Directing stem cell fate by controlled RNA interference

Biomaterials

Volumn 33, Issue 9, 2012, Pages 2608-2628

  Yau, Winifred Wing Yiu ^a   Rujitanaroj, Pim on ^a   Lam, Ling ^b   Chew, Sing Yian ^a  

^a Nanyang Technological University   (Singapore)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Enhanced differentiation; Gene knockdown; RNA interference; Scaffold based delivery

Indexed keywords

CYTOLOGY; GENES; GENETIC ENGINEERING; RNA;

AREA OF INTEREST; CONVENTIONAL METHODS; ENHANCED DIFFERENTIATIONS; GENE KNOCK DOWN; GENE SILENCING; RNA INTERFERENCE; SCAFFOLD-BASED DELIVERIES; STEM CELL DIFFERENTIATION;

STEM CELLS;

LIPOPLEX; MESSENGER RNA; MICRORNA; PLASMID DNA; SMALL INTERFERING RNA;

ADIPOGENESIS; ANGIOGENESIS; BIODEGRADATION; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CHONDROGENESIS; DNA TRANSFECTION; ELECTROPORATION; GENE SILENCING; HUMAN; LIPID STORAGE; MESENCHYMAL STEM CELL; MUSCLE DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA INTERFERENCE; STEM CELL;

EID: 84855950313     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.12.021     Document Type: Review

References (97)

1. Xu Z., Yu S., Hsu C.H., Eguchi J., Rosen E.D. The orphan nuclear receptor chicken ovalbumin upstream promoter-transcription factor II is a critical regulator of adipogenesis. Proc Natl Acad Sci USA 2008, 105:2421-2426.
2. Ling H.Y., Wen G.B., Feng S.D., Tuo Q.H., Ou H.S., Yao C.H., et al. MicroRNA-375 promotes 3T3-L1 adipocyte differentiation through modulation of extracellular signal-regulated kinase signalling. Clin Exp Pharmacol Physiol 2011, 38:239-246.
3. Kwong F.N., Richardson S.M., Evans C.H. Chordin knockdown enhances the osteogenic differentiation of human mesenchymal stem cells. Arthritis Res Ther 2008, 10:R65.
4. Kim Y.J., Bae S.W., Yu S.S., Bae Y.C., Jung J.S. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. JBone Miner Res 2009, 24:816-825.
5. Tay Y.M., Tam W.L., Ang Y.S., Gaughwin P.M., Yang H., Wang W., et al. MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 2008, 26:17-29.
6. Brett J.O., Renault V.M., Rafalski V.A., Webb A.E., Brunet A. The microRNA cluster miR-106b~25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging (Albany NY) 2011, 3:108-124.
7. Wegmuller D., Raineri I., Gross B., Oakeley E.J., Moroni C. Acassette system to study embryonic stem cell differentiation by inducible RNA interference. Stem Cells 2007, 25:1178-1185.
8. Wilson K.D., Hu S., Venkatasubrahmanyam S., Fu J.D., Sun N., Abilez O.J., et al. Dynamic microRNA expression programs during cardiac differentiation of human embryonic stem cells: role for miR-499. Circ Cardiovasc Genet 2010, 3:426-435.
9. Hwang K.C., Kim J.Y., Chang W., Kim D.S., Lim S., Kang S.M., et al. Chemicals that modulate stem cell differentiation. Proc Natl Acad Sci USA 2008, 105:7467-7471.
10. Krebs M.D., Alsberg E. Localized, targeted, and sustained siRNA delivery. Chemistry 2011, 17:3054-3062.
11. Nimesh S., Gupta N., Chandra R. Strategies and advances in nanomedicine for targeted siRNA delivery. Nanomedicine (Lond) 2011, 6:729-746.
12. Yao Y., Wang C., Varshney R.R., Wang D.A. Antisense makes sense in engineered regenerative medicine. Pharm Res 2009, 26:263-275.
13. Hribal M.L., Nakae J., Kitamura T., Shutter J.R., Accili D. Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. JCell Biol 2003, 162:535-541.
14. Hay D.C., Sutherland L., Clark J., Burdon T. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 2004, 22:225-235.
15. He Z., Li J., Zhen C., Feng L., Ding X. Knockdown of p53 by RNAi in ES cells facilitates RA-induced differentiation into muscle cells. Biochem Biophys Res Commun 2005, 335:676-683.
16. Tay Y., Zhang J., Thomson A.M., Lim B., Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008, 455:1124-1128.
17. Levy O., Ruvinov E., Reem T., Granot Y., Cohen S. Highly efficient osteogenic differentiation of human mesenchymal stem cells by eradication of STAT3 signaling. Int J Biochem Cell Biol 2010, 42:1823-1830.
18. Rao M., Sockanathan S. Molecular mechanisms of RNAi: implications for development and disease. Birth Defects Res C Embryo Today 2005, 75:28-42.
19. Carthew R.W., Sontheimer E.J. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 136:642-655.
20. Moore C.B., Guthrie E.H., Huang M.T., Taxman D.J. Short hairpin RNA (shRNA): design, delivery, and assessment of gene knockdown. Methods Mol Biol 2010, 629:141-158.
21. Hannon G.J. RNA interference. Nature 2002, 418:244-251.
22. Sluijter J.P., van Mil A., van Vliet P., Metz C.H., Liu J., Doevendans P.A., et al. MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells. Arterioscler Thromb Vasc Biol 2010, 30:859-868.
23. Zhao X., He X., Han X., Yu Y., Ye F., Chen Y., et al. MicroRNA-mediated control of oligodendrocyte differentiation. Neuron 2010, 65:612-626.
24. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 2007, 27:435-448.
25. Aziz A., Miyake T., Engleka K.A., Epstein J.A., McDermott J.C. Menin expression modulates mesenchymal cell commitment to the myogenic and osteogenic lineages. Dev Biol 2009, 332:116-130.
26. Ono Y., Gnocchi V.F., Zammit P.S., Nagatomi R. Presenilin-1 acts via Id1 to regulate the function of muscle satellite cells in a gamma-secretase-independent manner. JCell Sci 2009, 122:4427-4438.
27. Sharabi A.B., Lee S.H., Goodell M.A., Huang X.F., Chen S.Y. Enhanced generation of myeloid lineages in hematopoietic differentiation from embryonic stem cells by silencing transcriptional repressor Twist-2. Cloning Stem Cells 2009, 11:523-533.
28. Mei H., Ho M.K., Yung L.Y., Wu Z., Ip N.Y., Wong Y.H. Expression of Gα (z) in C2C12 cells restrains myogenic differentiation. Cell Signal 2011, 23:389-397.
29. Cordes K.R., Sheehy N.T., White M.P., Berry E.C., Morton S.U., Muth A.N., et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
30. Wurdak H., Zhu S., Min K.H., Aimone L., Lairson L.L., Watson J., et al. Asmall molecule accelerates neuronal differentiation in the adult rat. Proc Natl Acad Sci USA 2010, 107:16542-16547.
31. Yang Y., Li Y., Lv Y., Zhang S., Chen L., Bai C., et al. NRSF silencing induces neuronal differentiation of human mesenchymal stem cells. Exp Cell Res 2008, 314:2257-2265.
32. Huang Z., Wu Q., Guryanova O.A., Cheng L., Shou W., Rich J.N., et al. Deubiquitylase HAUSP stabilizes REST and promotes maintenance of neural progenitor cells. Nat Cell Biol 2011, 13:142-152.
33. Gadadhar A., Marr R., Lazarov O. Presenilin-1 regulates neural progenitor cell differentiation in the adult brain. JNeurosci 2011, 31:2615-2623.
34. Kim Y.H., Chung J.I., Woo H.G., Jung Y.S., Lee S.H., Moon C.H., et al. Differential regulation of proliferation and differentiation in neural precursor cells by the Jak pathway. Stem Cells 2010, 28:1816-1828.
35. Nara K., Kusafuka T., Yoneda A., Oue T., Sangkhathat S., Fukuzawa M. Silencing of MYCN by RNA interference induces growth inhibition, apoptotic activity and cell differentiation in a neuroblastoma cell line with MYCN amplification. Int J Oncol 2007, 30:1189-1196.
36. Jing L., Jia Y., Lu J., Han R., Li J., Wang S., et al. MicroRNA-9 promotes differentiation of mouse bone mesenchymal stem cells into neurons by Notch signaling. Neuroreport 2011, 22:206-211.
37. Valaperta R., Valsecchi M., Rocchetta F., Aureli M., Prioni S., Prinetti A., et al. Induction of axonal differentiation by silencing plasma membrane-associated sialidase Neu3 in neuroblastoma cells. JNeurochem 2007, 100:708-719.
38. Ichi S., Boshnjaku V., Shen Y.W., Mania-Farnell B., Ahlgren S., Sapru S., et al. Role of Pax3 acetylation in the regulation of Hes1 and Neurog2. Mol Biol Cell 2011, 22:503-512.
39. Tarantino C., Paolella G., Cozzuto L., Minopoli G., Pastore L., Parisi S., et al. miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J 2010, 24:3255-3263.
40. Ambasudhan R., Talantova M., Coleman R., Yuan X., Zhu S., Lipton S.A., et al. Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. Cell Stem Cell 2011, 9:113-118.
41. Yoo A.S., Sun A.X., Li L., Shcheglovitov A., Portmann T., Li Y., et al. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 2011, 476:228-231.
42. Zhao C., Sun G., Li S., Shi Y. Afeedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 2009, 16:365-371.
43. Aranha M.M., Santos D.M., Xavier J.M., Low W.C., Steer C.J., Sola S., et al. Apoptosis-associated microRNAs are modulated in mouse, rat and human neural differentiation. BMC Genomics 2010, 11:514.
44. Kwon I.S., Cho S.K., Kim M.J., Tsai M.J., Mitsuda N., Suh-Kim H., et al. Expression of Disabled 1 suppresses astroglial differentiation in neural stem cells. Mol Cell Neurosci 2009, 40:50-61.
45. Li G.H., Wei H., Chen Z.T., Lv S.Q., Yin C.L., Wang D.L. STAT3 silencing with lentivirus inhibits growth and induces apoptosis and differentiation of U251 cells. JNeurooncol 2009, 91:165-174.
46. Cottle D.L., McGrath M.J., Cowling B.S., Coghill I.D., Brown S., Mitchell C.A. FHL3 binds MyoD and negatively regulates myotube formation. JCell Sci 2007, 120:1423-1435.
47. Yamaguchi Y., Oohinata R., Naiki T., Irie K. Stau1 negatively regulates myogenic differentiation in C2C12 cells. Genes Cells 2008, 13:583-592.
48. Miraoui H., Severe N., Vaudin P., Pages J.C., Marie P.J. Molecular silencing of Twist1 enhances osteogenic differentiation of murine mesenchymal stem cells: implication of FGFR2 signaling. JCell Biochem 2010, 110:1147-1154.
49. Liu Y.B., Kharode Y., Bodine P.V., Yaworsky P.J., Robinson J.A., Billiard J. LPA induces osteoblast differentiation through interplay of two receptors: LPA1 and LPA4. JCell Biochem 2010, 109:794-800.
50. Hung S.C., Tsai C.C., Chen Y.J., Yew T.L., Chen L.L., Wang J.Y., et al. Hypoxia inhibits senescence and maintains mesenchymal stem cell properties through down-regulation of E2A-p21 by HIF-TWIST. Blood 2011, 117:459-469.
51. Kumar A., Salimath B.P., Schieker M., Stark G.B., Finkenzeller G. Inhibition of metastasis-associated gene 1 expression affects proliferation and osteogenic differentiation of immortalized human mesenchymal stem cells. Cell Prolif 2011, 44:128-138.
52. Andersen M.O., Nygaard J.V., Burns J.S., Raarup M.K., Nyengaard J.R., Bunger C., et al. siRNA nanoparticle functionalization of nanostructured scaffolds enables controlled multilineage differentiation of stem cells. Mol Ther 2010, 18:2018-2027.
53. Martin S.K., Fitter S., Bong L.F., Drew J.J., Gronthos S., Shepherd P.R., et al. NVP-BEZ235, a dual pan class I PI3 kinase and mTOR inhibitor, promotes osteogenic differentiation in human mesenchymal stromal cells. JBone Miner Res 2010, 25:2126-2137.
54. Chen J., Zhang J., Tu Q.S., Bonewald L.F., He X., Stein G., et al. Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1. JBone Miner Res 2011, 26:1953-1963.
55. Hu R., Liu W., Li H., Yang L., Chen C., Xia Z.Y., et al. ARunx2/miR-3960/miR-2861 regulatory feedback loop during mouse osteoblast differentiation. JBiol Chem 2011, 286:12328-12339.
56. Mizuno Y., Tokuzawa Y., Ninomiya Y., Yagi K., Yatsuka-Kanesaki Y., Suda T., et al. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 2009, 583:2263-2268.
57. Li Z., Hassan M.Q., Jafferji M., Aqeilan R.I., Garzon R., Croce C.M., et al. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. JBiol Chem 2009, 284:15676-15684.
58. Asahara H., Yamashita S., Andoh M., Ueno-Kudoh H., Sato T., Miyaki S. Sox9 directly promotes Bapx1 gene expression to repress Runx2 in chondrocytes. Exp Cell Res 2009, 315:2231-2240.
59. Hannan N.R., Wolvetang E.J. Adipocyte differentiation in human embryonic stem cells transduced with Oct4 shRNA lentivirus. Stem Cells Dev 2009, 18:653-660.
60. Bhandari D.R., Seo K.W., Roh K.H., Jung J.W., Kang S.K., Kang K.S. REX-1 expression and p38 MAPK activation status can determine proliferation/differentiation fates in human mesenchymal stem cells. PLoS One 2010, 5:e10493.
61. Huang J., Zhao L., Xing L., Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010, 28:357-364.
62. Wang T., Ren X., Xiong J., Zhang L., Qu J., Xu W. Tailless-like (TLX) protein promotes neuronal differentiation of dermal multipotent stem cells and benefits spinal cord injury in rats. Cell Mol Neurobiol 2011, 31:479-487.
63. Rawlings J.S., Rosler K.M., Harrison D.A. The JAK/STAT signaling pathway. JCell Sci 2004, 117:1281-1283.
64. Coppock H.A., Gilham D.E., Howell A., Clarke R.B. Cyclin-dependent kinase inhibitors and basement membrane interact to regulate breast epithelial cell differentiation and acinar morphogenesis. Cell Prolif 2007, 40:721-740.
65. Sonawane N.D., Szoka F.C., Verkman A.S. Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes. JBiol Chem 2003, 278:44826-44831.
66. Hamm A., Krott N., Breibach I., Blindt R., Bosserhoff A.K. Efficient transfection method for primary cells. Tissue Eng 2002, 8:235-245.
67. Ma Y., Jin J., Dong C., Cheng E.C., Lin H., Huang Y., et al. High-efficiency siRNA-based gene knockdown in human embryonic stem cells. RNA 2010, 16:2564-2569.
68. Ivanova P., Atanasova G., Poumay Y., Mitev V. Knockdown of PKD1 in normal human epidermal keratinocytes increases mRNA expression of keratin 10 and involucrin: early markers of keratinocyte differentiation. Arch Dermatol Res 2008, 300:139-145.
69. Aoyama K., Yamane A., Suga T., Suzuki E., Fukui T., Nakamura Y. Bone morphogenetic protein-2 functions as a negative regulator in the differentiation of myoblasts, but not as an inducer for the formations of cartilage and bone in mouse embryonic tongue. BMC Dev Biol 2011, 11:44.
70. Liao R., Sun J., Zhang L., Lou G., Chen M., Zhou D., et al. MicroRNAs play a role in the development of human hematopoietic stem cells. JCell Biochem 2008, 104:805-817.
71. Tzur G., Levy A., Meiri E., Barad O., Spector Y., Bentwich Z., et al. MicroRNA expression patterns and function in endodermal differentiation of human embryonic stem cells. PLoS One 2008, 3:e3726.
72. Takada T., Nemoto K., Yamashita A., Kato M., Kondo Y., Torii R. Efficient gene silencing and cell differentiation using siRNA in mouse and monkey ES cells. Biochem Biophys Res Commun 2005, 331:1039-1044.
73. Biewenga J.E., Destree O.H., Schrama L.H. Plasmid-mediated gene transfer in neurons using the biolistics technique. JNeurosci Methods 1997, 71:67-75.
74. Weaver J.C. Electroporation theory. Concepts and mechanisms. Methods Mol Biol 1995, 47:1-26.
75. Zoldan J., Lytton-Jean A.K., Karagiannis E.D., Deiorio-Haggar K., Bellan L.M., Langer R., et al. Directing human embryonic stem cell differentiation by non-viral delivery of siRNA in 3D culture. Biomaterials 2011, 32:7793-7800.
76. Hwang do W., Son S., Jang J., Youn H., Lee S., Lee D., et al. Abrain-targeted rabies virus glycoprotein-disulfide linked PEI nanocarrier for delivery of neurogenic microRNA. Biomaterials 2011, 32:4968-4975.
77. Tomas H., Pandita D., Santos J.L., Rodrigues J., Pego A.P., Granja P.L. Gene delivery into mesenchymal stem cells: a biomimetic approach using RGD nanoclusters based on poly(amidoamine) dendrimers. Biomacromolecules 2011, 12:472-481.
78. Love K.T., Mahon K.P., Levins C.G., Whitehead K.A., Querbes W., Dorkin J.R., et al. Lipid-like materials for low-dose, invivo gene silencing. Proc Natl Acad Sci USA 2010, 107:1864-1869.
79. Akinc A., Goldberg M., Qin J., Dorkin J.R., Gamba-Vitalo C., Maier M., et al. Development of lipidoid-siRNA formulations for systemic delivery to the liver. Mol Ther 2009, 17:872-879.
80. Akinc A., Zumbuehl A., Goldberg M., Leshchiner E.S., Busini V., Hossain N., et al. Acombinatorial library of lipid-like materials for delivery of RNAi therapeutics. Nat Biotechnol 2008, 26:561-569.
81. Vinas-Castells R., Holladay C., di Luca A., Diaz V.M., Pandit A. Snail1 down-regulation using small interfering RNA complexes delivered through collagen scaffolds. Bioconjug Chem 2009, 20:2262-2269.
82. Cao H., Jiang X., Chai C., Chew S.Y. RNA interference by nanofiber-based siRNA delivery system. JControl Release 2010, 144:203-212.
83. Rujitanaroj P.O., Wang Y.C., Wang J., Chew S.Y. Nanofiber-mediated controlled release of siRNA complexes for long term gene-silencing applications. Biomaterials 2011, 32:5915-5923.
84. Singh A., Suri S., Roy K. In-situ crosslinking hydrogels for combinatorial delivery of chemokines and siRNA-DNA carrying microparticles to dendritic cells. Biomaterials 2009, 30:5187-5200.
85. De Laporte L., Shea L.D. Matrices and scaffolds for DNA delivery in tissue engineering. Adv Drug Deliv Rev 2007, 59:292-307.
86. Malone R.W., Felgner P.L., Verma I.M. Cationic liposome-mediated RNA transfection. Proc Natl Acad Sci USA 1989, 86:6077-6081.
87. Mitchell D.A., Nair S.K. RNA-transfected dendritic cells in cancer immunotherapy. JClin Invest 2000, 106:1065-1069.
88. Xu J., Ganesh S., Amiji M. Non-condensing polymeric nanoparticles for targeted gene and siRNA delivery. Int J Pharm 2011.
89. Teo B.K., Goh S.H., Kustandi T.S., Loh W.W., Low H.Y., Yim E.K. The effect of micro and nanotopography on endocytosis in drug and gene delivery systems. Biomaterials 2011, 32:9866-9875.
90. Minakuchi Y., Takeshita F., Kosaka N., Sasaki H., Yamamoto Y., Kouno M., et al. Atelocollagen-mediated synthetic small interfering RNA delivery for effective gene silencing invitro and invivo. Nucleic Acids Res 2004, 32:e109.
91. Chew S.Y., Low W.C. Scaffold-based approach to direct stem cell neural and cardiovascular differentiation: an analysis of physical and biochemical effects. JBiomed Mater Res A 2011, 97:355-374.
92. Chen Q., Butler D., Querbes W., Pandey R.K., Ge P., Maier M.A., et al. Lipophilic siRNAs mediate efficient gene silencing in oligodendrocytes with direct CNS delivery. JControl Release 2010, 144:227-232.
93. Zhu L., Mahato R.I. Targeted delivery of siRNA to hepatocytes and hepatic stellate cells by bioconjugation. Bioconjug Chem 2010, 21:2119-2127.
94. Xie C., Hu J., Ma H., Zhang J., Chang L.J., Chen Y.E., et al. Three-dimensional growth of iPS cell-derived smooth muscle cells on nanofibrous scaffolds. Biomaterials 2011, 32:4369-4375.
95. Lu J., Guo S., Ebert B.L., Zhang H., Peng X., Bosco J., et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell 2008, 14:843-853.
96. Levay K., Slepak V.Z. Up- or downregulation of tescalcin in HL-60 cells is associated with their differentiation to either granulocytic or macrophage-like lineage. Exp Cell Res 2010, 316:1254-1262.
97. Maeda T., Shima Y., Sugiura S., Aizawa S., Tamai I. Changes of differentiation and proliferation in k562 cells with various levels of knockdown of cationic amino acid transporter 1. Drug Metab Pharmacokinet 2008, 23:181-187.