Ultrastructural analysis of the human lens fiber cell remodeling zone and the initiation of cellular compaction

Experimental Eye Research

Volumn 116, Issue , 2013, Pages 411-418

  Costello, M Joseph ^a   Mohamed, Ashik ^b   Gilliland, Kurt O ^a   Fowler, W Craig ^a   Johnsen, Sönke ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b L V PRASAD EYE INSTITUTE   (India)

^c DUKE UNIVERSITY   (United States)

Author keywords

Compaction; Differentiation; Electron microscopy; Fiber cell; Remodeling zone

Indexed keywords

CRYSTALLIN; FORMALDEHYDE; PARAFORMALDEHYDE;

ARTICLE; CELL FUNCTION; CELL SHAPE; CELL ULTRASTRUCTURE; CELLULAR COMPACTION; CONFOCAL MICROSCOPY; CYTOSKELETON; GAP JUNCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LENS EPITHELIUM; OPTICAL INSTRUMENTATION; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

COMPACTION; DIFFERENTIATION; ELECTRON MICROSCOPY; FIBER CELL; REMODELING ZONE;

ADULT; AGED; AGED, 80 AND OVER; CRYSTALLINS; CYTOSKELETON; GAP JUNCTIONS; HUMANS; LENS, CRYSTALLINE; MICROSCOPY, ELECTRON; MIDDLE AGED; YOUNG ADULT;

EID: 84887557713     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.10.015     Document Type: Article

References (48)

1. Al-Ghoul K.J., Costello M.J. Light microscopic variation of fiber cell size, shape and ordering in the equatorial plane of bovine and human lenses. Mol. Vis. 1997, 3:2.
2. Al-Ghoul K.J., Nordgren R.K., Kuszak A.J., Freel C.D., Costello M.J., Kuszak J.R. Structural evidence of human nuclear fiber compaction as a function of ageing and cataractogenesis. Exp. Eye Res. 2001, 72:199-214.
3. Alizadeh A., Clark J., Seeberger T., Hess J., Blankenship T., FitzGerald P.G. Characterization of a mutation in the lens-specific CP49 in the 129 strain of mouse. Investig. Ophthalmol. Vis. Sci. 2004, 45:884-891.
4. Augusteyn R.C., Vrensen G., Willekens B. The effect of paraformaldehyde fixation and PBS storage on the water content of the human lens. Mol. Vis. 2008, 14:90-94.
5. Bassnett S. On the mechanism of organelle degradation in the vertebrate lens. Exp. Eye Res. 2009, 88:133-139.
6. Bassnett S., Missey H., Vucemilo I. Molecular architecture of the lens fiber cell basal membrane complex. J.Cell Sci. 1999, 112(Pt 13):2155-2165.
7. Beebe D.C., Vasiliev O., Guo J., Shui Y.B., Bassnett S. Changes in adhesion complexes define stages in the differentiation of lens fiber cells. Investig. Ophthalmol. Vis. Sci. 2001, 42:727-734.
8. Biswas S.K., Lee J.E., Brako L., Jiang J.X., Lo W.K. Gap junctions are selectively associated with interlocking ball-and-sockets but not protrusions in the lens. Mol. Vis. 2010, 16:2328-2341.
9. Biswas S.K., et al. The tropomodulin1-actin network and CP49 beaded filaments regulate formation of undulating aquaporin junctions in mouse lens fiber cells. Investig. Ophthalmol. Vis. Sci. 2013, 54. (E-Abstract 5734).
10. Blankenship T.N., Hess J.F., FitzGerald P.G. Development- and differentiation-dependent reorganization of intermediate filaments in fiber cells. Investig. Ophthalmol. Vis. Sci. Mar. 2001, 42(3):735-742.
11. Costello M.J., Johnsen S., Metlapally S., Gilliland K.O., Frame L., Balasubramanian D. Multilamellar spherical particles as potential sources of excessive light scattering in human age-related nuclear cataracts. Exp. Eye Res. 2010, 91:881-889.
12. Costello M.J., Johnsen S., Metlapally S., Gilliland K.O., Ramamurthy B., Krishna P.V., Balasubramanian D. Ultrastructural analysis of damage to nuclear fiber cell membranes in advanced age-related cataracts from India. Exp. Eye Res. 2008, 87:147-158.
13. Costello M.J., McIntosh T.J., Robertson J.D. Membrane specializations in mammalian lens fiber cells: distribution of square arrays. Curr. Eye Res. 1985, 4:1183-1201.
14. Costello M.J., McIntosh T.J., Robertson J.D. Distribution of gap junctions and square array junctions in the mammalian lens. Investig. Ophthalmol. Vis. Sci. 1989, 30:975-989.
15. Costello M.J., Oliver T.N., Cobo L.M. Cellular architecture in age-related human nuclear cataracts. Investig. Ophthalmol. Vis. Sci. 1992, 33:3209-3227.
16. Costello M.J., et al. Simple fixation and storage protocol for preserving the internal structure of intact donor lenses and extracted human nuclear cataracts. Investig. Ophthalmol. Vis. Sci. 2012, 53. (ARVO E-Abstract 3031).
17. Costello M.J., Brennan L.A., Basu S., Chauss D., Mohamed A., Gilliland K.O., Johnsen S., Menko S., Kantorow M. Autophagy and mitophagy participate in ocular lens organelle degradation. Exp. Eye Res. 2013, 116:141-150.
18. David L.L., Varnum M.D., Lampi K.J., Shearer T.R. Calpain II in human lens. Investig. Ophthalmol. Vis. Sci. 1989, 30:269-275.
19. De Maria A., Shi Y., Kumar N.M., Bassnett S. Calpain expression and activity during lens fiber cell differentiation. J.Biol. Chem. 2009, 284:13542-13550.
20. Dickson D.H., Crock G.W. Interlocking patterns on primate lens fibers. Investig. Ophthalmol. 1972, 11:809-815.
21. Dickson D.H., Crock G.W. Fine structure of primate lens fibers. Cataract and Abnormalities of the Lens 1975, 49-58. Grune & Stratton, New York. J.G. Bellows (Ed.).
22. FitzGerald P.G. Lens intermediate filaments. Exp. Eye Res. 2009, 88:165-172.
23. Gokhin D.S., Nowak R.B., Kim N.E., Arnett E.E., Chen A.C., Sah R.L., Clark J.I., Fowler V.M. Tmod1 and CP49 synergize to control the fiber cell geometry, transparency, and mechanical stiffness of the mouse lens. PLoS One 2012, 7:e48734.
24. Goodenough D.A. Lens gap junctions: a structural hypothesis for nonregulated low-resistance intercellular pathways. Investig. Ophthalmol. Vis. Sci. 1979, 18:1104-1122.
25. Grey A.C., Schey K.L. Age-related changes in the spatial distribution of human lens alpha-crystallin products by MALDI imaging mass spectrometry. Investig. Ophthalmol. Vis. Sci. 2009, 50:4319-4329.
26. Jones C.E., Atchison D.A., Meder R., Pope J.M. Refractive index distribution and optical properties of the isolated human lens measured using magnetic resonance imaging (MRI). Vis. Res. 2005, 45:2352-2366.
27. Kuszak J.R., Brown H.G. Embryology and anatomy of the lens. Principles and Practice of Ophthalmology 1994, 82-96. W. B. Saunders, Philadelphia. D.M. Albert, F.A. Jakobiec (Eds.).
28. Kuszak J.R., Costello M.J. Structure of the vertebrate lens. Development of the Ocular Lens 2004, 71-118. Wiley and Sons Inc. F.J. Lovicu, M.L. Robinson (Eds.).
29. Kuszak J.R., Ennesser C.A., Umlas J., Macsai-Kaplan M.S., Weinstein R.S. The ultrastructure of fiber cells in primate lenses: a model for studying membrane senescence. J.Ultrastruct. Mol. Struct. Res. 1988, 100:60-74.
30. Kuwabara T. The maturation of the lens cell: a morphologic study. Exp. Eye Res. 1975, 20:427-443.
31. Lee A., Fischer R.S., Fowler V.M. Stabilization and remodeling of the membrane skeleton during lens fiber cell differentiation and maturation. Dev. Dyn. 2000, 217:257-270.
32. Lim J.C., Walker K.L., Sherwin T., Schey K.L., Donaldson P.J. Confocal microscopy reveals zones of membrane remodeling in the outer cortex of the human lens. Investig. Ophthalmol. Vis. Sci. 2009, 50:4304-4310.
33. Lindsey Rose K.M., Gourdie R.G., Prescott A.R., Quinlan R.A., Crouch R.K., Schey K.L. The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49. Investig. Ophthalmol. Vis. Sci. 2006, 47:1562-1570.
34. Lo W.K., Harding C.V. Square arrays and their role in ridge formation in human lens fibers. J.Ultrastruct. Res. 1984, 86:228-245.
35. Lo W.K., Harding C.V. Structure and distribution of gap junctions in lens epithelium and fiber cells. Cell Tissue Res. 1986, 244:253-263.
36. Lo W.K., Shaw A.P., Wen X.J. Actin filament bundles in cortical fiber cells of the rat lens. Exp. Eye Res. 1997, 65:691-701.
37. Maddala R., Skiba N.P., Lalane R., Sherman D.L., Brophy P.J., Rao P.V. Periaxin is required for hexagonal geometry and membrane organization of mature lens fibers. Dev. Biol. 2011, 357:179-190.
38. Metlapally S., Costello M.J., Gilliland K.O., Ramamurthy B., Krishna P.V., Balasubramanian D., Johnsen S. Analysis of nuclear fiber cell cytoplasmic texture in advanced cataractous lenses from Indian subjects using Debye-Bueche theory. Exp. Eye Res. 2008, 86:434-444.
39. Michael R., Bron A.J. The ageing lens and cataract: a model of normal and pathological ageing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:1278-1292.
40. Rafferty N.S., Goossens W. Cytoplasmic filaments in the crystalline lens of various species: functional correlations. Exp. Eye Res. 1978, 26:177-190.
41. Sandilands A., Prescott A.R., Hutcheson A.M., Quinlan R.A., Casselman J.T., FitzGerald P.G. Filensin is proteolytically processed during lens fiber cell differentiation by multiple independent pathways. Eur. J. Cell Biol. Jul 1995, 67(3):238-253.
42. Schietroma C., Fain N., Zampighi L.M., Lanzavecchia S., Zampighi G.A. The structure of the cytoplasm of lens fibers as determined by conical tomography. Exp. Eye Res. 2009, 88:566-574.
43. Taylor V.L., al-Ghoul K.J., Lane C.W., Davis V.A., Kuszak J.R., Costello M.J. Morphology of the normal human lens. Investig. Ophthalmol. Vis. Sci. 1996, 37:1396-1410.
44. Vrensen G., Van Marle J., Van Veen H., Willekens B. Membrane architecture as a function of lens fibre maturation: a freeze fracture and scanning electron microscopic study in the human lens. Exp. Eye Res. 1992, 54:433-446.
45. Vrensen G.F. Early cortical lens opacities: a short overview. Acta Ophthalmol. 2009, 87:602-610.
46. Zampighi G., Simon S.A., Robertson J.D., McIntosh T.J., Costello M.J. On the structural organization of isolated bovine lens fiber junctions. J.Cell Biol. 1982, 93:175-189.
47. Zampighi G.A., Hall J.E., Ehring G.R., Simon S.A. The structural organization and protein composition of lens fiber junctions. J.Cell Biol. 1989, 108:2255-2275.
48. Zhou C.J., Lo W.K. Association of clathrin, AP-2 adaptor and actin cytoskeleton with developing interlocking membrane domains of lens fibre cells. Exp. Eye Res. 2003, 77:423-432.