RNA-binding protein Lin28 in cancer and immunity

Cancer Letters

Volumn 375, Issue 1, 2016, Pages 108-113

  Jiang, Shuai ^a   Baltimore, David ^a  

^a California Institute of Technology   (United States)

Author keywords

Cancer; Immunity; Let 7; Lin28

Indexed keywords

LIN28 PROTEIN; MICRORNA; MICRORNA LET 7; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; LIN-28 PROTEIN, HUMAN;

CARCINOGENESIS; GENE EXPRESSION; HUMAN; IMMUNITY; METASTASIS; MOLECULAR PATHOLOGY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SHORT SURVEY; TUMOR IMMUNITY; ANIMAL; GENE EXPRESSION REGULATION; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNE SYSTEM; NEOPLASMS; RNA-BINDING PROTEINS;

EID: 84960338361     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.02.050     Document Type: Review

References (88)

1. Glisovic T., Bachorik J.L., Yong J., Dreyfuss G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 2008, 582:1977-1986.
2. Lunde B.M., Moore C., Varani G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol 2007, 8:479-490.
3. Chenard C.A., Richard S. New implications for the QUAKING RNA binding protein in human disease. J. Neurosci. Res 2008, 86:233-242.
4. Abdelmohsen K., Gorospe M. RNA-binding protein nucleolin in disease. RNA Biol 2012, 9:799-808.
5. Moss E.G., Lee R.C., Ambros V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 1997, 88:637-646.
6. Huang Y. A mirror of two faces: Lin28 as a master regulator of both miRNA and mRNA. Wiley Interdiscip. Rev. RNA 2012, 3:483-494.
7. Shyh-Chang N., Daley G.Q. Lin28: primal regulator of growth and metabolism in stem cells. Cell Stem. Cell 2013, 12:395-406.
8. Yates L.A., Norbury C.J., Gilbert R.J. The long and short of microRNA. Cell 2013, 153:516-519.
9. Huang J., Lyu H., Wang J., Liu B. MicroRNA regulation and therapeutic targeting of survivin in cancer. Am. J. Cancer Res 2015, 5:20-31.
10. Acunzo M., Romano G., Wernicke D., Croce C.M. MicroRNA and cancer - a brief overview. Adv. Biol. Regul 2015, 57:1-9.
11. Lee H.M., Nguyen D.T., Lu L.F. Progress and challenge of microRNA research in immunity. Front Genet 2014, 5:178.
12. O'Connell R.M., Baltimore D. MicroRNAs and hematopoietic cell development. Curr. Top. Dev. Biol 2012, 99:145-174.
13. O'Connell R.M., Rao D.S., Baltimore D. microRNA regulation of inflammatory responses. Annu. Rev. Immunol 2012, 30:295-312.
14. So A.Y., Zhao J.L., Baltimore D. The Yin and Yang of microRNAs: leukemia and immunity. Immunol. Rev 2013, 253:129-145.
15. Thornton J.E., Gregory R.I. How does Lin28 let-7 control development and disease?. Trends Cell Biol 2012, 22:474-482.
16. Rehfeld F., Rohde A.M., Nguyen D.T., Wulczyn F.G. Lin28 and let-7: ancient milestones on the road from pluripotency to neurogenesis. Cell Tissue Res 2015, 359:145-160.
17. Mayr F., Heinemann U. Mechanisms of Lin28-mediated miRNA and mRNA regulation-a structural and functional perspective. Int. J. Mol. Sci 2013, 14:16532-16553.
18. Nam Y., Chen C., Gregory R.I., Chou J.J., Sliz P. Molecular basis for interaction of let-7 microRNAs with Lin28. Cell 2011, 147:1080-1091.
19. Heo I., Joo C., Kim Y.K., Ha M., Yoon M.J., Cho J., et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009, 138:696-708.
20. Iliopoulos D., Hirsch H.A., Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 2009, 139:693-706.
21. Wang X., Cao L., Wang Y., Wang X., Liu N., You Y. Regulation of let-7 and its target oncogenes (Review). Oncol. Lett 2012, 3:955-960.
22. Murray M.J., Saini H.K., Siegler C.A., Hanning J.E., Barker E.M., van Dongen S., et al. Cclg, LIN28 Expression in malignant germ cell tumors downregulates let-7 and increases oncogene levels. Cancer Res 2013, 73:4872-4884.
23. Zhou J., Ng S.B., Chng W.J. LIN28/LIN28B: an emerging oncogenic driver in cancer stem cells. Int. J. Biochem. Cell Biol 2013, 45:973-978.
24. Feng C., Neumeister V., Ma W., Xu J., Lu L., Bordeaux J., et al. Lin28 regulates HER2 and promotes malignancy through multiple mechanisms. Cell Cycle 2012, 11:2486-2494.
25. Malik F., Korkaya H., Clouthier S.G., Wicha M.S. Lin28 and HER2: two stem cell regulators conspire to drive aggressive breast cancer. Cell Cycle 2012, 11:2780-2781.
26. Xie R., Wang Y., Nie W., Huang W., Song W., Wang Z., et al. Lin28B expression correlates with aggressive clinicopathological characteristics in breast invasive ductal carcinoma. Cancer Biother. Radiopharm 2014, 29:215-220.
27. Viswanathan S.R., Powers J.T., Einhorn W., Hoshida Y., Ng T.L., Toffanin S., et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat. Genet 2009, 41:843-848.
28. Dangi-Garimella S., Yun J., Eves E.M., Newman M., Erkeland S.J., Hammond S.M., et al. Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J. 2009, 28:347-358.
29. Yang J., Bennett B.D., Luo S., Inoue K., Grimm S.A., Schroth G.P., et al. LIN28A modulates splicing and gene expression programs in breast cancer cells. Mol. Cell. Biol 2015, 35:3225-3243.
30. Liu Y., Li H., Feng J., Cui X., Huang W., Li Y., et al. Lin28 induces epithelial-to-mesenchymal transition and stemness via downregulation of let-7a in breast cancer cells. PLoS ONE 2013, 8:e83083.
31. Wang L., Yuan C., Lv K., Xie S., Fu P., Liu X., et al. Lin28 mediates radiation resistance of breast cancer cells via regulation of caspase, H2A.X and Let-7 signaling. PLoS ONE 2013, 8:e67373.
32. Lv K., Liu L., Wang L., Yu J., Liu X., Cheng Y., et al. Lin28 mediates paclitaxel resistance by modulating p21, Rb and Let-7a miRNA in breast cancer cells. PLoS ONE 2012, 7:e40008.
33. Pan L., Gong Z., Zhong Z., Dong Z., Liu Q., Le Y., et al. Lin-28 reactivation is required for let-7 repression and proliferation in human small cell lung cancer cells. Mol. Cell. Biochem 2011, 355:257-263.
34. Oh J.S., Kim J.J., Byun J.Y., Kim I.A. Lin28-let7 modulates radiosensitivity of human cancer cells with activation of K-Ras. Int. J. Radiat. Oncol. Biol. Phys 2010, 76:5-8.
35. Wen J., Liu H., Wang Q., Liu Z., Li Y., Xiong H., et al. Genetic variants of the LIN28B gene predict severe radiation pneumonitis in patients with non-small cell lung cancer treated with definitive radiation therapy. Eur. J. Cancer 2014, 50:1706-1716.
36. Qiu J.L., Huang P.Z., You J.H., Zou R.H., Wang L., Hong J., et al. LIN28 expression and prognostic value in hepatocellular carcinoma patients who meet the Milan criteria and undergo hepatectomy. Chin J Cancer 2012, 31:223-232.
37. King C.E., Cuatrecasas M., Castells A., Sepulveda A.R., Lee J.S., Rustgi A.K. LIN28B promotes colon cancer progression and metastasis. Cancer Res 2011, 71:4260-4268.
38. Madison B.B., Liu Q., Zhong X., Hahn C.M., Lin N., Emmett M.J., et al. LIN28B promotes growth and tumorigenesis of the intestinal epithelium via Let-7. Genes Dev 2013, 27:2233-2245.
39. Parasramka M.A., Dashwood W.M., Wang R., Abdelli A., Bailey G.S., Williams D.E., et al. MicroRNA profiling of carcinogen-induced rat colon tumors and the influence of dietary spinach. Mol. Nutr. Food Res 2012, 56:1259-1269.
40. Wang T., Wang G., Hao D., Liu X., Wang D., Ning N., et al. Aberrant regulation of the LIN28A/LIN28B and let-7 loop in human malignant tumors and its effects on the hallmarks of cancer. Mol. Cancer 2015, 14:125.
41. Tummala R., Nadiminty N., Lou W., Zhu Y., Gandour-Edwards R., Chen H.W., et al. Lin28 promotes growth of prostate cancer cells and activates the androgen receptor. Am. J. Pathol 2013, 183:288-295.
42. Molenaar J.J., Domingo-Fernandez R., Ebus M.E., Lindner S., Koster J., Drabek K., et al. LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat. Genet 2012, 44:1199-1206.
43. Mao X.G., Hutt-Cabezas M., Orr B.A., Weingart M., Taylor I., Rajan A.K., et al. LIN28A facilitates the transformation of human neural stem cells and promotes glioblastoma tumorigenesis through a pro-invasive genetic program. Oncotarget 2013, 4:1050-1064.
44. Helland A., Anglesio M.S., George J., Cowin P.A., Johnstone C.N., House C.M., et al. Deregulation of MYCN, LIN28B and LET7 in a molecular subtype of aggressive high-grade serous ovarian cancers. PLoS ONE 2011, 6:e18064.
45. Kwon M.J., Shin Y.K. Regulation of ovarian cancer stem cells or tumor-initiating cells. Int. J. Mol. Sci 2013, 14:6624-6648.
46. Hsu K.F., Shen M.R., Huang Y.F., Cheng Y.M., Lin S.H., Chow N.H., et al. Overexpression of the RNA-binding proteins Lin28B and IGF2BP3 (IMP3) is associated with chemoresistance and poor disease outcome in ovarian cancer. Br. J. Cancer 2015, 113:414-424.
47. Alajez N.M., Shi W., Wong D., Lenarduzzi M., Waldron J., Weinreb I., et al. Lin28b promotes head and neck cancer progression via modulation of the insulin-like growth factor survival pathway. Oncotarget 2012, 3:1641-1652.
48. Jiang X., Huang H., Li Z., Li Y., Wang X., Gurbuxani S., et al. Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-associated leukemia. Cancer Cell 2012, 22:524-535.
49. Nguyen L.H., Robinton D.A., Seligson M.T., Wu L., Li L., Rakheja D., et al. Lin28b is sufficient to drive liver cancer and necessary for its maintenance in murine models. Cancer Cell 2014, 26:248-261.
50. Urbach A., Yermalovich A., Zhang J., Spina C.S., Zhu H., Perez-Atayde A.R., et al. Lin28 sustains early renal progenitors and induces Wilms tumor. Genes Dev 2014, 28:971-982.
51. Hamano R., Miyata H., Yamasaki M., Sugimura K., Tanaka K., Kurokawa Y., et al. High expression of Lin28 is associated with tumour aggressiveness and poor prognosis of patients in oesophagus cancer. Br. J. Cancer 2012, 106:1415-1423.
52. Chen C., Cao F., Bai L., Liu Y., Xie J., Wang W., et al. IKKbeta enforces a LIN28B/TCF7L2 positive feedback loop that promotes cancer cell stemness and metastasis. Cancer Res 2015, 75:1725-1735.
53. Tsialikas J., Romer-Seibert J. LIN28: roles and regulation in development and beyond. Development 2015, 142:2397-2404.
54. O'Day E., Le M.T., Imai S., Tan S.M., Kirchner R., Arthanari H., et al. An RNA-binding protein, Lin28, recognizes and remodels G-quartets in the MicroRNAs (miRNAs) and mRNAs it regulates. J. Biol. Chem 2015, 290:17909-17922.
55. Bussing I., Slack F.J., Grosshans H. let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med 2008, 14:400-409.
56. Boyerinas B., Park S.M., Hau A., Murmann A.E., Peter M.E. The role of let-7 in cell differentiation and cancer. Endocr. Relat. Cancer 2010, 17:F19-F36.
57. Ji J., Wang X.W. A Yin-Yang balancing act of the lin28/let-7 link in tumorigenesis. J. Hepatol 2010, 53:974-975.
58. Kolenda T., Przybyla W., Teresiak A., Mackiewicz A., Lamperska K.M. The mystery of let-7d - a small RNA with great power. Contemp. Oncol 2014, 18:293-301.
59. Li Y., Zhao Z., Xu C., Zhou Z., Zhu Z., You T. HMGA2 induces transcription factor Slug expression to promote epithelial-to-mesenchymal transition and contributes to colon cancer progression. Cancer Lett 2014, 355:130-140.
60. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
61. Ma X., Li C., Sun L., Huang D., Li T., He X., et al. Lin28/let-7 axis regulates aerobic glycolysis and cancer progression via PDK1. Nat. Commun 2014, 5:5212.
62. Sakurai M., Miki Y., Masuda M., Hata S., Shibahara Y., Hirakawa H., et al. LIN28: a regulator of tumor-suppressing activity of let-7 microRNA in human breast cancer. J. Steroid Biochem. Mol. Biol 2012, 131:101-106.
63. Voutsadakis I.A. The network of pluripotency, epithelial-mesenchymal transition, and prognosis of breast cancer. Breast Cancer (Dove Med Press) 2015, 7:303-319.
64. Zhu H., Shyh-Chang N., Segre A.V., Shinoda G., Shah S.P., Einhorn W.S., et al. The Lin28/let-7 axis regulates glucose metabolism. Cell 2011, 147:81-94.
65. Balzer E., Heine C., Jiang Q., Lee V.M., Moss E.G. LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 2010, 137:891-900.
66. Warrander F., Faas L., Kovalevskiy O., Peters D., Coles M., Antson A.A., et al. Lin28 proteins promote expression of 17 ~ 92 family miRNAs during amphibian development. Dev. Dyn 2015, 245:34-46.
67. Wilbert M.L., Huelga S.C., Kapeli K., Stark T.J., Liang T.Y., Chen S.X., et al. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol. Cell 2012, 48:195-206.
68. Hafner M., Max K.E., Bandaru P., Morozov P., Gerstberger S., Brown M., et al. Identification of mRNAs bound and regulated by human LIN28 proteins and molecular requirements for RNA recognition. RNA 2013, 19:613-626.
69. Dai Q., Luan G., Deng L., Lei T., Kang H., Song X., et al. Primordial dwarfism gene maintains Lin28 expression to safeguard embryonic stem cells from premature differentiation. Cell Rep 2014, 7:735-746.
70. Shyh-Chang N., Zhu H., Yvanka de Soysa T., Shinoda G., Seligson M.T., Tsanov K.M., et al. Lin28 enhances tissue repair by reprogramming cellular metabolism. Cell 2013, 155:778-792.
71. Smalheiser N.R. The RNA-centred view of the synapse: non-coding RNAs and synaptic plasticity. Philos. Trans. R. Soc. Lond. B. Biol Sci 2014, 369.
72. Cho J., Chang H., Kwon S.C., Kim B., Kim Y., Choe J., et al. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 2012, 151:765-777.
73. Peng S., Chen L.L., Lei X.X., Yang L., Lin H., Carmichael G.G., et al. Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem. Cells 2011, 29:496-504.
74. Beckers A., Van Peer G., Carter D.R., Gartlgruber M., Herrmann C., Agarwal S., et al. MYCN-driven regulatory mechanisms controlling LIN28B in neuroblastoma. Cancer Lett 2015, 366:123-132.
75. Sampson V.B., Rong N.H., Han J., Yang Q., Aris V., Soteropoulos P., et al. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res 2007, 67:9762-9770.
76. Chang T.C., Zeitels L.R., Hwang H.W., Chivukula R.R., Wentzel E.A., Dews M., et al. Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3384-3389.
77. Cai W.Y., Wei T.Z., Luo Q.C., Wu Q.W., Liu Q.F., Yang M., et al. The Wnt-beta-catenin pathway represses let-7 microRNA expression through transactivation of Lin28 to augment breast cancer stem cell expansion. J. Cell Sci 2013, 126:2877-2889.
78. Yuan J., Nguyen C.K., Liu X., Kanellopoulou C., Muljo S.A. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 2012, 335:1195-1200.
79. Zhou Y., Li Y.S., Bandi S.R., Tang L., Shinton S.A., Hayakawa K., et al. Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J. Exp. Med 2015, 212:569-580.
80. Lee Y.T., de Vasconcellos J.F., Yuan J., Byrnes C., Noh S.J., Meier E.R., et al. LIN28B-mediated expression of fetal hemoglobin and production of fetal-like erythrocytes from adult human erythroblasts ex vivo. Blood 2013, 122:1034-1041.
81. Beachy S.H., Onozawa M., Chung Y.J., Slape C., Bilke S., Francis P., et al. Enforced expression of Lin28b leads to impaired T-cell development, release of inflammatory cytokines, and peripheral T-cell lymphoma. Blood 2012, 120:1048-1059.
82. Rao S., Lee S.Y., Gutierrez A., Perrigoue J., Thapa R.J., Tu Z., et al. Inactivation of ribosomal protein L22 promotes transformation by induction of the stemness factor, Lin28B. Blood 2012, 120:3764-3773.
83. Chaudhuri A.A., So A.Y., Mehta A., Minisandram A., Sinha N., Jonsson V.D., et al. Oncomir miR-125b regulates hematopoiesis by targeting the gene Lin28A. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4233-4238.
84. Wang L.D., Rao T.N., Rowe R.G., Nguyen P.T., Sullivan J.L., Pearson D.S., et al. The role of Lin28b in myeloid and mast cell differentiation and mast cell malignancy. Leukemia 2015, 29:1320-1330.
85. Pobezinsky L.A., Etzensperger R., Jeurling S., Alag A., Kadakia T., McCaughtry T.M., et al. Let-7 microRNAs target the lineage-specific transcription factor PLZF to regulate terminal NKT cell differentiation and effector function. Nat. Immunol 2015, 16:517-524.
86. Li X., Zhang J., Gao L., McClellan S., Finan M.A., Butler T.W., et al. MiR-181 mediates cell differentiation by interrupting the Lin28 and let-7 feedback circuit. Cell Death Differ 2012, 19:378-386.
87. Boldin M.P., Baltimore D. MicroRNAs, new effectors and regulators of NF-kappaB. Immunol. Rev 2012, 246:205-220.
88. Baltimore D. NF-kappaB is 25. Nat. Immunol 2011, 12:683-685.