Expression of synaptic and phototransduction markers during photoreceptor development in the marmoset monkey Callithrix jacchus

Journal of Comparative Neurology

Volumn 512, Issue 2, 2009, Pages 218-231

  Hendrickson, Anita ^a,b   Troilo, David ^c   Djajadi, Hidayat ^a   Possin, Daniel ^b   Springer, Alan ^d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Arrestin; Cones; Opsin; Recoverin; Retina; Rods; Synaptophysin; Transducin

Indexed keywords

BINDING PROTEIN; CARBOXY TERMINAL BINDING PROTEIN 2; MARKER; MEMBRANE PROTEIN; OPSIN; RECOVERIN; RETINA S ANTIGEN; SYNAPSE RECEPTOR; SYNAPTIC VESICLE PROTEIN 2; SYNAPTOPHYSIN; TRANSDUCIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VISUAL PIGMENT; BIOLOGICAL MARKER; EYE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPARATIVE ANATOMY; CONTROLLED STUDY; MARMOSET; MORPHOLOGY; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CONE; RETINA DEVELOPMENT; RETINA FOVEA; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; CYTOLOGY; HISTOLOGY; HUMAN; MACACA; METABOLISM; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; PHYSIOLOGY;

ANIMALS; BIOLOGICAL MARKERS; CALLITHRIX; EYE PROTEINS; HUMANS; LIGHT SIGNAL TRANSDUCTION; MACACA; OPSINS; PHOTORECEPTOR CELLS; RECOVERIN; SYNAPSES;

EID: 58249083546     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21893     Document Type: Article

References (52)

1. Bajjalieh SM. 1999. Synaptic vesicle docking and fusion. Curr Opin Neurobiol 9:321-328.
2. Buckley K, Kelly RB. 1985. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284-1294.
3. Bumsted K, Hendrickson A. 1999. Distribution and development of shortwavelength cones differ between Macaca monkey and human fovea. J Comp Neurol 403:502-516.
4. Bumsted K, Jasoni C, Szel A, Hendrickson A. 1997. Spatial and temporal expression of cone opsins during monkey retinal development. J Comp Neurol 378:117-134.
5. Bumsted O'Brien KM, Cheng H, Jiang Y, Schulte D, Swaroop A, Hendrickson AE. 2004. Expression of photoreceptor-specific nuclear receptor NR2E3 in rod photoreceptors of fetal human retina. Invest Ophthalmol Vis Sci 45:2807-2812.
6. Chalupa LM. 2007. A reassessment of the role of activity in the formation of eye-specific retinogeniculate projections. Brain Res Rev 55:228-236.
7. Cook PM, Prusky G, Ramoa AS. 1999. The role of spontaneous retinal activity before eye opening in the maturation of form and function in the retinogeniculate pathway of the ferret. Vis Neurosci 16:491-501.
8. Craft CM, Whitmore DH. 1995. The arrestin superfamily: cone arrestins are a fourth family. FEBS Lett 362:247-255.
9. Diaz CM, Macnab LT, Williams SM, Sullivan RK, Pow DV. 2007. EAAT1 and D-serine expression are early features of human retinal development. Exp Eye Res 84:876-885.
10. Dorn EM, Hendrickson L, Hendrickson AE. 1995. The appearance of rod opsin during monkey retinal development. Invest Ophthalmol Vis Sci 36:2634-2651.
11. Elias RV, Sezate SS, Cao W, McGinnis JF. 2004. Temporal kinetics of the light/dark translocation and compartmentation of arrestin and alphatransducin in mouse photoreceptor cells. Mol Vis 10:672-681.
12. Georges P, Madigan MC, Provis JM. 1999. Apoptosis during development of the human retina: relationship to foveal development and retinal synaptogenesis. J Comp Neurol 413:198-208.
13. Haverkamp S, Haeseleer F, Hendrickson A. 2003. A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Vis Neurosci 20:589-600.
14. Hendrickson A. 1992. A morphological comparison of foveal development in man and monkey. Eye 6:136-144.
15. Hendrickson A, Drucker D. 1992. The development of parafoveal and mid-peripheral human retina. Behav Brain Res 49:21-31.
16. Hendrickson A, Kupfer C. 1976. The histogenesis of the fovea in the macaque monkey. Invest Ophthalmol Vis Sci 15:746-756.
17. Hendrickson A, Provis J. 2006. Comparison of development of the primate fovea centralis. In: Sernagor E, Harris B, Wong R, editors. Retinal development. Leiden: Cambridge University Press; p 126-49.
18. Hendrickson AE, Yuodelis C. 1984. The morphological development of the human fovea. Ophthalmology 91:603-612.
19. Hendrickson A, Troilo D, Possin D, Springer A. 2006. Development of the neural retina and its vasculature in the marmoset Callithrix jacchus. J Comp Neurol 497:270-286.
20. Hicks D, Molday RS. 1986. Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Exp Eye Res 42:55-71.
21. Hollenberg MJ, Spira AW. 1973. Human retinal development: ultrastructure of the outer retina. Am J Anat 137:357-385.
22. Johnson PT, Williams RR, Cusato K, Reese BE. 1999. Rods and cones project to the inner plexiform layer during development. J Comp Neurol 414:1-12.
23. Jusuf PR, Martin PR, Grunert U. 2006. Synaptic connectivity in the midgetparvocellular pathway of primate central retina. J Comp Neurol 494:260-274.
24. Koontz MA, Hendrickson AE. 1993. Comparison of immunolocalization patterns for the synaptic vesicle proteins p65 and synapsin I in macaque monkey retina. Synapse 14:268-282.
25. LaVail MM, Rapaport DH, Rakic P. 1991. Cytogenesis in the monkey retina. J Comp Neurol 309:86-114.
26. Lerea CL, Bunt-Milam AH, Hurley JB. 1989. Alpha transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron 3:367-376.
27. Martin PR, Grunert U. 1999. Analysis of the short wavelength-sensitive ("blue") cone mosaic in the primate retina: comparison of New World and Old World monkeys. J Comp Neurol 406:1-14.
28. Milam AH, Dacey DM, Dizhoor AM. 1993. Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10:1-12.
29. Milam AH, Hendrickson AE, Xiao M, Smith JE, Possin DE, John SK, Nishina PM. 2000. Localization of tubby-like protein 1 in developing and adult human retinas. Invest Ophthalmol Vis Sci 41:2352-2356.
30. Mimura Y, Mogi K, Kawano M, Fukui Y, Takeda J, Nogami H, Hisano S. 2002. Differential expression of two distinct vesicular glutamate transporters in the rat retina. Neuroreport 13:1925-1928.
31. Nir I, Ransom N. 1992. S-antigen in rods and cones of the primate retina: different labeling patterns are revealed with antibodies directed against specific domains in the molecule. J Histochem Cytochem 40:343-352.
32. Okada M, Erickson A, Hendrickson A. 1994. Light and electron microscopic analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for the synaptic vesicle protein, SV2. J Comp Neurol 339:535-558.
33. Packer O, Hendrickson AE, Curcio CA. 1990. Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina. J Comp Neurol 298:472-493.
34. Phillips IR. 1976. The reproductive potential of the common cotton-eared marmoset (Callithrix jacchus) in captivity. J Med Primatol 5:49-55.
35. Provis JM. 2001. Development of the primate retinal vasculature. Prog Ret Eye Res 20:799-821.
36. Provis JM, Van Driel D, Billson FA, Russell P. 1985. Development of the human retina: patterns of cell distribution and redistribution in the ganglion cell layer. J Comp Neurol 233:429-451.
37. Provis JM, Diaz CM, Dreher B. 1998. Ontogeny of the primate fovea: a central issue in retinal development. Prog Neurobiol 54:549-580.
38. Robinson SR. 1991. Development of the mammalian retina. In: Dreher B, Robinson SR, editors. Neuroanatomy of the visual pathways and their development. Boca Raton, FL: CRC Press. p 69-128.
39. Sears S, Erickson A, Hendrickson A. 2000. The spatial and temporal expression of outer segment proteins during development of Macaca monkey cones. Invest Ophthalmol Vis Sci 41:971-979.
40. Sherry DM, Wang MM, Bates J, Frishman LJ. 2003. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498.
41. Springer AD, Hendrickson AE. 2004. Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retina and pars plana growth. Vis Neurosci 21:775-790.
42. Springer AD, Hendrickson AE. 2005. Development of the primate area of high acuity, 3: temporal relationships between pit formation, retinal elongation and cone packing. Vis Neurosci 22:171-185.
43. Swain PK, Hicks D, Mears AJ, Apel IJ, Smith JE, John SK, Hendrickson A, Milam AH, Swaroop A. 2001. Multiple phosphorylated isoforms of NRL are expressed in rod photoreceptors. J Biol Chem 276:36824-36830.
44. tter JH. 2005. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168:825-836.
45. Troilo D, Howland HC, Judge SJ. 1993. Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Res 33:1301-1310.
46. Wang Y, Macke JP, Merbs SL, Zack DJ, Klaunberg B, Bennett J, Gearhart J, Nathans J. 1992. A locus control region adjacent to the human red and green visual pigment genes. Neuron 9:429-440.
47. Wikler KC, Rakic P, Bhattacharyya N, MacLeish PR. 1997. Early emergence of photoreceptor mosaicism in the primate retina revealed by a novel conespecific monoclonal antibody. J Comp Neurol 377:500-508.
48. Wilder HD, Grünert U, Lee BB, Martin PR. 1996. Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Vis Neurosci 13:335-352.
49. Xiao M, Hendrickson A. 2000. Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. J Comp Neurol 425:545-559.
50. Yan XX, Wiechmann AF. 1997. Early expression of recoverin in a unique population of neurons in the human retina. Anat Embryol 195:51-63.
51. Yuodelis C, Hendrickson A. 1986. A qualitative and quantitative analysis of the human fovea during development. Vis Res 26:847-855.
52. Zhang H, Cuenca N, Ivanova T, Church-Kopish J, Frederick JM, MacLeish PR, Baehr W. 2003. Identification and light-dependent translocation of a cone-specific antigen, cone arrestin, recognized by monoclonal antibody 7G6. Invest Ophthalmol Vis Sci 44:2858-2867.