes tumor cell invasion through the induction of matrix metalloproteinases. Mol Cell Biol 29:4906-4917.
42. Li H, et al. (2007) FoxO4 regulates tumor necrosis factor α-directed smooth muscle cell migration by activating matrix metalloproteinase 9 gene transcription. Mol Cell Biol 27:2676-2686. (Pubitemid 46581357)
43. Ahmad A, et al. (2010) FoxM1 down-regulation leads to inhibition of proliferation, migration and invasion of breast cancer cells through the modulation of extra-cellular matrix degrading factors. Breast Cancer Res Treat 122:337-346.
44. Ambati BK, et al. (2003) Sustained inhibition of corneal neovascularization by genetic ablation of CCR5. Invest Ophthalmol Vis Sci 44:590-593. (Pubitemid 36159703)
45. Ambati BK, Joussen AM, Kuziel WA, Adamis AP, Ambati J (2003) Inhibition of corneal neovascularization by genetic ablation of CCR2. Cornea 22:465-467. (Pubitemid 36759041)
46. Bergers G, et al. (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2:737-744.
47. Hawinkels LJ, et al. (2008) VEGF release by MMP-9-mediated heparan sulphate cleavage induces colorectal cancer angiogenesis. Eur J Cancer 44:1904-1913.
48. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML (2005) Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169:681-691. (Pubitemid 41002860)
49. Kami J, et al. (2008) Inhibition of choroidal neovascularization by blocking vascular endothelial growth factor receptor tyrosine kinase. Jpn J Ophthalmol 52:91-98. (Pubitemid 351624401)
50. Sanda T, et al. (2005) Antimyeloma effects of a novel synthetic retinoid Am80 (Tamibarotene) through inhibition of angiogenesis. Leukemia 19:901-909. (Pubitemid 40861997)
51. Arroyo AG, Iruela-Arispe ML (2010) Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc Res 86:226-235.
52. Ferrara N (2010) Binding to the extracellular matrix and proteolytic processing: Two key mechanisms regulating vascular endothelial growth factor action. Mol Biol Cell 21:687-690.
53. Bloushtain-Qimron N, et al. (2008) Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 105:14076-14081.
54. Muggerud AA, et al. (2010) Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res 12:R3.
55. Kaestner KH, Knochel W, Martinez DE (2000) Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 14:142-146. (Pubitemid 30070978)