Specific protein kinase C isoforms are required for rod photoreceptor differentiation

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18606-18617

  Pinzon Guzman, Carolina ^a   Zhang, Samuel Shao Min ^a   Barnstable, Colin J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRX PROTEIN; CYCLINE; OPSIN; PHORBOL 12 ACETATE 13 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; RECEPTOR PROTEIN; SERINE; SOMATOMEDIN C; STAT3 PROTEIN; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; HISTOLOGY; IMMUNOCYTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RETINA ROD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; INSULIN-LIKE GROWTH FACTOR I; ISOENZYMES; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN KINASE C; RETINAL ROD PHOTORECEPTOR CELLS; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE;

EID: 83455177588     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2578-11.2011     Document Type: Article

References (54)

1. Altshuler D, Cepko C (1992) A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. Development 114:947-957
2. Altshuler D, Lo Turco JJ, Rush J, Cepko C (1993) Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119:1317-1328
3. Ananthanarayanan B, Stahelin RV, Digman MA, Cho W (2003) Activation mechanisms of conventional protein kinaseCisoforms are determined by the ligand affinity and conformational flexibility of their C1 domains. J Biol Chem 278:46886-46894
4. Asao H, Fu XY (2000) Interferon-gamma has dual potentials in inhibiting or promoting cell proliferation. J Biol Chem 275:867-874
5. Asotra K, Macklin WB (1994) Developmental expression of protein kinase C isozymes in oligodendrocytes and their differential modulation by 4 beta-phorbol-12,13-dibutyrate. J Neurosci Res 39:273-289
6. Barber AJ, Nakamura M, Wolpert EB, Reiter CE, Seigel GM, Antonetti DA, Gardner TW (2001) Insulin rescues retinal neurons from apoptosis by a phosphatidylinositol 3-kinase/Akt-mediated mechanism that reduces the activation of caspase-3. J Biol Chem 276:32814-32821
7. Barnstable CJ (1980) Monoclonal antibodies which recognize different cell types in the rat retina. Nature 286:231-235
8. Biswas SK, Zhao, Nagalingam YA, Gardner TW, Sandirasegarane L (2008) PDGF-and insulin/IGF1-specific distinct modes of class IA PI 3-kinase activation in normal rat retinas and RGC-5 retinal ganglion cells. Invest Ophthalmol Vis Sci 49:3687-3698
9. Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, Dumont JE, Le Marchand-Brustel Y, Erneux C, Hue L, Schurmans S (2001) The lipid phosphatase SHIP2 controls insulin sensitivity Nature 409:92-97
10. Hernández-Sánchez C, López-Carranza A, Alarcón C, de la Rosa EJ, de Pablo F (1995) Autocrine/paracrine role of insulin-related growth factors in neurogenesis: local expression and effects on cell proliferation and differentiation in retina. Proc Natl Acad Sci U S A 92:9834-9838
11. Hicks D, Barnstable CJ (1987) Different rhodopsin monoclonal antibodies reveal different binding patterns on developing and adult rat retina. J Histochem Cytochem 35:1317-1328
12. Hollborn M, Jahn K, Limb GA, Kohen L, Wiedemann P, Bringmann A (2004) Characterization of the basic fibroblast growth factor-evoked proliferation of the human Muller cell line, MIO-M1. Graefes Arch Clin Exp Ophthalmol 242:414-422
13. Holt CE, Bertsch TW, Ellis HM, Harris WA (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15-26
14. Ishihara H, Sasaoka T, Hori H, Wada T, Hirai H, Haruta T, Langlois WJ, Kobayashi M (1999) Molecular cloning of rat SH2-containing inositol phosphatase 2 (SHIP2) and its role in the regulation of insulin signaling. Biochem Biophys Res Commun 260:265-272
15. Keeton AB, Bortoff KD, Franklin JL, Messina JL (2005) Blockade of rapid versus prolonged extracellularly regulated kinase 1/2 activation has differential effects on insulin-induced gene expression. Endocrinology 146:2716-2725
16. Kermer P, Klöcker N, Labes M, Bähr M (2000) Insulin-like growth factor-1 protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 in vivo. J Neurosci 20:2-8
17. Kheifets V, Mochly-Rosen D (2007) Insight into intra-and inter-molecular interactions of PKC: design of specific modulators of kinase function. Pharmacol Res 55:467-476
18. Kiepe D, Ciarmatori S, Hoeflich A, Wolf E, Tonshoff B (2005) Insulin-like growth factor (IGF)-I stimulates cell proliferation and induces IGF binding protein (IGFBP)-3 and IGFBP-5 gene expression in cultured growth plate chondrocytes via distinct signaling pathways. Endocrinology 146:3096-3104
19. Kosaka J, Suzuki A, Morii E, Nomura S (1998) Differential localization and expression of alpha and beta isoenzymes of protein kinase C in the rat retina. J Neurosci Res 54:655-663
20. Levine EM, Close J, Fero M, Ostrovsky A, Reh TA (2000) p27Kip1 regulates cell cycle withdrawal of late multipotent progenitor cells in the mammalian retina. Dev Biol 219:299-314
21. Liu MG, Xu X, Zhang SSM, Barnstable CJ (2008) Comparison of gene expression during in vivo and in vitro retina development. J Ocul Biol Dis Infor 1:59-72
22. Mellor H, Parker PJ (1998) The extended protein kinase C superfamily. Biochem J 332:281-292
23. Meyer-Franke A, Kaplan MR, Pfrieger FW, Barres BA (1995) Characteriza-tion of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15:805-819
24. Miki A (1996) Expression of alpha-, beta-, and gamma-subspecies of protein kinase C in the motor neurons in the embryonic and postnatal rat spinal cord. Neuroscience 72:805-814
25. Modanlou HD, Gharraee Z, Hasan J, Waltzman J, Nageotte S, Beharry KD (2006) Ontogeny of VEGF, IGF-I, and GH in neonatal rat serum, vitreous fluid, and retina from birth to weaning. Invest Ophthalmol Vis Sci 47:738-744
26. Morimoto T, Miyoshi T, Matsuda S, Tano Y, Fujikado T, Fujikado Y (2005) Transcorneal electrical stimulation rescues axotomized retinal ganglion cells by activating endogenous retinal IGF1 system. Invest Ophthalmol Vis Sci 6:2147-2155
27. Nakazawa T, Tamai M, Mori N (2002) Brain-derived neurotrophic factor prevents axotomized retinal ganglion cell death through MAPK and PI3K signaling pathways. Invest Ophthalmol Vis Sci 43:3319-3326
28. Narimatsu M, Maeda H, Itoh S, Atsumi T, Ohtani T, Nishida K, Itoh M, Kamimura D, Park SJ, Mizuno K, Miyazaki J, Hibi M, Ishihara K, Nakajima K, Hirano T (2001) Tissue specific autoregulation of the stat3 gene and its role in interleukin-6-induced survival signals in T cells. Mol Cell Biol 21:6615-6625
29. Oehrlein SA, Maelicke A, Herget T (1998) Expression of protein kinase C gene family members is temporally and spatially regulated during neural development in vitro. Eur J Cell Biol 77:323-337
30. Osborne NN, Barnett NL, Morris NJ, Huang FL (1992) The occurrence of three isoenzymes of protein kinase C (alpha, beta and gamma) in retinas of different species. Brain Res 570:161-166
31. Ozawa Y, Nakao K, Shimazaki T, Takeda J, Akira S, Ishihara K, Hirano T, Oguchi Y, Okano H (2004) Downregulation of STAT3 activation is required for presumptive rod photoreceptor cells to differentiate in the postnatal retina. Mol Cell Neurosci 262:258-270
32. Parrizas M, Saltiel AR, LeRoith D (1997) Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3'-kinase and mitogenactivated protein kinase pathways. J Biol Chem 272:154-161
33. Pesesse X, Deleu S, De Smedt F, Drayer L, Erneux C (1997) Identification of a second SH2-domain-containing protein closely related to the phosphatidylinositol polyphosphate 5-phosphatase SHIP. Biochem Biophys Res Commun 239:697-700
34. Rapaport DH, Wong LL, Wood ED, Yasamura D, LaVail MM (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474:304-324
35. Reh TA (1992) Cellular interactions determine neuronal phenotypes in rodent retinal cultures. J Neurobiol 23:1067-1083
36. Rhee KD, Goureau O, Chen S, Yang XJ (2004) Cytokine-induced activation of signal transducer and activator of transcription in photoreceptor precursors regulates rod differentiation in the developing mouse retina. J Neurosci 24:9779-9788
37. Sasaoka T, Wada T, Fukui K, Murakami S, Ishihara H, Suzuki R, Tobe K, Kadowaki T, Kobayashi M (2004) SH2-containing inositol phosphatase 2 predominantly regulates Akt2, and not Akt1, phosphorylation at the plasma membrane in response to insulin in 3T3-L1 adipocytes. J Biol Chem 15:14835-14843
38. Sparrow JR, Hicks D, Barnstable CJ (1990) Cell commitment and differentiation in explants of embryonic rat neural retina. Comparison with the developmental potential of dissociated retina. Dev Brain Res 51:69-84
39. Turner DL, Cepko CL (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131-136
40. Wada T, Sasaoka T, Funaki M, Hori H, Murakami S, Ishiki M, Haruta T, Asano T, Ogawa W, Ishihara H, Kobayashi M (2001) Overexpression of SH2-containing inositol phosphatase 2 results in negative regulation of insulin-induced metabolic actions in 3T3-L1 adipocytes via its 5'-phosphatase catalytic activity. Mol Cell Biol 21:1633-1646
41. Watanabe T, Raff MC (1990) Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 4:461-467
42. Watanabe T, Raff MC (1992) Diffusible rod-promoting signals in the developing rat retina. Development 114:899-906
43. Webster J, Prager D, Melmed S (1994) Insulin-like growth factor-1 activation of extracellular signal-related kinase-1 and-2 in growth hormonesecreting cells. Mol Endocrinol 8:539-544
44. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142-1145
45. Xie X, Chan KS, Cao F, Huang M, Li Z, Lee A, Weissman IL, Wu JC (2009) Imaging of STAT3 signaling pathway during mouse embryonic stem cell differentiation. Stem Cells Dev 18:205-214
46. Yang XJ (2004) Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Seminars in cell and developmental biology 15:91-103
47. Yoshimatsu T, Kawaguchi D, Oishi K, Takeda K, Akira S, Masuyama N, Gotoh Y (2006) Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133:2553-2563
48. Young RW (1985) Cell proliferation during postnatal development of the retina in the mouse. Brain Res 353:229-239
49. Zhang SS, Wei J, Qin H, Zhang L, Xie B, Hui P, Deisseroth A, Barnstable CJ, Fu XY (2004) STAT3-mediated signaling in the determination of rod photoreceptor cell fate in mouse retina. Invest Ophthalmol Vis Sci 45:2407-2412
50. Zhang SS, Fu XY, Barnstable CJ (2002) Tissue culture studies of retinal development. Methods 28:439-447
51. Zhang SS, Wei JY, Li C, Barnstable CJ, Fu XY (2003) Expression and activation of STAT proteins during mouse retina development. Exp Eye Res 76:421-431
52. Zhang S, Liu MG, Kano A., Zhan C, Fu XY, Barnstable CJ (2005) STAT3 activation in response to growth factors or cytokines participates in retina precursor proliferation. Exp Eye Res 81:103-115
53. Zhao S, Barnstable CJ (1996) Differential effects of bFGF on development of the rat retina. Brain Res 723:169-176
54. Zhao S, Thornquist SC, Barnstable CJ (1995) In vitro transdifferentiation of embryonic rat retinal pigment epithelium to neural retina. Brain Res 677:300-310.