Comparative proteomic analyses of macular and peripheral retina of cynomolgus monkeys (Macaca fascicularis)

Experimental Animals

Volumn 59, Issue 2, 2010, Pages 171-182

  Okamoto, Haru ^a,b   Umeda, Shinsuke ^b   Nozawa, Takehiro ^c   Suzuki, Michihiro T ^d   Yoshikawa, Yasuhiro ^e   Matsuura, Etsuko T ^b   Iwata, Takeshi ^a  

^a NATIONAL HOSPITAL ORGANIZATION TOKYO MEDICAL CENTER   (Japan)

^b OCHANOMIZU UNIVERSITY   (Japan)

^c AMR Incorporated   (Japan)

^d The Corporation for Production and Research of Laboratory Primates   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

2D gel electrophoresis; Macula; Mass spectrometry; Retina

Indexed keywords

ALPHA ENOLASE; ALPHA TROPOMYOSIN; ALPHA TUBULIN; BETA 2 TUBULIN; BETA 2C TUBULIN; BETA TUBULIN; CALRETICULIN; CONE PHOTORECEPTOR SPECIFIC ARRESTIN C; EPIDERMAL FATTY ACID BINDING PROTEIN; GAMMA SYNUCLEIN; GLUTAMATE AMMONIA LIGASE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 ALPHA; HEAT SHOCK PROTEIN 90 BETA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN B1; INITIATION FACTOR 4A; INITIATION FACTOR 4A I; INITIATION FACTOR 4A II; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE BETA; LAMIN B; LAMIN B2; MEMBRANE PROTEIN; NEUROFILAMENT L PROTEIN; NEUROFILAMENT PROTEIN; NEURON SPECIFIC ENOLASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHOROID; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MACACA; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; RETINA; RETINA MACULA DEGENERATION; RETINA MACULA LUTEA; TISSUE DISTRIBUTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; UNINDEXED SEQUENCE;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; MACACA FASCICULARIS; MACULA LUTEA; PEPTIDE MAPPING; PROTEOMICS; RETINAL DISEASES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

MACACA FASCICULARIS; PRIMATES;

EID: 77954594750     PISSN: 13411357     EISSN: None     Source Type: Journal    
DOI: 10.1538/expanim.59.171     Document Type: Article

References (52)

1. Alge, C.S., Suppmann, S., Priglinger, S.G., Neubauer, A.S., May, C.A., Hauck, S., Welge-Lussen, U., Uefflng, M., and Kampik, A. 2003. Comparative proteome analysis of native differentiated and cultured dedifferentiated human RPE cells. Invest. Ophthalmol. Vis. Sci. 44: 3629-3641.
2. Bennaars-Eiden, A., Higgins, L., Hertzel, A.V., Kapphahn, R.J., Ferrington, D.A., and Bernlohr, D.A. 2002. Covalent modification of epithelial fatty acid-binding protein by 4-hydroxynonenal in vitro and in vivo. Evidence for a role in antioxidant biology. J. Biol. Chem. 277: 50693-50702.
3. Bowes Rickman, C, Ebright, J.N., Zavodni, Z.J., Yu, L., Wang, T., Daiger, S.P., Wistow, G., Boon, K., and Hauser, M.A. 2006. Defining the human macula transcriptome and candidate retinal disease genes using EyeSAGE. Invest. Ophthalmol. Vis. Sci. 47: 2305-2316.
4. Butt, R.H., Pfeifer, T.A., Delaney, A., Grigliatti, T.A., Tetzlaff, W.G., and Coorssen, J.R. 2007. Enabling coupled quantitative genomics and proteomics analyses from rat spinal cord samples. Mol. Cell. Proteomics 6: 1574-1588.
5. Cavusoglu, N., Thierse, D., Mohand-Said, S., Chalmel, F., Poch, O., Van-Dorsselaer, A., Sahel, J.A., and Leveillard, T. 2003. Differential proteomic analysis of the mouse retina: the induction of crystallin proteins by retinal degeneration in the rdl mouse. Mol. Cell. Proteomics 2: 494-505.
6. Curcio, C.A., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, I.B., and Milam, A.H. 1991. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312: 610-624.
7. Distler, C. and Dreher, Z. 1996. Glia cells of the monkey retina-II. Müller cells. Vision Res. 36: 2381-2394.
8. Dreyfuss, G., Kim, V.N., and Kataoka, N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 3: 195-205.
9. El-Mofty, A., Gouras, P., Eisner, G., and Balazs, E.A. 1978. Macular degeneration in rhesus monkey (Macaca mulatta). Exp. Eye Res. 27: 499-502.
10. Ethen, CM., Reilly, C, Feng, X., Olsen, T.W., and Ferrington, D.A. 2006. The proteome of central and peripheral retina with progression of age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 47: 2280-2290.
11. Feller, S.M. 2001. Crk family adaptors-signalling complex formation and biological roles. Oncogene 20: 6348-6371.
12. Had, L., Faivre-Sarrailh, C, Legrand, C, Mery, J., Brugidou, J., and Rabie, A. 1994. Tropomyosin isoforms in rat neurons: the different developmental profiles and distributions of TM-4 and TMBr-3 are consistent with different functions. J. Cell Sci. 107: 2961-2973.
13. Haddad, S., Chen, C.A., Santangelo, S.L., and Seddon, J.M. 2006. The genetics of age-related macular degeneration: a review of progress to date. Surv. Ophthalmol. 51: 316-363.
14. Harwerth, R.S. and Smith, E.L. 3rd. 1985. Rhesus monkey as a model for normal vision of humans. Am. J. Optom. Physiol. Opt. 62: 633-641.
15. Hauck, S.M., Schoeffmann, S., Deeg, C.A., Gloeckner, C.J., Swiatek-de Lange, M., and Uefflng, M. 2005. Proteomic analysis of the porcine interphotoreceptor matrix. Proteomics 5: 3623-3636.
16. Hope, G.M., Dawson, W.W., Engel, H.M., Ulshafer, R.J., Kessler, M.J., and Sherwood, M.B. 1992. A primate model for age related macular drusen. Br. J. Ophthalmol. 76: 11-16.
17. Houle, F., Rousseau, S., Morrice, N., Luc, M., Mongrain, S., Turner, C.E., Tanaka, S., Moreau, P., and Huot, J. 2003. Extracellular signal-regulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. Mol. Biol. Cell 14: 1418-1432.
18. Ishibashi, K., Tian, J., and Handa, J.T. 2004. Similarity of mRNA phenotypes of morphologically normal macular and peripheral retinal pigment epithelial cells in older human eyes. Invest. Ophthalmol. Vis. Sci. 45: 3291-3301.
19. Ishibashi, T., Sorgente, N., Patterson, R., and Ryan, S.J. 1986. Pathogenesis of drusen in the primate. Invest. Ophthalmol. Vis. Sci. 27: 184-193.
20. Ji, H., Liu, Y.E., Jia, T., Wang, M., Liu, J., Xiao, G., Joseph, B.K., Rosen, C, and Shi, YE. 1997. Identification of a breast cancer-specific gene, BCSG1, by direct differential cDNA sequencing. Cancer Res. 57: 759-764.
21. Kingma, P.B., Bok, D., and Ong, D.E. 1998. Bovine epidermal fatty acid-binding protein: determination of ligand specificity and cellular localization in retina and testis. Biochemistry (Mosc) 37: 3250-3257.
22. Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E.N. Jr., Rux, J.J., Speicher, D.W., and Pierce, E.A. 2007. The proteome of the mouse photoreceptor sensory cilium complex. Mol. Cell. Proteomics 6: 1299-1317.
23. MacDonald, N.J., Shivers, W.Y, Narum, D.L., Plum, S.M., Wingard, J.N., Fuhrmann, S.R., Liang, H., Holland-Linn, J., Chen, D.H., and Sim, B.K. 2001. Endostatin binds tropomyosin. A potential modulator of the antitumor activity of endostatin. J. Biol. Chem. 276: 25190-25196.
24. Matsubara, T.A., Murata, T.A., Wu, G.S., Barren, E.A., and Rao, N.A. 2000. Isolation and culture of rat retinal microvessel endothelial cells using magnetic beads coated with antibodies to PECAM-1. Curr. Eye Res. 20: 1-7.
25. Monaco, W.A. and Wormington, CM. 1990. The rhesus monkey as an animal model for age-related maculopathy. Optom. Vis. Sci. 67: 532-537.
26. Nicolas, M.G., Fujiki, K., Murayama, K., Suzuki, M.T., Mineki, R., Hayakawa, M., Yoshikawa, Y., Cho, F., and Kanai, A. 1996. Studies on the mechanism of early onset macular degeneration in cynomolgus (Macaca fascicularis) monkeys. I. Abnormal concentrations of two proteins in the retina. Exp. Eye Res. 62: 211-219.
27. Nicolas, M.G., Fujiki, K., Murayama, K., Suzuki, M.T., Shindo, N., Hotta, Y., Iwata, R, Fujimura, T., Yoshikawa, Y., Cho, F., and Kanai, A. 1996. Studies on the mechanism of early onset macular degeneration in cynomolgus monkeys. n. Suppression of metallothionein synthesis in the retina in oxidative stress. Exp. Eye Res. 62: 399-108.
28. Nishizawa, Y., Komori, N., Usukura, J., Jackson, K.W., Tobin, S.L., and Matsumoto, H. 1999. Initiating ocular proteomics for cataloging bovine retinal proteins: microanalytical techniques permit the identification of proteins derived from a novel photoreceptor preparation. Exp. Eye Res. 69: 195-212.
29. Ordya, J.M., Brizeea, K.R., and Hanscheb, J. 1980 Visual acuity and foveal cone density in the retina of the aged rhesus monkey. Neurobiol. Aging 1: 133-140.
30. Oyster, C.W. 1999. The Human Eye: Structure and Function, Sinauer Associates Inc., Massachusetts.
31. Provis, J.M., Penfold, P.L., Cornish, E.E., Sandercoe, T.M., and Madigan, M.C. 2005. Anatomy and development of the macula: specialisation and the vulnerability to macular degeneration. Clin. Exp. Optom. 88: 269-281.
32. Radeke, M.J., Peterson, K.E., Johnson, L.V., and Anderson, D.H. 2007. Disease susceptibility of the human macula: differential gene transcription in the retinal pigmented epithelium/choroid. Exp. Eye Res. 85: 366-380.
33. Sakuma, H., Inana, G., Murakami, A., Higashide, T., and McLaren, M.J. 1996. Immunolocalization of X-arrestin in human cone photoreceptors. FEBS Lett. 382: 105-110.
34. Schevzov, G., Vrhovski, B., Bryce, N.S., Elmir, S., Qiu, M.R., O'Neill, G.M., Yang, N., Verrills, N.M., Kavallaris, M., and Gunning, P.W. 2005. Tissue-specific tropomyosin isoform composition. J. Histochem. Cytochem. 53: 557-570.
35. Sharon, D., Blackshaw, S., Cepko, C.L., and Dryja, T.P. 2002. Profile of the genes expressed in the human peripheral retina, macula, and retinal pigment epithelium determined through serial analysis of gene expression (SAGE). Proc. Natl.Acad. Sci. USA. 99: 315-320.
36. Snodderly, D.M., Auran, J.D., and Delori, F.C. 1984. The macular pigment, II. Spatial distribution in primate retinas. Invest. Ophthalmol. Vis. Sci. 25: 674-685.
37. Snodderly, D.M., Brown, P.K., Delori, F.C., and Auran, J.D. 1984. The macular pigment. I. Absorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Invest. Ophthalmol. Vis. Sci. 25: 660-673.
38. Snodderly, D.M., Weinhaus, R.S., and Choi, J.C. 1992. Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis). J. Neurosci. 12: 1169-1193.
39. Stafford, T.J. 1974. Maculopathy in an elderly sub-human primate. Mod. Probl. Ophthalmol. 12: 214-219.
40. Stafford, T.J., Anness, S.H., and Fine, B.S. 1984.Spontaneous degenerative maculopathy in the monkey. Ophthalmology 91: 513-521.
41. Stamm, S., Casper, D., Lees-Miller, J.P., and Helfman, D.M. 1993. Brain-specific tropomyosins TMBr-1 and TMBr-3 have distinct patterns of expression during development and in adult brain. Proc. Natl. Acad. Sci. U.S.A. 90: 9857-9861.
42. Sueoka, E., Goto, Y, Sueoka, N., Kai, Y, Kozu, T., and Fujiki, H. 1999. Heterogeneous nuclear ribonucleoprotein B1 as a new marker of early detection for human lung cancers. Cancer Res. 59: 1404-1407.
43. Surguchov, A., McMahan, B., Masliah, E., and Surgucheva, I. 2001. Synucleins in ocular tissues. J. Neurosci. Res. 65: 68-77.
44. Suzuki, M.T., Terao, K., and Yoshikawa, Y 2003. Familial early onset macular degeneration in cynomolgus monkeys (Macaca fascicularis). Primates 44: 291-294.
45. Umeda, S., Ayyagari, R., Allikmets, R., Suzuki, M.T., Karoukis, A.J., Ambasudhan, R., Zernant, J., Okamoto, H., Ono, R, Terao, K., Mizota, A., Yoshikawa, Y, Tanaka, Y, and Iwata, T. 2005. Early-onset macular degeneration with drusen in a cynomolgus monkey (Macaca fascicularis) pedigree: exclusion of 13 candidate genes and loci. Invest. Ophthalmol. Vis. Sci. 46: 683-691.
46. Umeda, S., Ayyagari, R., Suzuki, M.T., Ono, R, Iwata, R, Fujiki, K., Kanai, A., Takada, Y, Yoshikawa, Y, Tanaka, Y, and Iwata, T. 2003. Molecular cloning of ELOVL4 gene from cynomolgus monkey (Macaca fascicularis). Exp. Anim. 52: 129-135.
47. Umeda, S., Suzuki, M.T., Okamoto, H., Ono, R, Mizota, A., Terao, K., Yoshikawa, Y, Tanaka, Y, and Iwata, T. 2005. Molecular composition of drusen and possible involvement of anti-retinal autoimmunity in two different forms of macular degeneration in cynomolgus monkey (Macaca fascicularis). FASEBJ. 19: 1683-1685.
48. van Soest, S.S., de Wit, G.M., Essing, A.H., ten Brink, J.B., Kamphuis, W., de Jong, P.T., and Bergen, A.A. 2007. Comparison of human retinal pigment epithelium gene expression in macula and periphery highlights potential topographic differences in Bruch's membrane. Mol. Vis. 13: 1608-1617.
49. Wang, YD., Wu, J.D., Jiang, Z.L., Wang, Y.B., Wang, X.H., Liu, C, and Tong, M.Q. 2007. Comparative proteome analysis of neural retinas from type 2 diabetic rats by two-dimensional electrophoresis. Curr. Eye Res. 32: 891-901.
50. West, K.A., Yan, L., Shadrach, K., Sun, J., Hasan, A., Miyagi, M., Crabb, J.S., Hollyfleld, J.G., Marmorstein, A.D., and Crabb, J.W. 2003. Protein database, human retinal pigment epithelium. Mol. Cell. Proteomics 2: 37-49.
51. White, R., Gonsior, C, Kramer-Albers, E.M., Stohr, N., Huttelmaier, S., and Trotter, J. 2008. Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J. Cell Biol. 181: 579-586.
52. Zhang, J.C, Donate, R, Qi, X., Ziats, N.P., Juarez, J.C, Mazar, A.P., Pang, Y.P., and McCrae, K.R. 2002. The antiangiogenic activity of cleaved high molecular weight kininogen is mediated through binding to endothelial cell tropomyosin. Proc. Natl. Acad. Sci. U.S.A. 99: 12224-12229.