Primordial Dwarfism Gene Maintains Lin28 Expression to Safeguard Embryonic Stem Cells from Premature Differentiation

Cell Reports

Volumn 7, Issue 3, 2014, Pages 735-746

  Dai, Qian ^a   Luan, Guangxin ^a   Deng, Li ^a   Lei, Tingjun ^a   Kang, Han ^a   Song, Xu ^a   Zhang, Yujun ^a   Xiao, Zhi Xiong ^a   Li, Qintong ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LA RIBONUCLEOPROTEIN DOMAIN FAMILY MEMBER 7; MESSENGER RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN LIN28; REGULATOR PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; PROTEIN LARP7; RNA BINDING PROTEIN; ELONGIN; LARP7 PROTEIN, HUMAN; LIN-28 PROTEIN, MOUSE; PROTEIN BINDING; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; DWARFISM; EMBRYONIC STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIMORDIAL DWARFISM; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA STABILITY; BODY SIZE; CELL CULTURE; CELL DIVISION; CELL GROWTH; DISEASE ASSOCIATION; GENE; GENE SILENCING; HUMAN; LARP7 GENE; LOSS OF FUNCTION MUTATION; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DWARFISM; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN BINDING; RIBONUCLEOPROTEINS; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84899905149     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.053     Document Type: Article

References (65)

1. Alazami A.M., Al-Owain M., Alzahrani F., Shuaib T., Al-Shamrani H., Al-Falki Y.H., Al-Qahtani S.M., Alsheddi T., Colak D., Alkuraya F.S. Loss of function mutation in LARP7, chaperone of 7SK ncRNA, causes a syndrome of facial dysmorphism, intellectual disability, and primordial dwarfism. Hum. Mutat. 2012, 33:1429-1434.
2. Barboric M., Lenasi T., Chen H., Johansen E.B., Guo S., Peterlin B.M. 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development. Proc. Natl. Acad. Sci. USA 2009, 106:7798-7803.
3. Bottardi S., Zmiri F.A., Bourgoin V., Ross J., Mavoungou L., Milot E. Ikaros interacts with P-TEFb and cooperates with GATA-1 to enhance transcription elongation. Nucleic Acids Res. 2011, 39:3505-3519.
4. Byers S.A., Price J.P., Cooper J.J., Li Q., Price D.H. HEXIM2, a HEXIM1-related protein, regulates positive transcription elongation factor b through association with 7SK. J. Biol. Chem. 2005, 280:16360-16367.
5. Chang H.M., Martinez N.J., Thornton J.E., Hagan J.P., Nguyen K.D., Gregory R.I. Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation. Nature communications 2012, 3:923.
6. Cherrier T., Le Douce V., Eilebrecht S., Riclet R., Marban C., Dequiedt F., Goumon Y., Paillart J.C., Mericskay M., Parlakian A., et al. CTIP2 is a negative regulator of P-TEFb. Proc. Natl. Acad. Sci. USA 2013, 110:12655-12660.
7. Cho J., Chang H., Kwon S.C., Kim B., Kim Y., Choe J., Ha M., Kim Y.K., Kim V.N. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 2012, 151:765-777.
8. Collado M., Serrano M. Senescence in tumours: evidence from mice and humans. Nat. Rev. Cancer 2010, 10:51-57.
9. Dai Q., Lei T., Zhao C., Zhong J., Tang Y.Z., Chen B., Yang J., Li C., Wang S., Song X., et al. Cyclin K-containing kinase complexes maintain self-renewal in murine embryonic stem cells. J. Biol. Chem. 2012, 287:25344-25352.
10. De Los Angeles A., Loh Y.H., Tesar P.J., Daley G.Q. Accessing naïve human pluripotency. Curr. Opin. Genet. Dev. 2012, 22:272-282.
11. Elagib K.E., Mihaylov I.S., Delehanty L.L., Bullock G.C., Ouma K.D., Caronia J.F., Gonias S.L., Goldfarb A.N. Cross-talk of GATA-1 and P-TEFb in megakaryocyte differentiation. Blood 2008, 112:4884-4894.
12. Evans M. Discovering pluripotency: 30 years of mouse embryonic stem cells. Nature reviews 2011, 12:680-686.
13. Giacinti C., Bagella L., Puri P.L., Giordano A., Simone C. MyoD recruits the cdk9/cyclin T2 complex on myogenic-genes regulatory regions. J. Cell. Physiol. 2006, 206:807-813.
14. He N., Jahchan N.S., Hong E., Li Q., Bayfield M.A., Maraia R.J., Luo K., Zhou Q. A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb-dependent transcriptional elongation and tumorigenesis. Mol. Cell 2008, 29:588-599.
15. Heo I., Joo C., Cho J., Ha M., Han J., Kim V.N. Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell 2008, 32:276-284.
16. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., Poitras C., Thérien C., Bergeron D., Bourassa S., Greenblatt J., et al. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol. Cell 2007, 27:262-274.
17. Kaichi S., Takaya T., Morimoto T., Sunagawa Y., Kawamura T., Ono K., Shimatsu A., Baba S., Heike T., Nakahata T., Hasegawa K. Cyclin-dependent kinase 9 forms a complex with GATA4 and is involved in the differentiation of mouse ES cells into cardiomyocytes. J. Cell. Physiol. 2011, 226:248-254.
18. Klingseisen A., Jackson A.P. Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev. 2011, 25:2011-2024.
19. Krueger B.J., Jeronimo C., Roy B.B., Bouchard A., Barrandon C., Byers S.A., Searcey C.E., Cooper J.J., Bensaude O., Cohen E.A., et al. LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res. 2008, 36:2219-2229.
20. Lei X.X., Xu J., Ma W., Qiao C., Newman M.A., Hammond S.M., Huang Y. Determinants of mRNA recognition and translation regulation by Lin28. Nucleic Acids Res. 2012, 40:3574-3584.
21. Li Q., Price J.P., Byers S.A., Cheng D., Peng J., Price D.H. Analysis of the large inactive P-TEFb complex indicates that it contains one 7SK molecule, a dimer of HEXIM1 or HEXIM2, and two P-TEFb molecules containing Cdk9 phosphorylated at threonine 186. J. Biol. Chem. 2005, 280:28819-28826.
22. Li Q., Cooper J.J., Altwerger G.H., Feldkamp M.D., Shea M.A., Price D.H. HEXIM1 is a promiscuous double-stranded RNA-binding protein and interacts with RNAs in addition to 7SK in cultured cells. Nucleic Acids Res. 2007, 35:2503-2512.
23. Li W., Laishram R.S., Anderson R.A. The novel poly(A) polymerase Star-PAP is a signal-regulated switch at the 3'-end of mRNAs. Adv. Boil. Regul. 2013, 53:64-76.
24. Markert A., Grimm M., Martinez J., Wiesner J., Meyerhans A., Meyuhas O., Sickmann A., Fischer U. The La-related protein LARP7 is a component of the 7SK ribonucleoprotein and affects transcription of cellular and viral polymerase II genes. EMBO Rep. 2008, 9:569-575.
25. Marks H., Kalkan T., Menafra R., Denissov S., Jones K., Hofemeister H., Nichols J., Kranz A., Stewart A.F., Smith A., Stunnenberg H.G. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 2012, 149:590-604.
26. Mellman D.L., Gonzales M.L., Song C., Barlow C.A., Wang P., Kendziorski C., Anderson R.A. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 2008, 451:1013-1017.
27. Melton C., Judson R.L., Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010, 463:621-626.
28. Merkle F.T., Eggan K. Modeling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell 2013, 12:656-668.
29. Michels A.A., Fraldi A., Li Q., Adamson T.E., Bonnet F., Nguyen V.T., Sedore S.C., Price J.P., Price D.H., Lania L., Bensaude O. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J. 2004, 23:2608-2619.
30. Najmabadi H., Hu H., Garshasbi M., Zemojtel T., Abedini S.S., Chen W., Hosseini M., Behjati F., Haas S., Jamali P., et al. Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 2011, 478:57-63.
31. Nelson P.T., Hatzigeorgiou A.G., Mourelatos Z. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 2004, 10:387-394.
32. Nguyen V.T., Kiss T., Michels A.A., Bensaude O. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 2001, 414:322-325.
33. Nichols J., Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009, 4:487-492.
34. Nichols J., Smith A. Pluripotency in the embryo and in culture. Cold Spring Harb. Perspect. Biol. 2012, 4:a008128.
35. Okamura D., Maeda I., Taniguchi H., Tokitake Y., Ikeda M., Ozato K., Mise N., Abe K., Noce T., Izpisua Belmonte J.C., Matsui Y. Cell cycle gene-specific control of transcription has a critical role in proliferation of primordial germ cells. Genes Dev. 2012, 26:2477-2482.
36. Peirson S.N., Butler J.N., Foster R.G. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res. 2003, 31:e73.
37. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 2006, 23:297-305.
38. Robinton D.A., Daley G.Q. The promise of induced pluripotent stem cells in research and therapy. Nature 2012, 481:295-305.
39. Rybak A., Fuchs H., Smirnova L., Brandt C., Pohl E.E., Nitsch R., Wulczyn F.G. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 2008, 10:987-993.
40. Sano M., Schneider M.D. Cyclin-dependent kinase-9: an RNAPII kinase at the nexus of cardiac growth and death cascades. Circ. Res. 2004, 95:867-876.
41. Sano M., Abdellatif M., Oh H., Xie M., Bagella L., Giordano A., Michael L.H., DeMayo F.J., Schneider M.D. Activation and function of cyclin T-Cdk9 (positive transcription elongation factor-b) in cardiac muscle-cell hypertrophy. Nat. Med. 2002, 8:1310-1317.
42. Shinoda G., Shyh-Chang N., de Soysa T.Y., Zhu H., Seligson M.T., Shah S.P., Abo-Sido N., Yabuuchi A., Hagan J.P., Gregory R.I., et al. Fetal deficiency of lin28 programs life-long aberrations in growth and glucose metabolism. Stem Cells 2013, 31:1563-1573.
43. Shyh-Chang N., Daley G.Q. Lin28: primal regulator of growth and metabolism in stem cells. Cell Stem Cell 2013, 12:395-406.
44. Simone C., Giordano A. Abrogation of signal-dependent activation of the cdk9/cyclin T2a complex in human RD rhabdomyosarcoma cells. Cell Death Differ. 2007, 14:192-195.
45. Smith E., Lin C., Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev. 2011, 25:661-672.
46. Song S.H., Kim A., Ragoczy T., Bender M.A., Groudine M., Dean A. Multiple functions of Ldb1 required for beta-globin activation during erythroid differentiation. Blood 2010, 116:2356-2364.
47. Sunagawa Y., Morimoto T., Takaya T., Kaichi S., Wada H., Kawamura T., Fujita M., Shimatsu A., Kita T., Hasegawa K. Cyclin-dependent kinase-9 is a component of the p300/GATA4 complex required for phenylephrine-induced hypertrophy in cardiomyocytes. J. Biol. Chem. 2010, 285:9556-9568.
48. Tanabe K., Nakamura M., Narita M., Takahashi K., Yamanaka S. Maturation, not initiation, is the major roadblock during reprogramming toward pluripotency from human fibroblasts. Proc. Natl. Acad. Sci. USA 2013, 110:12172-12179.
49. Tazi J., Forne T., Jeanteur P., Cathala G., Brunel C. Mammalian U6 small nuclear RNA undergoes 3' end modifications within the spliceosome. Mol. Cell. Biol. 1993, 13:1641-1650.
50. Thornton J.E., Gregory R.I. How does Lin28 let-7 control development and disease?. Trends Cell Biol. 2012, 22:474-482.
51. Tiscornia G., Vivas E.L., Izpisúa Belmonte J.C. Diseases in a dish: modeling human genetic disorders using induced pluripotent cells. Nat. Med. 2011, 17:1570-1576.
52. Trippe R., Sandrock B., Benecke B.J. A highly specific terminal uridylyl transferase modifies the 3'-end of U6 small nuclear RNA. Nucleic Acids Res. 1998, 26:3119-3126.
53. Trippe R., Guschina E., Hossbach M., Urlaub H., Luhrmann R., Benecke B.J. Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase. RNA 2006, 12:1494-1504.
54. Viswanathan S.R., Daley G.Q., Gregory R.I. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
55. Wang S., Fischer P.M. Cyclin-dependent kinase 9: a key transcriptional regulator and potential drug target in oncology, virology and cardiology. Trends Pharmacol. Sci. 2008, 29:302-313.
56. Wilbert M.L., Huelga S.C., Kapeli K., Stark T.J., Liang T.Y., Chen S.X., Yan B.Y., Nathanson J.L., Hutt K.R., Lovci M.T., et al. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol. Cell 2012, 48:195-206.
57. Yang Z., Zhu Q., Luo K., Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 2001, 414:317-322.
58. Yik J.H., Chen R., Nishimura R., Jennings J.L., Link A.J., Zhou Q. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol. Cell 2003, 12:971-982.
59. Ying Q.L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
60. Young R.A. Control of the embryonic stem cell state. Cell 2011, 144:940-954.
61. Yu J., Thomson J.A. Pluripotent stem cell lines. Genes Dev. 2008, 22:1987-1997.
62. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
63. Zhou Q., Yik J.H. The Yin and Yang of P-TEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol. Mol. Biol. Rev. 2006, 70:646-659.
64. Zhou Q., Li T., Price D.H. RNA polymerase II elongation control. Annu. Rev. Biochem. 2012, 81:119-143.
65. Zhu H., Shah S., Shyh-Chang N., Shinoda G., Einhorn W.S., Viswanathan S.R., Takeuchi A., Grasemann C., Rinn J.L., Lopez M.F., et al. Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat. Genet. 2010, 42:626-630.