Mammalian STE20-like kinase 2, not kinase 1, mediates photoreceptor cell death during retinal detachment

Cell Death and Disease

Volumn 5, Issue , 2014, Pages

  Matsumoto, H ^a   Murakami, Y ^a   Kataoka, K ^a   Lin, H ^a   Connor, K M ^a   Miller, J W ^a   Zhou, D ^b   Avruch, J ^c   Vavvas, D G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b XIAMEN UNIVERSITY   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

apoptosis; mammalian STE20 like kinase; neurodegeneration; retinal detachment photoreceptor cell

Indexed keywords

CASPASE 3; CD11B ANTIGEN; CYTOCHROME C; FAS ANTIGEN; INHIBITOR OF APOPTOSIS PROTEIN; INTERLEUKIN 6; MAMMALIAN STE20 LIKE KINASE 1; MAMMALIAN STE20 LIKE KINASE 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN BAX; PROTEIN P73; PUMA PROTEIN; SURVIVIN; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; CASP3 PROTEIN, MOUSE; MST2 PROTEIN, MOUSE; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; STK4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DENSITY; CELL INFILTRATION; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RETINA DETACHMENT; UPREGULATION; WESTERN BLOTTING; ANIMAL; APOPTOSIS; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; CASPASE 3; MICE; MICE, KNOCKOUT; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN-SERINE-THREONINE KINASES; RETINAL DETACHMENT; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84904006974     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.218     Document Type: Article

References (67)

1. Trichonas G, Murakami Y, Thanos A, Morizane Y, Kayama M, Debouck CM et al. Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc Natl Acad Sci USA 2010; 107: 21695-21700.
2. Zacks DN, Zheng QD, Han Y, Bakhru R, Miller JW. FAS-mediated apoptosis and its relation to intrinsic pathway activation in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci 2004; 45: 4563-4569.
3. Zacks DN, Boehlke C, Richards AL, Zheng QD. Role of the Fas-signaling pathway in photoreceptor neuroprotection. Arch Ophthalmol 2007; 125: 1389-1395.
4. Besirli CG, Chinskey ND, Zheng QD, Zacks DN. Inhibition of retinal detachment-induced apoptosis in photoreceptors by a small peptide inhibitor of the fas receptor. Invest Ophthalmol Vis Sci 2010; 51: 2177-2184.
5. Dunaief JL, Dentchev T, Ying GS, Milam AH. The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 2002; 120: 1435-1442.
6. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 1998; 102: 783-791.
7. Hellstrom A, Smith LE, Dammann O. Retinopathy of prematurity. Lancet 2013; 382: 1445-1457.
8. Mitry D, Fleck BW, Wright AF, Campbell H, Charteris DG. Pathogenesis of rhegmatogenous retinal detachment: predisposing anatomy and cell biology. Retina 2010; 30: 1561-1572.
9. Arroyo JG, Yang L, Bula D, Chen DF. Photoreceptor apoptosis in human retinal detachment. Am J Ophthalmol 2005; 139: 605-610.
10. Campo RV, Sipperley JO, Sneed SR, Park DW, Dugel PU, Jacobsen J et al. Pars plana vitrectomy without scleral buckle for pseudophakic retinal detachments. Ophthalmology 1999; 106: 1811-1815; discussion 1816.
11. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003; 114: 457-467.
12. Pan D. Hippo signaling in organ size control. Genes Dev 2007; 21: 886-897.
13. Zeng Q, Hong W. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 2008; 13: 188-192.
14. Kango-Singh M, Singh A. Regulation of organ size: insights from the Drosophila Hippo signaling pathway. Dev Dyn 2009; 238: 1627-1637.
15. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010; 24: 862-874.
16. Avruch J, Zhou D, Fitamant J, Bardeesy N. Mst1/2 signalling to Yap: gatekeeper for liver size and tumour development. Br J Cancer 2011; 104: 24-32.
17. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007; 21: 2747-2761.
18. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 2008; 283: 5496-5509.
19. Zhang J, Smolen GA, Haber DA. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res 2008; 68: 2789-2794.
20. Vassilev A, Kaneko KJ, Shu H, Zhao Y, DePamphilis ML. TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev 2001; 15: 1229-1241.
21. Zhao B, Ye X, Yu J, Li L, Li W, Li S et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 2008; 22: 1962-1971.
22. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, Silke J et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 2006; 125: 1253-1267.
23. Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC et al. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci USA 2006; 103: 12405-12410.
24. Zhou D, Conrad C, Xia F, Park JS, Payer B, Yin Y et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16: 425-438.
25. Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci USA 2010; 107: 1431-1436.
26. Lu L, Li Y, Kim SM, Bossuyt W, Liu P, Qiu Q et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci USA 2010; 107: 1437-1442.
27. Strano S, Monti O, Pediconi N, Baccarini A, Fontemaggi G, Lapi E et al. The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA Damage. Mol Cell 2005; 18: 447-459.
28. Matallanas D, Romano D, Yee K, Meissl K, Kucerova L, Piazzolla D et al. RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol Cell 2007; 27: 962-975.
29. Lapi E, Di Agostino S, Donzelli S, Gal H, Domany E, Rechavi G et al. PML, YAP, and p73 are components of a proapoptotic autoregulatory feedback loop. Mol Cell 2008; 32: 803-814.
30. Downward J, Basu S. YAP and p73: a complex affair. Mol Cell 2008; 32: 749-750.
31. Romano D, Matallanas D, Weitsman G, Preisinger C, Ng T, Kolch W. Proapoptotic kinase MST2 coordinates signaling crosstalk between RASSF1A, Raf-1, and Akt. Cancer Res 2010; 70: 1195-1203.
32. Khokhlatchev A, Rabizadeh S, Xavier R, Nedwidek M, Chen T, Zhang XF et al. Identification of a novel Ras-regulated proapoptotic pathway. Curr Biol 2002; 12: 253-265.
33. Praskova M, Khoklatchev A, Ortiz-Vega S, Avruch J. Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins, RASSF1 and NORE1, and by Ras. Biochem J 2004; 381: 453-462.
34. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB et al. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 2006; 125: 987-1001.
35. Yuan Z, Lehtinen MK, Merlo P, Villen J, Gygi S, Bonni A. Regulation of neuronal cell death by MST1-FOXO1 signaling. J Biol Chem 2009; 284: 11285-11292.
36. Liu W, Wu J, Xiao L, Bai Y, Qu A, Zheng Z et al. Regulation of neuronal cell death by c-Abl-Hippo/MST2 signaling pathway. PLoS One 2012; 7: e36562.
37. Lee JK, Shin JH, Hwang SG, Gwag BJ, McKee AC, Lee J et al. MST1 functions as a key modulator of neurodegeneration in a mouse model of ALS. Proc Natl Acad Sci USA 2013; 110: 12066-12071.
38. Matsumoto H, Miller JW, Vavvas DG. Retinal detachment model in rodents by subretinal injection of sodium hyaluronate. J Vis Exp 2013; (79): doi:10.3791/50660.
39. Melino G, Bernassola F, Ranalli M, Yee K, Zong WX, Corazzari M et al. p73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J Biol Chem 2004; 279: 8076-8083.
40. Schilling T, Schleithoff ES, Kairat A, Melino G, Stremmel W, Oren M et al. Active transcription of the human FAS/CD95/TNFRSF6 gene involves the p53 family. Biochem Biophys Res Commun 2009; 387: 399-404.
41. Da CL, Xin Y, Zhao J, Luo XD. Significance and relationship between Yes-associated protein and survivin expression in gastric carcinoma and precancerous lesions. World J Gastroenterol 2009; 15: 4055-4061.
42. Avruch J, Zhou D, Bardeesy N. YAP oncogene overexpression supercharges colon cancer proliferation. Cell Cycle 2012; 11: 1090-1096.
43. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H et al. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci USA 2007; 104: 2425-2430.
44. Zacks DN, Han Y, Zeng Y, Swaroop A. Activation of signaling pathways and stress-response genes in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci 2006; 47: 1691-1695.
45. Fisher SK, Erickson PA, Lewis GP, Anderson DH. Intraretinal proliferation induced by retinal detachment. Invest Ophthalmol Vis Sci 1991; 32: 1739-1748.
46. Fisher SK, Lewis GP, Linberg KA, Barawid E, Verardo MR. Cellular Remodeling in Mammalian Retina Induced by Retinal Detachment. In: Kolb H, Fernandez E, Nelson R (eds). The Organization of the Retina and Visual System. University of Utah Health Sciences Center: Salt Lake City (UT), 1995.
47. Lewis GP, Matsumoto B, Fisher SK. Changes in the organization and expression of cytoskeletal proteins during retinal degeneration induced by retinal detachment. Invest Ophthalmol Vis Sci 1995; 36: 2404-2416.
48. Lewis GP, Sethi CS, Carter KM, Charteris DG, Fisher SK. Microglial cell activation following retinal detachment: a comparison between species. Mol Vis 2005; 11: 491-500.
49. Sethi CS, Lewis GP, Fisher SK, Leitner WP, Mann DL, Luthert PJ et al. Glial remodeling and neural plasticity in human retinal detachment with proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 2005; 46: 329-342.
50. Creasy CL, Chernoff J. Cloning and characterization of a member of the MST subfamily of Ste20-like kinases. Gene 1995; 167: 303-306.
51. Kim D, Shu S, Coppola MD, Kaneko S, Yuan ZQ, Cheng JQ. Regulation of proapoptotic mammalian ste20-like kinase MST2 by the IGF1-Akt pathway. PLoS One 2010; 5: e9616.
52. Zhou Y, Callendret B, Xu D, Brasky KM, Feng Z, Hensley LL et al. Dominance of the CD4(+) T helper cell response during acute resolving hepatitis A virus infection. JExp Med 2012; 209: 1481-1492.
53. O'Neill E, Rushworth L, Baccarini M, Kolch W. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1. Science 2004; 306: 2267-2270.
54. Chen J, Fujii K, Zhang L, Roberts T, Fu H. Raf-1 promotes cell survival by antagonizing apoptosis signal-regulating kinase 1 through a MEK-ERK independent mechanism. Proc Natl Acad Sci USA 2001; 98: 7783-7788.
55. Ehrenreiter K, Piazzolla D, Velamoor V, Sobczak I, Small JV, Takeda J et al. Raf-1 regulates Rho signaling and cell migration. J Cell Biol 2005; 168: 955-964.
56. Niault T, Sobczak I, Meissl K, Weitsman G, Piazzolla D, Maurer G et al. From autoinhibition to inhibition in trans: the Raf-1 regulatory domain inhibits Rok-alpha kinase activity. J Cell Biol 2009; 187: 335-342.
57. Roh MI, Murakami Y, Thanos A, Vavvas DG, Miller JW. Edaravone an ROS scavenger, ameliorates photoreceptor cell death after experimental retinal detachment. Invest Ophthalmol Vis Sci 2011; 52: 3825-3831.
58. Mantopoulos D, Murakami Y, Comander J, Thanos A, Roh M, Miller JW et al. Tauroursodeoxycholic acid (TUDCA) protects photoreceptors from cell death after experimental retinal detachment. PLoS One 2011; 6: e24245.
59. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002; 23: 549-555.
60. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010; 32: 593-604.
61. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
62. Murakami Y, Matsumoto H, Roh M, Suzuki J, Hisatomi T, Ikeda Y et al. Receptor interacting protein kinase mediates necrotic cone but not rod cell death in a mouse model of inherited degeneration. Proc Natl Acad Sci USA 2012; 109: 14598-14603.
63. Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, Lukacs NW et al. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 2008; 205: 2609-2621.
64. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318-1321.
65. Murakami Y, Matsumoto H, Roh M, Giani A, Kataoka K, Morizane Y et al. Programmed necrosis, not apoptosis, is a key mediator of cell loss and DAMP-mediated inflammation in dsRNA-induced retinal degeneration. Cell Death Differ 2014; 21: 270-277.
66. Taylor KR, Yamasaki K, Radek KA, Di Nardo A, Goodarzi H, Golenbock D et al. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J Biol Chem 2007; 282: 18265-18275.
67. Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E et al. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 2009; 15: 774-780.