Differential role of Jak-STAT signaling in retinal degenerations

FASEB Journal

Volumn 20, Issue 13, 2006, Pages

  Samardzija, Marijana ^a   Wenzel, Andreas ^a   Aufenberg, Svenja ^a   Thiersch, Markus ^a   Remé, Charlotte ^a   Grimm, Christian ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Apoptosis; Neuroprotection; Photoreceptor

Indexed keywords

INTERLEUKIN 6; JANUS KINASE; JANUS KINASE 2; PROTEIN KINASE B; STAT PROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DEGENERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; LIGHT EXPOSURE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; RETINA DEGENERATION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; LIGHT; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOTORECEPTOR; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; INTERLEUKIN-6; LIGHT; MICE; MICE, INBRED BALB C; PHOTORECEPTORS; PROTEIN-TYROSINE KINASES; RETINAL DEGENERATION; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 33845627240     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5895fje     Document Type: Article

References (67)

1. Reme, C. E., Grimm, C., Hafezi, F., Marti, A., and Wenzel, A. (1998) Apoptotic cell death in retinal degenerations. Prog. Retin. Eye Res. 17, 443-464
2. Wenzel, A., Grimm, C., Samardzija, M., and Reme, C. E. (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog. Retin. Eye Res. 24, 275-306
3. Grimm, C., Wenzel, A., Groszer, M., Mayser, H., Seeliger, M., Samardzija, M., Bauer, C., Gassmann, M., and Reme, C. E. (2002) HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat. Med. 8, 718-724
4. Wenzel, A., Grimm, C., Seeliger, M. W., Jaissle, G., Hafezi, F., Kretschmer, R., Zrenner, E., and Reme, C. E. (2001) Prevention of photoreceptor apoptosis by activation of the glucocorticoid receptor. Invest Ophthalmol. Vis. Sci. 42, 1653-1659
5. Imai, D., Yoneya, S., Gehlbach, P. L., Wei, L. L., and Mori, K. (2005) Intraocular gene transfer of pigment epithelium-derived factor rescues photoreceptors from light-induced cell death. J. Cell. Physiol. 202, 570-578
6. Organisciak, D. T., Darrow, R. A., Barsalou, L., Darrow, R. M., and Lininger, L. A. (1999) Light-induced damage in the retina: differential effects of dimethylthiourea on photoreceptor survival, apoptosis and DNA oxidation. Photochem. Photobiol. 70, 261-268
7. Ranchon, I., Chen, S., Alvarez, K., and Anderson, R. E. (2001) Systemic administration of phenyl-N-tert-butylnitrone protects the retina from light damage. Invest. Ophthalmol. Vis. Sci. 42, 1375-1379
8. Zhang, C., Lei, B., Lam, T. T., Yang, F., Sinha, D., and Tso, M. O. (2004) Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest. Ophthalmol. Vis. Sci. 45, 2753-2759
9. LaVail, M. M., Unoki, K., Yasumura, D., Matthes, M. T., Yancopoulos, G. D., and Steinberg, R. H. (1992) Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc. Natl. Acad. Sci. U. S. A. 89, 11249-11253
10. Tao, W., Wen, R., Goddard, M. B., Sherman, S. D., O'Rourke, P. J., Stabila, P. F., Bell, W. J., Dean, B. J., Kauper, K. A., and Budz, V. A., et al. (2002) Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa. Invest Ophthalmol. Vis. Sci. 43, 3292-3298
11. Cao, W., Tombran-Tink, J., Elias, R., Sezate, S., Mrazek, D., and McGinnis, J. F. (2001) In vivo protection of photoreceptors from light damage by pigment epithelium-derived factor. Invest. Ophthalmol. Vis. Sci. 42, 1646-1652
12. Grimm, C., Wenzel, A., Stanescu, D., Samardzija, M., Hotop, S., Groszer, M., Naash, M., Gassmann, M., and Reme, C. (2004) Constitutive overexpression of human erythropoietin protects the mouse retina against induced but not inherited retinal degeneration. J. Neurosci. 24, 5651-5658
13. Kaldi, I., Dittmar, M., Pierce, P., and Anderson, R. E. (2003) L-NAME protects against acute light damage in albino rats, but not against retinal degeneration in P23H and S334ter transgenic rats. Exp. Eye Res. 76, 453-461
14. Peterson, W. M., Wang, Q., Tzekova, R., and Wiegand, S. J. (2000) Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J. Neurosci. 20, 4081-4090
15. Harada, T., Harada, C., Kohsaka, S., Wada, E., Yoshida, K., Ohno, S., Mamada, H., Tanaka, K., Parada, L. F., and Wada, K. (2002) Microglia-Muller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J. Neurosci. 22, 9228-9236
16. Alonzi, T., Middleton, G., Wyatt, S., Buchman, V., Betz, U. A., Muller, W., Musiani, P., Poli, V., and Davies, A. M. (2001) Role of STAT3 and PI 3-kinase/Akt in mediating the survival actions of cytokines on sensory neurons. Mol. Cell. Neurosci. 18, 270-282
17. Ikeda, K., Tatsuno, T., Noguchi, H., and Nakayama, C. (2004) Ciliary neurotrophic factor protects rat retina cells in vitro and in vivo via PI3 kinase. Curr. Eye Res. 29, 349-355
18. Platanias, L. C. (2005) Mechanisms of type-I- and type-II-interferon- mediated signalling. Nat. Rev. Immunol. 5, 375-386
19. Stephanou, A. (2004) Role of STAT-1 and STAT-3 in ischaemia/reperfusion injury. J. Cell. Mol. Med. 8, 519-525
20. Calo, V., Migliavacca, M., Bazan, V., Macaluso, M., Buscemi, M., Gebbia, N., and Russo, A. (2003) STAT proteins: from normal control of cellular events to tumorigenesis. J. Cell. Physiol. 197, 157-168
21. Aaronson, D. S., and Horvath, C. M. (2002) A road map for those who don't know JAK-STAT. Science 296, 1653-1655
22. Krebs, D. L., and Hilton, D. J. (2000) SOCS: physiological suppressors of cytokine signaling. J. Cell Sci. 113, 2813-2819
23. Cao, W., Wen, R., Li, F., Lavail, M. M., and Steinberg, R. H. (1997) Mechanical injury increases bFGF and CNTF mRNA expression in the mouse retina. Exp. Eye Res. 65, 241-248
24. Casson, R. J., Chidlow, G., Wood, J. P., Vidal-Sanz, M., and Osborne, N. N. (2004) The effect of retinal ganglion cell injury on light-induced photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci. 45, 685-693
25. Nir, I., Liu, C., and Wen, R. (1999) Light treatment enhances photoreceptor survival in dystrophic retinas of Royal College of Surgeons rats. Invest. Ophthalmol. Vis. Sci. 40, 2383-2390
26. Walsh, N., Valter, K., and Stone, J. (2001) Cellular and subcellular patterns of expression of bFGF and CNTF in the normal and light stressed adult rat retina. Exp. Eye Res. 72, 495-501
27. Wen, R., Song, Y., Cheng, T., Matthes, M. T., Yasumura, D., LaVail, M. M., and Steinberg, R. H. (1995) Injury-induced upregulation of bFGF and CNTF mRNAS in the rat retina. J. Neurosci. 15, 7377-7385
28. Valter, K., Bisti, S., Gargini, C., Di Loreto, S., Maccarone, R., Cervetto, L., and Stone, J. (2005) Time course of neurotrophic factor upregulation and retinal protection against light-induced damage after optic nerve section. Invest. Ophthalmol. Vis. Sci. 46, 1748-1754
29. Beltran, W. A., Rohrer, H., and Aguirre, G. D. (2005) Immunolocalization of ciliary neurotrophic factor receptor alpha (CNTFRalpha) in mammalian photoreceptor cells. Mol. Vis. 11, 232-244
30. De Raad, S., Szczesny, P. J., Munz, K., and Reme, C. E. (1996) Light damage in the rat retina: glial fibrillary acidic protein accumulates in Muller cells in correlation with photoreceptor damage. Ophthal. Res. 28, 99-107
31. Hafezi, F., Steinbach, J. P., Marti, A., Munz, K., Wang, Z. Q., Wagner, E. F., Aguzzi, A., and Reme, C. E. (1997) The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 3, 346-349
32. Wenzel, A., Grimm, C., Samardzija, M., and Reme, C. E. (2003) The genetic modifier Rpe65Leu(450): effect on light damage susceptibility in c-Fos-deficient mice. Invest. Ophthalmol. Vis. Sci. 44, 2798-2802
33. Wenzel, A., Reme, C. E., Williams, T. P., Hafezi, F., and Grimm, C. (2001) The Rpe65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J. Neurosci. 21, 53-58
34. Bowes, C., Li, T., Danciger, M., Baxter, L. C., Applebury, M. L., and Farber, D. B. (1990) Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680
35. Naash, M. I., Ripps, H., Li, S., Goto, Y., and Peachey, N. S. (1996) Polygenic disease and retinitis pigmentosa: albinism exacerbates photoreceptor degeneration induced by the expression of a mutant opsin in transgenic mice. J. Neurosci. 16, 7853-7858
36. Strettoi, E., Pignatelli, V., Rossi, C., Porciatti, V., and Falsini, B. (2003) Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vision Res. 43, 867-877
37. Marc, R. E., Jones, B. W., Watt, C. B., and Strettoi, E. (2003) Neural remodeling in retinal degeneration. Prog. Retin. Eye Res. 22, 607-655
38. Bowes, C., Li, T., Frankel, W. N., Danciger, M., Coffin, J. M., Applebury, M. L., and Farber, D. B. (1993) Localization of a retroviral element within the rd gene coding for the β subunit of cGMP phosphodiesterase. Proc. Natl. Acad. Sci. U. S. A. 90, 2955-2959
39. Burdelya, L., Catlett-Falcone, R., Levitzki, A., Cheng, F., Mora, L. B., Sotomayor, E., Coppola, D., Sun, J., Sebti, S., and Dalton, W. S., et al. (2002) Combination therapy with AG-490 and interleukin 12 achieves greater antitumor effects than either agent alone. Mol. Cancer Ther. 1, 893-899
40. Meydan, N., Grunberger, T., Dadi, H., Shahar, M., Arpaia, E., Lapidot, Z., Leeder, J. S., Freedman, M., Cohen, A., and Gazit, A., et al. (1996) Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379, 645-648
41. Wang, L. H., Kirken, R. A., Erwin, R. A., Yu, C. R., and Farrar, W. L. (1999) JAK3, STAT, and MAPK signaling pathways as novel molecular targets for the tyrphostin AG-490 regulation of IL-2-mediated T cell response. J. Immunol. 162, 3897-3904
42. Battle, T. E., and Frank, D. A. (2002) The role of STATs in apoptosis. Curr. Mol. Med. 2, 381-392
43. Zhang, S. S., Wei, J. Y., Li, C., Barnstable, C. J., and Fu, X. Y. (2003) Expression and activation of STAT proteins during mouse retina development. Exp. Eye Res. 76, 421-431
44. Rhee, K. D., and Yang, X. J. (2003) Expression of cytokine signal transduction components in the postnatal mouse retina. Mol. Vis. 9, 715-722
45. Song, Y., Zhao, L., Tao, W., Laties, A. M., Luo, Z., and Wen, R. (2003) Photoreceptor protection by cardiotrophin-1 in transgenic rats with the rhodopsin mutation s334ter. Invest. Ophthalmol. Vis. Sci. 44, 4069-4075
46. Ji, J. Z., Elyaman, W., Yip, H. K., Lee, V. W., Yick, L. W., Hugon, J., and So, K. F. (2004) CNTF promotes survival of retinal ganglion cells after induction of ocular hypertension in rats: the possible involvement of STAT3 pathway. Eur. J. Neurosci. 19, 265-272
47. Dikdan, G. S., Saba, S. C., Dela Torre, A. N., Roth, J., Wang, S., and Koneru, B. (2004) Role of oxidative stress in the increased activation of signal transducers and activators of transcription-3 in the fatty livers of obese Zucker rats. Surgery 136, 677-685
48. Carballo, M., Conde, M., El Bekay, R., Martin-Nieto, J., Camacho, M. J., Monteseirin, J., Conde, J., Bedoya, F. J., and Sobrino, F. (1999) Oxidative stress triggers STAT3 tyrosine phosphorylation and nuclear translocation in human lymphocytes. J. Biol. Chem. 274, 17580-17586
49. Brunet, A., Datta, S. R., and Greenberg, M. E. (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297-305
50. Barber, A. J., Nakamura, M., Wolpert, E. B., Reiter, C. E., Seigel, G. M., Antonetti, D. A., and Gardner, T. W. (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
51. Datta, S. R., Brunet, A., and Greenberg, M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927
52. Johnson, L. E., van Veen, T., and Ekstrom, P. A. (2005) Differential Akt activation in the photoreceptors of normal and rd1 mice. Cell Tissue Res. 320, 213-222
53. Jomary, C., Cullen, J., and Jones, S. E. (2006) Inactivation of the Akt survival pathway during photoreceptor apoptosis in the retinal degeneration mouse. Invest. Ophthalmol. Vis. Sci. 47, 1620-1629
54. Yu, D. Y., Cringle, S., Valter, K., Walsh, N., Lee, D., and Stone, J. (2004) Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H rat. Invest. Ophthalmol. Vis. Sci. 45, 2013-2019
55. Wang, Y., Smith, S. B., Ogilvie, J. M., McCool, D. J., and Sarthy, V. (2002) Ciliary neurotrophic factor induces glial fibrillary acidic protein in retinal Muller cells through the JAK/STAT signal transduction pathway. Curr. Eye Res. 24, 305-312
56. Chun, M. H., Ju, W. K., Kim, K. Y., Lee, M. Y., Hofmann, H. D., Kirsch, M., and Oh, S. J. (2000) Upregulation of ciliary neurotrophic factor in reactive Muller cells in the rat retina following optic nerve transection. Brain Res. 868, 358-362
57. Harada, T., Harada, C., Nakayama, N., Okuyama, S., Yoshida, K., Kohsaka, S., Matsuda, H., and Wada, K. (2000) Modification of glial-neuronal cell interactions prevents photoreceptor apoptosis during light-induced retinal degeneration. Neuron 26, 533-541
58. Harada, C., Harada, T., Quah, H. M., Maekawa, F., Yoshida, K., Ohno, S., Wada, K., Parada, L. F., and Tanaka, K. (2003) Potential role of glial cell line-derived neurotrophic factor receptors in Muller glial cells during light-induced retinal degeneration. Neuroscience 122, 229-235
59. Murray, P., and Edgar, D. (2001) The regulation of embryonic stem cell differentiation by leukaemia inhibitory factor (LIF). Differentiation 68, 227-234
60. Cartwright, P., McLean, C., Sheppard, A., Rivett, D., Jones, K., and Dalton, S. (2005) LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132, 885-896
61. Graham, D. R., Overbeek, P. A., and Ash, J. D. (2005) Leukemia inhibitory factor blocks expression of Crx and Nrl transcription factors to inhibit photoreceptor differentiation. Invest. Ophthalmol. Vis. Sci. 46, 2601-2610
62. Sherry, D. M., Mitchell, R., Li, H., Graham, D. R., and Ash, J. D. (2005) Leukemia inhibitory factor inhibits neuronal development and disrupts synaptic organization in the mouse retina. J. Neurosci. Res. 82, 316-332
63. Neophytou, C., Vernallis, A. B., Smith, A., and Raff, M. C. (1997) Muller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development. Development 124, 2345-2354
64. Samardzija, M., Wenzel, A., Naash, M., Reme, C. E., and Grimm, C. (2006) Rpe65 as a modifier gene for inherited retinal degeneration. Eur. J. Neurosci. 23, 1028-1034
65. Xuan, Y. T., Guo, Y., Han, H., Zhu, Y., and Bolli, R. (2001) An essential role of the JAK-STAT pathway in ischemic preconditioning. Proc. Natl. Acad. Sci. U. S. A. 98, 9050-9055
66. Yamauchi, K., Osuka, K., Takayasu, M., Usuda, N., Nakazawa, A., Nakahara, N., Yoshida, M., Aoshima, C., Hara, M., and Yoshida, J. (2006) Activation of JAK/STAT signalling in neurons following spinal cord injury in mice. J. Neurochem. 96, 1060-1070
67. Kueng-Hitz, N., Grimm, C., Lansel, N., Hafezi, F., He, L., Fox, D. A., Reme, C. E., Niemeyer, G., and Wenzel, A. (2000) The retina of c-fos-/- mice: electrophysiologic, morphologic and biochemical aspects. Invest. Ophthalmol. Vis. Sci. 41, 909-916