The anemia of the newborn induces erythropoietin expression in the developing mouse retina

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 1, 2010, Pages

  Scheerer, N ^a   Dunker N ^a   Imagawa, S ^b   Yamamoto, M ^b   Suzuki, N ^b   Fandrey, J ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Apoptosis; Erythropoietin receptor; Neuroprotection; Retinal ganglion cells

Indexed keywords

ERYTHROPOIETIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PROTEIN BAX; TRANSFORMING GROWTH FACTOR BETA;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; IN VIVO STUDY; KIDNEY; LIVER; MOUSE; NEUROPROTECTION; NEWBORN; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA; RETINA DEVELOPMENT; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANEMIA; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; ERYTHROPOIETIN; ERYTHROPOIETIN, RECOMBINANT; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PHOTORECEPTOR CELLS; RETINA; RETINAL GANGLION CELLS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77954416831     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00108.2010     Document Type: Article

References (43)

1. Beier M, Franke A, Paunel-Gorgulu AN, Scheerer N, Dünker N. Transforming growth factor beta mediates apoptosis in the ganglion cell layer during all programmed cell death periods of the developing murine retina. Neurosci Res 56: 193-203, 2006.
2. Bocker-Meffert S, Rosenstiel P, Rohl C, Warneke N, Held-Feindt J, Sievers J, Lucius R. Erythropoietin and VEGF promote neural outgrowth from retinal explants in postnatal rats. Invest Ophthalmol Vis Sci 43: 2021-2026, 2002.
3. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, Itri LM, Cerami A. From the cover: erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 97: 10526-10531, 2000.
4. Cellerino A, Bahr M, Isenmann S. Apoptosis in the developing visual system. Cell Tissue Res 301: 53-69, 2000.
5. Chaum E. Retinal neuroprotection by growth factors: a mechanistic perspective. J Cell Biochem 88: 57-75, 2003.
6. Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LEH. Suppression of retinal neovascularization by erythropoietin siRNA in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci 50: 1329-1335, 2009.
7. Chen ZY, Asavaritikrai P, Prchal JT, Noguchi CT. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J Biol Chem 282: 25875-25883, 2007.
8. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
9. de la Rosa EJ, Diaz B, De PF. Organoculture of the chick embryonic neuroretina. Curr Top Dev Biol 36: 133-144, 1998.
10. Duenker N, Valenciano AI, Franke A, Hernandez-Sanchez C, Dressel R, Behrendt M, De PF, Krieglstein K, de la Rosa EJ. Balance of pro-apoptotic transforming growth factor-beta and anti-apoptotic insulin effects in the control of cell death in the postnatal mouse retina. Eur J Neurosci 22: 28-38, 2005.
11. Dünker N, Krieglstein K. Reduced programmed cell death in the retina and defects in lens and cornea of Tgfbeta2(-/-) Tgfbeta3(-/-) double-deficient mice. Cell Tissue Res 313: 1-10, 2003.
12. Dünker N, Schuster N, Krieglstein K. TGF-beta modulates programmed cell death in the retina of the developing chick embryo. Development 128: 1933-1942, 2001.
13. Fandrey J. Oxygen-dependent and tissue-specific regulation of erythropoietin gene expression. Am J Physiol Regul Integr Comp Physiol 286: R977-R988, 2004.
14. Franke AG, Gubbe C, Beier M, Duenker N. Transforming growth factor-beta and bone morphogenetic proteins: cooperative players in chick and murine programmed retinal cell death. J Comp Neurol 495: 263-278, 2006.
15. Frede S, Stockmann C, Freitag P, Fandrey J. Activation Of HIF-1 by bacterial lipopolysaccharides in human monocytes requires NF-kB. Biochem J 396: 517-527, 2006.
16. Fu QL, Wu W, Wang H, Li X, Lee VW, So KF. Up-regulated endogenous erythropoietin/erythropoietin receptor system and exogenous erythropoietin rescue retinal ganglion cells after chronic ocular hypertension. Cell Mol Neurobiol 28: 317-329, 2008.
17. Grimm C, Hermann DM, Bogdanova A, Hotop S, Kilic U, Wenzel A, Kilic E, Gassmann M. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin Cell Dev Biol 16: 531-538, 2005.
18. Grimm C, Wenzel A, Groszer M, Mayser H, Seeliger M, Samardzija M, Bauer C, Gassmann M, Reme CE. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med 8: 718-724, 2002.
19. Guerin MB, McKernan DP, O'Brien CJ, Cotter TG. Retinal ganglion cells: dying to survive. Int J Dev Biol 50: 665-674, 2006.
20. Gustmann S, Dünker N. In vivo-like organotypic murine retinal whole-mount culture. https://www.jove.com/index/Details.stp?ID=1634, 2010.
21. Hahn P, Lindsten T, Ying GS, Bennett J, Milam AH, Thompson CB, Dunaief JL. Proapoptotic Bcl-2 family members, Bax and Bak, are essential for developmental photoreceptor apoptosis. Invest Ophthalmol Vis Sci 44: 3598-3605, 2003.
22. Halvorsen S, Bechensteen AG. Physiology of erythropoietin during mammalian development. Acta Paediatr Suppl 91: 17-26, 2002.
23. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol Rev 72: 449-489, 1992.
24. Jelkmann W, Wagner K. Beneficial and ominous aspects of the pleiotropic action of erythropoietin. Ann Hematol 83: 673-686, 2004.
25. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 19: 2026-2028, 2005.
26. Kilic U, Kilic E, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Erythropoietin protects from axotomy-induced degeneration of retinal ganglion cells by activating ERK-1/-2. FASEB J 19: 249-251, 2005.
27. Masuda S, Okano M, Yamagishi K, Nagao M, Ueda M, Sasaki R. A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J Biol Chem 269: 19488-19493, 1994.
28. Morishita E, Masuda S, Nagao M, Yasuda Y, Sasaki R. Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death. Neuroscience 76: 105-116, 1997.
29. Morita M, Ohneda O, Yamashita T, Takahashi S, Suzuki N, Nakajima O, Kawauchi S, Ema M, Shibahara S, Udono T, Tomita K, Tamai M, Sogawa K, Yamamoto M, Fujii-Kuriyama Y. HLF/HIF-2α is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J 22: 1134-1146, 2003.
30. Obara N, Suzuki N, Kim K, Nagasawa T, Imagawa S, Yamamoto M. Repression via the GATA box is essential for tissue-specific erythropoietin gene expression. Blood 111: 5223-5232, 2008.
31. Pequignot MO, Provost AC, Salle S, Taupin P, Sainton KM, Marchant D, Martinou JC, Ameisen JC, Jais JP, Abitbol M. Major role of BAX in apoptosis during retinal development and in establishment of a functional postnatal retina. Dev Dyn 228: 231-238, 2003.
32. Samardzija M, Wenzel A, Aufenberg S, Thiersch M, Reme C, Grimm C. Differential role of Jak-STAT signaling in retinal degenerations. FASEB J 20: 2411-2413, 2006.
33. Semenza GL, Koury ST, Nejfelt MK, Gearhart JD, Antonarakis SE. Cell-type-specific and hypoxia-inducible expression of the human erythropoietin gene in transgenic mice. Proc Natl Acad Sci USA 88: 8725-8729, 1991.
34. Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 21: 9733-9743, 2001.
35. Stockmann C, Fandrey J. Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin Exp Pharmacol Physiol 33: 968-979, 2006.
36. Stolze I, Berchner-Pfannschmidt U, Freitag P, Wotzlaw C, Rossler J, Frede S, Acker H, Fandrey J. Hypoxia-inducible erythropoietin gene expression in human neuroblastoma cells. Blood 100: 2623-2628, 2002.
37. Suzuki N, Obara N, Yamamoto M. Use of gene-manipulated mice in the study of erythropoietin gene expression. Meth Enzymol 435: 157-177, 2007.
38. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J, Liu X, Wu H, Carmichael ST. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J Neurosci 26: 1269-1274, 2006.
39. Varela-Nieto I, de la Rosa EJ, Valenciano AI, Leon Y. Cell death in the nervous system: lessons from insulin and insulin-like growth factors. Mol Neurobiol 28: 23-50, 2003.
40. Vecino E, Hernandez M, Garcia M. Cell death in the developing vertebrate retina. Int J Dev Biol 48: 965-974, 2004.
41. Weishaupt JH, Rohde G, Polking E, Siren AL, Ehrenreich H, Bahr M. Effect of erythropoietin axotomy-induced apoptosis in rat retinal ganglion cells. Invest Ophthalmol Vis Sci 45: 1514-1522, 2004.
42. Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83: 59-67, 1995.
43. Yu X, Shacka JJ, Eells JB, Suarez-Quian C, Przygodzki RM, Beleslin-Cokic B, Lin CS, Nikodem VM, Hempstead B, Flanders KC, Costantini F, Noguchi CT. Erythropoietin receptor signalling is required for normal brain development. Development 129: 505-516, 2002.