TGF-β/β2-spectrin/CTCF-regulated tumor suppression in human stem cell disorder Beckwith-Wiedemann syndrome

Journal of Clinical Investigation

Volumn 126, Issue 2, 2016, Pages 527-542

  Chen, Jian ^a   Yao, Zhi Xing ^a   Chen, Jiun Sheng ^a   Gi, Young Jin ^a   Muñoz, Nina M ^a   Kundra, Suchin ^a   Herlong, H Franklin ^a   Jeong, Yun Seong ^a   Goltsov, Alexei ^a   Ohshiro, Kazufumi ^b   Mistry, Nipun A ^a   Zhang, Jianping ^a   Su, Xiaoping ^a   Choufani, Sanaa ^c   Mitra, Abhisek ^a   Li, Shulin ^a   Mishra, Bibhuti ^b   White, Jon ^b   Rashid, Asif ^a   Wang, Alan Yaoqi ^a   Javle, Milind ^a   Davila, Marta ^a   Michaely, Peter ^d   Weksberg, Rosanna ^c   Hofstetter, Wayne L ^a   Finegold, Milton J ^e   Shay, Jerry W ^d   Machida, Keigo ^f   Tsukamoto, Hidekazu ^f,g   Mishra, Lopa ^a,b,h   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g VETERANS AFFAIRS MEDICAL CENTER   (United States)

^h GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; POTASSIUM CHANNEL KCNQ1; SMAD3 PROTEIN; SOMATOMEDIN B; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR CTCF; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; ACTIN BINDING PROTEIN; CARRIER PROTEIN; CCCTC-BINDING FACTOR; CDKN1C PROTEIN, HUMAN; CDKN1C PROTEIN, MOUSE; FODRIN; IGF2 PROTEIN, HUMAN; IGF2 PROTEIN, MOUSE; KCNQ1 PROTEIN, HUMAN; KCNQ1 PROTEIN, MOUSE; REPRESSOR PROTEIN; SMAD3 PROTEIN, HUMAN; SMAD3 PROTEIN, MOUSE; TELOMERASE; TERT PROTEIN, HUMAN; TERT PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BECKWITH WIEDEMANN SYNDROME; CARCINOGENESIS; CHROMATIN; CHROMOSOME 11P; CHROMOSOME 11P15.5; CONTROLLED STUDY; FIBROBLAST; GENE LOCUS; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HETEROZYGOTE; HUMAN; HUMAN CELL; MOUSE; MULTIPLE CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SOMATIC MUTATION; ANIMAL; BIOSYNTHESIS; CHROMOSOME 11; GENETICS; HEP-G2 CELL LINE; KNOCKOUT MOUSE; METABOLISM; NEOPLASM;

ANIMALS; BECKWITH-WIEDEMANN SYNDROME; CARRIER PROTEINS; CHROMOSOMES, HUMAN, PAIR 11; CYCLIN-DEPENDENT KINASE INHIBITOR P57; HEP G2 CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR II; KCNQ1 POTASSIUM CHANNEL; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NEOPLASM PROTEINS; NEOPLASMS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TELOMERASE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84956893042     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80937     Document Type: Article

References (56)

1. Pettenati MJ, Haines JL, Higgins RR, Wappner RS, Palmer CG, Weaver DD. Wiedemann-Beckwith syndrome: presentation of clinical and cytogenetic data on 22 new cases and review of the literature. Hum Genet. 1986;74(2):143-154.
2. Weksberg R, Shuman C, Beckwith JB. Beckwith-Wiedemann syndrome. Eur J Hum Genet. 2010;18(1):8-14.
3. DeBaun MR, Tucker MA. Risk of cancer during the first four years of life in children from The Beckwith-Wiedemann Syndrome Registry. J Pediatr. 1998;132(3 pt 1):398-400.
4. Hadzic N, Finegold MJ. Liver neoplasia in children. Clin Liver Dis. 2011;15(2):443-462.
5. Keller RB, Demellawy DE, Quaglia A, Finegold M, Kapur RP. Methylation status of the chromosome arm 19q MicroRNA cluster in sporadic and androgenetic-biparental mosaicism-associated hepatic mesenchymal hamartoma. Pediatr Dev Pathol. 2015;18(3):218-227.
6. Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet. 2006;7(1):21-33.
7. Murrell A, et al. An association between variants in the IGF2 gene and Beckwith-Wiedemann syndrome: interaction between genotype and epigenotype. Hum Mol Genet. 2004;13(2):247-255.
8. Ishihara K, Oshimura M, Nakao M. CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell. 2006;23(5):733-742.
9. Sun FL, Dean WL, Kelsey G, Allen ND, Reik W. Transactivation of Igf2 in a mouse model of Beckwith-Wiedemann syndrome. Nature. 1997;389(6653):809-815.
10. Choufani S, Shuman C, Weksberg R. Molecular findings in Beckwith-Wiedemann syndrome. Am J Med Genet C Semin Med Genet. 2013;163C(2):131-140.
11. Sakatani T, et al. Loss of imprinting of Igf2 alters intestinal maturation and tumorigenesis in mice. Science. 2005;307(5717):1976-1978.
12. Harper J, Burns JL, Foulstone EJ, Pignatelli M, Zaina S, Hassan AB. Soluble IGF2 receptor rescues Apc(Min/+) intestinal adenoma progression induced by Igf2 loss of imprinting. Cancer Res. 2006;66(4):1940-1948.
13. Ravenel JD, et al. Loss of imprinting of insulinlike growth factor-II (IGF2) gene in distinguishing specific biologic subtypes of Wilms tumor. J Natl Cancer Inst. 2001;93(22):1698-1703.
14. Handoko L, et al. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet. 2011;43(7):630-638.
15. Fiorentino FP, Giordano A. The tumor suppressor role of CTCF. J Cell Physiol. 2012;227(2):479-492.
16. Bliek J, et al. Increased tumour risk for BWS patients correlates with aberrant H19 and not KCNQ1OT1 methylation: occurrence of KCNQ1OT1 hypomethylation in familial cases of BWS. Hum Mol Genet. 2001;10(5):467-476.
17. Weksberg R, et al. Tumor development in the Beckwith-Wiedemann syndrome is associated with a variety of constitutional molecular 11p15 alterations including imprinting defects of KCNQ1OT1. Hum Mol Genet. 2001;10(26):2989-3000.
18. Matsuoka S, et al. p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev. 1995;9(6):650-662.
19. Tsugu A, et al. Expression of p57(KIP2) potently blocks the growth of human astrocytomas and induces cell senescence. Am J Pathol. 2000;157(3):919-932.
20. Bourcigaux N, Gaston V, Logie A, Bertagna X, Le Bouc Y, Gicquel C. High expression of cyclin E and G1 CDK and loss of function of p57KIP2 are involved in proliferation of malignant sporadic adrenocortical tumors. J Clin Endocrinol Metab. 2000;85(1):322-330.
21. Lam WW, et al. Analysis of germline CDKN1C (p57KIP2) mutations in familial and sporadic Beckwith-Wiedemann syndrome (BWS) provides a novel genotype-phenotype correlation. J Med Genet. 1999;36(7):518-523.
22. Li M, et al. Imprinting status of 11p15 genes in Beckwith-Wiedemann syndrome patients with CDKN1C mutations. Genomics. 2001;74(3):370-376.
23. Massague J, Blain SW, Lo RS. TGFβ signaling in growth control, cancer, and heritable disorders. Cell. 2000;103(2):295-309.
24. Moses HL, Serra R. Regulation of differentiation by TGF-β. Curr Opin Genet Dev. 1996;6(5):581-586.
25. Shi Y, Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell. 2003;113(6):685-700.
26. Wu G, et al. Structural basis of Smad2 recognition by the Smad anchor for receptor activation. Science. 2000;287(5450):92-97.
27. Mishra L, Marshall B. Adaptor proteins and ubiquinators in TGF-β signaling. Cytokine Growth Factor Rev. 2006;17(1-2):75-87.
28. Tang Y, Katuri V, Dillner A, Mishra B, Deng CX, Mishra L. Disruption of transforming growth factor-β signaling in ELF β-spectrin-deficient mice. Science. 2003;299(5606):574-577.
29. Ross S, Cheung E, Petrakis TG, Howell M, Kraus WL, Hill CS. Smads orchestrate specific histone modifications and chromatin remodeling to activate transcription. EMBO J. 2006;25(19):4490-4502.
30. Stampfer MR, Garbe J, Levine G, Lichtsteiner S, Vasserot AP, Yaswen P. Expression of the telomerase catalytic subunit, hTERT, induces resistance to transforming growth factor β growth inhibition in p16INK4A(-) human mammary epithelial cells. Proc Natl Acad Sci U S A. 2001;98(8):4498-4503.
31. Cong Y, Shay JW. Actions of human telomerase beyond telomeres. Cell Res. 2008;18(7):725-732.
32. Choi J, et al. TERT promotes epithelial proliferation through transcriptional control of a Mycand Wnt-related developmental program. PLoS Genet. 2008;4(1):10.
33. Yao ZX, et al. Epigenetic silencing of β-spectrin, a TGF-β signaling/scaffolding protein in a human cancer stem cell disorder: Beckwith-Wiedemann syndrome. J Biol Chem. 2010;285(46):36112-36120.
34. Gao J, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269):pl1.
35. Cerami E, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401-404.
36. Bae DS, Blazanin N, Licata M, Lee J, Glick AB. Tumor suppressor and oncogene actions of TGFβ1 occur early in skin carcinogenesis and are mediated by Smad3. Mol Carcinog. 2009;48(5):441-453.
37. Piek E, et al. Functional characterization of transforming growth factor β signaling in Smad2-and Smad3-deficient fibroblasts. J Biol Chem. 2001;276(23):19945-19953.
38. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev. 2005;19(23):2783-2810.
39. Plasschaert RN, et al. CTCF binding site sequence differences are associated with unique regulatory and functional trends during embryonic stem cell differentiation. Nucleic Acids Res. 2014;42(2):774-789.
40. Nakahashi H, et al. A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep. 2013;3(5):1678-1689.
41. Chen CL, et al. Reciprocal regulation by TLR4 and TGF-β in tumor-initiating stem-like cells. J Clin Invest. 2013;123(7):2832-2849.
42. Majumdar A, et al. Hepatic stem cells and transforming growth factor β in hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol. 2012;9(9):530-538.
43. Bhowmick NA, et al. TGF-β signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science. 2004;303(5659):848-851.
44. Markowitz S, et al. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science. 1995;268(5215):1336-1338.
45. van Hattem WA, et al. Large genomic deletions of SMAD4, BMPR1A and PTEN in juvenile polyposis. Gut. 2008;57(5):623-627.
46. Hahn SA, et al. Allelotype of pancreatic adenocarcinoma using xenograft enrichment. Cancer Res. 1995;55(20):4670-4675.
47. Walczak EM, Hammer GD. Regulation of the adrenocortical stem cell niche: implications for disease. Nat Rev Endocrinol. 2015;11(1):14-28.
48. Simon DP, Hammer GD. Adrenocortical stem and progenitor cells: implications for adrenocortical carcinoma. Mol Cell Endocrinol. 2012;351(1):2-11.
49. Martin YC, Danaher EB, May CS, Weininger D, Van Drie JH. Strategies in drug design based on 3D-structures of ligands. Prog Clin Biol Res. 1989;291:177-181.
50. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature. 1995;375(6526):34-39.
51. Leighton PA, Saam JR, Ingram RS, Stewart CL, Tilghman SM. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev. 1995;9(17):2079-2089.
52. Eggenschwiler J, Ludwig T, Fisher P, Leighton PA, Tilghman SM, Efstratiadis A. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev. 1997;11(23):3128-3142.
53. Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet. 2002;32(3):426-431.
54. Zhang P, et al. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature. 1997;387(6629):151-158.
55. Cano-Gauci DF, et al. Glypican-3-deficient mice exhibit developmental overgrowth and some of the abnormalities typical of Simpson-Golabi-Behmel syndrome. J Cell Biol. 1999;146(1):255-264.
56. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest. 2004;113(2):160-168.