The epigenetic promotion of osteogenic differentiation of human adipose-derived stem cells by the genetic and chemical blockade of histone demethylase LSD1

Biomaterials

Volumn 35, Issue 23, 2014, Pages 6015-6025

  Ge, Wenshu ^a   Liu, Yunsong ^a   Chen, Tong ^a   Zhang, Xiao ^a   Lv, Longwei ^a   Jin, Chanyuan ^a   Jiang, Yong ^a   Shi, Lei ^b   Zhou, Yongsheng ^a  

^a PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Epigenetic drug; Histone methylation; Human adipose derived stem cells; Lysine specific demethylase 1; Osteogenic differentiation

Indexed keywords

ALKYLATION; AMINO ACIDS; BONE; GENE EXPRESSION; TISSUE ENGINEERING;

ADIPOSE DERIVED STEM CELLS; DEMETHYLASE; EPIGENETIC DRUG; HISTONE METHYLATION; OSTEOGENIC DIFFERENTIATION;

STEM CELLS;

HISTONE; HISTONE DEMETHYLASE; LYSINE DERIVATIVE; LYSINE SPECIFIC DEMETHYLASE 1; METHYL HISTONE H3 LYSINE 4; UNCLASSIFIED DRUG; KDM1A PROTEIN, HUMAN;

ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE TISSUE; CELL DIFFERENTIATION; CELL FATE; CELL THERAPY; CONTROLLED STUDY; DEMETHYLATION; ENZYME ACTIVITY; ENZYME MECHANISM; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN CELL; LENTIVIRINAE; MALE; MOUSE; NONHUMAN; OSTEOGENIC DIFFERENTIATION; PRIORITY JOURNAL; TISSUE ENGINEERING; XENOGRAFT; ADIPOCYTE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENETIC ENHANCEMENT; GENETIC EPIGENESIS; GENETICS; NUDE MOUSE; OSTEOBLAST; PHYSIOLOGY; PROCEDURES; STEM CELL; TISSUE SCAFFOLD;

ADIPOCYTES; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EPIGENESIS, GENETIC; GENETIC ENHANCEMENT; HISTONE DEMETHYLASES; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; OSTEOBLASTS; OSTEOGENESIS; STEM CELLS; TISSUE SCAFFOLDS;

EID: 84900015789     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.04.055     Document Type: Article

References (56)

1. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002, 13:4279-4295.
2. Levi B., James A.W., Nelson E.R., Li S., Peng M., Commons G.W., et al. Human adipose-derived stromal cells stimulate autogenous skeletal repair via paracrine Hedgehog signaling with calvarial osteoblasts. Stem Cells Dev 2011, 20:243-257.
3. De Toni F., Poglio S., Youcef A.B., Cousin B., Pflumio F., Bourin P., et al. Human adipose-derived stromal cells efficiently support hematopoiesis invitro and invivo: a key step for therapeutic studies. Stem Cells Dev 2011, 20:2127-2138.
4. Hicok K.C., Du Laney T.V., Zhou Y.S., Halvorsen Y.D., Hitt D.C., Cooper L.F., et al. Human adipose-derived adult stem cells produce osteoid invivo. Tissue Eng 2004, 10:371-380.
5. Yu L.H., Kim M.H., Park T.H., Cha K.S., Kim Y.D., Quan M.L., et al. Improvement of cardiac function and remodeling by transplanting adipose tissue-derived stromal cells into a mouse model of acute myocardial infarction. Int J Cardiol 2010, 139:166-172.
6. Hong L., Peptan I.A., Colpan A., Daw J.L. Adipose tissue engineering by human adipose-derived stromal cells. Cells Tissues Organs 2006, 183:133-140.
7. Levi B., James A.W., Nelson E.R., Vistnes D., Wu B., Lee M., et al. Human adipose derived stromal cells heal critical size mouse calvarial defects. PLoS One 2010, 5:e11177.
8. Rada T., Reis R.L., Gomes M.E. Adipose tissue-derived stem cells and their application in bone and cartilage tissue engineering. Tissue Eng Part B Rev 2009, 15:113-125.
9. Tapp H., Hanley E.N., Patt J.C., Gruber H.E. Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair. Exp Biol Med (Maywood) 2009, 234:1-9.
10. Chung M.T., Zimmermann A.S., Paik K.J., Morrison S.D., Hyun J.S., Lo D.D., et al. Isolation of human adipose-derived stromal cells using laser-assisted liposuction and their therapeutic potential in regenerative medicine. Stem Cells Transl Med 2013, 2:808-817.
11. Doi A., Park I.H., Wen B., Murakami P., Aryee M.J., Irizarry R., et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 2009, 41:1350-1353.
12. Ge W., Shi L., Zhou Y., Liu Y., Ma G.E., Jiang Y., et al. Inhibition of osteogenic differentiation of human adipose-derived stromal cells by retinoblastoma binding protein 2 repression of RUNX2-activated transcription. Stem Cells 2011, 29:1112-1125.
13. Sinha K.M., Yasuda H., Coombes M.M., Dent S.Y., de Crombrugghe B. Regulation of the osteoblast-specific transcription factor Osterix by NO66, a Jumonji family histone demethylase. EMBO J 2010, 29:68-79.
14. Tao Y., Wu M., Zhou X., Yin W., Hu B., de Crombrugghe B., et al. Structural insights into histone demethylase NO66 in interaction with osteoblast-specific transcription factor Osterix and gene repression. JBiol Chem 2013, 288:16430-16437.
15. Whyte W.A., Bilodeau S., Orlando D.A., Hoke H.A., Frampton G.M., Foster C.T., et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 2012, 482:221-225.
16. Qureshi A.T., Monroe W.T., Dasa V., Gimble J.M., Hayes D.J. miR-148b-nanoparticle conjugates for light mediated osteogenesis of human adipose stromal/stem cells. Biomaterials 2013, 34:7799-7810.
17. Harrison C. Epigenetic drugs: new modulators of readers and erasers. Nat Rev Drug Discov 2013, 12:188.
18. Kaiser J. Epigenetic drugs take on cancer. Science 2010, 330:576-578.
19. Lan F., Nottke A.C., Shi Y. Mechanisms involved in the regulation of histone lysine demethylases. Curr Opin Cell Biol 2008, 20:316-325.
20. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
21. Williams J.S., Chamarthi B., Goodarzi M.O., Pojoga L.H., Sun B., Garza A.E., et al. Lysine-specific demethylase 1: an epigenetic regulator of salt-sensitive hypertension. Am J Hypertens 2012, 25:812-817.
22. Forneris F., Binda C., Battaglioli E., Mattevi A. LSD1: oxidative chemistry for multifaceted functions in chromatin regulation. Trends Biochem Sci 2008, 33:181-189.
23. Kahl P., Gullotti L., Heukamp L.C., Wolf S., Friedrichs N., Vorreuther R., et al. Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res 2006, 66:11341-11347.
24. Wang J., Scully K., Zhu X., Cai L., Zhang J., Prefontaine G.G., et al. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 2007, 446:882-887.
25. Chen Y., Jie W., Yan W., Zhou K., Xiao Y. Lysine-specific histone demethylase 1 (LSD1): a potential molecular target for tumor therapy. Crit Rev Eukaryot Gene Expr 2012, 22:53-59.
26. Wang J., Lu F., Ren Q., Sun H., Xu Z., Lan R., et al. Novel histone demethylase LSD1 inhibitors selectively target cancer cells with pluripotent stem cell properties. Cancer Res 2011, 71:7238-7249.
27. Mosammaparast N., Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 2010, 79:155-179.
28. Greer E.L., Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 2012, 13:343-357.
29. Shi Y., Whetstine J.R. Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 2007, 25:1-14.
30. Wang Y., Zhang H., Chen Y., Sun Y., Yang F., Yu W., et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 2009, 138:660-672.
31. Foster C.T., Dovey O.M., Lezina L., Luo J.L., Gant T.W., Barlev N., et al. Lysine-specific demethylase 1 regulates the embryonic transcriptome and CoREST stability. Mol Cell Biol 2010, 30:4851-4863.
32. Rudolph T., Beuch S., Reuter G. Lysine-specific histone demethylase LSD1 and the dynamic control of chromatin. Biol Chem 2013, 394:1019-1028.
33. Adamo A., Sese B., Boue S., Castano J., Paramonov I., Barrero M.J., et al. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat Cell Biol 2011, 13:652-659.
34. Kerenyi M.A., Shao Z., Hsu Y.J., Guo G., Luc S., O'Brien K., et al. Histone demethylase Lsd1 represses hematopoietic stem and progenitor cell signatures during blood cell maturation. Elife 2013, 2:e00633.
35. Neelamegam R., Ricq E.L., Malvaez M., Patnaik D., Norton S., Carlin S.M., et al. Brain-penetrant LSD1 inhibitors can block memory consolidation. ACS Chem Neurosci 2012, 3:120-128.
36. Pollock J.A., Larrea M.D., Jasper J.S., McDonnell D.P., McCafferty D.G. Lysine-specific histone demethylase 1 inhibitors control breast cancer proliferation in ERalpha-dependent and -independent manners. ACS Chem Biol 2012, 7:1221-1231.
37. Liang Y., Quenelle D., Vogel J.L., Mascaro C., Ortega A., Kristie T.M. Anovel selective LSD1/KDM1A inhibitor epigenetically blocks herpes simplex virus lytic replication and reactivation from latency. MBio 2013, 4. e00558-12.
38. Lynch J.T., Harris W.J., Somervaille T.C. LSD1 inhibition: a therapeutic strategy in cancer?. Expert Opin Ther Targets 2012, 16:1239-1249.
39. Shang Y., Hu X., DiRenzo J., Lazar M.A., Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000, 103:843-852.
40. Shang Y., Brown M. Molecular determinants for the tissue specificity of SERMs. Science 2002, 295:2465-2468.
41. Shi L., Sun L., Li Q., Liang J., Yu W., Yi X., et al. Histone demethylase JMJD2B coordinates H3K4/H3K9 methylation and promotes hormonally responsive breast carcinogenesis. Proc Natl Acad Sci U S A 2011, 108:7541-7546.
42. Murray-Stewart T., Woster P.M., Casero R.A. The re-expression of the epigenetically silenced e-cadherin gene by a polyamine analogue lysine-specific demethylase-1 (LSD1) inhibitor in human acute myeloid leukemia cell lines. Amino Acids 2014, 46:585-594.
43. Murphy D.L., Karoum F., Pickar D., Cohen R.M., Lipper S., Mellow A.M., et al. Differential trace amine alterations in individuals receiving acetylenic inhibitors of MAO-A (clorgyline) or MAO-B (selegiline and pargyline). JNeural Transm Suppl 1998, 52:39-48.
44. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
45. Liang Y., Vogel J.L., Narayanan A., Peng H., Kristie T.M. Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat Med 2009, 15:1312-1317.
46. Lamour V., Detry C., Sanchez C., Henrotin Y., Castronovo V., Bellahcene A. Runx2- and histone deacetylase 3-mediated repression is relieved in differentiating human osteoblast cells to allow high bone sialoprotein expression. JBiol Chem 2007, 282:36240-36249.
47. Westendorf J.J. Transcriptional co-repressors of Runx2. JCell Biochem 2006, 98:54-64.
48. Jensen E.D., Nair A.K., Westendorf J.J. Histone deacetylase co-repressor complex control of Runx2 and bone formation. Crit Rev Eukaryot Gene Expr 2007, 17:187-196.
49. Ali S.A., Zaidi S.K., Dobson J.R., Shakoori A.R., Lian J.B., Stein J.L., et al. Transcriptional corepressor TLE1 functions with Runx2 in epigenetic repression of ribosomal RNA genes. Proc Natl Acad Sci U S A 2010, 107:4165-4169.
50. Pekowska A., Benoukraf T., Zacarias-Cabeza J., Belhocine M., Koch F., Holota H., et al. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J 2011, 30:4198-4210.
51. Yu Y., Wang B., Zhang K., Lei Z., Guo Y., Xiao H., et al. High expression of lysine-specific demethylase 1 correlates with poor prognosis of patients with esophageal squamous cell carcinoma. Biochem Biophys Res Commun 2013, 437:192-198.
52. Huang Y., Vasilatos S.N., Boric L., Shaw P.G., Davidson N.E. Inhibitors of histone demethylation and histone deacetylation cooperate in regulating gene expression and inhibiting growth in human breast cancer cells. Breast Cancer Res Treat 2012, 131:777-789.
53. Cho H.H., Park H.T., Kim Y.J., Bae Y.C., Suh K.T., Jung J.S. Induction of osteogenic differentiation of human mesenchymal stem cells by histone deacetylase inhibitors. JCell Biochem 2005, 96:533-542.
54. Hu X., Zhang X., Dai L., Zhu J., Jia Z., Wang W., et al. Histone deacetylase inhibitor trichostatin A promotes the osteogenic differentiation of rat adipose-derived stem cells by altering the epigenetic modifications on Runx2 promoter in a BMP signaling-dependent manner. Stem Cells Dev 2013, 22:248-255.
55. Maroni P., Brini A.T., Arrigoni E., de Girolamo L., Niada S., Matteucci E., et al. Chemical and genetic blockade of HDACs enhances osteogenic differentiation of human adipose tissue-derived stem cells by oppositely affecting osteogenic and adipogenic transcription factors. Biochem Biophys Res Commun 2012, 428:271-277.
56. Shakibaei M., Shayan P., Busch F., Aldinger C., Buhrmann C., Lueders C., et al. Resveratrol mediated modulation of Sirt-1/Runx2 promotes osteogenic differentiation of mesenchymal stem cells: potential role of Runx2 deacetylation. PLoS One 2012, 7:e35712.