A high-content imaging-based screening pipeline for the systematic identification of anti-progeroid compounds

Methods

Volumn 96, Issue , 2016, Pages 46-58

  Kubben, Nard ^a   Brimacombe, Kyle R ^b   Donegan, Megan ^a   Li, Zhuyin ^b,c   Misteli, Tom ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

FDA approved compounds; HGPS; High content imaging; High throughput screening; Progerin; Retinoids

Indexed keywords

2 [[2 [[2 [(2 AMINO 3 MERCAPTOPROPYL)AMINO] 3 METHYLPENTYL]OXY] 1 OXO 3 PHENYLPROPYL]AMINO] 4 (METHYLSULFONYL)BUTANOIC ACID ISOPROPYL ESTER; ADRENERGIC RECEPTOR STIMULATING AGENT; ANTI PROGEROID COMPOUND; CHEMICAL COMPOUND; CORTICOSTEROID; DEFLAZACORT; DIFLUCORTOLONE VALERATE; DOXOFYLLINE; DOXYCYCLINE; FLUDROCORTISONE ACETATE; HYDROCORTISONE SODIUM SUCCINATE; ISOPRENALINE; ISOTRETINOIN; LAMIN A; MEPREDNISONE; MILRINONE; MUTANT PROTEIN; NUCLEAR PROTEIN; PHOSPHODIESTERASE INHIBITOR; PREDNISOLONE ACETATE; PROCATEROL; PROGERIN; RESOCORTOL BUTYRATE; RETINOID; RIMEXOLONE; SALBUTAMOL SULFATE; TAZAROTENE; TREQUINSIN; TRIAMCINOLONE ACETONIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; CBX3 PROTEIN, HUMAN; H2AFX PROTEIN, HUMAN; HISTONE; LAMIN B; LAMIN B1; MOLECULAR LIBRARY; NONHISTONE PROTEIN; PRELAMIN A; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN; TUMOR SUPPRESSOR P53 BINDING PROTEIN 1;

ARTICLE; DNA DAMAGE; DRUG DEVELOPMENT; EPIGENETICS; HIGH CONTENT IMAGING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; HUTCHINSON GILFORD PROGERIA SYNDROME; IMAGING; MOLECULAR LIBRARY; PREMATURE AGING; PRIORITY JOURNAL; SKIN FIBROBLAST; ANTAGONISTS AND INHIBITORS; CELL AGING; CELL NUCLEUS; CHEMISTRY; DRUG EFFECTS; FIBROBLAST; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOLECULAR IMAGING; PATHOLOGY; PHARMACOLOGY; PLASMID; PRIMARY CELL CULTURE; PROCEDURES; PROGERIA; TRANSFORMED CELL LINE; ULTRASTRUCTURE;

CELL AGING; CELL LINE, TRANSFORMED; CELL NUCLEUS; CHROMOSOMAL PROTEINS, NON-HISTONE; EPIGENESIS, GENETIC; FIBROBLASTS; HIGH-THROUGHPUT SCREENING ASSAYS; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LAMIN TYPE A; LAMIN TYPE B; MOLECULAR IMAGING; PLASMIDS; PRIMARY CELL CULTURE; PROGERIA; RETINOIDS; SMALL MOLECULE LIBRARIES; TRANSFECTION; TUMOR SUPPRESSOR P53-BINDING PROTEIN 1;

EID: 84958174324     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2015.08.024     Document Type: Article

References (54)

1. Adam S.A., Butin-Israeli V., Cleland M.M., Shimi T., Goldman R.D. Disruption of lamin B1 and lamin B2 processing and localization by farnesyltransferase inhibitors. Nucleus 2013, 4:142-150.
2. Boisvert F.M., Ahmad Y., Gierlinski M., Charriere F., Lamont D., Scott M., Barton G., Lamond A.I. A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell. Proteomics: MCP 2012, 11(M111):011429.
3. Bosch-Presegue L., Raurell-Vila H., Marazuela-Duque A., Kane-Goldsmith N., Valle A., Oliver J., Serrano L., Vaquero A. Stabilization of Suv39H1 by SirT1 is part of oxidative stress response and ensures genome protection. Mol. Cell 2011, 42:210-223.
4. Broers J.L., Hutchison C.J., Ramaekers F.C. Laminopathies. J. Pathol. 2004, 204:478-488.
5. Burtner C.R., Kennedy B.K. Progeria syndromes and ageing: what is the connection?. Nat. Rev. Mol. Cell Biol. 2010, 11:567-578.
6. Campeau E., Ruhl V.E., Rodier F., Smith C.L., Rahmberg B.L., Fuss J.O., Campisi J., Yaswen P., Cooper P.K., Kaufman P.D. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009, 4:e6529.
7. Cao K., Graziotto J.J., Blair C.D., Mazzulli J.R., Erdos M.R., Krainc D., Collins F.S. Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci. Transl. Med. 2011, 3:89ra58.
8. Das B.C., Tang X.Y., Evans T. Design and synthesis of boron containing potential pan-RAR inverse agonists. Tetrahedron Lett. 2012, 53:1316-1318.
9. Dittmer T.A., Sahni N., Kubben N., Hill D.E., Vidal M., Burgess R.C., Roukos V., Misteli T. Systematic identification of pathological lamin A interactors. Mol. Biol. Cell 2014, 25:1493-1510.
10. Finley J. Alteration of splice site selection in the LMNA gene and inhibition of progerin production via AMPK activation. Med. Hypotheses 2014, 83:580-587.
11. Fong L.G., Ng J.K., Lammerding J., Vickers T.A., Meta M., Cote N., Gavino B., Qiao X., Chang S.Y., Young S.R., et al. Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J. Clin. Invest. 2006, 116:743-752.
12. Funkhouser C.M., Sknepnek R., Shimi T., Goldman A.E., Goldman R.D., Olvera de la Cruz M. Mechanical model of blebbing in nuclear lamin meshworks. Proc. Natl. Acad. Sci. U.S.A 2013, 110:3248-3253.
13. Gerhart-Hines Z., Dominy J.E., Blattler S.M., Jedrychowski M.P., Banks A.S., Lim J.H., Chim H., Gygi S.P., Puigserver P. The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Mol. Cell 2011, 44:851-863.
14. Gonzalez J.M., Pla D., Perez-Sala D., Andres V. A-type lamins and Hutchinson-Gilford progeria syndrome: pathogenesis and therapy. Front. Biosci. (Scholar Ed.) 2011, 3:1133-1146.
15. Gordon L.B., Kleinman M.E., Miller D.T., Neuberg D.S., Giobbie-Hurder A., Gerhard-Herman M., Smoot L.B., Gordon C.M., Cleveland R., Snyder B.D., et al. Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A 2012, 109:16666-16671.
16. Gordon L.B., Rothman F.G., Lopez-Otin C., Misteli T. Progeria: a paradigm for translational medicine. Cell 2014, 156:400-407.
17. Huang R., Southall N., Wang Y., Yasgar A., Shinn P., Jadhav A., Nguyen D.T., Austin C.P. The NCGC pharmaceutical collection: a comprehensive resource of clinically approved drugs enabling repurposing and chemical genomics. Sci. Transl. Med. 2011, 3:80ps16.
18. Kubben N., Adriaens M., Meuleman W., Voncken J.W., van Steensel B., Misteli T. Mapping of lamin A- and progerin-interacting genome regions. Chromosoma 2012, 121:447-464.
19. Kubben N., Voncken J.W., Konings G., van Weeghel M., van den Hoogenhof M.M., Gijbels M., van Erk A., Schoonderwoerd K., van den Bosch B., Dahlmans V., et al. Post-natal myogenic and adipogenic developmental: defects and metabolic impairment upon loss of A-type lamins. Nucleus 2011, 2:195-207.
20. Kudlow B.A., Kennedy B.K., Monnat R.J. Werner and Hutchinson-Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat. Rev. Mol. Cell Biol. 2007, 8:394-404.
21. Laberge R.M., Zhou L., Sarantos M.R., Rodier F., Freund A., de Keizer P.L., Liu S., Demaria M., Cong Y.S., Kapahi P., et al. Glucocorticoids suppress selected components of the senescence-associated secretory phenotype. Aging Cell 2012, 11:569-578.
22. Larrieu D., Britton S., Demir M., Rodriguez R., Jackson S.P. Chemical inhibition of NAT10 corrects defects of laminopathic cells. Science 2014, 344:527-532.
23. Liu B., Ghosh S., Yang X., Zheng H., Liu X., Wang Z., Jin G., Zheng B., Kennedy B.K., Suh Y., et al. Resveratrol rescues SIRT1-dependent adult stem cell decline and alleviates progeroid features in laminopathy-based progeria. Cell Metab. 2012, 16:738-750.
24. Liu B., Wang Z., Zhang L., Ghosh S., Zheng H., Zhou Z. Depleting the methyltransferase Suv39h1 improves DNA repair and extends lifespan in a progeria mouse model. Nat. Commun. 2013, 4:1868.
25. Liu Y., Rusinol A., Sinensky M., Wang Y., Zou Y. DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J. Cell Sci. 2006, 119:4644-4649.
26. Liu Y., Wang Y., Rusinol A.E., Sinensky M.S., Liu J., Shell S.M., Zou Y. Involvement of xeroderma pigmentosum group A (XPA) in progeria arising from defective maturation of prelamin A. FASEB J. 2008, 22:603-611.
27. Lopez-Mejia I.C., de Toledo M., Chavey C., Lapasset L., Cavelier P., Lopez-Herrera C., Chebli K., Fort P., Beranger G., Fajas L., et al. Antagonistic functions of LMNA isoforms in energy expenditure and lifespan. EMBO Rep. 2014, 15:529-539.
28. Miwako I., Kagechika H. Tamibarotene. Drugs Today 2007, 43:563-568. (Barcelona, Spain: 1998).
29. Moise A.R. Pharmacology of Retinoid Receptors. Tocris Biosci. Sci. Rev. Ser. 2014, 1-12.
30. Musich P.R., Zou Y. Genomic instability and DNA damage responses in progeria arising from defective maturation of prelamin A. Aging 2009, 1:28-37.
31. Osorio F.G., Barcena C., Soria-Valles C., Ramsay A.J., de Carlos F., Cobo J., Fueyo A., Freije J.M., Lopez-Otin C. Nuclear lamina defects cause ATM-dependent NF-kappaB activation and link accelerated aging to a systemic inflammatory response. Genes Dev. 2012, 26:2311-2324.
32. Park S.J., Ahmad F., Philp A., Baar K., Williams T., Luo H., Ke H., Rehmann H., Taussig R., Brown A.L., et al. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 2012, 148:421-433.
33. Pegoraro G., Kubben N., Wickert U., Gohler H., Hoffmann K., Misteli T. Ageing-related chromatin defects through loss of the NURD complex. Nat. Cell Biol. 2009, 11:1261-1267.
34. Pegoraro G., Voss T.C., Martin S.E., Tuzmen P., Guha R., Misteli T. Identification of mammalian protein quality control factors by high-throughput cellular imaging. PLoS One 2012, 7:e31684.
35. Pelz O., Gilsdorf M., Boutros M. Web cellHTS2: a web-application for the analysis of high-throughput screening data. BMC Bioinf. 2010, 11:185.
36. Price N.L., Gomes A.P., Ling A.J., Duarte F.V., Martin-Montalvo A., North B.J., Agarwal B., Ye L., Ramadori G., Teodoro J.S., et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012, 15:675-690.
37. Prokocimer M., Barkan R., Gruenbaum Y. Hutchinson-Gilford progeria syndrome through the lens of transcription. Aging Cell 2013, 12:533-543.
38. Rennel E., Gerwins P. How to make tetracycline-regulated transgene expression go on and off. Anal. Biochem. 2002, 309:79-84.
39. Richards S.A., Muter J., Ritchie P., Lattanzi G., Hutchison C.J. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N-acetyl cysteine. Hum. Mol. Genet. 2011, 20:3997-4004.
40. Roukos V., Voss T.C., Schmidt C.K., Lee S., Wangsa D., Misteli T. Spatial dynamics of chromosome translocations in living cells. Science 2013, 341:660-664.
41. Sadaie M., Salama R., Carroll T., Tomimatsu K., Chandra T., Young A.R., Narita M., Perez-Mancera P.A., Bennett D.C., Chong H., et al. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev. 2013, 27:1800-1808.
42. Scaffidi P., Misteli T. Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 2005, 11:440-445.
43. Scaffidi P., Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006, 312:1059-1063.
44. Scaffidi P., Misteli T. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat. Cell Biol. 2008, 10:452-459.
45. Shah P.P., Donahue G., Otte G.L., Capell B.C., Nelson D.M., Cao K., Aggarwala V., Cruickshanks H.A., Rai T.S., McBryan T., et al. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev. 2013, 27:1787-1799.
46. Sullivan T., Escalante-Alcalde D., Bhatt H., Anver M., Bhat N., Nagashima K., Stewart C.L., Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 1999, 147:913-920.
47. Swift J., Ivanovska I.L., Buxboim A., Harada T., Dingal P.C., Pinter J., Pajerowski J.D., Spinler K.R., Shin J.W., Tewari M., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341:1240104.
48. Toth J.I., Yang S.H., Qiao X., Beigneux A.P., Gelb M.H., Moulson C.L., Miner J.H., Young S.G., Fong L.G. Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc. Natl. Acad. Sci. U.S.A 2005, 102:12873-12878.
49. Villa-Bellosta R., Rivera-Torres J., Osorio F.G., Acin-Perez R., Enriquez J.A., Lopez-Otin C., Andres V. Defective extracellular pyrophosphate metabolism promotes vascular calcification in a mouse model of Hutchinson-Gilford progeria syndrome that is ameliorated on pyrophosphate treatment. Circulation 2013, 127:2442-2451.
50. P.S. Walker, Tazarotene in the treatment of psoriasis FDA advisory committee meeting. <>, 2004. http://www.fda.gov/ohrms/dockets/ac/04/slides/2004-4062S1_02_Allergan-Presentation.ppt.
51. Wang R.H., Sengupta K., Li C., Kim H.S., Cao L., Xiao C., Kim S., Xu X., Zheng Y., Chilton B., et al. Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice. Cancer Cell 2008, 14:312-323.
52. Yang S.H., Chang S.Y., Ren S., Wang Y., Andres D.A., Spielmann H.P., Fong L.G., Young S.G. Absence of progeria-like disease phenotypes in knock-in mice expressing a non-farnesylated version of progerin. Hum. Mol. Genet. 2011, 20:436-444.
53. Yang S.H., Meta M., Qiao X., Frost D., Bauch J., Coffinier C., Majumdar S., Bergo M.O., Young S.G., Fong L.G. A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J. Clin. Invest. 2006, 116:2115-2121.
54. Yang S.H., Qiao X., Farber E., Chang S.Y., Fong L.G., Young S.G. Eliminating the synthesis of mature lamin A reduces disease phenotypes in mice carrying a Hutchinson-Gilford progeria syndrome allele. J. Biol. Chem. 2008, 283:7094-7099.