Three-dimensional aspects of matrix assembly by cellsin the developing cornea

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

Volumn 111, Issue 2, 2014, Pages 687-692

  Young, Robert D ^a   Knupp, Carlo ^a   Pinali, Christian ^a   Png, Kenneth M Y ^b   Ralphs, James R ^c   Bushby, Andrew J ^b   Starborg, Tobias ^d   Kadler, Karl E ^d   Quantock, Andrew J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COLLAGEN;

ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CHICKEN; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CORNEA; CORNEA CELL; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; FOURIER ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; THREE DIMENSIONAL IMAGING; TISSUE SECTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRAMICROTOMY;

ANIMALS; CHICK EMBRYO; COLLAGEN; CORNEA; CORNEAL KERATOCYTES; EXTRACELLULAR MATRIX; FOURIER ANALYSIS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PSEUDOPODIA;

EID: 84892580513     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1313561110     Document Type: Article

References (45)

1. Ricard-Blum S (2011) The collagen family. Cold Spring Harb Perspect Biol 3(1):a004978.
2. Gelse K, Pöschl E, Aigner T (2003) Collagens?Structure, function, and biosynthesis. Adv Drug Deliv Rev 55(12):1531-1546.
3. Boote C, Dennis S, Huang Y, Quantock AJ, Meek KM (2005) Lamellar orientation in human cornea in relation to mechanical properties. J Struct Biol 149(1):1-6.
4. Trelstad RL, Coulombre AJ (1971) Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol 50(3):840-858.
5. Ruggeri A, Benazzo F, Reale E (1979) Collagen fibrils with straight and helicoidal microfibrils: A freeze-fracture and thin-section study. J Ultrastruct Res 68(1):101-108.
6. Holmes DF, et al. (2001) Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization. Proc Natl Acad Sci USA 98(13):7307-7312.
7. Raspanti M, Reguzzoni M, Protasoni M, Martini D (2011) Evidence of a discrete axial structure in unimodal collagen fibrils. Biomacromolecules 12(12):4344-4347.
8. Kadler KE, Holmes DF, Trotter JA, Chapman JA (1996) Collagen fibril formation. Biochem J 316(Pt 1):1-11.
9. Holmes DF, Kadler KE (2005) The precision of lateral size control in the assembly of corneal collagen fibrils. J Mol Biol 345(4):773-784.
10. Birk DE, Fitch JM, Babiarz JP, Linsenmayer TF (1988) Collagen type I and type V are present in the same fibril in the avian corneal stroma. J Cell Biol 106(3):999-1008.
11. Linsenmayer TF, et al. (1993) Type V collagen: Molecular structure and fibrillar organization of the chicken α 1(V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J Cell Biol 121(5):1181-1189.
12. Birk DE, Fitch JM, Babiarz JP, Doane KJ, Linsenmayer TF (1990) Collagen fibrillogenesis in vitro: Interaction of types I and V collagen regulates fibril diameter. J Cell Sci 95(Pt 4): 649-657.
13. Birk DE (2001) Type V collagen: Heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32(3):223-237.
14. Segev F, et al. (2006) Structural abnormalities of the cornea and lid resulting from collagen V mutations. Invest Ophthalmol Vis Sci 47(2):565-573.
15. Birk DE, Trelstad RL (1986) Extracellular compartments in tendon morphogenesis: Collagen fibril, bundle, and macroaggregate formation. J Cell Biol 103(1):231-240.
16. Birk DE, Zycband E (1994) Assembly of the tendon extracellular matrix during development. J Anat 184(Pt 3):457-463.
17. Birk DE, Zycband EI, Woodruff S, Winkelmann DA, Trelstad RL (1997) Collagen fibrillogenesis in situ: Fibril segments become long fibrils as the developing tendon matures. Dev Dyn 208(3):291-298.
18. Zhang G, et al. (2005) Development of tendon structure and function: Regulation of collagen fibrillogenesis. J Musculoskelet Neuronal Interact 5(1):5-21.
19. Canty EG, et al. (2004) Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol 165(4):553-563.
20. Humphries SM, Lu Y, Canty EG, Kadler KE (2008) Active negative control of collagen fibrillogenesis in vivo. Intracellular cleavage of the type I procollagen propeptides in tendon fibroblasts without intracellular fibrils. J Biol Chem 283(18):12129-12135.
21. Starborg T, Lu Y, Huffman A, Holmes DF, Kadler KE (2009) Electron microscope 3D reconstruction of branched collagen fibrils in vivo. Scand J Med Sci Sports 19(4): 547-552.
22. Giraud-Guille MM (1996) Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int Rev Cytol 166:59-101.
23. Giraud-Guille MM, Besseau L, Martin R (2003) Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36(10):1571-1579.
24. Guo X, et al. (2007) Morphologic characterization of organized extracellular matrix deposition by ascorbic acid-stimulated human corneal fibroblasts. Invest Ophthalmol Vis Sci 48(9):4050-4060.
25. Saeidi N, et al. (2012) Molecular crowding of collagen: A pathway to produce highlyorganized collagenous structures. Biomaterials 33(30):7366-7374.
26. Hay ED (1980) Development of the vertebrate cornea. Int Rev Cytol 63:263-322.
27. Hay ED, Revel JP (1969) Fine Structure of the Developing Avian Cornea. Monographs in Developmental Biology (S Karger, New York).
28. Birk DE, Trelstad RL (1984) Extracellular compartments in matrix morphogenesis: Collagen fibril, bundle, and lamellar formation by corneal fibroblasts. J Cell Biol 99(6):2024-2033.
29. Hekking LHP, et al. (2009) Focused ion beam-scanning electron microscope: Exploring large volumes of atherosclerotic tissue. J Microsc 235(3):336-347.
30. Knott G, Marchman H, Wall D, Lich B (2008) Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J Neurosci 28(12):2959-2964.
31. Armer HEJ, et al. (2009) Imaging transient blood vessel fusion events in zebrafish by correlative volume electron microscopy. PLoS ONE 4(11):e7716.
32. Bushby AJ, et al. (2011) Imaging three-dimensional tissue architectures by focused ion beam scanning electron microscopy. Nat Protoc 6(6):845-858.
33. Heymann JA, et al. (2006) Site-specific 3D imaging of cells and tissues with a dual beam microscope. J Struct Biol 155(1):63-73.
34. Leighton SB (1981) SEM images of block faces, cut by a miniature microtome within the SEM?A technical note. Scan Electron Microsc 233(Pt 2):73-76.
35. Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2(11):e329.
36. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of threedimensional image data using IMOD. J Struct Biol 116(1):71-76.
37. Toole BP, Trelstad RL (1971) Hyaluronate production and removal during corneal development in the chick. Dev Biol 26(1):28-35.
38. Quantock AJ, Young RD (2008) Development of the corneal stroma, and the collagenproteoglycan associations that help define its structure and function. Dev Dyn 237(10): 2607-2621.
39. Hasty DL, Hay ED (1977) Freeze-fracture studies of the developing cell surface. I. The plasmalemma of the corneal fibroblast. J Cell Biol 72(3):667-686.
40. Bueno EM, Saeidi N, Melotti S, Ruberti JW (2009) Effect of serum and insulin modulation on the organization and morphology of matrix synthesized by bovine corneal stromal cells. Tissue Eng Part A 15(11):3559-3573.
41. Goh WI, et al. (2011) Rif-mDia1 interaction is involved in filopodium formation independent of Cdc42 and Rac effectors. J Biol Chem 286(15):13681-13694.
42. Gealy C, et al. (2009) Actin and type I collagen propeptide distribution in the developing chick cornea. Invest Ophthalmol Vis Sci 50(4):1653-1658.
43. Starborg T, et al. (2013) Using transmission electron microscopy and 3View to determine collagen fibril size and three-dimensional organization. Nat Protoc 8(7): 1433-1448.
44. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11(7):36-42.
45. Ress DB, Harlow ML, Marshall RM, McMahan UJ (2004) Methods for generating highresolution structural models from electron microscope tomography data. Structure 12(10):1763-1774.