Long non-coding RNA NEAT1 promotes non-small cell lung cancer progression through regulation of miR-377-3p-E2F3 pathway

Oncotarget

Volumn 7, Issue 32, 2016, Pages 51784-51814

  Sun, Chengcao ^a   Li, Shujun ^a,b   Zhang, Feng ^a   Xi, Yongyong ^a   Wang, Liang ^a   Bi, Yongyi ^a   Li, Dejia ^a  

^a WUHAN UNIVERSITY   (China)

^b Wuhan Hospital for the Prevention and Treatment of Occupational Diseases   (China)

Author keywords

E2F3; Hsa miRNA 377 3p (miR 377 3p); Long non coding RNA NEAT1 (lncRNA NEAT1); Non small cell lung cancer (NSCLC); Tumorigenesis

Indexed keywords

LONG NON CODING RNA NEAT1; LONG UNTRANSLATED RNA; MICRORNA; MICRORNA 377 3P; TRANSCRIPTION FACTOR E2F3; UNCLASSIFIED DRUG; E2F3 PROTEIN, HUMAN; MIRN377 MICRORNA, HUMAN; NEAT1 LONG NON-CODING RNA, HUMAN;

ADULT; AGED; ARTICLE; BIOINFORMATICS; CANCER GROWTH; CANCER PROGNOSIS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC REGULATION; HUMAN; LUCIFERASE ASSAY; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; TUMOR GROWTH; A-549 CELL LINE; ANIMAL; BAGG ALBINO MOUSE; DISEASE EXACERBATION; GENETICS; LUNG TUMOR; METABOLISM; MIDDLE AGED; MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VERY ELDERLY;

A549 CELLS; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DISEASE PROGRESSION; E2F3 TRANSCRIPTION FACTOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; RNA, LONG NONCODING; SIGNAL TRANSDUCTION;

EID: 84982242270     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10108     Document Type: Article

References (90)

1. IARC Globocan 2012. Cancer Fact Sheet: Lung Cancer Mortality Worldwide in 2012.
2. Sun C, Li S, Yang C, Xi Y, Wang L, Zhang F and Li D. MicroRNA-187-3p mitigates non-small cell lung cancer (NSCLC) development through down-regulation of BCL6. Biochem Biophys Res Commun. 2016; 471:82-88.
3. Laskin JJ and Sandler AB. State of the art in therapy for non-small cell lung cancer. Cancer Invest. 2005; 23:427-442.
4. Tong AW. Small RNAs and non-small cell lung cancer. Curr Mol Med. 2006; 6:339-349.
5. Sekido Y, Fong KM and Minna JD. Molecular genetics of lung cancer. Annu Rev Med. 2003; 54:73-87.
6. Sun C, Li S and Li D. Hsa-miR-134 suppresses non-small cell lung cancer (NSCLC) development through downregulation of CCND1. Oncotarget. 2016. doi: 10.18632/ oncotarget.8482.
7. Sun C, Huang C, Li S, Yang C, Xi Y, Wang L, Zhang F, Fu Y and Li D. Hsa-miR-326 targets CCND1 and inhibits non-small cell lung cancer development. Oncotarget. 2016; 7:8341-8359. doi: 10.18632/oncotarget.7071.
8. Sun CC, Li SJ, Zhang F, Pan JY, Wang L, Yang CL, Xi YY and Li DJ. Hsa-miR-329 exerts tumor suppressor function through down-regulation of MET in non-small cell lung cancer. Oncotarget. 2016. doi: 10.18632/oncotarget.7517.
9. Yang C, Sun C, Liang X, Xie S, Huang J and Li D. Integrative analysis of microRNA and mRNA expression profiles in non-small-cell lung cancer. Cancer Gene Ther. 2016; 23:90-97. doi: 10.1038/cgt.2016.5.
10. Sun C, Li S, Yang C, Xi Y, Wang L, Zhang F and Li D. MicroRNA-187-3p mitigates non-small cell lung cancer (NSCLC) development through down-regulation of BCL6. Biochem Biophys Res Commun. 2016; 471:82-88.
11. Mercer TR, Dinger ME and Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009; 10:155-159.
12. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R and Shiekhattar R. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010; 143:46-58.
13. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T and Rinn JL. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010; 142:409-419.
14. Geisler S, Lojek L, Khalil AM, Baker KE and Coller J. Decapping of long noncoding RNAs regulates inducible genes. Mol Cell. 2012; 45:279-291.
15. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E and Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007; 129:1311-1323.
16. Pandey GK, Mitra S, Subhash S, Hertwig F, Kanduri M, Mishra K, Fransson S, Ganeshram A, Mondal T, Bandaru S, Ostensson M, Akyurek LM, Abrahamsson J, Pfeifer S, Larsson E and Shi L, et al. The risk-associated long noncoding RNA NBAT-1 controls neuroblastoma progression by regulating cell proliferation and neuronal differentiation. Cancer Cell. 2014; 26:722-737.
17. Garzon R, Volinia S, Papaioannou D, Nicolet D, Kohlschmidt J, Yan PS, Mrozek K, Bucci D, Carroll AJ, Baer MR, Wetzler M, Carter TH, Powell BL, Kolitz JE, Moore JO and Eisfeld AK, et al. Expression and prognostic impact of lncRNAs in acute myeloid leukemia. Proc Natl Acad Sci U S A. 2014; 111:18679-18684.
18. Yang F, Huo XS, Yuan SX, Zhang L, Zhou WP, Wang F and Sun SH. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell. 2013; 49:1083-1096.
19. Barnhill LM, Williams RT, Cohen O, Kim Y, Batova A, Mielke JA, Messer K, Pu M, Bao L, Yu AL and Diccianni MB. High expression of CAI2, a 9p21-embedded long noncoding RNA, contributes to advanced-stage neuroblastoma. Cancer Res. 2014; 74:3753-3763.
20. Yang F, Zhang L, Huo XS, Yuan JH, Xu D, Yuan SX, Zhu N, Zhou WP, Yang GS, Wang YZ, Shang JL, Gao CF, Zhang FR, Wang F and Sun SH. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology. 2011; 54:1679-1689.
21. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, Cao X, Jing X, Wang X, Siddiqui J, Wei JT and Robinson D, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol. 2011; 29:742-749.
22. Yang F, Zhang L, Huo XS, Yuan JH, Xu D, Yuan SX, Zhu N, Zhou WP, Yang GS, Wang YZ, Shang JL, Gao CF, Zhang FR, Wang F and Sun SH. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology. 2011; 54:1679-1689.
23. Wang F, Yuan JH, Wang SB, Yang F, Yuan SX, Ye C, Yang N, Zhou WP, Li WL, Li W and Sun SH. Oncofetal long noncoding RNA PVT1 promotes proliferation and stem cell-like property of hepatocellular carcinoma cells by stabilizing NOP2. Hepatology. 2014; 60:1278-1290.
24. Yuan SX, Wang J, Yang F, Tao QF, Zhang J, Wang LL, Yang Y, Liu H, Wang ZG, Xu QG, Fan J, Liu L, Sun SH and Zhou WP. Long noncoding RNA DANCR increases stemness features of hepatocellular carcinoma via de-repression of CTNNB1. Hepatology. 2015.
25. Yuan SX, Yang F, Yang Y, Tao QF, Zhang J, Huang G, Yang Y, Wang RY, Yang S, Huo XS, Zhang L, Wang F, Sun SH and Zhou WP. Long noncoding RNA associated with microvascular invasion in hepatocellular carcinoma promotes angiogenesis and serves as a predictor for hepatocellular carcinoma patients' poor recurrence-free survival after hepatectomy. Hepatology. 2012; 56:2231-2241.
26. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ and Zhou MM. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010; 38:662-674.
27. Pasmant E, Laurendeau I, Heron D, Vidaud M, Vidaud D and Bieche I. Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res. 2007; 67:3963-3969.
28. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB and van de Vijver MJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010; 464:1071-1076.
29. Wang KC and Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011; 43:904-914.
30. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E and Chang HY. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010; 329:689-693.
31. Yuan JH, Yang F, Wang F, Ma JZ, Guo YJ, Tao QF, Liu F, Pan W, Wang TT, Zhou CC, Wang SB, Wang YZ, Yang Y, Yang N, Zhou WP and Yang GS, et al. A long noncoding RNA activated by TGF-beta promotes the invasionmetastasis cascade in hepatocellular carcinoma. Cancer Cell. 2014; 25:666-681.
32. de Kok JB, Verhaegh GW, Roelofs RW, Hessels D, Kiemeney LA, Aalders TW, Swinkels DW and Schalken JA. DD3(PCA3), a very sensitive and specific marker to detect prostate tumors. Cancer Res. 2002; 62:2695-2698.
33. Hutchinson JN, Ensminger AW, Clemson CM, Lynch CR, Lawrence JB and Chess A. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics. 2007; 8:39.
34. Zeng C, Xu Y, Xu L, Yu X, Cheng J, Yang L, Chen S and Li Y. Inhibition of long non-coding RNA NEAT1 impairs myeloid differentiation in acute promyelocytic leukemia cells. BMC Cancer. 2014; 14:693.
35. Sasaki YT, Ideue T, Sano M, Mituyama T and Hirose T. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci U S A. 2009; 106:2525-2530.
36. Chen LL and Carmichael GG. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol Cell. 2009; 35:467-478.
37. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A and Lawrence JB. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell. 2009; 33:717-726.
38. Sunwoo H, Dinger ME, Wilusz JE, Amaral PP, Mattick JS and Spector DL. MEN epsilon/beta nuclear-retained noncoding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 2009; 19:347-359.
39. Fox AH and Lamond AI. Paraspeckles. Cold Spring Harb Perspect Biol. 2010; 2:a687.
40. Nakagawa S and Hirose T. Paraspeckle nuclear bodies-useful uselessness? Cell Mol Life Sci. 2012; 69:3027-3036.
41. Naganuma T and Hirose T. Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol. 2013; 10:456-461.
42. Choudhry H, Albukhari A, Morotti M, Haider S, Moralli D, Smythies J, Schodel J, Green CM, Camps C, Buffa F, Ratcliffe P, Ragoussis J, Harris AL and Mole DR. Tumor hypoxia induces nuclear paraspeckle formation through HIF-2alpha dependent transcriptional activation of NEAT1 leading to cancer cell survival. Oncogene. 2015; 34:4546.
43. Chakravarty D, Sboner A, Nair SS, Giannopoulou E, Li R, Hennig S, Mosquera JM, Pauwels J, Park K, Kossai M, MacDonald TY, Fontugne J, Erho N, Vergara IA, Ghadessi M and Davicioni E, et al. The oestrogen receptor alpharegulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat Commun. 2014; 5:5383.
44. Musgrove EA, Caldon CE, Barraclough J, Stone A and Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer. 2011; 11:558-572.
45. Wang TC, Cardiff RD, Zukerberg L, Lees E, Arnold A and Schmidt EV. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature. 1994; 369:669-671.
46. Zeng X, Shaikh FY, Harrison MK, Adon AM, Trimboli AJ, Carroll KA, Sharma N, Timmers C, Chodosh LA, Leone G and Saavedra HI. The Ras oncogene signals centrosome amplification in mammary epithelial cells through cyclin D1/Cdk4 and Nek2. Oncogene. 2010; 29:5103-5112.
47. Yu Q, Geng Y and Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature. 2001; 411:1017-1021.
48. Gautschi O, Ratschiller D, Gugger M, Betticher DC and Heighway J. Cyclin D1 in non-small cell lung cancer: a key driver of malignant transformation. Lung Cancer. 2007; 55:1-14.
49. Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, Robker RL, Richards JS, McGinnis LK, Biggers JD, Eppig JJ, Bronson RT, Elledge SJ and Weinberg RA. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature. 1996; 384:470-474.
50. Vieira FQ, Costa-Pinheiro P, Almeida-Rios D, Graca I, Monteiro-Reis S, Simoes-Sousa S, Carneiro I, Sousa EJ, Godinho MI, Baltazar F, Henrique R and Jeronimo C. SMYD3 contributes to a more aggressive phenotype of prostate cancer and targets Cyclin D2 through H4K20me3. Oncotarget. 2015; 6:13644-13657. doi: 10.18632/oncotarget.3767.
51. Harper JW, Adami GR, Wei N, Keyomarsi K and Elledge SJ. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993; 75:805-816.
52. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW and Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993; 75:817-825.
53. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, Zhang P, Dobrowolski S, Bai C, Connell-Crowley L, Swindell E and Et A. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell. 1995; 6:387-400.
54. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T and Rinn JL. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010; 142:409-419.
55. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R and Shiekhattar R. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010; 143:46-58.
56. Geisler S, Lojek L, Khalil AM, Baker KE and Coller J. Decapping of long noncoding RNAs regulates inducible genes. Mol Cell. 2012; 45:279-291.
57. Yang F, Zhang L, Huo XS, Yuan JH, Xu D, Yuan SX, Zhu N, Zhou WP, Yang GS, Wang YZ, Shang JL, Gao CF, Zhang FR, Wang F and Sun SH. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology. 2011; 54:1679-1689.
58. Barnhill LM, Williams RT, Cohen O, Kim Y, Batova A, Mielke JA, Messer K, Pu M, Bao L, Yu AL and Diccianni MB. High expression of CAI2, a 9p21-embedded long noncoding RNA, contributes to advanced-stage neuroblastoma. Cancer Res. 2014; 74:3753-3763.
59. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB and van de Vijver MJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010; 464:1071-1076.
60. Nie FQ, Zhu Q, Xu TP, Zou YF, Xie M, Sun M, Xia R and Lu KH. Long non-coding RNA MVIH indicates a poor prognosis for non-small cell lung cancer and promotes cell proliferation and invasion. Tumour Biol. 2014; 35:7587-7594.
61. Pasmant E, Laurendeau I, Heron D, Vidaud M, Vidaud D and Bieche I. Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res. 2007; 67:3963-3969.
62. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, Cao X, Jing X, Wang X, Siddiqui J, Wei JT and Robinson D, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol. 2011; 29:742-749.
63. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E and Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007; 129:1311-1323.
64. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ and Zhou MM. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010; 38:662-674.
65. Yang F, Huo XS, Yuan SX, Zhang L, Zhou WP, Wang F and Sun SH. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell. 2013; 49:1083-1096.
66. Pan LJ, Zhong TF, Tang RX, Li P, Dang YW, Huang SN and Chen G. Upregulation and clinicopathological significance of long non-coding NEAT1 RNA in NSCLC tissues. Asian Pac J Cancer Prev. 2015; 16:2851-2855.
67. Mercer TR, Dinger ME and Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009; 10:155-159.
68. Tani H, Torimura M and Akimitsu N. The RNA degradation pathway regulates the function of GAS5 a non-coding RNA in mammalian cells. Plos One. 2013; 8:e55684.
69. Kino T, Hurt DE, Ichijo T, Nader N and Chrousos GP. Noncoding RNA gas5 is a growth arrest-and starvationassociated repressor of the glucocorticoid receptor. Sci Signal. 2010; 3:a8.
70. Ma MZ, Chu BF, Zhang Y, Weng MZ, Qin YY, Gong W and Quan ZW. Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218-5p. Cell Death Dis. 2015; 6:e1583.
71. Zhen L, Yun-Hui L, Hong-Yu D, Jun M and Yi-Long Y. Long noncoding RNA NEAT1 promotes glioma pathogenesis by regulating miR-449b-5p/c-Met axis. Tumour Biol. 2016; 37:673-683.
72. Zehavi L, Schayek H, Jacob-Hirsch J, Sidi Y, Leibowitz-Amit R and Avni D. MiR-377 targets E2F3 and alters the NF-kB signaling pathway through MAP3K7 in malignant melanoma. Mol Cancer. 2015; 14:68.
73. Wang R, Ma Y, Yu D, Zhao J and Ma P. miR-377 functions as a tumor suppressor in human clear cell renal cell carcinoma by targeting ETS1. Biomed Pharmacother. 2015; 70:64-71.
74. Chen G, Lu L, Liu C, Shan L and Yuan D. MicroRNA-377 suppresses cell proliferation and invasion by inhibiting TIAM1 expression in hepatocellular carcinoma. Plos One. 2015; 10:e117714.
75. Wang R, Ma Y, Yu D, Zhao J and Ma P. miR-377 functions as a tumor suppressor in human clear cell renal cell carcinoma by targeting ETS1. Biomed Pharmacother. 2015; 70:64-71.
76. Chen G, Lu L, Liu C, Shan L and Yuan D. MicroRNA-377 suppresses cell proliferation and invasion by inhibiting TIAM1 expression in hepatocellular carcinoma. Plos One. 2015; 10:e117714.
77. Bracken AP, Ciro M, Cocito A and Helin K. E2F target genes: unraveling the biology. Trends Biochem Sci. 2004; 29:409-417.
78. Rady B, Chen Y, Vaca P, Wang Q, Wang Y, Salmon P and Oberholzer J. Overexpression of E2F3 promotes proliferation of functional human beta cells without induction of apoptosis. Cell Cycle. 2013; 12:2691-2702.
79. Takahashi Y, Rayman JB and Dynlacht BD. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 2000; 14:804-816.
80. DeGregori J and Johnson DG. Distinct and Overlapping Roles for E2F Family Members in Transcription, Proliferation and Apoptosis. Curr Mol Med. 2006; 6:739-748.
81. Humbert PO, Verona R, Trimarchi JM, Rogers C, Dandapani S and Lees JA. E2f3 is critical for normal cellular proliferation. Genes Dev. 2000; 14:690-703.
82. Cooper CS, Nicholson AG, Foster C, Dodson A, Edwards S, Fletcher A, Roe T, Clark J, Joshi A, Norman A, Feber A, Lin D, Gao Y, Shipley J and Cheng SJ. Nuclear overexpression of the E2F3 transcription factor in human lung cancer. Lung Cancer. 2006; 54:155-162.
83. Foster CS, Falconer A, Dodson AR, Norman AR, Dennis N, Fletcher A, Southgate C, Dowe A, Dearnaley D, Jhavar S, Eeles R, Feber A and Cooper CS. Transcription factor E2F3 overexpressed in prostate cancer independently predicts clinical outcome. Oncogene. 2004; 23:5871-5879.
84. Sherr CJ and McCormick F. The RB and p53 pathways in cancer. Cancer Cell. 2002; 2:103-112.
85. Olsson AY, Feber A, Edwards S, Te PR, Giddings I, Merson S and Cooper CS. Role of E2F3 expression in modulating cellular proliferation rate in human bladder and prostate cancer cells. Oncogene. 2007; 26:1028-1037.
86. Sun C, Sang M, Li S, Sun X, Yang C, Xi Y, Wang L, Zhang F, Bi Y, Fu Y and Li D. Hsa-miR-139-5p inhibits proliferation and causes apoptosis associated with downregulation of c-Met. Oncotarget. 2015; 6:39756-39792. doi: 10.18632/oncotarget.5476.
87. Sun C, Li S and Li D. Sulforaphane mitigates muscle fibrosis in mdx mice via Nrf2-mediated inhibition of TGFbeta/ Smad signaling. J Appl Physiol (1985). 2015:721-2015.
88. Sun C, Liu Z, Li S, Yang C, Xue R, Xi Y, Wang L, Wang S, He Q, Huang J, Xie S, Jiang W and Li D. Down-regulation of c-Met and Bcl2 by microRNA-206, activates apoptosis, and inhibits tumor cell proliferation, migration and colony formation. Oncotarget. 2015; 6:25533-25574. doi: 10.18632/oncotarget.4575.
89. Sun CC, Li SJ, Yang CL, Xue RL, Xi YY, Wang L, Zhao QL and Li DJ. Sulforaphane Attenuates Muscle Inflammation in Dystrophin-deficient mdx Mice via NF-E2-related Factor 2 (Nrf2)-mediated Inhibition of NF-kappaB Signaling Pathway. J Biol Chem. 2015; 290:17784-17795.
90. Sun C, Yang C, Xue R, Li S, Zhang T, Pan L, Ma X, Wang L and Li D. Sulforaphane alleviates muscular dystrophy in mdx mice by activation of Nrf2. J Appl Physiol (1985). 2015; 118:224-237.