Analysis of a new allele of limb deformity (Id) reveals tissue- and age-specific transcriptional effects of the Ld Global Control Region

International Journal of Developmental Biology

Volumn 51, Issue 4, 2007, Pages 273-281

  Pavel, Emilia ^a   Zhao, Wenning ^a   Powell, Kimerly A ^b   Weinstein, Michael ^a   Kirschner, Lawrence S ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c 544 TMRF ^*  (United States)

Author keywords

Formin; Global control region; Gremlin; Limb development; Transcriptional control

Indexed keywords

ALLELE; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE LOSS; GENE MUTATION; GENETIC TRANSCRIPTION; HOMOZYGOSITY; LIMB BUD; LIMB DEFORMITY; LIMB DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL;

AGE FACTORS; ALLELES; ANIMALS; FETAL PROTEINS; GENE DELETION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIMB BUD; LOWER EXTREMITY; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MUTATION; NUCLEAR PROTEINS; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC;

MUS;

EID: 34347238200     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.062249ep     Document Type: Article

References (53)

1. ADAMSKA, M., MACDONALD, B.T. and MEISLER, M.H. (2003). Doubleridge, a mouse mutant with defective compaction of the apical ectodermal ridge and normal dorsal-ventral patterning of the limb. Dev Biol 255: 350-62.
2. BOZZOLA, J.J. and RUSSELL, L.D. (1999). Electron microscopy: Principles and techniques for biologists. Jones and Bartlett, Sudbury, MA.
3. CAO, X., WEI, G., FANG, H., GUO, J., WEINSTEIN, M., MARSH, C.B., OSTROWSKI, M.C. and TRIDANDAPANI, S. (2004). The inositol 3-phosphatase pten negatively regulates fc gamma receptor signaling, but supports toll-like receptor 4 signaling in murine peritoneal macrophages. J Immunol 172: 4851-7.
4. CAPDEVILA, J., TSUKUI, T., RODRIQUEZ ESTEBAN, C., ZAPPAVIGNA, V. and IZPISUA BELMONTE, J.C. (1999). Control of vertebrate limb outgrowth by the proximal factor meis2 and distal antagonism of bmps by gremlin. Mol Cell A: 839-49.
5. CHAO, C.W., CHAN, D.C., KUO, A. and LEDER, P. (1998). The mouse formin (fmn) gene: Abundant circular rna transcripts and gene-targeted deletion analysis. Mol Med 4: 614-28.
6. CRICK, A.P., BABBS, C., BROWN, J.M. and MORRISS-KAY, G.M. (2003). Developmental mechanisms underlying Polydactyly in the mouse mutant doublefoot. J Anat 202: 21-6.
7. DESCHAMPS, J. and VAN NES, J. (2005). Developmental regulation of the hox genes during axial morphogenesis in the mouse. Development 132: 2931-42.
8. GRZESCHIK, K.-H. (2002). Human limb malformations; an approach to the molecular basis of development. Int. J. Dev. Biol. 46: 983-991.
9. GURRIERI, F., KJAER, K.W., SANGIORGI, E. and NERI, G. (2002). Limb anomalies: Developmental and evolutionary aspects. Am J Med Genet 115: 231-44.
10. HARAMIS, A.G., BROWN, J.M. and ZELLER, R. (1995). The limb deformity mutation disrupts the shh/fgf-4 feedback loop and regulation of 5′ hoxd genes during limb pattern formation. Development 121: 4237-45.
11. HAYES, C., RUMP, A., CADMAN, M.R., HARRISON, M., EVANS, E.P., LYON, M.F., MORRISS-KAY, G.M., ROSENTHAL, A. and BROWN, S.D. (2001). A high-resolution genetic, physical and comparative gene map of the doublefoot (dbf) region of mouse chromosome 1 and the region of conserved synteny on human chromosome 2q35. Genomics 78: 197-205.
12. IGUCHI, H., CHAN, J.S., SEIDAH, N.G. and CHRETIEN, M. (1984). Tissue distribution and molecular forms of a novel pituitary protein in the rat. Neuroendocrinology 39: 453-8.
13. KHOKHA, M.K., HSU, D., BRUNET, L.J., DIONNE, M.S. and HARLAND, R.M. (2003). Gremlin is the bmp antagonist required for maintenance of shh and fgf signals during limb patterning. Nat Genet 34: 303-7.
14. KIRSCHNER, L.S., KUSEWITT, D.F., MATYAKHINA, L., TOWNS, W.H., 2ND, CARNEY, J.A., WESTPHAL, H. and STRATAKIS, C.A. (2005). A mouse model for the carney complex tumor syndrome develops neoplasia in cyclic amp-responsive tissues. Cancer Res 65: 4506-14.
15. KIRSCHNER, L.S., TAYMANS, S.E., PACK, S., PAK, E., PIKE, B.L., CHANDRASEKHARAPPA, S.C., ZHUANG, Z. and STRATAKIS, C.A. (1999). Genomic mapping of chromosomal region 2p15-p21 (d2s378-d2s391): Integration of genemap'98 within a framework of yeast and bacterial artificial chromosomes. Genomics 62: 21-33.
16. KLEINEBRECHT, J., SELOW, J. and WINKLER, W. (1982). The mouse mutant limb-deformity (Id). Anat Anz 152: 313-24.
17. KLEINJAN, D.A. and VAN HEYNINGEN, V. (2005). Long-range control of gene expression: Emerging mechanisms and disruption in disease. Am J Hum Genet 76: 8-32.
18. LEWIN, S.O. and OPITZ, J.M. (1986). Fibular a/hypoplasia: Review and documentation of the fibular developmental field. Am J Med Genet Suppl 2: 215-38.
19. LIM, W., HEARLE, N., SHAH, B., MURDAY, V., HODGSON, S.V., LUCASSEN, A., ECCLES, D., TALBOT, I., NEALE, K., LIM, A.G. et al. (2003). Further observations on Ikb1/stk11 status and cancer risk in peutz-jeghers syndrome. Br J Cancer 89: 308-13.
20. LU, M.M., YANG, H., ZHANG, L., SHU, W., BLAIR, D.G. and MORRISEY, E.E. (2001). The bone morphogenic protein antagonist gremlin regulates proximal-distal patterning of the lung. Dev Dyn 222: 667-80.
21. LYON, M.F., QUINNEY, R., GLENISTER, P.H., KERSCHER, S., GUILLOT, P. and BOYD, Y. (1996). Doublefoot: A new mouse mutant affecting development of limbs and head. Genet Res 68: 221-31.
22. MAAS, R., ELFERING, S., GLASER, T. and JEPEAL, L. (1994). Deficient outgrowth of the ureteric bud underlies the renal agenesis phenotype in mice manifesting the limb deformity (Id) mutation. Dev Dyn 199: 214-28.
23. MAAS, R.L., ZELLER, R., WOYCHIK, R.P., VOGT, T.F. and LEDER, P. (1990). Disruption of formin-encoding transcripts in two mutant limb deformity alleles. Nature 346: 853-5.
24. MACDONALD, B.T., ADAMSKA, M. and MEISLER, M.H. (2004). Hypomorphic expression of dkk1 in the doubleridge mouse: Dose dependence and compensatory interactions with Irp6. Development 131: 2543-52.
25. MARIANI, F.V. and MARTIN, G.R. (2003). Deciphering skeletal patterning: Clues from the limb. Nature 423: 319-25.
26. MCKUSICK, V.A. (2003). Online Mendelian Inheritance in Man, OMIM (TM). McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University (Baltimore, MD) and National Center for Biotechnology Information, National Library of Medicine (Bethesda, MD).URL http://www.ncbi.nlm.nih.gov/ omim. Accessed 17 Feb 2007
27. MERINO, R., RODRIGUEZ-LEON, J., MACIAS, D., GANAN, Y., ECONOMIDES, A.N. and HURLE, J.M. (1999). The bmp antagonist gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126: 5515-22.
28. MESSING, A., BEHRINGER, R.R., SPLAPAK, J.R., LEMKE, G., PALMITER, R.D. and BRINSTER, R.L. (1990). Insertional mutation at the Id locus (again!) in a line of transgenic mice. Mouse Genome 1990: 107.
29. MICHOS, O., PANMAN, L., VINTERSTEN, K., BEIER, K., ZELLER, R. and ZUNIGA, A. (2004). Gremlin-mediated bmp antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131: 3401-10.
30. MILLS, A.A., ZHENG, B., WANG, X.J., VOGEL, H., ROOP, D.R. and BRADLEY, A. (1999). P63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398: 708-13.
31. NISWANDER, L. (2002). Interplay between the molecular signals that control vertebrate limb development. Int J Dev Biol 46: 877-81.
32. NIEDERMAIER, M., SCHWABE, G.C., FEES, S., HELMRICH, A., BRIESKE, N., SEEMANN, P., HECHT, J., SEITZ, V., STRICKER, S., LESCHIK, G. et al. (2005). An inversion involving the mouse shh locus results in brachydactyly through dysregulation of shh expression. J Clin Invest 115: 900-9.
33. PAN, Y., LIU, Z., SHEN, J. and KOPAN, R. (2005). Notch1 and 2 cooperate in limb ectoderm to receive an early jagged2 signal regulating interdigital apoptosis. Dev Biol 286: 472-82.
34. PEARCE, J.J., PENNY, G. and ROSSANT, J. (1999). A mouse cerberus/dan-related gene family. Dev Biol 209: 98-110.
35. POWELL, K.A., LATSON, L., IBIWOYE, M.O., WOLFMAN, A., GRABINER, M.D., ZBOROWSKI, M., SAKAI, Y. and MIDURA, R.J. (2005). In vivo longitudinal assessment of bone resorption in a fibular osteotomy model using micro-computed tomography. Iowa Orthop J 25: 123-8.
36. SAGAI, T., MASUYA, H., TAMURA, M., SHIMIZU, K., YADA, Y., WAKANA, S., GONDO, Y., NODA, T. and SHIROISHI, T. (2004). Phylogenetic conservation of a limb-specific, cis-acting regulator of sonic hedgehog (shh). Mamm Genome 15: 23-34.
37. SHI, W., ZHAO, J., ANDERSON, K.D. and WARBURTON, D. (2001). Gremlin negatively modulates bmp-4 induction of embryonic mouse lung branching morphogenesis. Am J Physiol Lung Cell Mol Physiol 280: L1030-9.
38. STOPPER, G.F. and WAGNER, G.P. (2005). Of chicken wings and frog legs: A smorgasbord of evolutionary variation in mechanisms of tetrapod limb development. Dev Biol 288: 21-39.
39. SUN, X., LEWANDOSKI, M., MEYERS, E.N., LIU, Y.H., MAXSON, R.E., JR. and MARTIN, G.R. (2000). Conditional inactivation of fgf4 reveals complexity of signalling during limb bud development. Nat Genet 25: 83-6.
40. TICKLE, C. (2003). Patterning systems - from one end of the limb to the other. Dev Cell 4: 449-58.
41. TOPOL, L.Z., MARX, M., LAUGIER, D., BOGDANOVA, N.N., BOUBNOV, N.V., CLAUSEN, P.A., CALOTHY, G. and BLAIR, D.G. (1997). Identification of drm, a novel gene whose expression is suppressed in transformed cells and which can inhibit growth of normal but not transformed cells in culture. Mol Cell Biol 17: 4801-10.
42. WANG, C.C., CHAN, D.C. and LEDER, P. (1997). The mouse formin (fmn) gene: Genomic structure, novel exons and genetic mapping. Genomics 39: 303-11.
43. WARD-BAILEY, P.F., HARRIS, B.S., DONAHUE, L.R., BRONSON, R.T. and DAVISSON, M.T. (2006). Mutant mouse resource web site, (ed.: The Jackson Labs, Bar Harbor, ME.
44. WESTPHAL, C.H., MULLER, L., ZHOU, A., ZHU, X., BONNER-WEIR, S., SCHAMBELAN, M., STEINER, D.F., LINDBERG, I. and LEDER, P. (1999). The neuroendocrine protein 7b2 is required for peptide hormone processing in vivo and provides a novel mechanism for pituitary cushing's disease. Cell 96: 689-700.
45. WOYCHIK, R.P., GENEROSO, W.M., RUSSELL, L.B., CAIN, K.T., CACHEIRO, N.L, BULTMAN, S.J., SELBY, P.B., DICKINSON, M.E., HOGAN, B.L. and RUTLEDGE, J.C. (1990). Molecular and genetic characterization of a radiation-induced structural rearrangement in mouse chromosome 2 causing mutations at the limb deformity and agouti loci. Proc Natl Acad Sci USA 87: 2588-92.
46. WOYCHIK, R.P., STEWART, T.A., DAVIS, L.G., D'EUSTACHIO, P. and LEDER, P. (1985). An inherited limb deformity caused by insertional mutagenesis in a transgenic mouse. Nature 318: 36-40.
47. WYNSHAW-BORIS, A., RYAN, G., DENG, C.X., CHAN, D.C., JACKSON-GRUSBY, L., LARSON, D., DUNMORE, J.H. and LEDER, P. (1997). The role of a single formin isoform in the limb and renal phenotypes of limb deformity. Mol Med 3: 372-84.
48. YANG, A., SCHWEITZER, R., SUN, D., KAGHAD, M., WALKER, N., BRONSON, R.T., TABIN, C., SHARPE, A., CAPUT, D., CRUM, C. et al. (1999). P63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398: 714-8.
49. ZELLER, R., HARAMIS, A.G., ZUNIGA, A., MCGUIGAN, C., DONO, R., DAVIDSON, G., CHABANIS, S. and GIBSON, T. (1999). Formin defines a large family of morphoregulatory genes and functions in establishment of the polarising region. Cell Tissue Res 296: 85-93.
50. ZELZER, E. and OLSEN, B.R. (2003). The genetic basis for skeletal diseases. Nature 423: 343-8.
51. ZUNIGA, A. (2005). Globalisation reaches gene regulation: The case for vertebrate limb development. Curr Opin Genet Dev 15: 403-9.
52. ZUNIGA, A., HARAMIS, A.P., MCMAHON, A.P. and ZELLER, R. (1999). Signal relay by bmp antagonism controls the shh/fgf4 feedback loop in vertebrate limb buds. Nature 401: 598-602.
53. ZUNIGA, A., MICHOS, O., SPITZ, F., HARAMIS, A.P., PANMAN, L., GALLI, A., VINTERSTEN, K., KLASEN, C., MANSFIELD, W., KUC, S. et al. (2004). Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for gremlin expression. Genes Dev 18: 1553-64.