Identification of Four Highly Conserved Genes between Breakpoint Hotspots BP1 and BP2 of the Prader-Willi/Angelman Syndromes Deletion Region That Have Undergone Evolutionary Transposition Mediated by Flanking Duplicons

American Journal of Human Genetics

Volumn 73, Issue 4, 2003, Pages 898-925

  Chai, J H ^a   Locke, D P ^b   Greally, J M ^c   Knoll, J H M ^d   Ohta, T ^a,e   Dunai, J ^c   Yavor, A ^b   Eichler, E E ^b   Nicholls, R D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

^e NAGASAKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ANIMAL MODEL; ARTICLE; CHROMOSOME 7; CONTROLLED STUDY; CYFIP1 GENE; DNA FLANKING REGION; DNA TRANSPOSITION; EVOLUTION; GCP5 GENE; GENE; GENE DELETION; GENE DUPLICATION; GENE IDENTIFICATION; GENE REPLICATION; GENOMICS; HAPPY PUPPET SYNDROME; HERC2 GENE; HUMAN; MOUSE; NIPA1 GENE; NIPA2 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PRADER WILLI SYNDROME; PRIORITY JOURNAL; PROTEIN DOMAIN; PUFFER FISH;

ANIMALIA; INVERTEBRATA; PRIMATES; TAKIFUGU; TETRAODONTIDAE; VERTEBRATA;

EID: 0142027581     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/378816     Document Type: Article

References (84)

1. Amos-Landgraf JM, Ji Y, Wayne G, Depinet T, Wandstrat SB, Daniel JD, Rogan PK, Schwartz S, Nicholls RD (1999) Chromosome breakage in the Prader-Willi and Angelman syndromes involves recombination between large, transcribed repeats at proximal and distal breakpoints. Am J Hum Genet 65:370-386
2. Boccaccio I, Glatt-Deeley H, Watrin F, Roëckel N, Lalande M, Muscatelli F (1999) The human MAGEL2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region. Hum Mol Genet 8:2497-2505
3. Buiting K, Korner C, Ulrich B, Wahle E, Horsthemke B (1999) The human gene for the poly(A)-specific ribonuclease (PARN) maps to 16p13 and has a truncated copy in the Prader-Willi/Angelman syndrome region on 15q11→q13. Cytogenet Cell Genet 87:125-131
4. Buiting K, Saitoh S, Gross S, Dittrich B, Schwartz S, Nicholls RD, Horsthemke B (1995) Inherited microdeletions in the Angelman and Prader-Willi syndromes define an imprinting centre on human chromosome 15. Nat Genet 9:395-400
5. Butler MG, Bittel DC, Kibiryeva N, Talebizadeh Z, Thompson T. Behavioral differences among subjects with Prader-Willi syndrome and type I and type II deletions and maternal disomy. Pediatrics, in press
6. Butler MG, Bittel D, Talebizadeh Z (2002) Prader-Willi syndrome and a deletion/duplication within the 15q11-q13 region. J Med Genet 39:202-204
7. Cavaillé J, Buiting K, Kiefmann M, Lalande M, Brannan CI, Horsthemke B, Bachellerie JP, Brosius J (2000) Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc Natl Acad Sci USA 97:14311-14316
8. Chai JH, Locke DP, Ohta T, Greally JM, Nicholls RD (2001) Retrotransposed genes such as Frat3 in the mouse chromosome 7C Prader-Willi syndrome region acquire the imprinted status of their insertion site. Mamm Genome 12: 813-821
9. Cheng SD, Spinner NB, Zackai EH, Knoll JH (1994) Cytogenetic and molecular characterization of inverted duplicated chromosomes 15 from 11 patients. Am J Hum Genet 55:753-759
10. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834
11. Chluba-de Tapia J, de Tapia M, Jaggin V, Eberle AN (1997) Cloning of a human multispanning membrane protein cDNA: evidence for a new protein family. Gene 197:195-204
12. Christian SL, Fantes JA, Mewborn SK, Huang B, Ledbetter DH (1999) Large genomic duplicons map to sites of instability in the Prader-Willi/Angelman syndrome chromosome region (15q11-q13). Hum Mol Genet 8:1025-1037
13. Clayton-Smith J, Driscoll DJ, Waters MF, Webb T, Andrews T, Malcolm S, Pembrey ME, Nicholls RD (1993) Difference in methylation patterns within the D15S9 region of chromosome 15q11-13 in first cousins with Angelman syndrome and Prader-Willi syndrome. Am J Med Genet 47:683-686
14. Cornillon S, Pech E, Benghezal M, Ravanel K, Gaynor E, Letourneur F, Bruckert F, Cosson P (2000) Phg1p is a nine-transmembrane protein superfamily member involved in dictyostelium adhesion and phagocytosis. J Biol Chem 275: 34287-34292
15. Crosby AH, Proukakis C (2002) Is the transportation highway the right road for hereditary spastic paraplegia? Am J Hum Genet 71:1009-1016
16. Culiat CT, Stubbs LJ, Woychik RP, Russell LB, Johnson DK, Rinchik EM (1995) Deficiency of the β3 subunit of the type A γ-aminobutyric acid receptor causes cleft palate in mice. Nat Genet 11:344-346
17. de los Santos T, Schweizer J, Rees CA, Francke U (2000) Small evolutionarily conserved RNA, resembling C/D box small nucleolar RNA, is transcribed from PWCR1, a novel imprinted gene in the Prader-Willi deletion region, which is highly expressed in brain. Am J Hum Genet 67:1067-1082
18. Dhar M, Webb LS, Smith L, Hauser L, Johnson D, West DB (2000) A novel ATPase on mouse chromosome 7 is a candidate gene for increased body fat. Physiol Genomics 4:93-100
19. Fantes JA, Mewborn SK, Lese CM, Hedrick J, Brown RL, Dyomin V, Chaganti RS, Christian SL, Ledbetter DH (2002) Organisation of the pericentromeric region of chromosome 15: at least four partial gene copies are amplified in patients with a proximal duplication of 15q. J Med Genet 39:170-177
20. Fernandez J, Yaman I, Sarnow P, Snider MD, Hatzoglou M (2002) Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2α. J Biol Chem 277:19198-19205
21. Fink JK, Jones SM, Sharp GB, Lange BM, Otterud B, Leppert M (1996) Hereditary spastic paraplegia linked to chromosome 15q: analysis of candidate genes. Neurology 46:835-836
22. Fink JK, Wu CT, Jones SM, Sharp GB, Lange BM, Lesicki A, Reinglass T, Varvil T, Otterud B, Leppert M (1995) Autosomal dominant familial spastic paraplegia: tight linkage to chromosome 15q. Am J Hum Genet 56:188-192
23. Gabriel JM, Higgins MJ, Gebuhr TC, Shows TB, Saitoh S, Nicholls RD (1998) A model system to study genomic imprinting of human genes. Proc Natl Acad Sci USA 95:14857-14862
24. Gabriel JM, Merchant M, Ohta T, Ji Y, Caldwell RG, Ramsey MJ, Tucker JD, Longnecker RM, Nicholls RD (1999) A transgene insertion creating a heritable chromosome deletion mouse model of Prader-Willi and Angelman syndromes. Proc Natl Acad Sci USA 96:9258-9263
25. Gimelli G, Pujana MA, Patricelli MG, Russo S, Giardino D, Larizza L, Cheung J, Armengol L, Schinzel A, Estivill X, Zuffardi O (2003) Genomic inversions of human chromosome 15q11-q13 in mothers of Angelman syndrome patients with class II (BP2/3) deletions. Hum Mol Genet 12:849-858
26. Gray TA, Hernandez L, Carey AH, Schaldach MA, Smithwick MJ, Rus K, Marshall Graves JA, Stewart CL, Nicholls RD (2000) The ancient source of a distinct gene family encoding proteins featuring RING and C3H zinc finger motifs with abundant expression in developing brain and nervous system. Genomics 66:76-86
27. Gray TA, Saitoh S, Nicholls RD (1999) An imprinted, mammalian bicistronic transcript encodes two independent proteins. Proc Natl Acad Sci USA 96:5616-5621
28. Greally JM, Starr DJ, Hwang S, Song L, Jaarola M, Zemel S (1998) The mouse H19 locus mediates a transition between imprinted and non-imprinted DNA replication patterns. Hum Mol Genet 7:91-95
29. Hagiwara N, Katarova Z, Siracusa LD, Brilliant MH (2003) Nonneuronal expression of the GABA(A) β3 subunit gene is required for normal palate development in mice. Dev Biol 254:93-101
30. Henegariu O, Heerema NA, Lowe Wright L, Bray-Ward P, Ward DC, Vance GH (2001) Improvements in cytogenetic slide preparation: controlled chromosome spreading, chemical aging and gradual denaturing. Cytometry 43:101-109
31. Herzing LB, Kim SJ, Cook EH Jr, Ledbetter DH (2001) The human aminophospholipid-transporting ATPase gene ATP10C maps adjacent to UBE3A and exhibits similar imprinted expression. Am J Hum Genet 68:1501-1505
32. Hollander GA, Zuklys S, Morel C, Mizoguchi E, Mobisson K, Kimpson S, Terhorst C, Wishart W, Golan DE, Bhan AK, Burakoff SJ (1998) Monoallelic expression of the interleukin-2 locus. Science 279:2118-2121
33. Homanics GE, Delorey TM, Firestone LL, Quinlan JJ, Handforth A, Harrison NL, Krasowshi MD, Rick CE, Korpi ER, Makela R, Brilliant MH, Hagiwara N, Ferguson C, Snyder K, Olsen RW (1997) Mice devoid of γ-aminobutyrate type A receptor β3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci USA 94:4143-4148
34. Huang B, Crolla JA, Christian SL, Wolf-Ledbetter ME, Macha ME, Papenhausen PN, Ledbetter DH (1997) Refined molecular characterization of the breakpoints in small inv dup(15) chromosomes. Hum Genet 99:11-17
35. Jay P, Rougeulle C, Massacrier A, Moncla A, Mattei MG, Malzac P, Roeckel N, Taviaux S, Lefranc JL, Cau P, Berta P, Lalande M, Muscatelli F (1997) The human necdin gene, NDN, is maternally imprinted and located in the Prader-Willi syndrome chromosomal region. Nat Genet 17:357-361
36. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074-1080
37. Ji Y, Walkowicz MJ, Buiting K, Johnson DK, Tarvin RE, Rinchik EM, Horsthemke B, Stubbs L, Nicholls RD (1999) The ancestral gene for transcribed, low-copy repeats in the Prader-Willi/Angelman region encodes a large protein implicated in protein trafficking, which is deficient in mice with neuromuscular and spermiogenic abnormalities. Hum Mol Genet 8:533-542
38. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21:799-811
39. Jong MTC, Gray TA, Ji Y, Glenn CC, Saitoh S, Driscoll DJ, Nicholls RD (1999) A novel imprinted gene, encoding a RING zinc-finger protein, and overlapping antisense transcript in the Prader-Willi syndrome critical region. Hum Mol Genet 8:783-793
40. Kitsberg D, Selig S, Brandeis M, Simon I, Keshet I, Driscoll DJ, Nicholls RD, Cedar H (1993) Allele-specific replication timing of imprinted gene regions. Nature 364:459-463
41. Knoll JH, Cheng SD, Lalande M (1994) Allele specificity of DNA replication timing in the Angelman/Prader-Willi syndrome imprinted chromosomal region. Nat Genet 6:41-46
42. Knoll JHM, Lichter P (1994) In situ hybridization to metaphase chromosomes and interphase nuclei. In: Dracopoli NC, Haines JL, Korf BR, Moir DT, Morton CC, Seidman CE, Seidman JG (eds) Current protocols in human genetics, vol 1. John Wiley, New York, pp 4.3.1-4.3.28
43. Knoll JH, Nicholls RD, Magenis RE, Glatt K, Graham JM Jr, Kaplan L, Lalande M (1990) Angelman syndrome: three molecular classes identified with chromosome 15q11q13-specific DNA markers. Am J Hum Genet 47:149-155
44. Kobayashi K, Kuroda S, Fukata M, Nakamura T, Nagase T, Nomura N, Matsuura Y, Yoshida-Kubomura N, Iwamatsu A, Kaibuchi K (1998) p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J Biol Chem 273:291-295
45. Köster F, Schinke B, Niemann S, Hermans-Borgmeyer I (1998) Identification of shyc, a novel gene expressed in the murine developing and adult nervous system. Neurosci Letters 252: 69-71
46. Leana-Cox J, Jenkins L, Palmer CG, Plattner R, Sheppard L, Flejter WL, Zackowski J, Tsien F, Schwanz S (1994) Molecular cytogenetic analysis of inv dup(15) chromosomes, using probes specific for the Prader-Willi/Angelman syndrome region: clinical implications. Am J Hum Genet 54: 748-756
47. Lee S, Kozlov S, Hernandez L, Chamberlain SJ, Brannan CI, Stewart CL, Wevrick R (2000) Expression and imprinting of MAGEL2 suggest a role in Prader-Willi syndrome and the homologous murine imprinting phenotype. Hum Mol Genet 9:1813-1819
48. Lehman AL, Nakatsu Y, Ching A, Bronson RT, Oakey RJ, Keiper-Hrynko N, Finger JN, Durham-Pierre (1998) A very large protein with diverse functional motifs is deficient in rjs (runty, jerky, sterile) mice. Proc Natl Acad Sci USA 95: 9436-9441
49. Locke DP, Yavor AM, Lehoczky J, Chang J, Dewar K, Zhao S, Nicholls RD, Schwanz S, Eichler EE (2001) Structure and evolution of genomic duplication in 15q11-q13. Am J Hum Genet 69:179
50. Lossie AC, Whitney MM, Amidon D, Dong HJ, Chen P, Theriaque D, Huston A, Nicholls RD, Zori RT, Williams CA, Driscoll DJ (2001) Distinct phenotypes distinguish the molecular classes of Angelman syndrome. J Med Genet 38:834-845
51. Lunyak VV, Burgess R, Prefontaine GG, Nelson C, Sze SH, Chenoweth J, Schwartz P, Pevzner PA, Glass C, Mandel G, Rosenfeld MG (2002) Corepresser-dependent silencing of chromosomal regions encoding neuronal genes. Science 298: 1747-1752
52. MacDonald HR, Wevrick R (1997) The necdin gene is deleted in Prader-Willi syndrome and is imprinted in human and mouse. Hum Mol Genet 6:1873-1878
53. Meguro M, Kashiwagi A, Mitsuya K, Nakao M, Kondo I, Saitoh S, Oshimura M (2001) A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Nat Genet 28: 19-20
54. Morales J, Hiesinger PR, Schroeder AJ, Kume K, Verstreken P, Jackson FR, Nelson DL, Hassan BA (2002) Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34:961-972
55. Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635-8642
56. Mostoslavsky R, Singh N, Tenzen T, Goldmit M, Gabay C, Elizur S, Qi P, Reubinoff BE, Chess A, Cedar H, Bergman Y (2001) Asynchronous replication and allelic exclusion in the immune system. Nature 414:221-225
57. Murphy SM, Preble AM, Patel UK, O'Connell KL, Dias DP, Moritz M, Agard D, Stults JT, Stearns T (2001) GCP5 and GCP6: two new members of the human γ-tubulin complex. Mol Biol Cell 12:3340-3352
58. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L (2002) Rac function and regulation during Drosophila development. Nature 416:438-442
59. Nicholls RD (1999) Incriminating gene suspects, Prader-Willi style. Nat Genet 23:132-134
60. Nicholls RD, Gottlieb W, Russell LB, Davda M, Horsthemke, B, Rinchik EM (1993) Evaluation of potential models for imprinted and nonimprinted components of human chromosome 15q11-q13 syndromes by fine-structure homology mapping in the mouse. Proc Natl Acad Sci USA 90:2050-2054
61. Nicholls RD, Knepper JL (2001) Genome organization, function and imprinting in Prader-Willi and Angelman syndromes. Annu Rev Genomics Hum Genet 2:153-175
62. Osborne LR, Li M, Pober B, Chitayat D, Bodurtha J, Mandel A, Costa T, Grebe T, Cox S, Tsui LC, Scherer SM (2001) A 1.5 million-base pair inversion polymorphism in families with Williams-Beuren syndrome. Nat Genet 29:321-325
63. Pan CJ, Lei KJ, Annabi B, Hemrika W, Chou JY (1998) Transmembrane topology of glucose-6-phosphatase. J Biol Chem 273:6144-6148
64. Proudfoot NJ, Furger A, Dye MJ (2002) Integrating mRNA processing with transcription. Cell 108:501-512
65. Pujana MA, Nadal M, Gratacos M, Peral B, Csiszar K, Gonzalez-Sarmiento R, Sumoy L, Estivill X (2001) Additional complexity on human chromosome 15q: identification of a set of newly recognized duplicons (LCR15) on 15q11-q13, 15q24, and 15q26. Genome Res 11:98-111
66. Qiu Z, Nicoll DA, Philipson KD (2001) Helix packing of functionally important regions of the cardiac Na(+)-Ca(2+) exchanger. J Biol Chem 276:194-199
67. Rainier S, Chai J-H, Tokarz D, Nicholls RD, Fink JK (2003) NIPA1 gene mutations cause autosomal dominant hereditary spastic paraplegia (SPG6) Am J Hum Genet 73:967-971 [in this issue]
68. Rinchik EM, Stoye JP, Frankel WN, Coffin J, Kwon BS, Russell LB (1993) Molecular analysis of viable spontaneous and radiation-induced albino (c)-locus mutations in the mouse. Mutat Res 286:199-207
69. Ritchie RJ, Mattei MG, Lalande M (1998) A large polymorphic repeat in the pericentromeric region of human chromosome 15q contains three partial gene duplications. Hum Mol Genet 7:1253-1260
70. Roberts SE, Dennis NR, Browne CE, Willatt L, Woods CG, Cross I, Jacobs PA, Thomas NS (2002) Characterisation of interstitial duplications and triplications of chromosome 15q11-q13. Hum Genet 110:227-234
71. Runte M, Huttenhofer A, Gross S, Kiefmann M, Horsthemke B, Buiting K (2001) The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolar RNA species and as an antisense RNA for UBE3A. Hum Mol Genet 10: 2687-2700
72. Saitoh S, Buiting K, Rogan PK, Buxton JL, Driscoll DJ, Arnemann J, Konig R, Malcolm S, Horsthemke B, Nicholls RD (1996) Minimal definition of the imprinting center and fixation of chromosome 15q11-q13 epigenotype by imprinting mutations. Proc Natl Acad Sci USA 93:7811-7815
73. Schenck A, Bardoni B, Moro A, Bagni C, Mandel JL (2001) A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc Natl Acad Sci USA 98:8844-8849
74. Schimmöller F, Diaz E, Muhlbauer B, Pfeffer SR (1998) Characterization of a 76 kDa endosomal, multispanning membrane protein that is highly conserved throughout evolution. Gene 216:311-318
75. Sheets MD, Ogg SC, Wickens MP (1990) Point mutations in AAUAAA and the poly (A) addition site: effects on the accuracy and efficiency of cleavage and polyadenylation in vitro. Nucleic Acids Res 18:5799-5805
76. Simon I, Tenzen T, Reubinoff BE, Hillman D, McCarrey JR, Cedar H (1999) Asynchronous replication of imprinted genes is established in the gametes and maintained during development. Nature 401:929-932
77. Spritz RA, Bailin T, Nicholls RD, Lee ST, Park SK, Mascari MJ, Butler MG (1997) Hypopigmentation in the Prader-Willi syndrome correlates with P gene deletion but not with haplotype of the hemizygous P allele. Am J Med Genet 71: 57-62
78. Sugasawa T, Lenzen G, Simon S, Hidaka J, Cahen A, Guillaume JL, Camoin L, Strosberg AD, Nahmias C (2001) The iodocyanopindolol and SM-11044 binding protein belongs to the TM9SF multispanning membrane protein superfamily. Gene 273:227-237
79. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
80. Turner BM (2002) Cellular memory and the histone code. Cell 111:285-291
81. Walkowicz M, Ji Y, Ren X, Horsthemke B, Russell LB, Johnson D, Rinchik EM, Nicholls RD, Stubbs L (1999) Molecular characterization of radiation- and chemically induced mutations associated with neuromuscular tremors, runting, juvenile lethality, and sperm defects in jdf2 mice. Mamm Genome 10:870-878
82. Worthington MT, Pelo JW, Sachedina MA, Applegate JL, Arseneau KO, Pizarro TT (2002) RNA binding properties of the AU-rich element-binding recombinant Nup475/TIS11/ tristetraprolin protein. J Biol Chem 277:48558-48564
83. Wu M, Rinchik EM, Johnson DK (2000) An integrated deletion and physical map encompassing 171Rl, a chromosome 7 locus required for peri-implantation survival in the mouse. Genomics 67:228-231
84. Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63:405-445