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<span>Protein Structure and Function</span>
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<p>The interests of this section are in the area of protein structure as it relates to function, with a focus on the interactions of components involved in cell differentiation survival and maintenance. Our research at NEI has applied these interests to systems in the retina.</p>
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<p>Our section has been studying pigment epithelium-derived factor (PEDF), a protein that acts in neuronal differentiation and survival in cells derived from the retina and CNS. PEDF inhibits angiogenesis and its expression is down- regulated over the replicative lifespan of mammals. This interesting factor is secreted by retinal pigment epithelial cells into the interphotoreceptor matrix, where it acts on photoreceptor cells. Its importance in the development, maintenance, and function of the retina and CNS is evident in animal models for inherited and light-induced retinal degeneration, as well as for degeneration of spinal cord motor neurons.</p><p>Much of our progress in understanding PEDF has relied on our development of overexpression systems that yielded recombinant proteins as functionally active neurotrophic factors identical to the native protein and ideal for biochemical, biophysical, and biological studies. The cDNA sequence for PEDF predicts a unique protein with strong homology to members of the serine protease inhibitor (serpin) superfamily. For this reason, we first studied PEDF as a serpin. We established that PEDF belongs with the subgroup of noninhibitory serpins and that it has characteristics of a substrate rather than an inhibitor of serine proteases. Moreover, a region from its amino-terminus confers the neurotrophic activity to the PEDF polypeptide, not requiring the serpin reactive loop (the structural determinant for serpin inhibition). We concluded that PEDF’s neurotrophic activity must be mediated by a mechanism independent of serine protease inhibition, and we proposed that during evolution this serpin might have lost its inhibitory activity and gained neurotrophic function. These findings provided an example of the separation of inhibitory and other activities in a serpin.</p><p>Our investigations were next directed toward the hypothesis that PEDF’s neurotrophic activity is mediated by interactions with cell surfaces. Focusing on retinoblastoma and cerebellar granule cells, we prospected for PEDF receptors and found evidence for 1) a saturable, specific, and high-affinity class of receptors on the surface of both cells, with characteristics of an 80-kDa plasma membrane protein, and 2) the amino-terminal region in PEDF that interacts with the receptor. Furthermore, using a yeast two-hybrid screening, we identified a novel gene from pigment epithelium of the human retina that codes for a PEDF-binding partner, which we term PEDF-R. We studied PEDF-R as a receptor for PEDF and found that the PEDF-R polypeptide has specific and high binding affinity for PEDF, has a potent phospholipase A(2) activity that liberates fatty acids, and is associated with eukaryotic cell membranes. Most importantly, PEDF binding stimulates the enzymatic phospholipase A(2) activity of PEDF-R. Our work, the first step in the biological activity of PEDF is the binding to receptors on the surface of target cells, i.e., PEDF-R, a phospholipase-linked membrane protein with high affinity for PEDF, suggests a molecular pathway by which ligand/receptor interaction on the cell surface could generate a cellular signal, a significant advance in the elucidation of PEDF’s mechanism of action.</p><p>We also investigated the association of PEDF with extracellular matrixes (ECM) and found that PEDF can interact with glycosaminoglycans and collagens. In the folded PEDF protein, the binding sites for these two ECM components are distinct and separated from each other, from the binding site for the receptor and from the serpin exposed loop. Our functional studies showed that glycosaminoglycans can act as positive modulators of the PEDF-receptor interactions. These findings are significant because the association of PEDF with ECMs may be used in vivo to regulate this protein, i.e., by spatial and temporal localization and/or controlling its activities.</p><p>We also studied the effects of matrix metalloproteinases (MMP) type-2 and type-9 on PEDF and demonstrated that they can fully degrade PEDF in a calcium dependent-fashion, abolishing its neurotrophic and antiangiogenic activities. Moreover, we found that hypoxia and VEGF can decrease PEDF protein levels by stimulating the MMP-mediated proteolytic degradation of PEDF. Interestingly, the expression and secretion of MMP-2/-9 and of VEGF correlate positively with the progression of neovascular ocular diseases, while the levels of PEDF correlate inversely. Most importantly, these results reveal a novel post-translational mechanism for downregulating PEDF by MMP-mediated proteolytic degradation that explains hypoxia-provoked increases in the VEGF/PEDF ratio, angiogenesis and/or neuronal death.</p><p>In preparation for protein therapeutics, we explored direct delivery of the PEDF protein to the choroid and retina. We demonstrated the permeability properties of the sclera and choroid/RPE to PEDF. Upon subconjunctival delivery, this relatively large protein traversed the sclera-choroid-RPE layers to reach the retina. Our conclusions suggest that subconjunctival routes of PEDF protein delivery offer novel, feasible and minimally invasive means for administration in the clinic.</p><p>We hope our PEDF research lays the groundwork for the development of therapies for diseases involving defective neuronal differentiation or cell survival, such as retinitis pigmentosa, age-related macular degeneration, and amyotrophic lateral sclerosis. The reported antiangiogenic effects of PEDF suggest it may also be useful in treating diseases in which new blood vessel formation plays a role, such as diabetic retinopathy, age-related macular degeneration, tumor growth, and rheumatoid arthritis.</p><p>The role of a cell-surface receptor in the mechanisms of action of PEDF represents a key aspect of regulation. Along these lines, our studies focus on structure-function relationships and enzymatic characterization of PEDF receptors, and their distribution in the normal and diseased retina. Consistent with our goal of elucidating the mechanisms of action of PEDF, we are interested in signal transduction and the expression of genes affected by PEDF’s stimuli. Given that protein therapeutics pose great challenges in development, production, delivery, safety, and stability, future work will be directed toward the molecular design of potent PEDF peptides for ocular treatment to achieve altered binding specificity and prevention of side effects, and the development of sustained delivery systems for PEDF in animal models of retinal and CNS diseases.</p>
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<h2>Selected publications</h2>
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<p>Samtani S, Amaral J, Campos MM, Fariss R, Becerra SP.: Doxycycline-mediated Inhibition of Choroidal Neovascularization. <em>Invest Ophthalmol Vis Sci.</em> 2009 Jun 10, 2009. <a href="http://www.ncbi.nlm.nih.gov/pubmed/19516001">PubMed</a></p><p>Becerra SP, Perez-Mediavilla LA, Weldon JE, Locatelli-Hoops S, Senanayake P, Notari L, Notario V, Hollyfield JG.: Pigment epithelium-derived factor binds to hyaluronan. Mapping of a hyaluronan binding site.<em> J Biol Chem.</em> 283(48):33310-20, 2008. Epub 2008 Sep 19. <a href="http://www.ncbi.nlm.nih.gov/pubmed/18805795">PubMed</a></p><p>Perruccio EM, Rowlette LL, Comes N, Locatelli-Hoops S, Notari L, Becerra SP, Borrs T.: Dexamethasone increases pigment epithelium-derived factor in perfused human eyes. <em>Curr Eye Res.</em> 33(5):507-15, 2008. <a href="http://www.ncbi.nlm.nih.gov/pubmed/18568889">PubMed</a></p><p>Lilja AE, Chang WL, Barry PA, Becerra SP, Shenk TE.: Functional genetic analysis of rhesus cytomegalovirus: Rh01 is an epithelial cell tropism factor. <em>J Virol.</em> 82(5):2170-81, 2008. Epub 2007 Dec 19. <a href="http://www.ncbi.nlm.nih.gov/pubmed/18094178">PubMed</a></p><p>Notari, L, Baladron, V., Aroca-Aguilar, J.D., Balko, N., Heredia, R., Meyer, C., Notario, P.M., Saravanamuthu, S., Nueda, M.L., Sanchez-Sanchez, F., Escribano, J., Laborda, J., Becerra, S.P.: Identification of a lipase-linked cell membrane receptor for pigment epithelium-derived factor. <em>J. Biol. Chem.</em> 281,38022-38037, 2006. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=17032652&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Amaral, J., Campos, M.M., Becerra, S.P., Fariss, R.N.: A novel imaging technique for experimental choroidal neovascularization. <em>Invest. Ophthalmol. Vis. Sci.</em> 47, 5163-5170, 2006. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=17122098&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Becerra, S.P.: Focus on Molecules: Pigment epithelium-derived factor (PEDF). <em>Exp. Eye Res. </em>82:739-40, 2006. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=16364294&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Amaral, J., Fariss, R.N, Campos,M.M., Robison, Jr,W.G., Kim,H., Lutz, R., Becerra, S.P.: Transscleral-RPE permeability of PEDF and ovalbumin proteins: implications for subconjunctival protein delivery. <em>Invest. Ophthalmol. Vis. Sci. </em>46, 4383-92, 2005. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=16303924&query_hl=72&itool=pubmed_docsum">PubMed</a></p><p>Notari, L., Miller, A., Martnez, A., Amaral, J., Ju, M., Robinson, G., Smith, L.E.H., Becerra, S.P.: Pigment epithelium-derived factor is a substrate for matrix metalloproteinase type 2 and type 9: implications for downregulation in hypoxia. <em>Invest. Ophthalmol. Vis. Sci.</em> 46, 2736-2747, 2005. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=16043845&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Becerra, S.P., Fariss, R.N., Wu, Y.-Q., Montuenga, L., Wong, P., Pfeffer, B.A.: Pigment epithelium-derived factor in the monkey retinal pigment epithelium and interphotoreceptor matrix: apical secretion and distribution. Exp Eye Res. 78, 223-234, 2004. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=14729355&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Alberdi, E.M., Weldon, J.E., Becerra, S.P.: Glycosaminoglycans in human retinoblastoma cells: Heparan sulfate, a modulator of the pigment epithelium-derived factor-receptor interactions. <em>BMC Biochemistry</em> 4:1, 2003 (19 February 2003) <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=12625842&query_hl=1&itool=pubmed_docsum">PubMed</a></p><p>Becerra, S.P., Amaral, J.: Erythropoietin–an endogenous retinal survival factor. <em>N. Engl. J. Med.</em> 347, 1968-1970, 2002. Review. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12477950&dopt=Abstract">PubMed</a></p><p>Meyer, C., Notari, L., and Becerra, S.P.: Mapping the type I collagen-binding site on pigment epithelium-derived factor. Implications for its antiangiogenic activity. <em>J. Biol Chem.</em> 277, 45400-45407, 2002. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12237317&dopt=Abstract">PubMed</a></p><p>Bilak, S.R., Bilak, M.M., Corse, A.M., Royal, W., Becerra, S.P., Kuncl, R.W.: Pigment Epithelium-Derived Factor is Elevated in CSF of Patients with ALS. <em>J. Neurochem.</em> 81, 178-184, 2002 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12067231&dopt=Abstract">PubMed</a></p><p>Gao, G., Li, Y., Fant, J., Crosson, C.E., Becerra, S.P., and Ma J.X.: Difference in ischemic regulation of vascular endothelial growth factor and pigment epithelium–derived factor in brown norway and sprague dawley rats contributing to different susceptibilities to retinal neovascularization. <em>Diabetes</em> 51, 1218-25, 2002 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11916948&dopt=Abstract">PubMed</a></p><p>Kuncl, R.W., Bilak, M.M., Bilak, S.R., Corse, A.M., Royal, W., Becerra, S.P.: Pigment epithelium-derived factor is elevated in CSF of patients with amyotrophic lateral sclerosis. <em>J. Neurochem.</em> 81, 178-184, 2002 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=12067231&dopt=Abstract">PubMed</a></p><p>Aymerich, M.S., Alberdi, E., Martinez, A., and Becerra, S.P.: Evidence for pigment epithelium-derived factor (PEDF) receptors in the neural retina. <em>Invest. Ophthalmol. Vis. Sci.</em> 42, 3287-3293, 2001 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11726635&dopt=Abstract">PubMed</a></p><p>Nomura, T., Yabe, T. Mochizuki, H., Reiser, J., Becerra, S.P. and Schwartz, J.P.: Survival effects of pigment epithelium-derived factor (PEDF) expressed by a lentiviral vector in rat cerebellar granule cells. <em>Dev. Neurosci.</em> 23, 145-52, 2001 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=11509837&dopt=Abstract">PubMed</a></p><p>Cayouette, M., Smith, S.B., Becerra, S.P., and Gravel, C.: Pigment epithelium-derived factor delays the death of photoreceptors in mouse models of inherited retinal degenerations <em>Neurobiol. Disease</em> 6, 523-532, 1999 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=10600408&dopt=Abstract">PubMed</a></p><p>Alberdi, E., Aymerich, M.S., and Becerra, S.P.: Binding of pigment epithelium-derived factor (PEDF) to retinoblastoma and cerebellar granule cells: Evidence for a PEDF receptor <em>J. Biol. Chem.</em> 274, 31605-31612, 1999 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=10531367&dopt=Abstract">PubMed</a></p><p>Houenou, L.J., D=Costa, A.P., Li, L., Turgeon, V.L., Enyadike, C., Alberdi, E., and Becerra, S.P.: Pigment epithelium-derived factor (PEDF) promotes the survival and differentiation of developing spinal motor neurons <em>J. Comparative Neurology</em> 412, 506-514, 1999. <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=10441236&dopt=Abstract">PubMed</a></p><p>Alberdi, E., Hyde, C.C., and Becerra, S.P.: Pigment epithelium-derived factor binds to glycosaminoglycans: Analysis of binding site. <em>Biochemistry</em> 37, 10643-10652, 1998 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9692954&dopt=Abstract">PubMed</a></p><p>Perez-Mediavilla, L.A., Chew, C., Campochiaro, P.A., Nickells, R.W., Notario, V., Zack, D.J. and Becerra, S.P. Sequence and expression analysis of bovine pigment epithelium-derived factor (PEDF). <em>Biochim. Biophys. Acta</em> 1398, 203-214, 1998 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9689919&dopt=Abstract">PubMed</a></p><p>Araki, T., Taniwaki, T., Becerra, S.P., Chader, G.J., and Schwartz, J.P.: Pigment epithelium-derived factor (PEDF) differentially protects immature but not mature cerebellar granule cells against apoptotic cell death. <em>J. Neurosci. Res.</em> 53, 7-15, 1998 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9670988&dopt=Abstract">PubMed</a></p><p>Sugita, Y., Becerra, S.P., Chader, G.J., and Schwartz, J.P.: Pigment epithelium-derived factor (PEDF) has direct effects on microglia and indirect effects on astrocytes in culture. <em>J. Neurosci. Res.</em> 49, 710-718, 1997 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9335258&dopt=Abstract">PubMed</a></p><p>Taniwaki, T., Hirashima, N., Becerra, S.P., Chader, G.J., Etcheberrigaray, R., and Schwartz, J.P.: Pigment epithelium-derived factor protects cultured cerebellar granule cells against glutamate-induce neurotoxicity. <em>J. Neurochem.</em> 68, 26-32, 1997 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=8978706&dopt=Abstract">PubMed</a></p><p>Becerra, S.P.: Structure-function relationships of PEDF: A noninhibitory serpin with neurotrophic activity. <em>Adv. Exp. Med. Biol.</em> 425, 223-237, 1997 <a href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9433504&dopt=Abstract">PubMed</a></p>
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<h2>Protein Structure and Function key staff</h2>
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<td headers="view-title-table-column" class="views-field views-field-title"><a href="/research/research-labs-and-branches/we-are-nei-intramural/s-becerra" hreflang="en">S. Patricia Becerra, Ph.D.</a> </td>
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<td headers="view-field-lab-staff-title-table-column" class="views-field views-field-field-lab-staff-title">Senior Investigator </td>
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<td headers="view-field-email-table-column" class="views-field views-field-field-email"><a href="mailto:becerras@nei.nih.gov">becerras@nei.nih.gov</a> </td>
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<td headers="view-field-phone-table-column" class="views-field views-field-field-phone">301-496-6514 </td>
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<div class="js-view-dom-id-978806f28df24f223ff3921660740063246d56b812729c598d167684811acafc lab-alumni">
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<img loading="lazy" src="/sites/default/files/styles/thumbnail/public/2022-07/Serpin1-lipid_thumb.png?itok=zqylcO8D" width="200" height="200" alt="" />
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<a class="c-teaser__link" href="/about/news-and-events/news/nih-study-finds-loss-youth-protein-may-drive-aging-eye">
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NIH study finds loss of ‘youth’ protein may drive aging in the eye
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<p class="c-teaser__date">
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<time datetime="2022-07-18T13:43:28-04:00">July 18, 2022</time>
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<div class="c-teaser__summary">
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Loss of the protein pigment epithelium-derived factor (PEDF), which protects retinal support cells, may drive age-related changes in the retina, according to a new study in mice from the National Eye Institute.
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<img loading="lazy" src="/sites/default/files/styles/thumbnail/public/2021-11/hiPSC-RPE_creditFlores-Bellver.jpg?itok=XGQ66VKJ" width="200" height="200" alt="Retinal pigment epithelial cells stained green and magenta" />
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<a class="c-teaser__link" href="/about/news-and-events/news/cu-researchers-provide-first-evidence-linking-extracellular-vesicles-drusen-formation-and-age">
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CU Researchers Provide First Evidence Linking Extracellular Vesicles with Drusen Formation and Age-Related Macular Degeneration
|
||
</a>
|
||
</h3>
|
||
<p class="c-teaser__date">
|
||
<time datetime="2021-11-12T18:08:50-05:00">November 12, 2021</time>
|
||
</p>
|
||
<div class="c-teaser__summary">
|
||
CellSight researchers at the University of Colorado School of Medicine are offering the first evidence connecting drusen formation, or yellowish deposits that accumulate under the retina, with extracellular vesicles and age-related macular degeneration.
|
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<img loading="lazy" src="/sites/default/files/styles/thumbnail/public/2021-06/AmacrineandPhotoreceptor_large.jpg?itok=4Z7_riu1" width="200" height="200" alt="Cells with red nuclei and long green processes" />
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<a class="c-teaser__link" href="/about/news-and-events/news/scientists-unravel-function-sight-saving-growth-factor">
|
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Scientists unravel the function of a sight-saving growth factor
|
||
</a>
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</h3>
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<p class="c-teaser__date">
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<time datetime="2021-06-16T15:08:53-04:00">June 16, 2021</time>
|
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</p>
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<div class="c-teaser__summary">
|
||
Researchers at the National Eye Institute (NEI) have determined how certain short protein fragments, called peptides, can protect neuronal cells found in the light-sensing retina layer at the back of the eye.
|
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</div>
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