Maternal gametic transmission of translocations or inversions of human chromosome 11p15.5 results in regional DNA hypermethylation and downregulation of CDKN1C expression

Genomics

Volumn 99, Issue 1, 2012, Pages 25-35

  Smith, Adam C ^a   Suzuki, Masako ^b   Thompson, Reid ^b   Choufani, Sanaa ^c   Higgins, Michael J ^d   Chiu, Idy W ^c   Squire, Jeremy A ^e   Greally, John M ^b   Weksberg, Rosanna ^c,f  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e QUEEN S UNIVERSITY   (Canada)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Balanced chromosome translocation; Beckwith Wiedemann syndrome; Chromosome 11p15.5; DNA methylation microarray; Genomic imprinting

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; DNA; POTASSIUM CHANNEL KCNQ1; SOMATOMEDIN B; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE;

ARTICLE; BECKWITH WIEDEMANN SYNDROME; CDKN1C GENE; CHROMOSOME 11; CHROMOSOME 11P; CHROMOSOME BREAKAGE; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; CHROMOSOME INVERSION; CHROMOSOME TRANSLOCATION 11; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; EXTRACHROMOSOMAL INHERITANCE; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC REGULATION; GENOME IMPRINTING; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PATHOPHYSIOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TELOMERE;

BECKWITH-WIEDEMANN SYNDROME; CENTROMERE; CHROMOSOME BREAKPOINTS; CHROMOSOME INVERSION; CHROMOSOMES, HUMAN, PAIR 11; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENOMIC IMPRINTING; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INSULIN-LIKE GROWTH FACTOR II; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; TRANSLOCATION, GENETIC;

EID: 84855190073     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2011.10.007     Document Type: Article

References (49)

1. DeBaun M.R., Tucker M.A. Risk of cancer during the first four years of life in children from The Beckwith-Wiedemann Syndrome Registry. J. Pediatr. 1998, 132:398-400.
2. Weksberg R., Nishikawa J., Caluseriu O., Fei Y.L., Shuman C., Wei C., Steele L., Cameron J., Smith A., Ambus I., Li M., Ray P.N., Sadowski P., Squire J. 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, 10:426-431.
3. Rump P., Zeegers M.P., van Essen A.J. Tumor risk in Beckwith-Wiedemann syndrome: a review and meta-analysis. Am J Med Genet A 2005, 136:95-104.
4. Fitzpatrick G.V., Soloway P.D., Higgins M.J. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet. 2002, 32:426-431.
5. Diaz-Meyer N., Day C.D., Khatod K., Maher E.R., Cooper W., Reik W., Junien C., Graham G., Algar E., Der Kaloustian V.M., Higgins M.J. Silencing of CDKN1C (p57KIP2) is associated with hypomethylation at KvDMR1 in Beckwith-Wiedemann syndrome. J Med Genet 2003, 40:797-801.
6. Du M., Zhou W., Beatty L.G., Weksberg R., Sadowski P.D. The KCNQ1OT1 promoter, a key regulator of genomic imprinting in human chromosome 11p15.5. Genomics 2004, 84:288-300.
7. Cooper W.N., Luharia A., Evans G.A., Raza H., Haire A.C., Grundy R., Bowdin S.C., Riccio A., Sebastio G., Bliek J., Schofield P.N., Reik W., Macdonald F., Maher E.R. Molecular subtypes and phenotypic expression of Beckwith-Wiedemann syndrome. Eur. J. Hum. Genet. 2005, 13:1025-1032.
8. Weksberg R., Shuman C., Smith A.C. Beckwith-Wiedemann syndrome. Am J Med Genet C Semin Med Genet 2005, 137:12-23.
9. Weksberg R., Smith A.C., Squire J., Sadowski P. Beckwith-Wiedemann syndrome demonstrates a role for epigenetic control of normal development. Hum. Mol. Genet. 2003, 12:R61-R68. Spec No 1.
10. Diaz-Meyer N., Yang Y., Sait S.N., Maher E.R., Higgins M.J. Alternative mechanisms associated with silencing of CDKN1C in Beckwith-Wiedemann syndrome. J Med Genet 2005, 42:648-655.
11. Sasaki K., Soejima H., Higashimoto K., Yatsuki H., Ohashi H., Yakabe S., Joh K., Niikawa N., Mukai T. Japanese and North American/European patients with Beckwith-Wiedemann syndrome have different frequencies of some epigenetic and genetic alterations. Eur. J. Hum. Genet. 2007, 15:1205-1210.
12. Weksberg R., Shen D.R., Fei Y.L., Song Q.L., Squire J. Disruption of insulin-like growth factor 2 imprinting in Beckwith-Wiedemann syndrome. Nat. Genet. 1993, 5:143-150.
13. Smilinich N.J., Day C.D., Fitzpatrick G.V., Caldwell G.M., Lossie A.C., Cooper P.R., Smallwood A.C., Joyce J.A., Schofield P.N., Reik W., Nicholls R.D., Weksberg R., Driscoll D.J., Maher E.R., Shows T.B., Higgins M.J. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8064-8069.
14. Murakami K., Oshimura M., Kugoh H. Suggestive evidence for chromosomal localization of non-coding RNA from imprinted LIT1. J. Hum. Genet. 2007, 52:926-933.
15. Bliek J., Maas S.M., Ruijter J.M., Hennekam R.C., Alders M., Westerveld A., Mannens M.M. 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, 10:467-476.
16. Gaston V., Le Bouc Y., Soupre V., Burglen L., Donadieu J., Oro H., Audry G., Vazquez M.P., Gicquel C. Analysis of the methylation status of the KCNQ1OT and H19 genes in leukocyte DNA for the diagnosis and prognosis of Beckwith-Wiedemann syndrome. Eur. J. Hum. Genet. 2001, 9:409-418.
17. Sparago A., Cerrato F., Vernucci M., Ferrero G.B., Silengo M.C., Riccio A. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nat. Genet. 2004, 36:958-960.
18. Niemitz E.L., DeBaun M.R., Fallon J., Murakami K., Kugoh H., Oshimura M., Feinberg A.P. Microdeletion of LIT1 in familial Beckwith-Wiedemann syndrome. Am. J. Hum. Genet. 2004, 75:844-849.
19. Hoovers J.M., Kalikin L.M., Johnson L.A., Alders M., Redeker B., Law D.J., Bliek J., Steenman M., Benedict M., Wiegant J., Lengauer C., Taillon-Miller P., Schlessinger D., Edwards M.C., Elledge S.J., Ivens A., Westerveld A., Little P., Mannens M., Feinberg A.P. Multiple genetic loci within 11p15 defined by Beckwith-Wiedemann syndrome rearrangement breakpoints and subchromosomal transferable fragments. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:12456-12460.
20. Gribble S.M., Prigmore E., Burford D.C., Porter K.M., Ng B.L., Douglas E.J., Fiegler H., Carr P., Kalaitzopoulos D., Clegg S., Sandstrom R., Temple I.K., Youings S.A., Thomas N.S., Dennis N.R., Jacobs P.A., Crolla J.A., Carter N.P. The complex nature of constitutional de novo apparently balanced translocations in patients presenting with abnormal phenotypes. J Med Genet 2005, 42:8-16.
21. Sismani C., Kitsiou-Tzeli S., Ioannides M., Christodoulou C., Anastasiadou V., Stylianidou G., Papadopoulou E., Kanavakis E., Kosmaidou-Aravidou Z., Patsalis P.C. Cryptic genomic imbalances in patients with de novo or familial apparently balanced translocations and abnormal phenotype. Mol. Cytogenet. 2008, 1:15.
22. Li M., Squire J., Shuman C., Fei Y.L., Atkin J., Pauli R., Smith A., Nishikawa J., Chitayat D., Weksberg R. Imprinting status of 11p15 genes in Beckwith-Wiedemann syndrome patients with CDKN1C mutations. Genomics 2001, 74:370-376.
23. Lee M.P., DeBaun M.R., Mitsuya K., Galonek H.L., Brandenburg S., Oshimura M., Feinberg A.P. Loss of imprinting of a paternally expressed transcript, with antisense orientation to KVLQT1, occurs frequently in Beckwith-Wiedemann syndrome and is independent of insulin-like growth factor II imprinting. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5203-5208.
24. Lee M.P., Hu R.J., Johnson L.A., Feinberg A.P. Human KVLQT1 gene shows tissue-specific imprinting and encompasses Beckwith-Wiedemann syndrome chromosomal rearrangements. Nat. Genet. 1997, 15:181-185.
25. Sait S.N., Nowak N.J., Singh-Kahlon P., Weksberg R., Squire J., Shows T.B., Higgins M.J. Localization of Beckwith-Wiedemann and rhabdoid tumor chromosome rearrangements to a defined interval in chromosome band 11p15.5. Genes Chromosomes Cancer 1994, 11:97-105.
26. Squire J.A., Li M., Perlikowski S., Fei Y.L., Bayani J., Zhang Z.M., Weksberg R. Alterations of H19 imprinting and IGF2 replication timing are infrequent in Beckwith-Wiedemann syndrome. Genomics 2000, 65:234-242.
27. Norman A.M., Read A.P., Clayton-Smith J., Andrews T., Donnai D. Recurrent Wiedemann-Beckwith syndrome with inversion of chromosome (11)(p11.2p15.5). Am J Med Genet 1992, 42:638-641.
28. Karnes P.S., Tran T.N., Cui M.Y., Bogenmann E., Shimada H., Ying K.L. Establishment of a rhabdoid tumor cell line with a specific chromosomal abnormality, 46, XY, t(11;22)(p15.5;q11.23). Cancer Genet Cytogenet 1991, 56:31-38.
29. Khulan B., Thompson R.F., Ye K., Fazzari M.J., Suzuki M., Stasiek E., Figueroa M.E., Glass J.L., Chen Q., Montagna C., Hatchwell E., Selzer R.R., Richmond T.A., Green R.D., Melnick A., Greally J.M. Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res. 2006, 16:1046-1055.
30. Bird A.P. CpG-rich islands and the function of DNA methylation. Nature 1986, 321:209-213.
31. Robertson K.D. DNA methylation and human disease. Nat. Rev. Genet. 2005, 6:597-610.
32. Takai D., Jones P.A. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3740-3745.
33. Weber M., Davies J.J., Wittig D., Oakeley E.J., Haase M., Lam W.L., Schubeler D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 2005, 37:853-862.
34. Weber M., Hellmann I., Stadler M.B., Ramos L., Paabo S., Rebhan M., Schubeler D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 2007, 39:457-466.
35. Weksberg R., Teshima I., Williams B.R., Greenberg C.R., Pueschel S.M., Chernos J.E., Fowlow S.B., Hoyme E., Anderson I.J., Whiteman D.A., et al. Molecular characterization of cytogenetic alterations associated with the Beckwith-Wiedemann syndrome (BWS) phenotype refines the localization and suggests the gene for BWS is imprinted. Hum. Mol. Genet. 1993, 2:549-556.
36. South S.T., Whitby H., Maxwell T., Aston E., Brothman A.R., Carey J.C. Co-occurrence of 4p16.3 deletions with both paternal and maternal duplications of 11p15: modification of the Wolf-Hirschhorn syndrome phenotype by genetic alterations predicted to result in either a Beckwith-Wiedemann or Russell-Silver phenotype. Am J Med Genet A 2008, 146A:2691-2697.
37. Dracopoli N.C. Current protocols in human genetics 1994, 2. Wiley, New York, NY, (looseleaf).
38. Weksberg R., Shuman C., Caluseriu O., Smith A.C., Fei Y.L., Nishikawa J., Stockley T.L., Best L., Chitayat D., Olney A., Ives E., Schneider A., Bestor T.H., Li M., Sadowski P., Squire J. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum. Mol. Genet. 2002, 11:1317-1325.
39. Royo J.L., Hidalgo M., Ruiz A. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nat. Protoc. 2007, 2:1734-1739.
40. Royo J.L., Pascual M.H., Salinas A., Tello F.J., Rivero Mdel C., Herrero E.F., Real L.M., Ruiz A. Pyrosequencing protocol requiring a unique biotinylated primer. Clin Chem Lab Med 2006, 44:435-441.
41. Beatty B., Mai S., Squire J. FISH: A Practical Approach 2002, Oxford University Press, Oxford, New York.
42. Rutledge R.G., Cote C. Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acids Res. 2003, 31:e93.
43. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
44. Guo L., Choufani S., Ferreira J., Smith A., Chitayat D., Shuman C., Uxa R., Keating S., Kingdom J., Weksberg R. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev. Biol. 2008, 320:79-91.
45. Kohda M., Hoshiya H., Katoh M., Tanaka I., Masuda R., Takemura T., Fujiwara M., Oshimura M. Frequent loss of imprinting of IGF2 and MEST in lung adenocarcinoma. Mol. Carcinog. 2001, 31:184-191.
46. Mitsuya K., Meguro M., Lee M.P., Katoh M., Schulz T.C., Kugoh H., Yoshida M.A., Niikawa N., Feinberg A.P., Oshimura M. LIT1, an imprinted antisense RNA in the human KvLQT1 locus identified by screening for differentially expressed transcripts using monochromosomal hybrids. Hum. Mol. Genet. 1999, 8:1209-1217.
47. Tanaka K., Shiota G., Meguro M., Mitsuya K., Oshimura M., Kawasaki H. Loss of imprinting of long QT intronic transcript 1 in colorectal cancer. Oncology 2001, 60:268-273.
48. Nuwaysir E.F., Huang W., Albert T.J., Singh J., Nuwaysir K., Pitas A., Richmond T., Gorski T., Berg J.P., Ballin J., McCormick M., Norton J., Pollock T., Sumwalt T., Butcher L., Porter D., Molla M., Hall C., Blattner F., Sussman M.R., Wallace R.L., Cerrina F., Green R.D. Gene expression analysis using oligonucleotide arrays produced by maskless photolithography. Genome Res. 2002, 12:1749-1755.
49. Workman C., Jensen L.J., Jarmer H., Berka R., Gautier L., Nielser H.B., Saxild H.H., Nielsen C., Brunak S., Knudsen S. A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol. 2002, 3. research0048.