Reduced BMP Signaling Results in Hindlimb Fusion with Lethal Pelvic/Urogenital Organ Aplasia: A New Mouse Model of Sirenomelia

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Suzuki, Kentaro ^a,b   Adachi, Yasuha ^a,b   Numata, Tomokazu ^a,b   Nakada, Shoko ^a,b   Yanagita, Motoko ^c   Nakagata, Naomi ^b   Evans, Sylvia M ^d,e   Graf, Daniel ^f   Economides, Aris ^g   Haraguchi, Ryuma ^h   Moon, Anne M ⁱ   Yamada, Gen ^a,b  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g REGENERON PHARMACEUTICALS INC   (United States)

^h EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

ⁱ WEIS CENTER FOR RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; CRE RECOMBINASE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR TBX4; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APLASIA; ARTICLE; CELL FATE; CLOACA; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; FIBULA; GENE; GENE DISRUPTION; GENE MAPPING; GENETIC ANALYSIS; HINDLIMB; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; ISL1 GENE; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; PELVIS APLASIA; PHENOTYPE; PHYSICAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SIRENOMELIA; TISSUE DISTRIBUTION; UROGENITAL SYSTEM; UROGENITAL TRACT APLASIA;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; BONE MORPHOGENETIC PROTEINS; DISEASE MODELS, ANIMAL; ECTROMELIA; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HINDLIMB; LIM-HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; PHENOTYPE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UROGENITAL ABNORMALITIES;

MUS;

EID: 84866460613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043453     Document Type: Article

References (62)

1. Garrido-Allepuz C, Haro E, Gonzalez-Lamuno D, Martinez-Frias ML, Bertocchini F, et al. (2011) A clinical and experimental overview of sirenomelia: insight into the mechanisms of congenital limb malformations. Dis Model Mech 4: 289-299.
2. Kallen B, Castilla EE, Lancaster PA, Mutchinick O, Knudsen LB, et al. (1992) The cyclops and the mermaid: an epidemiological study of two types of rare malformation. J Med Genet 29: 30-35.
3. Stevenson RE, Jones KL, Phelan MC, Jones MC, Barr M, et al. (1986) Vascular steal: the pathogenetic mechanism producing sirenomelia and associated defects of the viscera and soft tissues. Pediatrics 78: 451-457.
4. Kallen B, Winberg J, (1974) Caudal mesoderm pattern of anomalies: from renal agenesis to sirenomelia. Teratology 9: 99-111.
5. Opitz JM, Zanni G, Reynolds JF Jr, Gilbert-Barness E, (2002) Defects of blastogenesis. Am J Med Genet 115: 269-286.
6. de Santa Barbara P, Roberts DJ, (2002) Tail gut endoderm and gut/genitourinary/tail development: a new tissue-specific role for Hoxa13. Development 129: 551-561.
7. Kimmel SG, Mo R, Hui CC, Kim PC, (2000) New mouse models of congenital anorectal malformations. J Pediatr Surg 35: 227-230 discussion 230-231.
8. Penington EC, Hutson JM, (2003) The absence of lateral fusion in cloacal partition. J Pediatr Surg 38: 1287-1295.
9. Yamada G, Satoh Y, Baskin LS, Cunha GR, (2003) Cellular and molecular mechanisms of development of the external genitalia. Differentiation 71: 445-460.
10. Yamada G, Suzuki K, Haraguchi R, Miyagawa S, Satoh Y, et al. (2006) Molecular genetic cascades for external genitalia formation: an emerging organogenesis program. Dev Dyn 235: 1738-1752.
11. Haraguchi R, Motoyama J, Sasaki H, Satoh Y, Miyagawa S, et al. (2007) Molecular analysis of coordinated bladder and urogenital organ formation by Hedgehog signaling. Development 134: 525-533.
12. Haraguchi R, Matsumaru D, Nakagata N, Miyagawa S, Suzuki K, et al. (2012) The Hedgehog Signal Induced Modulation of Bone Morphogenetic Protein Signaling: An Essential Signaling Relay for Urinary Tract Morphogenesis. PLoS ONE In press.
13. Mildenberger H, Kluth D, Dziuba M, (1988) Embryology of bladder exstrophy. J Pediatr Surg 23: 166-170.
14. Haraguchi R, Mo R, Hui CC, Motoyama J, Makino S, et al. (2001) Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128: 4241-4250.
15. Benazet JD, Zeller R, (2009) Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb Perspect Biol 1: a001339.
16. Arnold SJ, Robertson EJ, (2009) Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91-103.
17. Morrisey EE, Hogan BL, (2010) Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18: 8-23.
18. Wang J, Greene SB, Martin JF, (2011) BMP signaling in congenital heart disease: new developments and future directions. Birth Defects Res A Clin Mol Terato 91: 441-448.
19. Warburton D, Bellusci S, (2004) The molecular genetics of lung morphogenesis and injury repair. Paediatr Respir Rev 5: Suppl A: S283-287.
20. Dudley AT, Lyons KM, Robertson EJ, (1995) A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9: 2795-2807.
21. Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, et al. (1995) BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev 9: 2808-2820.
22. Zakin L, Reversade B, Kuroda H, Lyons KM, De Robertis EM, (2005) Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development 132: 2489-2499.
23. Winnier G, Blessing M, Labosky PA, Hogan BL, (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-2116.
24. Yang L, Cai CL, Lin L, Qyang Y, Chung C, et al. (2006) Isl1Cre reveals a common Bmp pathway in heart and limb development. Development 133: 1575-1585.
25. Kawakami Y, Marti M, Kawakami H, Itou J, Quach T, et al. (2011) Islet1-mediated activation of the beta-catenin pathway is necessary for hindlimb initiation in mice. Development 138: 4465-4473.
26. Stocker JT, Heifetz SA, (1987) Sirenomelia. A morphological study of 33 cases and review of the literature. Perspect Pediatr Pathol 10: 7-50.
27. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
28. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, et al. (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
29. Park EJ, Sun X, Nichol P, Saijoh Y, Martin JF, et al. (2008) System for tamoxifen-inducible expression of cre-recombinase from the Foxa2 locus in mice. Dev Dyn 237: 447-453.
30. Zhu J, Nakamura E, Nguyen MT, Bao X, Akiyama H, et al. (2008) Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell 14: 624-632.
31. Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, et al. (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130: 6361-6374.
32. Goncalves A, Zeller R, (2011) Genetic analysis reveals an unexpected role of BMP7 in initiation of ureteric bud outgrowth in mouse embryos. PLoS ONE 6: e19370.
33. Solloway MJ, Robertson EJ, (1999) Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126: 1753-1768.
34. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, et al. (2006) Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2: e216.
35. Bonilla-Claudio M, Wang J, Bai Y, Klysik E, Selever J, et al. (2012) Bmp signaling regulates a dose-dependent transcriptional program to control facial skeletal development. Development 139: 709-719.
36. Moon AM, Capecchi MR, (2000) Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet 26: 455-459.
37. Benazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, et al. (2009) A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323: 1050-1053.
38. Zakany J, Zacchetti G, Duboule D, (2007) Interactions between HOXD and Gli3 genes control the limb apical ectodermal ridge via Fgf10. Dev Biol 306: 883-893.
39. Selever J, Liu W, Lu MF, Behringer RR, Martin JF, (2004) Bmp4 in limb bud mesoderm regulates digit pattern by controlling AER development. Dev Biol 276: 268-279.
40. Yamaguchi TP, Bradley A, McMahon AP, Jones S, (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211-1223.
41. Zeller R, Lopez-Rios J, Zuniga A, (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845-858.
42. Zakany J, Kmita M, Duboule D, (2004) A dual role for Hox genes in limb anterior-posterior asymmetry. Science 304: 1669-1672.
43. Bastida MF, Sheth R, Ros MA, (2009) A BMP-Shh negative-feedback loop restricts Shh expression during limb development. Development 136: 3779-3789.
44. Browne M, Fitchev P, Adley B, Crawford SE, (2004) Sirenomelia with an angiomatous lumbosacral myelocystocele in a full-term infant. J Perinatol 24: 329-331.
45. Taori KB, Mitra K, Ghonga NP, Gandhi RO, Mammen T, et al. (2002) Sirenomelia sequence (mermaid): Report of three cases. Indian J Radiol Imaging 12: 399-401.
46. Chen H, Lun Y, Ovchinnikov D, Kokubo H, Oberg KC, et al. (1998) Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19: 51-55.
47. Loomis CA, Harris E, Michaud J, Wurst W, Hanks M, et al. (1996) The mouse Engrailed-1 gene and ventral limb patterning. Nature 382: 360-363.
48. Naiche LA, Papaioannou VE, (2007) Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134: 93-103.
49. Ouimette JF, Jolin ML, L'Honore A, Gifuni A, Drouin J, (2010) Divergent transcriptional activities determine limb identity. Nat Commun 1: 35.
50. Naiche LA, Arora R, Kania A, Lewandoski M, Papaioannou VE, (2011) Identity and fate of Tbx4-expressing cells reveal developmental cell fate decisions in the allantois, limb, and external genitalia. Dev Dyn 240: 2290-2300.
51. Ohta S, Suzuki K, Tachibana K, Tanaka H, Yamada G, (2007) Cessation of gastrulation is mediated by suppression of epithelial-mesenchymal transition at the ventral ectodermal ridge. Development 134: 4315-4324.
52. Barr M Jr, (1988) Comments on "Origin of Abnormality in a Human Simelian Foetus as Elucidated by Our Knowledge of Vertebrate Development". Teratology 38: 487-491.
53. O'Rahilly R, Muller F, (1989) Interpretation of some median anomalies as illustrated by cyclopia and symmelia. Teratology 40: 409-421.
54. Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, et al. (2001) Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev Biol 236: 421-435.
55. Yuan S, Schoenwolf GC, (2000) Islet-1 marks the early heart rudiments and is asymmetrically expressed during early rotation of the foregut in the chick embryo. Anat Rec 260: 204-207.
56. Chevallier A, Kieny M, Mauger A, (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41: 245-258.
57. Chang W, Lin Z, Kulessa H, Hebert J, Hogan BL, et al. (2008) Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet 4: e1000050.
58. Zouvelou V, Passa O, Segklia K, Tsalavos S, Valenzuela DM, et al. (2009) Generation and functional characterization of mice with a conditional BMP7 allele. Int J Dev Biol 53: 597-603.
59. Feil R, Wagner J, Metzger D, Chambon P, (1997) Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237: 752-757.
60. Omori A, Harada M, Ohta S, Villacorte M, Sugimura Y, et al. (2011) Epithelial Bmp (Bone morphogenetic protein) signaling for bulbourethral gland development: a mouse model for congenital cystic dilation. Congenit Anom (Kyoto) 51: 102-109.
61. Harada M, Murakami H, Okawa A, Okimoto N, Hiraoka S, et al. (2009) FGF9 monomer-dimer equilibrium regulates extracellular matrix affinity and tissue diffusion. Nat Genet 41: 289-298.
62. Suzuki K, Haraguchi R, Ogata T, Barbieri O, Alegria O, et al. (2008) Abnormal urethra formation in mouse models of split-hand/split-foot malformation type 1 and type 4. Eur J Hum Genet 16: 36-44.