Mitogen-activated protein kinase pathway mediates /V-(4-hydroxyphenyl) retinamide-induced neuronal differentiation in the ARPE-19 human retinal pigment epithelial cell line

Journal of Neurochemistry

Volumn 106, Issue 2, 2008, Pages 591-602

  Samuel, William ^a   Kutty, R Krishnan ^a   Sekhar, Sonia ^a   Vijayasarathy, Camasamudram ^b   Wiggert, Barbara ^a   Redmond, T Michael ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

Activator protein 1; c fos; c jun; c jun N terminal kinase; Calretinin; Extracellular signal regulated kinase; Retinal pigment epithelium; Stress activated protein kinase

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CALRETININ; FENRETINIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PROTEIN C FOS; PROTEIN C JUN; PROTEIN P90; RAF PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; ANTINEOPLASTIC AGENT; CALBINDIN; ENZYME INHIBITOR;

ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; ONCOGENE C FOS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; DRUG INTERACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; NERVE CELL; NEURITE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME;

ANTINEOPLASTIC AGENTS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELL LINE; DRUG INTERACTIONS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FENRETINIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NEURITES; NEURONS; PIGMENT EPITHELIUM OF EYE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 51649112230     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05409.x     Document Type: Article

References (50)

1. Bok D. (1993) The retinal pigment epithelium: a versatile partner in vision. J. Cell Sci. 17, 189-195.
2. Camerini T., Mariani L., De Palo G., Marubini E., Di Mauro M. G., Decensi A., Costa A. and Veronesi U. (2001) Safety of the synthetic retinoid fenretinide: long-term results from a controlled clinical trial for the prevention of contralateral breast cancer. J. Clin. Oncol. 19, 1664-1670.
3. Chambon P. (1994) The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol. 5, 115-125.
4. Chen S., Samuel W., Fariss R. N., Duncan T., Kutty R. K. and Wiggert B. (2003) Differentiation of human retinal pigment epithelial cells into neuronal phenotype by N-(4-hydroxyphenyl)retinamide. J. Neurochem. 84, 972-981.
5. Clifford J. L., Menter D. G., Wang M., Lotan R. and Lippman S. M. (1999) Retinoid receptor-dependent and -independent effects of N- (4-hydroxyphenyl) retinamide in F9 embryonal carcinoma cells. Cancer Res. 59, 14-18.
6. Cowan K. J. and Storey K. B. (2003) Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J. Exp. Biol. 206, 1107-1115.
7. Dmitrovsky E. (1997) N-(4-hydroxyphenyl)retinamide activation of a distinct pathway signaling apoptosis. J. Natl Cancer Inst. 89, 1179-1181.
8. Dunn K. C., Aotaki-Keen A. E., Putkey F. R. and Hjelmeland L. M. (1996) ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62, 155-169.
9. Dutt K., Scott M., Sternberg P. P., Linser P. J. and Srinivasan A. (1993) Transdifferentiation of adult human pigment epithelium into retinal cells by transfection with an activated H-ras proto-oncogene. DNA Cell Biol. 12, 667-673.
10. Favata M. F., Horiuchi K. Y., Manos E. J. et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632.
11. Finnemann S. C., Bonilha V. L., Marmorstein A. D. and Rodriguez- Boulan E. (1997) Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc. Natl Acad. Sci. USA 94, 12932-12937.
12. Fischer A. J. and Reh T. A. (2001) Transdifferentiation of pigmented epithelial cells: a source of retinal stem cells? Dev. Neurosci. 23, 268-276.
13. Guan K., Chang H., Rolletschek A. and Wobus A. M. (2001) Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res. 305, 171-176.
14. Hirai S., Izawa M., Osada S., Spyrou G. and Ohno S. (1996) Activation of the JNK pathway by distantly related protein kinases, MEKK and MUK. Oncogene 12, 641-650.
15. Holtkamp G. M., Van Rossem M., de Vos A. F., Willekens B., Peek R. and Kijlstra A. (1998) Polarized secretion of IL-6 and IL-8 by human retinal pigment epithelial cells. Clin. Exp. Immunol. 112, 34-43.
16. Ikegami Y., Mitsuda S. and Araki M. (2002) Neural cell differentiation from retinal pigment epithelial cells of the newt: an organ culture model for the urodele retinal regeneration. J. Neurobiol. 50, 209-220.
17. Karin M. (1995) The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270, 16483-16486.
18. Kutty R. K., Kutty G., Samuel W., Duncan T., Bridges C. C., El-Sherbeeny A., Nagineni C. N., Smith S. B. and Wiggert B. (2001) Molecular characterization and developmental expression of NORPEG, a novel gene induced by retinoic acid. J. Biol. Chem. 276, 2831-2840.
19. Leppa S. and Bohmann D. (1999) Diverse functions ofJNK signaling and c-jun in stress response and apoptosis. Oncogene 18, 6158-6162.
20. Leppa S., Saffrich R., Ansorge W. and Bohmann D. (1998) Differential regulation of c-jun by ERK and JNK during PC12 cell differentiation. EMBO J. 17, 4404-4413.
21. Li Z., Theus M. H. and Wei L. (2006) Role of ERK 1/2 signaling in neuronal differentiation of cultured embryonic stem cells. Dev. Growth Differ. 48, 513-523.
22. Luo J., Kintner D. B., Shull G. E. and Sun D. (2007) ERK1/2-p90RSK- mediated phosphorylation of Na+/H+ exchanger isoform 1. A role in ischemic neuronal death. J. Biol. Chem. 282, 28274-28284.
23. Malone W., Perloff M., Crowell J., Sigman C. and Higley H. (2003) Fenretinide: a prototype cancer prevention drug. Expert Opin. Investig. Drugs, 12, 1829-1842.
24. McCubrey J. A., Steelman L. S., Abrams S. L. et al. (2006) Roles ofthe RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv. Enzyme Regul. 46, 249-279.
25. Monje P., Marinissen M. J. and Gutkind J. S. (2003) Phosphorylation of the carboxyl-terminal transactivation domain of c-fos by extracellular signal-regulated kinase mediates the transcriptional activation of AP-1 and cellular transformation induced by platelet-derived growth factor. Mol. Cell. Biol. 23, 7030-7043.
26. Moor A. N., Gan X. T., Karmazyn M. and Fliegel L. (2001) Activation of Na+/H+ exchanger-directed protein kinases in the ischemic and ischemic-reperfused rat myocardium. J. Biol. Chem. 276, 16113-16122.
27. Morooka T. and Nishida E. (1998) Requirement of p38 mitogen-acti- vated protein kinase for neuronal differentiation in PC12 cells. J. Biol. Chem. 273, 24285-24288.
28. Munch G., Gasic-Milenkovic J., Dukic-Stefanovic S., Kuhla B., Hein- rich K., Riederer P., Huttunen H. J., Founds H. and Sajithlal G. (2003) Microglial activation induces cell death, inhibits neurite outgrowth and causes neurite retraction of differentiated neuro- blastoma cells. Exp. Brain Res. 150, 1-8.
29. Nag T. C. and Wadhwa S. (1999) Developmental expression of cal- retinin immunoreactivity in the human retina and a comparison with two other EF-hand calcium binding proteins. Neuroscience 91, 41-50.
30. Pang L., Sawada T., Decker S. J. and Saltiel A. R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588.
31. Pearson G., Robinson F., Beers Gibson T., Xu B. E., Karandikar M., Berman K. and Cobb M. H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183.
32. Pittack C., Jones M. and Reh T. A. (1991) Basic fibroblast growth factor induces retinal pigment epithelium to generate neural retina in vitro. Development 113, 577-588.
33. Pochet R., Blachier F., Malaisse W., Parmentier M., Pasteels B., Pohl V., Resibois A., Rogers J. and Roman A. (1989) Calbindin-D28 in mammalian brain, retina, and endocrine pancreas: immunohisto- chemical comparison with calretinin. Adv. Exp. Med. Biol. 255, 435-443.
34. Radu R. A., Han Y., Bui T. V., Nusinowitz S., Bok D., Lichter J., Widder K., Travis G. H. and Mata N. L. (2005) Reductions in serum vitamin A arrest accumulation of toxic retinal fluorophores: a potential therapy for treatment of lipofuscin-based retinal diseases. Invest. Ophthalmol. Vis. Sci. 46, 4393-4401.
35. Robinson M. J., Stippec S. A., Goldsmith E., White M. A. and Cobb M. H. (1998) A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transfor mation. Curr. biol. 8, 1141-1150
36. Sabichi A L., Hendricks D T., Bober M A and Birrer M J (1998) Retinoic acid receptor beta expression and growth inhibition of gynecologic cancer cells by the synthetic retinoid N-(4-hydroxy- phenyl) retinamide J Natl Cancer Inst 90, 597-605
37. Samuel W., Kutty R K., Nagineni S., Gordon J S., Prouty S M., Chandraratna R A and Wiggert B (2001) Regulation of stearoyl coenzyme A desaturase expression in human retinal pigment epithelial cells by retinoic acid J Biol Chem 276, 28744-28750
38. Samuel W., Nagineni C. N., Kutty R. K., Parks W. T., Gordon J. S., Prouty S. M., Hooks J. J. and Wiggert B. (2002) Transforming growth factor-beta regulates stearoyl coenzyme A desaturase expression through a Smad signaling pathway. J Biol Chem 277, 59-66.
39. Samuel W., Kutty R. K., Nagineni S., Vijayasarathy C., Chandraratna R. A. and Wiggert B. (2006) N-(4-hydroxyphenyl)retinamide induces apoptosis in human retinal pigment epithelial cells: retinoic acid receptors regulate apoptosis, reactive oxygen species generation, and the expression of heme oxygenase-1 and Gadd153. J Cell Physiol 209, 854-865.
40. Shaulian E. and Karin M. (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4, E131-E136.
41. Singh U. S., Pan J., Kao Y. L., Joshi S., Young K. L. and Baker K. M. (2003) Tissue transglutaminase mediates activation of RhoA and MAP kinase pathways during retinoic acid-induced neuronal differentiation of SH-SY5Y cells. J Biol Chem 278, 391-399.
42. Tiwari M., Kumar A., Sinha R. A. et al (2006) Mechanism of 4-HPR-induced apoptosis in glioma cells: evidences suggesting role of mitochondrial-mediated pathway and endoplasmic reticulum stress. Carcinogenesis 27, 2047-2058.
43. Waetzig V. and Herdegen T. (2003) The concerted signaling of ERK1/ 2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins. Mol Cell Neurosci 24, 238-249.
44. Wang X., Fu S., Wang Y., Yu P., Hu J., Gu W., Xu X. M. and Lu P. (2007) Interleukin-1beta mediates proliferation and differentiation of multipotent neural precursor cells through the activation of SAPK/JNK pathway. Mol Cell Neurosci 36, 343-354.
45. Whitmarsh A. J. and Davis R. J. (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74, 589-607.
46. Yan R. T., Ma W. X. and Wang S. Z. (2001) Neurogenin2 elicits the genesis of retinal neurons from cultures of nonneural cells. Proc Natl Acad. Sci. USA 98, 15014-15019.
47. Yu Y. M., Han P. L. and Lee J. K. (2003) JNK pathway is required for retinoic acid-induced neurite outgrowth of human neuroblastoma, SH-SY5Y. Neuroreport 14, 941-945.
48. Zentrich E., Han S. Y., Pessoa-Brandao L., Butterfield L. and Heasley L. E. (2002) Collaboration of JNKs and ERKs in nerve growth factor regulation of the neurofilament light chain promoter in PC12 cells. J. Biol. Chem. 277, 4110-4118.
49. Zhao S., Rizzolo L. J. and Barnstable C. J. (1997) Differentiation and transdifferentiation of the retinal pigment epithelium. Int. Rev. Cytol. 171, 225-266.
50. Zheng J. Q. and Poo M. M. (2007) Calcium signaling in neuronal motility. Annu. Rev. Cell Dev. Biol. 23, 375-404.