A comparative study of vertebrate corneal structure: the evolution of a refractive lens
Open accessAbstract
PURPOSE: Although corneal curvature plays an important role in determining the refractive power of the vertebrate eye, the mechanisms controlling corneal shape remain largely unknown. To address this question, we performed a comparative study of vertebrate corneal structure to identify potential evolutionarily based changes that correlate with the development of a corneal refractive lens. METHODS: Nonlinear optical (NLO) imaging of second-harmonic-generated (SHG) signals was used to image collagen and three-dimensionally reconstruct the lamellar organization in corneas from different vertebrate clades. RESULTS: Second-harmonic-generated images taken normal to the corneal surface showed that corneal collagen in all nonmammalian vertebrates was organized into sheets (fish and amphibians) or ribbons (reptiles and birds) extending from limbus to limbus that were oriented nearly orthogonal (ranging from 77.7°-88.2°) to their neighbors. The slight angular offset (2°-13°) created a rotational pattern that continued throughout the full thickness in fish and amphibians and to the very posterior layers in reptiles and birds. Interactions between lamellae were limited to "sutural" fibers in cartilaginous fish, and occasional lamellar branching in fish and amphibians. There was a marked increase in lamellar branching in higher vertebrates, such that birds ≫ reptiles > amphibians > fish. By contrast, mammalian corneas showed a nearly random collagen fiber organization with no orthogonal, chiral pattern. CONCLUSIONS: Our data indicate that nonmammalian vertebrate corneas share a common orthogonal collagen structural organization that shows increased lamellar branching in higher vertebrate species. Importantly, mammalian corneas showed a different structural organization, suggesting a divergent evolutionary background.
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Mammalian corneas do not have an orthogonal arrangement of adjacent lamellae, whereas non-mammalian vertebrate corneas share a common orthogonal collagen structural organisation, suggesting a divergent evolutionary background.
“The technique was recently used to show that mammalian corneas do not have an orthogonal arrangement of adjacent lamellae, whereas non-mammalian vertebrate corneas share a common orthogonal collagen structural organisation, which suggests that they have a divergent evolutionary background (Winkler et al., 2015).”
From Corneal structure and transparency (2015) · cites this paper as Winkler et al., 2015
In the human cornea, there is no orthogonal arrangement between adjacent lamellae, not even in the posterior stroma.
“Both scanning electron microscopy (Radner et al., 1998) and non-linear SHG microscopy (Winkler et al., 2015) have shown that, in the human cornea, there is no orthogonal arrangement between adjacent lamellae (Fig. 1b), not even in the posterior stroma.”
From Corneal structure and transparency (2015) · cites this paper as Winkler et al., 2015
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- [1]1. Swamynathan SK, Crawford MA, Robison WG Jr, Kanungo J, Piatigorsky J. Adaptive differences in the structure and macromolecular compositions of the air and water corneas of the '' four-eyed '' fish ( Anableps anableps ). FASEB J . 2003;7: 1996-2005.
- [2]2. Baylor ER. Air and water vision of the Atlantic flying fish, Cypselurus heterurus . Nature . 1967;214:307-309.
- [3]3. Jester JV , Winkler M, Jester BE, Nien C, Chai D, Brown DJ. Evaluating corneal collagen organization using high resolution non linear optical (NLO) macroscopy. Eye Contact Lens . 2010; 36:260-264.
- [4]4. Winkler M, Chai D, Kriling S, et al. Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics. Invest Ophthalmol Vis Sci . 2011;52: 8818-8827.
- [5]5. Winkler M, Shoa G, Xie Y , et al. Three-dimensional distribution of transverse collagen fibers in the anterior human corneal stroma. Invest Ophthalmol Vis Sci . 2013;54:7293-7301.
- [6]6. Thomasy SM, Raghunathan VK, Winkler M, et al. Elastic modulus and collagen organization of the rabbit cornea: epithelium to endothelium. Acta Biomater . 2014;10:785-791.
- [7]7. Morishige N, Petroll WM, Nishida T, Kenney MC, Jester JV . Noninvasive corneal stromal collagen imaging using twophoton-generated second-harmonic signals. J Cataract Refract Surg . 2006;32:1784-1791.
- [8]8. Trelstad RL. The bilaterally asymmetrical architecture of the submammalian corneal stroma resembles a cholesteric liquid crystal. Dev Biol . 1982;92:133-134.
- [9]9. Payrau P , Pouliquen Y , Faure MP , Offret G. Ultrastructure des fibres suturales de la cornee des poissons Elasmobranches. Arch Ophthalmol (Paris) . 1965;25:745-754.
- [10]10. Trelstad RL, Coulombre AJ. Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol . 1971;50:840-858.
- [12]12. Conrad GW, Paulsen AQ, Luer CA. Embryonic development of the cornea in the eye of the clearnose skate, Raja eglanteria : I. Stromal development in the absence of an endothelium. J Exp Zool . 1994;269:263-276.
- [13]13. Goldman JN, Benedek GB. The relationship between morphology and transparency in the nonswelling corneal stroma of the shark. Invest Ophthalmol Vis Sci . 1967;6:574-600.
- [14]14. Van Horn DL, Edelhauser HF , Schultz RO. Ultrastructure of the primary spectacle and cornea of the sea lamprey. J Ultrastruct Res . 1969;26:454-464.
- [15]15. Hay ED, Revel JP . Fine Structure of the Developing Avian Cornea . Vol. 1. S. Karger: New York; 1969.
- [16]16. Birk DE, Trelstad RL. Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J Cell Biol . 1986;103:231-240.
- [17]17. Birk DE, Trelstad RL. Extracellular compartments in matrix morphogenesis: collagen fibril, bundle, and lamellar formation by corneal fibroblasts. J Cell Biol . 1984;99:2024-2033.
- [18]18. Young RD, Knupp C, Pinali C, et al. Three-dimensional aspects of matrix assembly by cells in the developing cornea. Proc Natl Acad Sci U S A . 2014;111:687-692.
- [19]19. Polack FM. Morphology of the cornea. I. Study with silver stains. Am J Ophthalmol . 1961;51:1051-1056.
- [20]20. Coulombre A, Coulombre J, Mehta H. The skeleton of the eye: I. Conjunctival papillae and scleral ossicles. Dev Biol . 1962;5: 382-401.
- [21]21. Lee LP, Szema R. Inspirations from biological optics for advanced photonic systems. Science . 2005;310:1148-1150.
- [22]22. Mullaney J, Coffey V , Fenton M. Atavistic ocular ossicle. Br J Ophthalmol . 1971;55:243.
- [23]23. Haustein J. On the ultrastructure of the developing and adult mouse corneal stroma. Anat Embryol (Berl) . 1983;168:291305.
- [24]24. Meek KM, Boote C. The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma. Prog Retin Eye Res . 2009;28:369-392.
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Corneal structure and transparency
Meek, K. M., & Knupp, C. (2015) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2015.07.001 · Cited by 853 · see citing works
- Authors
- Winkler, M., Shoa, G., Tran, S. T., Xie, Y., Thomasy, S., Raghunathan, V. K., Murphy, C., Brown, D. J., & Jester, J. V.
- Affiliations
- University of California, Irvine (US)
- University of California, Davis (US)
- Corresponding author
- Jester, James V.
- Venue
- Investigative Opthalmology & Visual Science
- Published
- 2015-04-30
- Volume
- 56
- Issue
- 4
- Pages
- 2764
- ISSN
- 0146-0404 (ISSN-L)
- 1552-5783
- PMC
- PMC4416662
- OpenAlex
- W2400665456
- Cited by
- 50
- References
- 0
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 6 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 9 · 2016: 3 · 2015: 2
- FWCI
- 5.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Investigative Ophthalmology & Visual Science (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Eye Institute (EY018665, R01EY018665)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Corneal surgery and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Ocular Disorders and Treatments
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Corneal Surgery and Treatments
- Keywords
- corneal collagen, corneal structure, corneal curvature, lamellar structure, collagen fiber orientation, Chondrichthyes, mammals, non-mammalian vertebrates, second harmonic generation microscopy
- MeSH terms
- Amphibians, Anatomy, Comparative, Animals, Birds, Collagen, Cornea, Biological Evolution, Fishes, Humans, Lens, Crystalline, Mammals, Reptiles, Species Specificity, Surface Properties, Vertebrates, Nonlinear Dynamics, Microscopy, Confocal, Imaging, Three-Dimensional
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