Loss of imprinting of IGF2 and the epigenetic progenitor model of cancer

American Journal of Stem Cells

Volumn 1, Issue 1, 2012, Pages 59-74

  Leick, Mark B ^a   Shoff, Christopher J ^a   Wang, Erwin C ^a   Congress, Jaclyn L ^a   Gallicano, G Ian ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer stem cell; Epigenetic; Insulin like growth factor 2 (IGF2); Loss of imprinting; Progenitor

Indexed keywords

BIOLOGICAL MARKER; DNA METHYLTRANSFERASE 1; POLYCOMB REPRESSIVE COMPLEX 2; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR EZH2; ZINC FINGER PROTEIN;

ALLELE; BECKWITH WIEDEMANN SYNDROME; BREAST CANCER; CANCER STEM CELL; CARCINOGENESIS; CHROMATIN; COLON CANCER; COLORECTAL CARCINOMA; DNA METHYLATION; DNA PROTEIN COMPLEX; EPIGENETICS; ESOPHAGEAL ADENOCARCINOMA; GENE DOSAGE; GENE OVEREXPRESSION; GENOME IMPRINTING; HISTONE METHYLATION; HUMAN; INTRACELLULAR SIGNALING; LUNG CANCER; METASTASIS; MOLECULAR IMPRINTING; NEPHROBLASTOMA; NONHUMAN; OVARY CARCINOMA; PERIPHERAL LYMPHOCYTE; PROSTATE CANCER; RECEPTOR UPREGULATION; REVIEW; SILVER RUSSELL SYNDROME; SOLID TUMOR; STOMACH CANCER;

EID: 85026339189     PISSN: None     EISSN: 21604150     Source Type: Journal    
DOI: None     Document Type: Review

References (124)

1. Institute NC. Surveillance Epidemiology and End Results: SEER stat fact sheets. 2009; 2009:
2. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, Jones DL, Visvader J, Weissman IL and Wahl GM. Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer research 2006; 66: 9339.
3. Gao JX and Zhou Q. Epigenetic progenitors in tumor initiation and development. Drug Discovery Today: Disease Models 2009; 6: 5-12.
4. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA and Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD and Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences 2003; 100: 3983.
7. Collins AT, Berry PA, Hyde C, Stower MJ and Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer research 2005; 65: 10946.
8. Foshay K, Miera A, Stuart A, Fingland N, Mobley S and Gallicano G. Unraveling the complex nature of prostate cancer stem cells. Cancer Biomarkers 2007; 3: 233-244.
9. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T and Moriwaki H. Characterization of CD133 hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochemical and biophysical research communications 2006; 351: 820-824.
10. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H and Wan D. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. International journal of cancer 2007; 120: 1444-1450.
11. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH and Simeone DM. Phenotypic characterization of human colorectal cancer stem cells. Proceedings of the National Academy of Sciences 2007; 104: 10158.
12. O'Brien CA, Pollett A, Gallinger S and Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2006; 445: 106-110.
13. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C and De Maria R. Identification and expansion of human coloncancer-initiating cells. Nature 2006; 445: 111-115.
14. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF and Simeone DM. Identification of pancreatic cancer stem cells. Cancer research 2007; 67: 1030.
15. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF and Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences 2007; 104: 973.
16. Allan AL, Vantyghem SA, Tuck AB and Chambers AF. Tumor dormancy and cancer stem cells: implications for the biology and treatment of breast cancer metastasis. Breast disease 2007; 26: 87-98.
17. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
18. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V and Stewart R. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917.
19. Li F, Tiede B, Massagué J and Kang Y. Beyond tumorigenesis: cancer stem cells in metastasis. Cell research 2006; 17: 3-14.
20. Kucia M and Ratajczak MZ. Stem cells as a two edged sword-from regeneration to tumor formation. Journal of physiology and pharmacology 2006; 57: 5.
21. Cui H, Cruz-Correa M, Giardiello FM, Hutcheon DF, Kafonek DR, Brandenburg S, Wu Y, He X, Powe NR and Feinberg AP. Loss of IGF2 imprinting: a potential marker of colorectal cancer risk. Science 2003; 299: 1753.
22. Jelinic P and Shaw P. Loss of imprinting and cancer. Journal of Pathology 2007; 211: 261-268.
23. Sturm KS, Flannery ML and Pedersen RA. Abnormal development of embryonic and extraembryonic cell lineages in parthenogenetic mouse embryos. Developmental Dynamics 1994; 201: 11-28.
24. Reik W, Constancia M, Dean W, Davies K, Bowden L, Murrell A, Feil R, Walter J and Kelsey G. Ig/2 imprinting in development and disease. Chromosomes today 2000; 13: 93.
25. Sasaki HK, Ishihara K and Kato R. Mechanisms of Igf2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. Journal of Biochemistry 2000; 127: 711.
26. Arney KL. H19 and Igf2-enhancing the confusion? Trends in Genetics 2003; 19: 17-23.
27. Engel N and Bartolomei MS. Mechanisms of insulator function in gene regulation and genomic imprinting. International review of cytology 2003; 232: 89-127.
28. Murrell A, Heeson S and Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nature genetics 2004; 36: 889-893.
29. Bell AC and Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000; 405: 482-485.
30. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM and Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000; 405: 486-489.
31. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, Ohlsson R and Lobanenkov VV. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Current Biology 2000; 10: 853-856.
32. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, Hou A, Vu TH and Hoffman AR. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Molecular and cellular biology 2008; 28: 6473.
33. Yusufzai TM, Tagami H, Nakatani Y and Felsenfeld G. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Molecular cell 2004; 13: 291-298.
34. Zhang H, Niu B, Hu JF, Ge S, Wang H, Li T, Ling J, Steelman BN, Qian G and Hoffman AR. Interruption of intrachromosomal looping by CCCTC binding factor decoy proteins abrogates genomic imprinting of human insulin-like growth factor II. The Journal of cell biology 2011; 193: 475.
35. Ideraabdullah FY, Abramowitz LK, Thorvaldsen JL, Krapp C, Wen SC, Engel N and Bartolomei MS. Novel cis-regulatory function in ICR-mediated imprinted repression of H19. Developmental biology 2011;
36. Vu TH, Nguyen AH and Hoffman AR. Loss of IGF2 imprinting is associated with abrogation of long-range intrachromosomal interactions in human cancer cells. Human molecular genetics 2010; 19: 901.
37. Morison IM, Ramsay JP and Spencer HG. A census of mammalian imprinting. Trends in Genetics 2005; 21: 457-465.
38. DeChiara TM, Robertson EJ and Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 1991; 64: 849-859.
39. Sun FL, Dean WL, Kelsey G, Allen ND and Reik W. Transactivation of Igf2 in a mouse model of Beckwith-Wiedemann syndrome. Nature 1997; 389: 809-815.
40. Uribe-Lewis S, Woodfine K, Stojic L and Murrell A. Molecular mechanisms of genomic imprinting and clinical implications for cancer. Expert Reviews in Molecular Medicine 2011; 13:
41. Holm TM, Jackson-Grusby L, Brambrink T, Yamada Y, Rideout Iii WM and Jaenisch R. Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell 2005; 8: 275-285.
42. Rogler CE, Yang D, Rossetti L, Donohoe J, Alt E, Chang CJ, Rosenfeld R, Neely K and Hintz R. Altered body composition and increased frequency of diverse malignancies in insulin-like growth factor-II transgenic mice. Journal of Biological Chemistry 1994; 269: 13779.
43. Binder G, Seidel AK, Weber K, Haase M, Wollmann HA, Ranke MB and Eggermann T. IGF-II serum levels are normal in children with Silver-Russell syndrome who frequently carry epimutations at the IGF2 locus. Journal of Clinical Endocrinology & Metabolism 2006; 91: 4709.
44. Cui H. Loss of imprinting of IGF2 as an epigenetic marker for the risk of human cancer. Disease markers 2007; 23: 105-112.
45. Woodson K, Flood A, Green L, Tangrea JA, Hanson J, Cash B, Schatzkin A and Schoenfeld P. Loss of insulin-like growth factor-II imprinting and the presence of screen-detected colorectal adenomas in women. Journal of the National Cancer Institute 2004; 96: 407.
46. Sakatani T, Kaneda A, Iacobuzio-Donahue CA, Carter MG, de Boom Witzel S, Okano H, Ko MS, Ohlsson R, Longo DL and Feinberg AP. Loss of imprinting of Igf2 alters intestinal maturation and tumorigenesis in mice. Science 2005; 307: 1976-1978.
47. Feinberg AP, Ohlsson R and Henikoff S. The epigenetic progenitor origin of human cancer. Nature reviews genetics 2006; 7: 21-33.
48. Sparago A, Cerrato F, Vernucci M, Ferrero GB, Silengo MC and Riccio A. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nature genetics 2004; 36: 958-960.
49. Fu VX, Dobosy JR, Desotelle JA, Almassi N, Ewald JA, Srinivasan R, Berres M, Svaren J, Weindruch R and Jarrard DF. Aging and cancer-related loss of insulin-like growth factor 2 imprinting in the mouse and human prostate. Cancer research 2008; 68: 6797.
50. Bhusari S, Yang B, Kueck J, Huang W and Jarrard DF. Insulin-like growth factor-2 (IGF2) loss of imprinting marks a field defect within human prostates containing cancer. The Prostate 2011;
51. Kaneda A, Wang CJ, Cheong R, Timp W, Onyango P, Wen B, Iacobuzio-Donahue CA, Ohlsson R, Andraos R, Pearson MA, Sharov AA, Longo DL, Ko MS, Levchenko A and Feinberg AP. Enhanced sensitivity to IGF-II signaling links loss of imprinting of IGF2 to increased cell proliferation and tumor risk. Proceedings of the National Academy of Sciences of the United States of America 2007; 104: 20926-20931.
52. Rainier S, Johnson LA, Dobry CJ, Ping AJ, Grundy PE and Feinberg AP. Relaxation of imprinted genes in human cancer. Nature 1993; 362: 747-749.
53. Bjornsson HT, Brown LJ, Fallin MD, Rongione MA, Bibikova M, Wickham E, Fan JB and Feinberg AP. Epigenetic specificity of loss of imprinting of the IGF2 gene in Wilms tumors. Journal of the National Cancer Institute 2007; 99: 1270.
54. Fukuzawa R, Anaka MR, Heathcott RW, McNoe LA, Morison IM, Perlman EJ and Reeve AE. Wilms tumour histology is determined by distinct types of precursor lesions and not epigenetic changes. The Journal of pathology 2008; 215: 377-387.
55. Hubertus J, Lacher M, Rottenkolber M, MÜLler-HÖCker J, Berger M, Stehr M, Von Schweinitz D and Kappler R. Altered expression of imprinted genes in Wilms tumors. Oncology reports 2011; 25: 817-823.
56. Hajdu M, Singer S, Maki RG, Schwartz GK, Keohan ML and Antonescu CR. IGF2 over-expression in solitary fibrous tumours is independent of anatomical location and is related to loss of imprinting. The Journal of pathology 2010; 221: 300-307.
57. Zhao R, DeCoteau JF, Geyer CR, Gao M, Cui H and Casson AG. Loss of imprinting of the insulin-like growth factor II (IGF2) gene in esophageal normal and adenocarcinoma tissues. Carcinogenesis 2009; 30: 2117.
58. Dammann RH, Kirsch S, Schagdarsurengin U, Dansranjavin T, Gradhand E, Schmitt WD and Hauptmann S. Frequent aberrant methylation of the imprinted IGF2/H19 locus and LINE1 hypomethylation in ovarian carcinoma. International journal of oncology 2010; 36: 171-179.
59. Murphy SK, Huang Z, Wen Y, Spillman MA, Whitaker RS, Simel LR, Nichols TD, Marks JR and Berchuck A. Frequent IGF2/H19 domain epigenetic alterations and elevated IGF2 expression in epithelial ovarian cancer. Molecular cancer research 2006; 4: 283.
60. Zuo QS, Yan R, Feng DX, Zhao R, Chen C, Jiang YM, Curz-Correa M, Casson AG, Kang XD and Han F. Loss of imprinting and abnormal expression of the insulin-like growth factor 2 gene in gastric cancer. Molecular carcinogenesis 50: 390-396.
61. Lu Y, Lu P, Zhu Z, Xu H and Zhu X. Loss of imprinting of insulin-like growth factor 2 is associated with increased risk of lymph node metastasis and gastric corpus cancer. Journal of Experimental & Clinical Cancer Research 2009; 28: 125.
62. Grbesa I, Marinkovic M, Ivkic M, Kruslin B, Novak-Kujundzic R, Pegan B, Bogdanovic O, Bedekovic V and Gall-Troselj K. Loss of imprinting of IGF2 and H19, loss of heterozygosity of IGF2R and CTCF, and Helicobacter pylori infection in laryngeal squamous cell carcinoma. Journal of molecular medicine 2008; 86: 1057-1066.
63. Shetty PJ, Movva S, Pasupuleti N, Vedicherlla B, Vattam KK, Venkatasubramanian S, Ahuja YR and Hasan Q. Regulation of IGF2 transcript and protein expression by altered methylation in breast cancer. Journal of cancer research and clinical oncology 2011; 137: 339-345.
64. Ito Y, Koessler T, Ibrahim AEK, Rai S, Vowler SL, Abu-Amero S, Silva AL, Maia AT, Huddleston JE and Uribe-Lewis S. Somatically acquired hypomethylation of IGF2 in breast and colorectal cancer. Human molecular genetics 2008; 17: 2633.
65. Miroglio A, Jammes H, Tost J, Ponger L, Gut IG, Abdalaoui HE, Coste J, Chaussade S, Arimondo PB and Lamarque D. Specific hypomethylated CpGs at the IGF2 locus act as an epigenetic biomarker for familial adenomatous polyposis colorectal cancer. Epigenomics 2010; 2: 365-375.
66. Liou JM, Shun CT, Liang JT, Chiu HM, Chen MJ, Chen CC, Wang HP, Wu MS and Lin JT. Plasma insulin-like growth factor-binding protein-2 levels as diagnostic and prognostic biomarker of colorectal cancer. Journal of Clinical Endocrinology & Metabolism 2010; 95: 1717.
67. Ohta M, Sugimoto T, Seto M, Mohri D, Asaoka Y, Tada M, Tanaka Y, Yamaji Y, Kanai F and Kawabe T. Genetic alterations in colorectal cancers with demethylation of insulin-like growth factor II. Human pathology 2008; 39: 1301-1308.
68. Sasaki J, Konishi F, Kawamura YJ, Kai T, Takata O and Tsukamoto T. Clinicopathological characteristics of colorectal cancers with loss of imprinting of insulin-like growth factor 2. International journal of cancer 2006; 119: 80-83.
69. Cheng YW, Idrees K, Shattock R, Khan SA, Zeng Z, Brennan CW, Paty P and Barany F. Loss of imprinting and marked gene elevation are 2 forms of aberrant IGF2 expression in colorectal cancer. International Journal of Cancer 2010; 127: 568-577.
70. Reya T, Morrison SJ, Clarke MF and Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
71. Jordan CT, Guzman ML and Noble M. Cancer stem cells. New England Journal of Medicine 2006; 355: 1253-1261.
72. Bonnet D and Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature medicine 1997; 3: 730-737.
73. Kelly PN, Dakic A, Adams JM, Nutt SL and Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 2007; 317: 337.
74. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. NATURE-LONDON-2006; 444: 756.
75. Matsui W, Wang Q, Barber JP, Brennan S, Smith BD, Borrello I, McNiece I, Lin L, Ambinder RF and Peacock C. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer research 2008; 68: 190.
76. Pearce DJ, Taussig D, Zibara K, Smith LL, Ridler CM, Preudhomme C, Young BD, Rohatiner AZ, Lister TA and Bonnet D. AML engraftment in the NOD/SCID assay reflects the outcome of AML: implications for our understanding of the heterogeneity of AML. Blood 2006; 107: 1166-1173.
77. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM and Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008; 456: 593-598.
78. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E and Reubinoff BE. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nature genetics 2006; 39: 232-236.
79. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC and Yu W. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nature genetics 2007; 39: 237-242.
80. Baylin SB and Ohm JE. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nature Reviews Cancer 2006; 6: 107-116.
81. Issa JPJ and Kantarjian HM. Targeting DNA methylation. Clinical Cancer Research 2009; 15: 3938.
82. Cashen AF, Schiller GJ, O'Donnell MR and DiPersio JF. Multicenter, phase II study of decitabine for the first-line treatment of older patients with acute myeloid leukemia. Journal of Clinical Oncology 2010; 28: 556.
83. Kantarjian H, Issa JPJ, Rosenfeld CS, Bennett JM, Albitar M, DiPersio J, Klimek V, Slack J, de Castro C and Ravandi F. Decitabine improves patient outcomes in myelodysplastic syndromes. Cancer 2006; 106: 1794-1803.
84. Kaminskas E, Farrell A, Abraham S, Baird A, Hsieh LS, Lee SL, Leighton JK, Patel H, Rahman A and Sridhara R. Approval summary: azacitidine for treatment of myelodysplastic syndrome subtypes. Clinical cancer research 2005; 11: 3604.
85. Issa JPJ, Garcia-Manero G, Giles FJ, Mannari R, Thomas D, Faderl S, Bayar E, Lyons J, Rosenfeld CS and Cortes J. Phase 1 study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-2'-deoxycytidine (decitabine) in hematopoietic malignancies. Blood 2004; 103: 1635.
86. Silverman LR, Demakos EP, Peterson BL, Kornblith AB, Holland JC, Odchimar-Reissig R, Stone RM, Nelson D, Powell BL and DeCastro CM. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. Journal of Clinical Oncology 2002; 20: 2429.
87. Oki Y, Aoki E and Issa JPJ. Decitabine--bedside to bench. Critical reviews in oncology/ hematology 2007; 61: 140-152.
88. Herman JG and Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. New England Journal of Medicine 2003; 349: 2042-2054.
89. Tsai HC and Baylin SB. Cancer epigenetics: linking basic biology to clinical medicine. Cell research 2011; 21: 502-517.
90. Whittaker SJ, Demierre MF, Kim EJ, Rook AH, Lerner A, Duvic M, Scarisbrick J, Reddy S, Robak T and Becker JC. Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. Journal of Clinical Oncology 2010; 28: 4485.
91. Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, Zain J, Prince HM, Leonard JP and Geskin LJ. Phase II multiinstitutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. Journal of Clinical Oncology 2009; 27: 5410.
92. Duvic M and Zhang C. Clinical and laboratory experience of vorinostat (suberoylanilide hydroxamic acid) in the treatment of cutaneous T-cell lymphoma. British journal of cancer 2006; 95: S13-S19.
93. Gore SD, Baylin S, Sugar E, Carraway H, Miller CB, Carducci M, Grever M, Galm O, Dauses T and Karp JE. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer research 2006; 66: 6361.
94. Cameron EE, Bachman KE, Myöhänen S, Herman JG and Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nature genetics 1999; 21: 103-107.
95. van Engeland M, Derks S, Smits KM, Meijer GA and Herman JG. Colorectal cancer epigenetics: complex simplicity. Journal of Clinical Oncology 2011; 29: 1382.
96. Baba Y, Nosho K, Shima K, Huttenhower C, Tanaka N, Hazra A, Giovannucci EL, Fuchs CS and Ogino S. Hypomethylation of the IGF2 DMR in colorectal tumors, detected by bisulfite pyrosequencing, is associated with poor prognosis. Gastroenterology 2010; 139: 1855-1864.
97. Kaaks R, Stattin P, Villar S, Poetsch AR, Dossus L, Nieters A, Riboli E, Palmqvist R, Hallmans G and Plass C. Insulin-like growth factor-II methylation status in lymphocyte DNA and colon cancer risk in the Northern Sweden Health and Disease cohort. Cancer research 2009; 69: 5400.
98. Kenner KA, Hill DE, Olefsky JM and Kusari J. Regulation of protein tyrosine phosphatases by insulin and insulin-like growth factor I. Journal of Biological Chemistry 1993; 268: 25455.
99. Polychronakos C, Guyda HJ, Janthly UMA and Posner BI. Effects of mannose-6-phosphate on receptor-mediated endocytosis of insulin-like growth factor-II. Endocrinology 1990; 127: 1861.
100. Waterland RA, Lin JR, Smith CA and Jirtle RL. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Human molecular genetics 2006; 15: 705-716.
101. Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE and Heijmans BT. Periconceptional maternal folic acid use of 400 μg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 2009; 4: e7845.
102. Sakatani T, Wei M, Katoh M, Okita C, Wada D, Mitsuya K, Meguro M, Ikeguchi M, Ito H, Tycko B and Oshimura M. Epigenetic heterogeneity at imprinted loci in normal populations. Biochemical & Biophysical Research Communications 2001; 283: 1124-1130.
103. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Akiyama M, Hideshima T and Chauhan D. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors. Cancer cell 2004; 5: 221-230.
104. Harper J, Burns JL, Foulstone EJ, Pignatelli M, Zaina S and Hassan AB. Soluble IGF2 receptor rescues ApcMin/ intestinal adenoma progression induced by Igf2 loss of imprinting. Cancer research 2006; 66: 1940.
105. Chen HL, Li T, Qiu XW, Wu J, Ling JQ, Sun ZH, Wang W, Chen W, Hou A and Vu TH. Correction of aberrant imprinting of IGF2 in human tumors by nuclear transfer-induced epigenetic reprogramming. The EMBO journal 2006; 25: 5329-5338.
106. Jouvenot Y, Ginjala V, Zhang L, Liu PQ, Oshimura M, Feinberg AP, Wolffe AP, Ohlsson R and Gregory PD. Targeted regulation of imprinted genes by synthetic zinc-finger transcription factors. Gene therapy 2003; 10: 513-522.
107. Vorwerk P, Wex H, Bessert C, Hohmann B, Schmidt U and Mittler U. Loss of imprinting of IGF-II gene in children with acute lymphoblastic leukemia. Leukemia research 2003; 27: 807-812.
108. Byun HM, Wong HL, Birnstein EA, Wolff EM, Liang G and Yang AS. Examination of IGF2 and H19 loss of imprinting in bladder cancer. Cancer research 2007; 67: 10753.
109. Ito Y, Koessler T, Ibrahim AE, Rai S, Vowler SL, Abu-Amero S, Silva AL, Maia AT, Huddleston JE, Uribe-Lewis S, Woodfine K, Jagodic M, Nativio R, Dunning A, Moore G, Klenova E, Bingham S, Pharoah PD, Brenton JD, Beck S, Sandhu MS and Murrell A. Somatically acquired hypomethylation of IGF2 in breast and colorectal cancer. Human molecular genetics 2008; 17: 2633-2643.
110. Yueling W, Xinyuan Y and Xu L. Study of loss of imprinting of insulin-like growth factor II and H19 genes in cervical carcinoma. Journal of Xi'an Jiaotong University (Medical Sciences) 2006; 04.
111. Schuster AE, Schneider DT, Fritsch MK, Grundy P and Perlman EJ. Genetic and genetic expression analyses of clear cell sarcoma of the kidney. Laboratory investigation 2003; 83: 1293-1299.
112. Watanabe N, Haruta M, Soejima H, Fukushi D, Yokomori K, Nakadate H, Okita H, Hata J, Fukuzawa M and Kaneko Y. Duplication of the paternal IGF2 allele in trisomy 11 and elevated expression levels of IGF2 mRNA in congenital mesoblastic nephroma of the cellular or mixed type. Genes, Chromosomes and Cancer 2007; 46: 929-935.
113. Maenaka S, Hikichi T, Imai MA, Minamoto T and Kawahara E. Loss of imprinting in IGF2 in colorectal carcinoma assessed by microdissection. Oncology reports 2006; 15: 791-795.
114. Nakano S, Murakami K, Meguro M, Soejima H, Higashimoto K, Urano T, Kugoh H, Mukai T, Ikeguchi M and Oshimura M. Expression profile of LIT1/KCNQ1OT1 and epigenetic status at the KvDMR1 in colorectal cancers. Cancer science 2006; 97: 1147-1154.
115. Honda S, Arai Y, Haruta M, Sasaki F, Ohira M, Yamaoka H, Horie H, Nakagawara A, Hiyama E and Todo S. Loss of imprinting of IGF2 correlates with hypermethylation of the H19 differentially methylated region in hepatoblastoma. British journal of cancer 2008; 99: 1891-1899.
116. Grbesa I, Ivkic M, Pegan B and Gall-Troselj K. Loss of imprinting and promoter usage of the IGF2 in laryngeal squamous cell carcinoma. Cancer letters 2006; 238: 224-229.
117. Dejeux E, Olaso R, Dousset B, Audebourg A, Gut IG, Terris B and Tost J. Hypermethylation of the IGF2 differentially methylated region 2 is a specific event in insulinomas leading to loss-of-imprinting and overexpression. Endocrine-related cancer 2009; 16: 939.
118. Stier S, Neuhaus T, Albers P, Wernert N, Grünewald E, Forkert R, Vetter H and Ko Y. Loss of imprinting of the insulin-like growth factor 2 and the H19 gene in testicular seminomas detected by real-time PCR approach. Archives of Toxicology 2006; 80: 713-718.
119. Gallagher EM, O'Shea DM, Fitzpatrick P, Harrison M, Gilmartin B, Watson JA, Clarke T, Leonard MO, McGoldrick A and Meehan M. Recurrence of urothelial carcinoma of the bladder: a role for insulin-like growth factor-II loss of imprinting and cytoplasmic E-cadherin immunolocalization. Clinical Cancer Research 2008; 14: 6829.
120. Mummert SK, Lobanenkov VA and Feinberg AP. Association of chromosome arm 16q loss with loss of imprinting of insulin-like growth factor-II in Wilms tumor. Genes, Chromosomes and Cancer 2005; 43: 155-161.
121. Satoh Y, Nakadate H, Nakagawachi T, Higashimoto K, Joh K, Masaki Z, Uozumi J, Kaneko Y, Mukai T and Soejima H. Genetic and epigenetic alterations on the short arm of chromosome 11 are involved in a majority of sporadic Wilms' tumours. British journal of cancer 2006; 95: 541-547.
122. Brown KW, Power F, Moore B, Charles AK and Malik KTA. Frequency and timing of loss of imprinting at 11p13 and 11p15 in Wilms' tumor development. Molecular Cancer Research 2008; 6: 1114.
123. Vuononvirta R, Sebire NJ, Dallosso AR, Reis-Filho JS, Williams RD, Mackay A, Fenwick K, Grigoriadis A, Ashworth A and Pritchard-Jones K. Perilobar nephrogenic rests are nonobligate molecular genetic precursor lesions of IGF2-associated Wilms tumours. Clinical cancer research: an official journal of the American Association for Cancer Research 2008; 14: 7635.
124. Haruta M, Arai Y, Sugawara W, Watanabe N, Honda S, Ohshima J, Soejima H, Nakadate H, Okita H and Hata J. Duplication of paternal IGF2 or loss of maternal IGF2 imprinting occurs in half of Wilms tumors with various structural WT1 abnormalities. Genes, Chromosomes and Cancer 2008; 47: 712-727.