The choroid as a sclera growth regulator

Experimental Eye Research

Volumn 114, Issue , 2013, Pages 120-127

  Summers, Jody A ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Choroid; Emmetropization; Myopia; Sclera

Indexed keywords

ACCOMMODATION; ARTICLE; BLOOD VESSEL PERMEABILITY; CHOROID; CORNEA; EMMETROPIA; EXTRACELLULAR MATRIX; EYE DEVELOPMENT; GENE EXPRESSION; GROWTH REGULATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REFRACTION ERROR; RETINA; SCLERA; SIGNAL TRANSDUCTION; TISSUE INTERACTION; VISION; VISUAL STIMULATION;

CHOROID; EMMETROPIZATION; MYOPIA; SCLERA;

ANIMALS; AXIAL LENGTH, EYE; CHOROID; EMMETROPIA; HUMANS; MYOPIA; SCLERA;

EID: 84881228922     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.03.008     Document Type: Article

References (72)

1. Alm A., Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp. Eye Res. 1973, 15:15-29.
2. Alm A., Nilsson S.F. Uveoscleral outflow-a review. Exp. Eye Res. 2009, 88:760-768.
3. Bitzer M., Feldkaemper M., Schaeffel F. Visually induced changes in components of the retinoic acid system in fundal layers of the chick. Exp. Eye Res. 2000, 70:97-106.
4. Bok J., Raft S., Kong K.A., Koo S.K., Drager U.C., Wu D.K. Transient retinoic acid signaling confers anterior-posterior polarity to the inner ear. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:161-166.
5. Coulombe J.N., Kos K. Target tissue influence on somatostatin expression in the avian ciliary ganglion. Ann. N. Y. Acad. Sci. 1997, 814:209-225.
6. Coulombe J.N., Nishi R. Stimulation of somatostatin expression in developing ciliary ganglion neurons by cells of the choroid layer. J.Neurosci. 1991, 11:553-562.
7. Etchevers H.C., Vincent C., Le Douarin N.M., Couly G.F. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 2001, 128:1059-1068.
8. Fischer A.J., Wallman J., Mertz J.R., Stell W.K. Localization of retinoid binding proteins, retinoid receptors, and retinaldehyde dehydrogenase in the chick eye. J.Neurocytol. 1999, 28:597-609.
9. Frank R.N., Amin R.H., Eliott D., Puklin J.E., Abrams G.W. Basic fibroblast growth factor and vascular endothelial growth factor are present in epiretinal and choroidal neovascular membranes. Am. J. Ophthalmol. 1996, 122:393-403.
10. Giummarra L., Murphy M.J., Goodyear M.J., Crewther S.G. Microarray analysis of chick retina/RPE/choroid during recovery from form deprivation myopia (FDM). Invest. Ophthalmol. Vis. Sci. 2010, 51. [ARVO E-abstract #1674].
11. Green W.R. The choroid. Ophthalmic Pathology: An Atlas and Textbook 1986, W.B. Saunders, Philadelphia. third ed. W.H. Spencer (Ed.).
12. Grierson I., Heathcote L., Hiscott P., Hogg P., Briggs M., Hagan S. Hepatocyte growth factor/scatter factor in the eye. Prog. Retin. Eye Res. 2000, 19:779-802.
13. Guggenheim J.A., McBrien N.A. Form-deprivation myopia induces activation of scleral matrix metalloproteinase-2 in tree shrew. Invest. Ophthalmol. Vis. Sci. 1996, 37:1380-1395.
14. Hansen M.B. Neurohumoral control of gastrointestinal motility. Physiol. Res. 2003, 52:1-30.
15. He L., Frost M.R., Siegwart J.T., Norton T.T. Gene expression signatures in tree shrew choroid during lens-induced myopia, recovery, and plus-lens wear. Invest. Ophthalmol. Vis. Sci. 2012, 53. [ARVO E-abstract #3454].
16. Hochgreb T., Linhares V.L., Menezes D.C., Sampaio A.C., Yan C.Y., Cardoso W.V., Rosenthal N., Xavier-Neto J. Acaudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 2003, 130:5363-5374.
17. Howlett M.H., McFadden S.A. Spectacle lens compensation in the pigmented guinea pig. Vis. Res. 2009, 49:219-227.
18. Hung L.F., Wallman J., Smith E.L. Vision-dependent changes in the choroidal thickness of macaque monkeys. Invest. Ophthalmol. Vis. Sci. 2000, 41:1259-1269.
19. Junghans B.M., Crewther S.G., Liang H., Crewther D.P., Wareing L., Pirie B. Lymphatics in the chick choroid?. Aust. N.Z. J. Ophthalmol. 1996, 24:47-49.
20. Krebs W., Krebs I.P. Ultrastructural evidence for lymphatic capillaries in the primate choroid. Arch. Ophthalmol. 1988, 106:1615-1616.
21. Kuriyama F., Ueda Y., Araki M. Complete reconstruction of the retinal laminar structure from a cultured retinal pigment epithelium is triggered by altered tissue interaction and promoted by overlaid extracellular matrices. Dev. Neurobiol. 2009, 69:950-958.
22. Kvanta A., Algvere P.V., Berglin L., Seregard S. Subfoveal fibrovascular membranes in age-related macular degeneration express vascular endothelial growth factor. Invest. Ophthalmol. Vis. Sci. 1996, 37:1929-1934.
23. Leu S.T., Batni S., Radeke M.J., Johnson L.V., Anderson D.H., Clegg D.O. Drusen are cold spots for proteolysis: expression of matrix metalloproteinases and their tissue inhibitor proteins in age-related macular degeneration. Exp. Eye Res. 2002, 74:141-154.
24. Machem S. Limb development. Cell Signaling and Growth Factors in Development 2006, 523-618. Wiley-VCH Verlag Gmbh & Co. K. Unsicker, K. Kreiglstein (Eds.).
25. Marzani D., Wallman J. Growth of the two layers of the chick sclera is modulated reciprocally by visual conditions. Invest. Ophthalmol. Vis. Sci. 1997, 38:1726-1739.
26. McFadden S.A., Howlett M.H., Mertz J.R. Retinoic acid signals the direction of ocular elongation in the guinea pig eye. Vis. Res. 2004, 44:643-653.
27. McFadden S.A., Howlett M.H., Mertz J.R., Wallman J. Acute effects of dietary retinoic acid on ocular components in the growing chick. Exp. Eye Res. 2006, 83:949-961.
28. Mertz J.R., Wallman J. Choroidal retinoic acid synthesis: a possible mediator between refractive error and compensatory eye growth. Exp. Eye Res. 2000, 70:519-527.
29. Mey J., McCaffery P., Drager U.C. Retinoic acid synthesis in the developing chick retina. J.Neurosci. 1997, 17:7441-7449.
30. Mitsuda S., Yoshii C., Ikegami Y., Araki M. Tissue interaction between the retinal pigment epithelium and the choroid triggers retinal regeneration of the newt Cynops pyrrhogaster. Dev. Biol. 2005, 280:122-132.
31. Moring A.G., Baker J.R., Norton T.T. Modulation of glycosaminoglycan levels in tree shrew sclera during lens-induced myopia development and recovery. Invest. Ophthalmol. Vis. Sci. 2007, 48:2947-2956.
32. Napoli J.L. Physiological insights into all-trans-retinoic acid biosynthesis. Biochim. Biophys. Acta 2011, 1821:152-167.
33. Nickla D.L., Wildsoet C., Wallman J. Compensation for spectacle lenses involves changes in proteoglycan synthesis in both the sclera and choroid. Curr. Eye Res. 1997, 16:320-326.
34. Noden D.M. Periocular mesenchyme: neural crest and mesodermal interactions. Ocular Anatomy, Embryology and Teratology 1982, 79-119. Harper & Row, Philadelphia. F.A. Jakobiec (Ed.).
35. Norton T.T., Rada J.A. Reduced extracellular matrix in mammalian sclera with induced myopia. Vis. Res. 1995, 35:1271-1281.
36. Ogata N.,M., Matsushima M., Takada Y., Tobe T., Takahashi K., Yi X., Yamamoto C., Yamada H., Uyama M. Expression of basic fibroblast growth factor mRNA in developing choroidal neovascularization. Curr. Eye Res. 1996, 15:1008-1018.
37. Pendrak K., Papastergiou G.I., Lin T., Laties A.M., Stone R.A. Choroidal vascular permeability in visually regulated eye growth. Exp. Eye Res. 2000, 70:629-637.
38. Polska E., Simader C., Weigert C., Doelemeyer G., Kolodjaschna A., Scharmann J., O.Schmetterer L. Regulation of choroidal blood flow during combined changes in intraocular pressure and arterial blood pressure. Invest. Ophthalmol. Vis. Sci. 2007, 48:3768-3774.
39. Rada J.A., Delrow J. Changes in gene expression during the recovery from experimental myopia. Invest. Ophthalmol. Vis. Sci. 2004, 45. (ARVO E-abstract #1160).
40. Rada J.A., Palmer L. Choroidal regulation of scleral glycosaminoglycan synthesis during recovery from induced myopia. Invest. Ophthalmol. Vis. Sci. 2007, 48:2957-2966.
41. Rada J.A., Wiechmann A.F. Ocular expression of avian thymic hormone: changes during the recovery from induced myopia. Mol. Vis. 2009, 15:778-792.
42. Rada J.A., McFarland A.L., Cornuet P.K., Hassell J.R. Proteoglycan synthesis by scleral chondrocytes is modulated by a vision dependent mechanism. Curr. Eye Res. 1992, 11:767-782.
43. Rada J.A., Matthews A.L., Brenza H. Regional proteoglycan synthesis in the sclera of experimentally myopic chicks. Exp. Eye Res. 1994, 59:747-760.
44. Rada J.A., Perry C.A., Slover M.L., Achen V.R. Gelatinase A and TIMP-2 expression in the fibrous sclera of myopic and recovering chick eyes. Invest. Ophthalmol. Vis. Sci. 1999, 40:3091-3099.
45. Rada J.A., Nickla D.L., Troilo D. Decreased proteoglycan synthesis associated with form deprivation myopia in mature primate eyes. Invest. Ophthalmol. Vis. Sci. 2000, 4:2050-2058.
46. Rada J.A., Huang Y., Rada K.G. Identification of choroidal ovotransferrin as a potential ocular growth regulator. Curr. Eye Res. 2001, 22:121-132.
47. Rada J.A., Johnson J.M., Achen V.R., Rada K.G. Inhibition of scleral proteoglycan synthesis blocks deprivation-induced axial elongation in chicks. Exp. Eye Res. 2002, 74:205-215.
48. Rada J.A., Wiechmann A.F., Hollaway L.R., Baggenstoss B.A., Weigel P.H. Increased hyaluronan synthase-2 mRNA expression and hyaluronan accumulation with choroidal thickening: response during recovery from induced myopia. Invest. Ophthalmol. Vis. Sci. 2010, 51:6172-6179.
49. Rada J.A., Hollaway L.R., Lam W., Li N., Napoli J.L. Identification of RALDH2 as a visually regulated retinoic acid synthesizing enzyme in the chick choroid. Invest. Ophthalmol. Vis. Sci. 2012, 53:1649-1662.
50. Saint-Geniez M., Maldonado A.E., D'Amore P.A. VEGF expression and receptor activation in the choroid during development and in the adult. Invest. Ophthalmol. Vis. Sci. 2006, 47:3135-3142.
51. Saint-Geniez M., Kurihara T., Sekiyama E., Maldonado A.E., D'Amore P.A. An essential role for RPE-derived soluble VEGF in the maintenance of the choriocapillaris. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18751-18756.
52. Schrodl F., De Laet A., Tassignon M.J., Van Bogaert P.P., Brehmer A., Neuhuber W.L., Timmermans J.P. Intrinsic choroidal neurons in the human eye: projections, targets, and basic electrophysiological data. Invest. Ophthalmol. Vis. Sci. 2003, 44:3705-3712.
53. Shelton L., Troilo D., Lerner M.R., Gusev Y., Brackett D.J., Rada J.S. Microarray analysis of choroid/RPE gene expression in marmoset eyes undergoing changes in ocular growth and refraction. Mol. Vis. 2008, 14:1465-1479.
54. Siegwart J.T., Norton T.T. The susceptible period for deprivation-induced myopia in tree shrew. Vis. Res. 1998, 38:3505-3515.
55. Siegwart J.T., Norton T.T. Regulation of the mechanical properties of tree shrew sclera by the visual environment. Vis. Res. 1999, 39:387-407.
56. Simon P., Feldkaemper M., Bitzer M., Ohngemach S., Schaeffel F. Early transcriptional changes of retinal and choroidal TGFbeta-2, RALDH-2, and ZENK following imposed positive and negative defocus in chickens. Mol. Vis. 2004, 10:588-597.
57. Spilsbury K., Garrett K.L., Shen W.Y., Constable I.J., Rakoczy P.E. Overexpression of vascular endothelial growth factor (VEGF) in the retinal pigment epithelium leads to the development of choroidal neovascularization. Am. J. Pathol. 2000, 157:135-144.
58. Steen B., Sejersen S., Berglin L., Seregard S., Kvanta A. Matrix metalloproteinases and metalloproteinase inhibitors in choroidal neovascular membranes. Invest. Ophthalmol. Vis. Sci. 1998, 39:2194-2200.
59. De Stefano M.E., Mugnaini E. Fine structure of the choroidal coat of the avian eye. Lymphatic vessels. Invest. Ophthalmol. Vis. Sci. 1997, 38:1241-1260.
60. Stone R.A., Khurana T.S. Gene profiling in experimental models of eye growth: clues to myopia pathogenesis. Vis. Res. 2010, 50:2322-2333.
61. Stubinger K., Brehmer A., Neuhuber W.L., Reitsamer H., Nickla D., Schrodl F. Intrinsic choroidal neurons in the chicken eye: chemical coding and synaptic input. Histochem. Cell. Biol. 2010, 134:145-157.
62. Sugita A., Inokuchi T. Lymphatic sinus-like structures in choroid. Jpn. J. Ophthalmol. 1992, 36:436-442.
63. Summers Rada J.A., Hollaway L.R. Regulation of the biphasic decline in scleral proteoglycan synthesis during the recovery from induced myopia. Exp. Eye Res. 2011, 92:394-400.
64. Summers Rada J.A., Datson N.A., Troilo D. Early changes in gene expression in RPE/Choroid of marmoset eyes in response to image defocus. Invest. Ophthalmol. Vis. Sci. 2011, [ARVO E-abstract #6300].
65. Torczynski E. Choroid and suprachoroid. Ocular Anatomy, Embryology, and Teratology 1982, 553-585. Harper & Row, Philadelphia. F.A. Jakobiec (Ed.).
66. Troilo D., Nickla D.L., Wildsoet C.F. Choroidal thickness changes during altered eye growth and refractive state in a primate. Invest. Ophthalmol. Vis. Sci. 2000, 41:1249-1258.
67. Troilo D., Nickla D.L., Mertz J.R., Summers Rada J.A. Change in the synthesis rates of ocular retinoic acid and scleral glycosaminoglycan during experimentally altered eye growth in marmosets. Invest. Ophthalmol. Vis. Sci. 2006, 47:1768-1777.
68. Wallman J., Winawer J. Homeostasis of eye growth and the question of myopia. Neuron 2004, 43:447-486.
69. Wallman J., Wildsoet C., Xu A., Gottlieb M.D., Nickla D.L., Marran L., Krebs W., Christensen A.M. Moving the retina: choroidal modulation of refractive state. Vis. Res. 1995, 35:37-50.
70. Yoshii C., Ueda Y., Okamoto M., Araki M. Neural retinal regeneration in the anuran amphibian Xenopus laevis post-metamorphosis: transdifferentiation of retinal pigmented epithelium regenerates the neural retina. Dev. Biol. 2007, 303:45-56.
71. Zhao S., Overbeek P.A. Regulation of choroid development by the retinal pigment epithelium. Mol. Vis. 2001, 7:277-282.
72. Zhu X., Park T.W., Winawer J., Wallman J. In a matter of minutes, the eye can know which way to grow. Invest. Ophthalmol. Vis. Sci. 2005, 46:2238-2241.