The expression of preaxial polydactyly is influenced by modifying genetic elements and is not maintained by chromosomal inversion in an avian biomedical model

Cytogenetic and Genome Research

Volumn 136, Issue 1, 2012, Pages 50-68

  Robb, E A ^a   Delany, M E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomedical model; Breeding strategies; Chicken; Epistasis; Fine mapping; FISH; Inversion; LMBR1; Preaxial polydactyly; Recombination; Silkie breed; SNP; ZRS

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMOSOME; CHROMOSOME INVERSION; CONTROLLED STUDY; EMBRYO; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE DELETION; GENE EXPRESSION; GENE MAPPING; GENETIC EPISTASIS; GENETIC VARIABILITY; HETEROZYGOSITY; LMBR1 GENE; NONHUMAN; PHENOTYPE; POINT MUTATION; POLYDACTYLY; PREAXIAL POLYDACTYL; PRIORITY JOURNAL; REGULATORY SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ZONE OF POLARIZING ACTIVITY REGULATORY SEQUENCE;

ANIMALS; BASE SEQUENCE; BIRDS; CHROMOSOME INVERSION; CHROMOSOME MAPPING; HEDGEHOG PROTEINS; HETEROZYGOTE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRONS; MICE; MOLECULAR SEQUENCE DATA; PHENOTYPE; POINT MUTATION; POLYDACTYLY; POLYMORPHISM, SINGLE NUCLEOTIDE; REGULATORY SEQUENCES, NUCLEIC ACID; RETROSPECTIVE STUDIES; SEQUENCE ALIGNMENT; WILLS;

AVES; VERTEBRATA;

EID: 84856459409     PISSN: 14248581     EISSN: 14219794     Source Type: Journal    
DOI: 10.1159/000335005     Document Type: Article

References (70)

1. Abplanalp H: Inbred lines as genetic resources of chickens. Poult Sci Rev 4:29-39(1992).
2. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T: Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev Cell 16:47-57(2009).
3. Baba TW, Giroir BP, Humphries EH: Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology 144:139-151(1985).
4. Biesecker LG: Polydactyly: How many disorders and how many genes? 2010 update. Dev Dyn 240:931-942(2011).
5. Blanc I, Bach A, Robert B: Unusual pattern of Sonic hedgehog expression in the polydactylous mouse mutant Hemimelic extra-toes. Int J Dev Biol 46:969-974(2002).
6. Bond CJ: On the left-sided incidence of the supernumerary digit in heterodactylous fowls. J Genet 10:87-91(1920).
7. Bond CJ: Further observations on polydactyly and heterodactyly in fowls. J Genet 14:253-256(1926).
8. Bouldin CM, Harfe BD: Aberrant FGF signaling, independent of ectopic hedgehog signaling, initiates preaxial polydactyly in Dorking chickens. Dev Biol 334:133-141(2009).
9. Chang H, Delany ME: Karyotype stability of the DT40 chicken B cell line: macrochromosome variation and cytogenetic mosaicism. Chromosome Res 12:299-307(2004).
10. Chase HB: Inheritance of polydactyly in the mouse. Genetics 36:697-710(1951).
11. Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, et al: Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev Biol 236:421-435(2001).
12. Danforth CH: Heredity of polydactyly in the cat. J Hered 38:107-112(1947).
13. Delany ME, Gessaro TM, Rodrigue KL, Daniels LM: Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach. Cytogenet Genome Res 117:54-63(2007).
14. Dennis SM, Leipold HW: Ovine congenital defects. Vet Bull 49:233-239(1979).
15. Dorshorst B, Okimoto R, Ashwell C: Genomic regions associated with dermal hyperpigmentation, polydactyly and other morphological traits in the Silkie chicken. J Hered 101:339-350(2010).
16. Dunn IC, Paton IR, Clelland AK, Sebastian S, Johnson EJ, et al: The chicken polydactyly (Po) locus causes allelic imbalance and ectopic expression of Shh during limb development. Dev Dyn 240:1163-1172(2011).
17. Elferink MG, van As P, Veenendaal T, Crooijmans RP, Groenen MA: Regional differences in recombination hotspots between two chicken populations. BMC Genet 11:11(2010).
18. Everman DB: Hands and feet, in Stevenson RE, Hall JG (eds): Human Malformations and Related Anomalies, 2nd ed., pp 935-996 (Oxford University Press, Oxford 2006).
19. Furniss D, Lettice LA, Taylor IB, Critchley PS, Giele H, et al: A variant in the sonic hedgehog regulatory sequence (ZRS) is associated with triphalangeal thumb and deregulates expression in the developing limb. Hum Mol Genet 17:2417-2423(2008).
20. Gorbach D, Mote B, Totir L, Fernando R, Rothschild M: Polydactyl inheritance in the pig. J Hered 101:469-475(2010).
21. Groenen MA, Wahlberg P, Foglio M, Cheng HH, Megens HJ, et al: A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19:510-519(2009).
22. Gurnett CA, Bowcock AM, Dietz FR, Morcuende JA, Murray JC, Dobbs MB: Two novel point mutations in the long-range SHH enhancer in three families with triphalangeal thumb and preaxial polydactyly. Am J Med Genet A 143:27-32(2007).
23. Huang YQ, Deng XM, Du ZQ, Qiu X, Du X, et al: Single nucleotide polymorphisms in the chicken Lmbr1 gene are associated with chicken polydactyly. Gene 374:10-18(2006).
24. Hurst LD, Brunton CF, Smith NG: Small introns tend to occur in GC-rich regions in some but not all vertebrates. Trends Genet 15:437-439(1999).
25. Ianakiev P, van Baren MJ, Daly M, Toledo S, Cavalcanti MG, et al: Acheiropodia is caused by a genomic deletion in C7orf2, the human orthologue of the Lmbr1 gene. Am J Hum Genet 68:38-45(2001).
26. International Chicken Genome Sequencing Consortium (ICGSC): Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695-716(2004).
27. Jeong SY, Kim BY, Yu JE: De novo pericentric inversion of chromosome 9 in congenital anomaly. Yonsei Med J 51:775-780(2010).
28. Johnson JL, Leipold HW, Schalles RR: Hereditary polydactyly in Simmental cattle. J Hered 72:205-208(1981).
29. Kong A, Gudbjartsson DF, Jonsdottir GM, Gudjonsson SA, Richardsson B, et al: A high resolution recombination map of the human genome. Nat Genet 31:241-247(2002).
30. Kraus P, Fraidenraich D, Loomis CA: Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mech Dev 100:45-58(2001).
31. Krebs O, Schreiner CM, Scott WJ, Bell SM, Robbins DJ, et al: Replicated anterior zeugopod (raz): a polydactylous mouse mutant with lowered Shh signaling in the limb bud. Development 130:6037-6047(2003).
32. Kren V: Genetics of the polydactyly-luxate syndrome in the Norway rat, Rattus norvegicus. Acta Univ Carol Med Monogr 68:1-103(1975).
33. Laan M, Kallioniemi OP, Hellsten E, Alitalo K, Peltonen L, Palotie A: Mechanically stretched chromosomes as targets for high-resolution FISH mapping. Genome Res 5:13-20(1995).
34. Ladjali-Mohammedi K, Bitgood JJ, Tixier-Boichard M, Ponce de Leon FA: International System for Standardized Avian karyotypes (ISSAK): standardized banded karyotypes of the domestic fowl (Gallus domesticus). Cytogenet Cell Genet 86:271-276(1999).
35. Lettice LA, Horikoshi T, Heaney SJ, van Baren MJ, van der Linde HC, et al: Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc Natl Acad Sci USA 99:7548-7553(2002).
36. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, et al: A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12:1725-1735(2003).
37. Lettice LA, Hill AE, Devenney PS, Hill RE: Point mutations in a distant sonic hedgehog cisregulator generate a variable regulatory output responsible for preaxial polydactyly. Hum Mol Genet 17:978-985(2008).
38. Lima L, Macieira-Coelho A: Parameters of aging in chicken embryo fibroblasts cultivated in vitro. Exp Cell Res 70:279-284(1972).
39. Lodder EM, Eussen BH, van Hassel DA, Hoogeboom AJ, Poddighe PJ, et al: Implication of long-distance regulation of the HOXA cluster in a patient with postaxial polydactyly. Chromosome Res 17:737-744(2009).
40. Maas SA, Fallon JF: Isolation of the chicken Lmbr1 coding sequence and characterization of its role during chick limb development. Dev Dyn 229:520-528(2004).
41. Maas SA, Fallon JF: Single base pair change in the long-range Sonic hedgehog limb-specific enhancer is a genetic basis for preaxial polydactyly. Dev Dyn 232:345-348(2005).
42. Maas SA, Suzuki T, Fallon JF: Identification of spontaneous mutations within the longrange limb-specific sonic hedgehog enhancer (ZRS) that alter sonic hedgehog expression in the chicken limb mutants oligozeugodactyly and Silkie breed. Dev Dyn 240:1212-1222(2011).
43. Meunier J, Duret L: Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 21:984-990(2004).
44. Niedermaier M, Schwabe GC, Fees S, Helmrich A, Brieske N, et al: An inversion involving the mouse Shh locus results in brachydactyly through dysregulation of Shh expression. J Clin Invest 115:900-909(2005).
45. O'Hare TH, Delany ME: Genetic variation exists for telomeric array organization within and among the genomes of normal, immortalized, and transformed chicken systems. Chromosome Res 17:947-964(2009).
46. Oro AE, Higgins KM, Hu Z, Bonifas JM, Epstein EH, Scott MP: Basal cell carcinomas in mice overexpressing Sonic hedgehog. Science 276:817-821(1997).
47. Park K, Kang J, Subedi KP, Ha JH, Park C: Canine polydactyl mutations with heterogeneous origin in the conserved intronic sequence of LMBR1. Genetics 179:2163-2172(2008).
48. Pisenti JM, Delany ME, Taylor RL, Abbott UK, Abplanalp H, et al: Avian genetic resources at risk. An assessment and proposal for conservation of genetic stocks in the USA and Canada. Davis (CA): University of California Division of Agriculture and Natural Resources, Genetic Resources Conservation Program. http://grcp.ucdavis.edu/publications/index.htm. Available from: Report No. 20(1999).
49. Pitel F, Berge R, Coquerelle G, Crooijmans RP, Groenen MA, et al: Mapping the naked neck (NA) and polydactyly (PO) mutants of the chicken with microsatellite molecular markers. Genet Sel Evol 32:73-86(2000).
50. Punnett RC, Pease MS: Notes on polydactyly. J Genet 21:341-366(1929).
51. Riddle RD, Johnson RL, Laufer E, Tabin C: Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401-1416(1993).
52. Robb EA, Gitter CL, Cheng HH, Delany ME: Chromosomal mapping and candidate gene discovery of chicken developmental mutants and genome-wide variation analysis of MHC congenics. J Hered 102:141-156(2011).
53. Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T: Elimination of a long-range cisregulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132:797-803(2005).
54. Sakai WH: Polydactyly in a Vaux's swift. Wilson J Ornithol 118:424-426(2006).
55. Samuels ML, Witmer JW: Statistics for the Life Sciences, 2nd ed. (Prentice Hall, Englewood Cliffs, 1999).
56. Sharpe J, Lettice L, Heckser-Sorensen J, Fox M, Hill R, Krumlauf R: Identification of Sonic hedgehog as a candidate gene responsible for the polydactylous mouse mutant Sasquatch. Curr Biol 9:97-100(1999).
57. Sonoda E, Sasaki MS, Buerstedde J-M, Bezzubova O, Shinohara A, et al: Rad51 deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17:598-608(1998).
58. Struthers J: On the development of the bones of the foot of the horse, and of digital bones generally and on a case of polydactyly in the horse. J Anat Physiol 28:51-62(1893).
59. Sturkie PD: Suppression of polydactyly in the domestic fowl by low temperature. J Exp Zool 93:325-346(1943).
60. Sun M, Ma F, Zeng X, Liu Q, Zhao XL, et al: Triphalangeal thumb-polysyndactyly syndrome and syndactyly type IV are caused by genomic duplications involving the long range, limb-specific SHH enhancer. J Med Genet 45:589-595(2008).
61. The American Poultry Association. The American Standard of Perfection (American Poultry Association, Inc., Mendon, MA, 1998).
62. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680(1994).
63. Uehlinger V: A recessive mutation (pd) determinant of polydactyly in Xenopus laevis D. (Batraciens anoures). [French]. J Embryol Exp Morphol 21:207-218(1969).
64. Wada Y, Yamada Y, Nishibori M, Yasue H: Complete nucleotide sequence of mitochondrial genome in Silkie fowl (Gallus gallus var. domesticus). J Poult Sci 41:76-82(2004).
65. Wang ZQ, Tian SH, Shi YZ, Zhou PT, Wang ZY, et al: A single C to T transition in intron 5 of LMBR1 gene is associated with triphalangeal thumb-polysyndactyly syndrome in a Chinese family. Biochem Biophys Res Commun 355:312-317(2007).
66. Warren DC: Inheritance of polydactylism in the fowl. Genetics 29:217-231(1944).
67. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191(2009).
68. Wieczorek D, Pawlik B, Li Y, Akarsu NA, Caliebe A, et al: A specific mutation in the distant sonic hedgehog cis-regulator (ZRS) causes Werner mesomelic syndrome while complete ZRS duplications underlie Haas type polysyndactyly and preaxial polydactyly with or without triphalangeal thumb. Hum Mutat 31:81-89(2010).
69. Williams EJ, Hurst LD: The proteins of linked genes evolve at similar rates. Nature 407:900-903(2000).
70. Yang Y, Drossopoulou G, Chuang PT, Duprez D, Marti E, et al: Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124:4393-4404(1997).