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Originally published In Press as doi:10.1074/jbc.M206355200 on September 3, 2002

J. Biol. Chem., Vol. 277, Issue 45, 43319-43326, November 8, 2002
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In Vivo Regulation of Phosphoinositide 3-Kinase in Retina through Light-induced Tyrosine Phosphorylation of the Insulin Receptor beta -Subunit*

Raju V. S. RajalaDagger §, Mark E. McClellanDagger §, John D. AshDagger §||, and Robert E. AndersonDagger §||**

From the Departments of || Cell Biology, Dagger  Ophthalmology, and ** Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma 73104 and the § Dean A. McGee Eye Institute, Oklahoma City, Oklahoma 73104

Recently, we have shown that phosphoinositide 3-kinase (PI3K) in bovine rod outer segment (ROS) is activated in vitro by tyrosine phosphorylation of the C-terminal tail of the insulin receptor (Rajala, R. V. S., and Anderson, R. E. (2001) Invest. Ophthal. Vis. Sci. 42, 3110-3117). In this study, we have investigated the in vivo mechanism of PI3K activation in the rodent retina and report the novel finding that light stimulates tyrosine phosphorylation of the beta -subunit of the insulin receptor (IRbeta ) in ROS membranes, which leads to the association of PI3K enzyme activity with IRbeta . Retinas from light- or dark-adapted mice and rats were homogenized and immunoprecipitated with antibodies against phosphotyrosine, IRbeta , or the p85 regulatory subunit of PI3K, and PI3K activity was measured using PI-4,5-P2 as substrate. We observed a light-dependent increase in tyrosine phosphorylation of IRbeta and an increase in PI3K enzyme activity in isolated ROS and in anti-phosphotyrosine and anti-IRbeta immunoprecipitates of retinal homogenates. The light effect was localized to photoreceptor neurons and is independent of insulin secretion. Our results suggest that light induces tyrosine phosphorylation of IRbeta in outer segment membranes, which leads to the binding of p85 through its N-terminal Src homology 2 domain and the generation of PI-3,4,5-P3. We suggest that the physiological role of this process may be to provide neuroprotection of the retina against light damage by activating proteins that protect against stress-induced apoptosis.

* This work was supported by NEI, National Institutes of Health, Grants EY00871, EY04149, and EY12190; Research to Prevent Blindness Inc. (New York, NY); The Foundation Fighting Blindness (Baltimore, MD); the Samuel Roberts Nobel Foundation, Inc. (Ardmore, OK); Presbyterian Health Foundation (Oklahoma City, OK); the Oklahoma Center for Advancement of Science and Technology (Oklahoma City, OK); and the Knights Templar Eye Foundation (Chicago, IL).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: 608 Stanton L. Young Blvd., Rm. 409, Oklahoma City, OK 73104. Tel.: 405-271-8255; Fax: 405-271-8128; E-mail: raju-rajala@ouhsc.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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