The cause and consequence of fiber cell compaction in the vertebrate lens

Experimental Eye Research

Volumn 156, Issue , 2017, Pages 50-57

  Bassnett, Steven ^a   Costello, M Joseph ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

Compaction; Crystallin; GRIN; Lens; Oncotic pressure; Refractive index; Volume control

Indexed keywords

ARTICLE; FIBER CELL COMPACTION; FIBER OPTICS; HUMAN; LENS EPITHELIUM CELL; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; REFRACTION INDEX; TISSUE GROWTH; VERTEBRATE; ACCOMMODATION; ANIMAL; CELL SHAPE; CYTOLOGY; EYE REFRACTION; GROWTH, DEVELOPMENT AND AGING; LENS; METABOLISM; PHYSIOLOGY;

CRYSTALLIN;

ACCOMMODATION, OCULAR; ANIMALS; CELL SHAPE; CRYSTALLINS; HUMANS; LENS, CRYSTALLINE; REFRACTION, OCULAR;

EID: 84962023213     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2016.03.009     Document Type: Article

References (93)

1. al-Ghoul, K.J., Costello, M.J., Morphological changes in human nuclear cataracts of late-onset diabetics. Exp. Eye Res. 57 (1993), 469–486.
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. 72 (2001), 199–214.
3. Al-Khudari, S., Donohue, S.T., Al-Ghoul, W.M., Al-Ghoul, K.J., Age-related compaction of lens fibers affects the structure and optical properties of rabbit lenses. BMC Ophthalmol., 7, 2007, 19.
4. Augusteyn, R.C., Growth of the human eye lens. Mol. Vis. 13 (2007), 252–257.
5. Augusteyn, R.C., On the growth and internal structure of the human lens. Exp. Eye Res. 90 (2010), 643–654.
6. Augusteyn, R.C., Growth of the eye lens: I. Weight accumulation in multiple species. Mol. Vis. 20 (2014), 410–426.
7. Augusteyn, R.C., Growth of the eye lens: II. Allometric studies. Mol. Vis. 20 (2014), 427–440.
8. Augusteyn, R.C., Jones, C.E., Pope, J.M., Age-related development of a refractive index plateau in the human lens: evidence for a distinct nucleus. Clin. Exp. Optom. 91 (2008), 296–301.
9. Augusteyn, R.C., Nankivil, D., Mohamed, A., Maceo, B., Pierre, F., Parel, J.M., Human ocular biometry. Exp. Eye Res. 102 (2012), 70–75.
10. Axelrod, D., Lerner, D., Sands, P.J., Refractive index within the lens of a goldfish eye determined from the paths of thin laser beams. Vis. Res. 28 (1988), 57–65.
11. Barer, K., Joseph, S., Refractometry of living cells. I. Basic principles. Q. J. Microsc. Sci. 95 (1954), 399–423.
12. Bassnett, S., Three-dimensional reconstruction of cells in the living lens: the relationship between cell length and volume. Exp. Eye Res. 81 (2005), 716–723.
13. Bassnett, S., Winzenburger, P.A., Morphometric analysis of fibre cell growth in the developing chicken lens. Exp. Eye Res. 76 (2003), 291–302.
14. Bellows, J.G., Phakochronology. The study of dating structural changes in the lens. Br. J. Ophthalmol. 52 (1968), 540–545.
15. Bours, J., Fodisch, H.J., Human fetal lens: wet and dry weight with increasing gestational age. Ophthalmic Res. 18 (1986), 363–368.
16. Brown, N., Dating the onset of cataract. Trans. Ophthalmol. Soc. U. K. 96 (1976), 18–23.
17. Brown, N., Cataract in childhood: photograph methods in assessment. Br. J. Ophthalmol. 61 (1977), 135–140.
18. Brown, N.A., Sparrow, J.M., Bron, A.J., Central compaction in the process of lens growth as indicated by lamellar cataract. Br. J. Ophthalmol. 72 (1988), 538–544.
19. Campbell, M.C., Measurement of refractive index in an intact crystalline lens. Vis. Res. 24 (1984), 409–415.
20. Castoro, J.A., Bettelheim, F.A., Distribution of the total and non-freezable water in rat lenses. Exp. Eye Res. 43 (1986), 185–191.
21. Costello, M.J., McIntosh, T.J., Robertson, J.D., Membrane specializations in mammalian lens fiber cells: distribution of square arrays. Curr. Eye Res. 4 (1985), 1183–1201.
22. Costello, M.J., McIntosh, T.J., Robertson, J.D., Distribution of gap junctions and square array junctions in the mammalian lens. Invest. Ophthalmol. Vis. Sci. 30 (1989), 975–989.
23. Costello, M.J., Mohamed, A., Gilliland, K.O., Fowler, W.C., Johnsen, S., Ultrastructural analysis of the human lens fiber cell remodeling zone and the initiation of cellular compaction. Exp. Eye Res. 116 (2013), 411–418.
24. David, L.L., Azuma, M., Shearer, T.R., Cataract and the acceleration of calpain-induced beta-crystallin insolubilization occurring during normal maturation of rat lens. Invest. Ophthalmol. Vis. Sci. 35 (1994), 785–793.
25. De Maria, A., Shi, Y., Kumar, N.M., Bassnett, S., Calpain expression and activity during lens fiber cell differentiation. J. Biol. Chem. 284 (2009), 13542–13550.
26. Dickson, D.H., Crock, G.W., Interlocking patterns on primate lens fibers. Invest. Ophthalmol. 11 (1972), 809–815.
27. Dubbelman, M., Van der Heijde, G.L., The shape of the aging human lens: curvature, equivalent refractive index and the lens paradox. Vis. Res. 41 (2001), 1867–1877.
28. Ebihara, L., Korzyukov, Y., Kothari, S., Tong, J.J., Cx46 hemichannels contribute to the sodium leak conductance in lens fiber cells. Am. J. Physiol. Cell Physiol. 306 (2014), C506–C513.
29. Faulkner-Jones, B., Zandy, A.J., Bassnett, S., RNA stability in terminally differentiating fibre cells of the ocular lens. Exp. Eye Res. 77 (2003), 463–476.
30. Freel, C.D., al-Ghoul, K.J., Kuszak, J.R., Costello, M.J., Analysis of nuclear fiber cell compaction in transparent and cataractous diabetic human lenses by scanning electron microscopy. BMC Ophthalmol., 3, 2003, 1.
31. Gao, J., Sun, X., Moore, L.C., Brink, P.R., White, T.W., Mathias, R.T., The effect of size and species on lens intracellular hydrostatic pressure. Invest. Ophthalmol. Vis. Sci. 54 (2013), 183–192.
32. Gao, J., Sun, X., Moore, L.C., White, T.W., Brink, P.R., Mathias, R.T., Lens intracellular hydrostatic pressure is generated by the circulation of sodium and modulated by gap junction coupling. J. Gen. Physiol. 137 (2011), 507–520.
33. Gao, J., Sun, X., White, T.W., Delamere, N.A., Mathias, R.T., Feedback regulation of intracellular hydrostatic pressure in surface cells of the lens. Biophys. J. 109 (2015), 1830–1839.
34. Gladstone, J.H., Dale, T.P., Researches on the refraction, dispersion and sensitiveness of liquids. Philos. Trans. R. Soc. Lond. 153 (1864), 317–343.
35. Glasser, A., Campbell, M.C., Biometric, optical and physical changes in the isolated human crystalline lens with age in relation to presbyopia. Vis. Res. 39 (1999), 1991–2015.
36. Harding, C.V., Hughes, W.L., Bond, V.P., Schork, P., Autoradiographic localization of tritiated thymidine in wholemount preparations of lens epithelium. Arch. Ophthalmol. 63 (1960), 58–65.
37. Hoshino, M., Uesugi, K., Yagi, N., Mohri, S., Regini, J., Pierscionek, B., Optical properties of in situ eye lenses measured with X-ray Talbot interferometry: a novel measure of growth processes. PLoS One, 6, 2011, e25140.
38. 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. 45 (2005), 2352–2366.
39. Kenworthy, A.K., Magid, A.D., Oliver, T.N., McIntosh, T.J., Colloid osmotic pressure of steer alpha- and beta-crystallins: possible functional roles for lens crystallin distribution and structural diversity. Exp. Eye Res. 59 (1994), 11–30.
40. Kreuzer, R.O., Sivak, J.G., Spherical-aberration of the fish lens – interspecies variation and age. J. Comp. Physiol. 154 (1984), 415–422.
41. Kuszak, J., Alcala, J., Maisel, H., The surface morphology of embryonic and adult chick lens-fiber cells. Am. J. Anat. 159 (1980), 395–410.
42. Kuszak, J.R., Costello, M.J., Structure of the vertebrate lens. Lovicu, F.J., Robinson, M.L., (eds.) Development of the Ocular Lens, 2004, Cambridge University Press, Cambridge.
43. 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. 100 (1988), 60–74.
44. Kuszak, J.R., Zoltoski, R.K., Sivertson, C., Fibre cell organization in crystalline lenses. Exp. Eye Res. 78 (2004), 673–687.
45. Kuwabara, T., The maturation of the lens cell: a morphologic study. Exp. Eye Res. 20 (1975), 427–443.
46. Lahm, D., Lee, L.K., Bettelheim, F.A., Age dependence of freezable and nonfreezable water content of normal human lenses. Invest. Ophthalmol. Vis. Sci. 26 (1985), 1162–1165.
47. 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. Invest. Ophthalmol. Vis. Sci. 50 (2009), 4304–4310.
48. Lo, W.K., Biswas, S.K., Brako, L., Shiels, A., Gu, S., Jiang, J.X., Aquaporin-0 targets interlocking domains to control the integrity and transparency of the eye lens. Invest. Ophthalmol. Vis. Sci. 55 (2014), 1202–1212.
49. Lo, W.K., Harding, C.V., Square arrays and their role in ridge formation in human lens fibers. J. Ultrastruct. Res. 86 (1984), 228–245.
50. Ma, H., Hata, I., Shih, M., Fukiage, C., Nakamura, Y., Azuma, M., Shearer, T.R., Lp82 is the dominant form of calpain in young mouse lens. Exp. Eye Res. 68 (1999), 447–456.
51. Ma, H., Shih, M., Hata, I., Fukiage, C., Azuma, M., Shearer, T.R., Protein for Lp82 calpain is expressed and enzymatically active in young rat lens. Exp. Eye Res. 67 (1998), 221–229.
52. Mathias, R.T., Steady-state voltages, ion fluxes, and volume regulation in syncytial tissues. Biophys. J. 48 (1985), 435–448.
53. Mathias, R.T., Kistler, J., Donaldson, P., The lens circulation. J. Membr. Biol. 216 (2007), 1–16.
54. Mathias, R.T., White, T.W., Gong, X., Lens gap junctions in growth, differentiation, and homeostasis. Physiol. Rev. 90 (2010), 179–206.
55. McAvoy, J.W., Cell division, cell elongation and distribution of alpha-, beta- and gamma-crystallins in the rat lens. J. Embryol. Exp. Morphol. 44 (1978), 149–165.
56. Mochizuki, T., Masai, I., The lens equator: a platform for molecular machinery that regulates the switch from cell proliferation to differentiation in the vertebrate lens. Dev. Growth Differ. 56 (2014), 387–401.
57. Moffat, B.A., Atchison, D.A., Pope, J.M., Age-related changes in refractive index distribution and power of the human lens as measured by magnetic resonance micro-imaging in vitro. Vis. Res. 42 (2002), 1683–1693.
58. Mutti, D.O., Zadnik, K., Adams, A.J., The equivalent refractive index of the crystalline lens in childhood. Vis. Res. 35 (1995), 1565–1573.
59. Patterson, J.W., Fournier, D.J., The effect of tonicity on lens volume. Invest. Ophthalmol. 15 (1976), 866–869.
60. Philipson, B., Distribution of protein within the normal rat lens. Invest. Ophthalmol. 8 (1969), 258–270.
61. Pierscionek, B., Bahrami, M., Hoshino, M., Uesugi, K., Regini, J., Yagi, N., The eye lens: age-related trends and individual variations in refractive index and shape parameters. Oncotarget 6 (2015), 30532–30544.
62. Pierscionek, B., Smith, G., Augusteyn, R.C., The refractive increments of bovine alpha-, beta-, and gamma-crystallins. Vis. Res. 27 (1987), 1539–1541.
63. Pierscionek, B.K., Refractive index of the human lens surface measured with an optic fibre sensor. Ophthalmic Res. 26 (1994), 32–35.
64. Pierscionek, B.K., Refractive index contours in the human lens. Exp. Eye Res. 64 (1997), 887–893.
65. Pierscionek, B.K., Belaidi, A., Bruun, H.H., Optical development in the foetal bovine lens. Exp. Eye Res. 77 (2003), 639–641.
66. Pierscionek, B.K., Regini, J.W., The gradient index lens of the eye: an opto-biological synchrony. Prog. Retin Eye Res. 31 (2012), 332–349.
67. Rafferty, N.S., Smith, R., Analysis of cell-populations of Normal and injured mouse lens epithelium .1. Cell-cycle. Anat. Rec. 186 (1976), 105–113.
68. Shi, Y., De Maria, A., Lubura, S., Sikic, H., Bassnett, S., The penny pusher: a cellular model of lens growth. Invest. Ophthalmol. Vis. Sci. 56 (2015), 799–809.
69. Shi, Y., Tu, Y., De Maria, A., Mecham, R.P., Bassnett, S., Development, composition, and structural arrangements of the ciliary zonule of the mouse. Invest. Ophthalmol. Vis. Sci. 54 (2013), 2504–2515.
70. Shih, M., Lampi, K.J., Shearer, T.R., David, L.L., Cleavage of beta crystallins during maturation of bovine lens. Mol. Vis., 4, 1998, 4.
71. Siebinga, I., Vrensen, G.F., De Mul, F.F., Greve, J., Age-related changes in local water and protein content of human eye lenses measured by Raman microspectroscopy. Exp. Eye Res. 53 (1991), 233–239.
72. Sikic, H., Shi, Y., Lubura, S., Bassnett, S., A stochastic model of eye lens growth. J. Theor. Biol. 376 (2015), 15–31.
73. Sivak, J.G., West, J.A., Campbell, M.C., Growth and optical development of the ocular lens of the squid (Sepioteuthis lessoniana). Vis. Res. 34 (1994), 2177–2187.
74. Smith, P., A further investigation of the pathology of glaucoma. R. Lond. Ophthalmic Hosp. Rep. 10 (1882), 25–43.
75. Smith, P., On the growth of the crystalline lens. Trans. Ophthalmol. Soc. U. K. 3 (1883), 79–99.
76. Stirling, R.J., Wakely, J., Changes in the surface morphology of lens fibres in the developing chick eye in relation to lens transparency. J. Anat. 155 (1987), 11–22.
77. Takamura, Y., Kubo, E., Tsuzuki, S., Akagi, Y., Apoptotic cell death in the lens epithelium of rat sugar cataract. Exp. Eye Res. 77 (2003), 51–57.
78. 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. Invest. Ophthalmol. Vis. Sci. 37 (1996), 1396–1410.
79. Ueda, Y., Fukiage, C., Shih, M., Shearer, T.R., David, L.L., Mass measurements of C-terminally truncated alpha-crystallins from two-dimensional gels identify Lp82 as a major endopeptidase in rat lens. Mol. Cell Proteom. 1 (2002), 357–365.
80. Vaghefi, E., Kim, A., Donaldson, P.J., Active maintenance of the gradient of refractive Index is required to sustain the optical properties of the lens. Invest. Ophthalmol. Vis. Sci. 56 (2015), 7195–7208.
81. Vaghefi, E., Pontre, B.P., Jacobs, M.D., Donaldson, P.J., Visualizing ocular lens fluid dynamics using MRI: manipulation of steady state water content and water fluxes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301 (2011), R335–R342.
82. Veretout, F., Delaye, M., Tardieu, A., Molecular basis of eye lens transparency. Osmotic pressure and X-ray analysis of alpha-crystallin solutions. J. Mol. Biol. 205 (1989), 713–728.
83. Veretout, F., Tardieu, A., The protein concentration gradient within eye lens might originate from constant osmotic pressure coupled to differential interactive properties of crystallins. Eur. Biophys. J. 17 (1989), 61–68.
84. 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. 54 (1992), 433–446.
85. Willekens, B., Vrensen, G., Lens fiber organization in four avian species: a scanning electron microscopic study. Tissue Cell 17 (1985), 359–377.
86. Wilmarth, P.A., Taube, J.R., Riviere, M.A., Duncan, M.K., David, L.L., Proteomic and sequence analysis of chicken lens crystallins reveals alternate splicing and translational forms of beta B2 and beta A2 crystallins. Invest. Ophthalmol. Vis. Sci. 45 (2004), 2705–2715.
87. Wistow, G., Piatigorsky, J., Recruitment of enzymes as lens structural proteins. Science 236 (1987), 1554–1556.
88. Wu, J.J., Wu, W., Tholozan, F.M., Saunter, C.D., Girkin, J.M., Quinlan, R.A., A dimensionless ordered pull-through model of the mammalian lens epithelium evidences scaling across species and explains the age-dependent changes in cell density in the human lens. J. R. Soc. Interface, 12, 2015, 20150391.
89. Yorio, T., Bentley, P.J., Distribution of the extracellular space of the amphibian lens. Exp. Eye Res. 23 (1976), 601–608.
90. 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. 93 (1982), 175–189.
91. 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. 108 (1989), 2255–2275.
92. Zhao, H., Brown, P.H., Magone, M.T., Schuck, P., The molecular refractive function of lens gamma-crystallins. J. Mol. Biol. 411 (2011), 680–699.
93. Zhao, H., Brown, P.H., Schuck, P., On the distribution of protein refractive index increments. Biophys. J. 100 (2011), 2309–2317.