Ω-Crystallin of the Scallop Lens: A DIMERIC ALDEHYDE DEHYDROGENASE CLASS 1/2 ENZYME-CRYSTALLIN

Joram Piatigorsky,Zbynek Kozmik,Joseph Horwitz,Linlin Ding,Eleonora Carosa,W Gerald Robison,Peter J Steinbach,Ernst R Tamm

doi:10.1074/jbc.m005625200

Abstract

While many of the diverse crystallins of the transparent lens of vertebrates are related or identical to metabolic enzymes, much less is known about the lens crystallins of invertebrates. Here we investigate the complex eye of scallops. Electron microscopic inspection revealed that the anterior, single layered corneal epithelium overlying the cellular lens contains a regular array of microvilli that we propose might contribute to its optical properties. The sole crystallin of the scallop eye lens was found to be homologous to Omega-crystallin, a minor crystallin in cephalopods related to aldehyde dehydrogenase (ALDH) class 1/2. Scallop Omega-crystallin (officially designated ALDH1A9) is 55-56% identical to its cephalopod homologues, while it is 67 and 64% identical to human ALDH 2 and 1, respectively, and 61% identical to retinaldehyde dehydrogenase/eta-crystallin of elephant shrews. Like other enzyme-crystallins, scallop Omega-crystallin appears to be present in low amounts in non-ocular tissues. Within the scallop eye, immunofluorescence tests indicated that Omega-crystallin expression is confined to the lens and cornea. Although it has conserved the critical residues required for activity in other ALDHs and appears by homology modeling to have a structure very similar to human ALDH2, scallop Omega-crystallin was enzymatically inactive with diverse substrates and did not bind NAD or NADP. In contrast to mammalian ALDH1 and -2 and other cephalopod Omega-crystallins, which are tetrameric proteins, scallop Omega-crystallin is a dimeric protein. Thus, ALDH is the most diverse lens enzyme-crystallin identified so far, having been used as a lens crystallin in at least two classes of molluscs as well as elephant shrews.

Highlights

While many of the diverse crystallins of the transparent lens of vertebrates are related or identical to metabolic enzymes, much less is known about the lens crystallins of invertebrates
The sole crystallin of the scallop eye lens was found to be homologous to ⍀-crystallin, a minor crystallin in cephalopods related to aldehyde dehydrogenase (ALDH) class 1/2
It has conserved the critical residues required for activity in other ALDHs and appears by homology modeling to have a structure very similar to human ALDH2, scallop ⍀-crystallin was enzymatically inactive with diverse substrates and did not bind NAD or NADP

Summary

Introduction

While many of the diverse crystallins of the transparent lens of vertebrates are related or identical to metabolic enzymes, much less is known about the lens crystallins of invertebrates. The sole crystallin of the scallop eye lens was found to be homologous to ⍀-crystallin, a minor crystallin in cephalopods related to aldehyde dehydrogenase (ALDH) class 1/2. The crystallins comprise approximately 90% of the watersoluble proteins of the cellular lens of vertebrates and are critical for the optical properties of this transparent ocular tissue. The abundant ␣A- and ␣B-crystallins influence the optical properties of the vertebrate lens and act as molecular chaperones to protect against protein aggregation during aging [15] We have called this dual use of a single protein, gene sharing [7, 16]. Elephant shrews have another ALDH1 gene called ALDH1-nl (for non-lens), which is expressed in the liver [24]

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