Skip to main content

The protein concentration gradient within eye lens might originate from constant osmotic pressure coupled to differential interactive properties of crystallins

Abstract

A protein concentration gradient exists from the center to the periphery of most lenses, the origin of which is still a matter of debate. The gradient, which contributes to the lens optical quality, seems to be accompanied by an uneven distribution of the crystallin classes, with the nucleus usually enriched in γ-and the cortex in α-crystallins. Since the osmotic pressure within the lens seems to be constant and since a rather different interaction behaviour of α-and γ-crystallins was demonstrated in previous studies, we propose that the maintenance of a constant osmotic pressure through the lens is sufficient to induce and stabilize a protein concentration gradient. The theoretical treatment has been worked out and the validity of the hypothesis has been demonstrated with colloidal osmotic pressure measurements of lens cortical and nuclear cytoplasmic extracts as a function of protein concentration. To account for the observed lens concentration gradient, however, a small additional concentration gradient in the opposite direction, involving an ion or small molecule, might be required.

This is a preview of subscription content, access via your institution.

References

  • Amoore JE, Bartley W, van Heyningen R (1959) Distribution of sodium and potassium within cattle lens. Biochem J 72: 126–133

    CAS  Article  Google Scholar 

  • Benedek GG (1971) Theory of transparency of the eye. Appl Opt 10:459–473

    CAS  Article  Google Scholar 

  • Bindels JG (1982) Structural studies on soluble lens proteins related to aging. PhD Thesis. Nijmegen

  • Campbell MCW (1984) Measurement of refractive index in an intact crystalline lens. Vision Res 24:409–415

    CAS  Article  Google Scholar 

  • Clark JI, Delaye M, Hammer P, Menge L (1982) Preparation and characterization of native lens cell cytoplasm. Curr Eye Res 1:695–704

    CAS  Article  Google Scholar 

  • Cotlier E, Kwan B, Beaty C (1968) The lens as an osmometer and the effects of medium osmolarity on water transport, 86Rb efflux and 86Rb transport by the lens. Biochim Biophys Acta 150:705–722

    CAS  Article  Google Scholar 

  • Delaye M, Tardieu A (1983) Short range order of crystallin protein accounts for eye lens transparency. Nature (London) 302:415–417

    CAS  Article  Google Scholar 

  • Delaye M, Danford-Kaplan ME, Clark JI, Krop B, Gulik-Krzywicki T, Tardieu A (1987) Effect of calcium on the calf lens cytoplasm. Exp Eye Res 44:601–616

    CAS  Article  Google Scholar 

  • Duncan G, Jacob TJC (1984) The lens as a physical system. In: Davson H (ed) The eye. Academic Press, London New York, pp 159–206

    Chapter  Google Scholar 

  • Eisenberg H (1976) Biological macromolecules and polyelectrolytes in solution. Clarendon Press, Oxford

    Google Scholar 

  • Garner WH, Hilal SH, Lee SW, Spector A (1986) Sodium-23 magnetic resonance imaging of the eye and lens. Proc Natl Acad Sci USA 83:1901–1905

    CAS  Article  Google Scholar 

  • Goodenough DA, Dick JSB, Lyons JE (1980) Lens metabolic cooperation: a study of mouse lens transport and permeability visualised with freeze-substitution autoradiography and electron microscopy. J Cell Biol 86:576–589

    CAS  Article  Google Scholar 

  • Guinrer A, Fournet G (1955) Small angle scattering of X-rays. J Wiley, New York

    Google Scholar 

  • Huizinga A, Bot ACC, de Mul FFM, Vrensen GFJM, Greve J (1989) Local variation in absolute water content of human and rabbit eye lenses measured by raman spectroscopy. Exp Eye Res 48:487–496

    CAS  Article  Google Scholar 

  • Kinsey VE, Reddy DVN (1965) Studies of the crystalline lens. XI The relative role of the epithelium and capsule in transport. Invest Ophthal 4:104–121

    CAS  PubMed  Google Scholar 

  • Parsegian VA, Rand RP, Fuller NL, Rau DC (1986) Osmotic stress for the direct measurement of intermolecular forces. Methods Enzymol 127:400–416

    CAS  Article  Google Scholar 

  • Piatigorsky J (1981) Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 19:134–153

    CAS  Article  Google Scholar 

  • Pierscionek B, Smith G, Augusteyn RC (1987) The refractive increments of bovine α-, β-, and γ-crystallins. Vison Res 27:1539–1541

    CAS  Article  Google Scholar 

  • Prouty MS, Schechter AN, Parsegian VA (1985) Chemical potential measurements of deoxyhemoglobin S polymerization: Determination of the phase diagram of an assembling protein. J Mol Biol 184:517–528

    CAS  Article  Google Scholar 

  • Reiff TR (1986) A colloid osmotic model of macromolecular aggregation to explain tissue water loss in aging. Exp Gerontol 21:267–276

    CAS  Article  Google Scholar 

  • Siezen RJ, Fisch MR, Sligsby C, Benedek GB (1985) Opacification of γ-crystallin solutions from calf lens in relation to cold cataract formation. Proc Natl Acad Sci USA 82:1701–1705

    CAS  Article  Google Scholar 

  • Siezen RJ, Wu E, Kaplan ED, Thomson JA, Benedek GB (1988) Rat lens γ-crystallins: characterization of the six gene products and their spatial and temporal distribution resulting from differential synthesis. J Mol Biol 199:475–490

    CAS  Article  Google Scholar 

  • Slingsby C (1985) Structural variation in lens crystallins. TIBS 10:281–284

    CAS  Google Scholar 

  • Tardieu A, Delaye M (1988) Eye lens proteins and transparency: from light transmission theory to solution X-ray structural analysis. Annu Rev Biophys Biophys Chem 17:47–70

    CAS  Article  Google Scholar 

  • Thomson JA, Schurtenberger P, Thurston GM, Benedek GB (1987) Binary liquid phase separation and critical phenomena in a protein/water solution. Proc Natl Acad Sci USA 84:7079–7083

    CAS  Article  Google Scholar 

  • Trokel SL (1962) The physical basis for transparency of the crystalline lens. Invest Ophthalmol 1:493–501

    CAS  PubMed  Google Scholar 

  • Vérétout F, Delaye M, Tardieu A (1989) The molecular basis of eye lens transparency: osmotic pressure and X-ray analysis of α-crystallin solutions. J Mol Biol 205:713–728

    Article  Google Scholar 

  • Wistow G, Turnell B, Summers L, Slingsby C, Moss D, Miller L, Lindley P, Blundell T (1983) X-ray analysis of the eye lens protein γ II-crystallin at 1.9 Å resolution. J Mol Biol 170:175–202

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vérétout, 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, 61–68 (1989). https://doi.org/10.1007/BF00257103

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00257103

Key words

  • Eye lens
  • osmotic pressure
  • crystallins concentration gradient