Genetic analysis of hedgehog signaling in ventral body wall development and the onset of omphalocele formation

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Matsumaru, Daisuke ^a   Haraguchi, Ryuma ^a,d   Miyagawa, Shinichi ^a,e   Motoyama, Jun ^b   Nakagata, Naomi ^a   Meijlink, Frits ^c   Yamada, Gen ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b DOSHISHA UNIVERSITY   (Japan)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e NATIONAL INSTITUTES OF NATURAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARISTALESS LIKE HOMEOBOX 4; GENE PRODUCT; SONIC HEDGEHOG PROTEIN; TAMOXIFEN; TRANSCRIPTION FACTOR GLI3; UNCLASSIFIED DRUG; GLI3 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FINGER MALFORMATION; GENE ACTIVITY; GENE INTERACTION; GENE MUTATION; GENETIC ANALYSIS; HETEROZYGOSITY; HYPOPLASIA; MORPHOGENESIS; MOUSE; NONHUMAN; OMPHALOCELE; PHENOTYPIC VARIATION; PUBIC SYMPHYSIS DIASTASIS; UROGENITAL TRACT MALFORMATION; ANIMAL; ANIMAL EMBRYO; DOSE RESPONSE; EMBRYO DEVELOPMENT; GENE THERAPY; GENETICS; METHODOLOGY; MOUSE MUTANT; MUTATION; PATHOLOGY; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION; UMBILICAL HERNIA;

ERINACEIDAE;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GENE THERAPY; HEDGEHOG PROTEINS; HERNIA, UMBILICAL; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, MUTANT STRAINS; MUTATION; NERVE TISSUE PROTEINS; PHENOTYPE; PUBIC SYMPHYSIS DIASTASIS; SIGNAL TRANSDUCTION;

EID: 79251602124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016260     Document Type: Article

References (98)

1. Kaufman MH (1992) The atlas of mouse development. London; San Diego: Academic Press. xvi, 512.
2. Brewer S, Williams T (2004) Finally, a sense of closure? Animal models of human ventral body wall defects. Bioessays 26: 1307-1321.
3. Eggenschwiler J, Ludwig T, Fisher P, Leighton P, Tilghman S, et al. (1997) Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith- Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev 11: 3128-3142.
4. Achiron R, Soriano D, Lipitz S, Mashiach S, Goldman B, et al. (1995) Fetal midgut herniation into the umbilical cord: improved definition of ventral abdominal anomaly with the use of transvaginal sonography. Ultrasound Obstet Gynecol 6: 256-260.
5. Mann S, Blinman T, Douglas Wilson R (2008) Prenatal and postnatal management of omphalocele. Prenat Diagn 28: 626-632.
6. Sadler T (2006) Langman's medical embryology. Philadelphia: Lippincott Williams & Wilkins, xiii, 371.
7. Glasser JG (2009) Omphalocele and Gastroschisis. eMedicine: Medscape.
8. Weber T, Au-Fliegner M, Downard C, Fishman S (2002) Abdominal wall defects. Curr Opin Pediatr 14: 491-497.
9. Sadler T (2010) The embryologic origin of ventral body wall defects. Semin Pediatr Surg 19: 209-214.
10. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, et al. (1999) Calreticulin is essential for cardiac development. J Cell Biol 144: 857-868.
11. Taeusch HW, Ballard RA, Gleason CA, Avery ME (2005) Avery's diseases of the newborn. Philadelphia, Pa: W.B. Saunders, xxi, 1633.
12. Hirano M, Kiyonari H, Inoue A, Furushima K, Murata T, et al. (2006) A new serine/threonine protein kinase, Omphk1, essential to ventral body wall formation. Dev Dyn 235: 2229-2237.
13. Yazbeck S, Ndoye M, Khan AH (1986) Omphalocele: a 25-year experience. J Pediatr Surg 21: 761-763.
14. Aspelund G, Langer J (2006) Abdominal wall defects. Current Paediatrics 16: 192-198.
15. Perovic SV (1999) Atlas of Congenital Anomalies of the External Genitalia; Perovic, V. S, editors. Belgrad, Yugoslavia: Refot-Arka.
16. Langer J (2003) Abdominal wall defects. World J Surg 27: 117-124.
17. Ludwig M, Ching B, Reutter H, Boyadjiev S (2009) Bladder exstrophyepispadias complex. Birth Defects Res A Clin Mol Teratol 85: 509-522.
18. Suzuki K, Economides A, Yanagita M, Graf D, Yamada G (2009) New horizons at the caudal embryos: coordinated urogenital/reproductive organ formation by growth factor signaling. Curr Opin Genet Dev 19: 491-496.
19. Carey J (2001) Exstrophy of the cloaca and the OEIS complex: one and the same. Am J Med Genet 99: 270.
20. Bohring A (2002) OEIS complex, VATER, and the ongoing difficulties in terminology and delineation. Am J Med Genet 107: 72-76.
21. Stepan H, Horn L, Bennek J, Faber R (1999) Congenital hernia of the abdominal wall: a differential diagnosis of fetal abdominal wall defects. Ultrasound Obstet Gynecol 13: 207-209.
22. Lin C, Kioussi C, O'Connell S, Briata P, Szeto D, et al. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401: 279-282.
23. Kitamura K, Miura H, Miyagawa-Tomita S, Yanazawa M, Katoh-Fukui Y, et al. (1999) Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126: 5749-5758.
24. Nottoli T, Hagopian-Donaldson S, Zhang J, Perkins A, Williams T (1998) AP-2- null cells disrupt morphogenesis of the eye, face, and limbs in chimeric mice. Proc Natl Acad Sci U S A 95: 13714-13719.
25. Dunker N, Krieglstein K (2002) Tgfbeta2 2/2 Tgfbeta3 2/2 double knockout mice display severe midline fusion defects and early embryonic lethality. Anat Embryol (Berl) 206: 73-83.
26. Sun J, Liu YH, Chen H, Nguyen MP, Mishina Y, et al. (2007) Deficient Alk3- mediated BMP signaling causes prenatal omphalocele-like defect. Biochem Biophys Res Commun 360: 238-243.
27. Goldman D, Hackenmiller R, Nakayama T, Sopory S, Wong C, et al. (2006) Mutation of an upstream cleavage site in the BMP4 prodomain leads to tissuespecific loss of activity. Development 133: 1933-1942.
28. Ogi H, Suzuki K, Ogino Y, Kamimura M, Miyado M, et al. (2005) Ventral abdominal wall dysmorphogenesis of Msx1/Msx2 double-mutant mice. Anat Rec A Discov Mol Cell Evol Biol 284: 424-430.
29. Brewer S, Williams T (2004) Loss of AP-2alpha impacts multiple aspects of ventral body wall development and closure. Dev Biol 267: 399-417.
30. Schorle H, Meier P, Buchert M, Jaenisch R, Mitchell P (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381: 235-238.
31. Zhang J, Hagopian-Donaldson S, Serbedzija G, Elsemore J, Plehn-Dujowich D, et al. (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381: 238-241.
32. Lu M, Pressman C, Dyer R, Johnson R, Martin J (1999) Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401: 276-278.
33. Gage P, Suh H, Camper S (1999) Dosage requirement of Pitx2 for development of multiple organs. Development 126: 4643-4651.
34. Varjosalo M, Taipale J (2008) Hedgehog: functions and mechanisms. Genes Dev 22: 2454-2472.
35. Riddle R, Johnson R, Laufer E, Tabin C (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
36. Jiang J, Hui C (2008) Hedgehog signaling in development and cancer. Dev Cell 15: 801-812.
37. McGlinn E, Tabin C (2006) Mechanistic insight into how Shh patterns the vertebrate limb. Curr Opin Genet Dev 16: 426-432.
38. Zhu J, Nakamura E, Nguyen M, 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.
39. Zeller R, López-Ríos J, Zuniga A (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845-858.
40. te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans H, et al. (2002) Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298: 827-830.
41. Litingtung Y, Dahn R, Li Y, Fallon J, Chiang C (2002) Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418: 979-983.
42. Milenkovic L, Goodrich L, Higgins K, Scott M (1999) Mouse patched1 controls body size determination and limb patterning. Development 126: 4431-4440.
43. Butterfield N, Metzis V, McGlinn E, Bruce S, Wainwright B, et al. (2009) Patched 1 is a crucial determinant of asymmetry and digit number in the vertebrate limb. Development 136: 3515-3524.
44. Mao J, Barrow J, McMahon J, Vaughan J, McMahon A (2005) An ES cell system for rapid, spatial and temporal analysis of gene function in vitro and in vivo. Nucleic Acids Res 33: e155.
45. Pan Y, Wang C, Wang B (2009) Phosphorylation of Gli2 by protein kinase A is required for Gli2 processing and degradation and the Sonic Hedgehog-regulated mouse development. Dev Biol 326: 177-189.
46. Ovchinnikov DA, Selever J, Wang Y, Chen YT, Mishina Y, et al. (2006) BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev Biol 295: 103-115.
47. Lallemand Y, Nicola MA, Ramos C, Bach A, Cloment CS, et al. (2005) Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development 132: 3003-3014.
48. Bassett E, Williams T, Zacharias A, Gage P, Fuhrmann S, et al. (2010) AP- 2alpha knockout mice exhibit optic cup patterning defects and failure of optic stalk morphogenesis. Hum Mol Genet 19: 1791-1804.
49. Hill P, Gotz K, Ruther U (2009) A SHH-independent regulation of Gli3 is a significant determinant of anteroposterior patterning of the limb bud. Dev Biol 328: 506-516.
50. Hui CC, Joyner AL (1993) A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3: 241-246.
51. Kim P, Mo R, Hui Cc C (2001) Murine models of VACTERL syndrome: Role of sonic hedgehog signaling pathway. J Pediatr Surg 36: 381-384.
52. Panman L, Drenth T, Tewelscher P, Zuniga A, Zeller R (2005) Genetic interaction of Gli3 and Alx4 during limb development. Int J Dev Biol 49: 443-448.
53. Qu S, Niswender KD, Ji Q, van der Meer R, Keeney D, et al. (1997) Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development 124: 3999-4008.
54. Qu S, Tucker SC, Ehrlich JS, Levorse JM, Flaherty LA, et al. (1998) Mutations in mouse Aristaless-like4 cause Strong's luxoid polydactyly. Development 125: 2711-2721.
55. Takahashi M, Tamura K, Buscher D, Masuya H, Yonei-Tamura S, et al. (1998) The role of Alx-4 in the establishment of anteroposterior polarity during vertebrate limb development. Development 125: 4417-4425.
56. Kuijper S, Feitsma H, Sheth R, Korving J, Reijnen M, et al. (2005) Function and regulation of Alx4 in limb development: complex genetic interactions with Gli3 and Shh. Dev Biol 285: 533-544.
57. Masuya H, Sagai T, Moriwaki K, Shiroishi T (1997) Multigenic control of the localization of the zone of polarizing activity in limb morphogenesis in the mouse. Dev Biol 182: 42-51.
58. Kuijper S, Beverdam A, Kroon C, Brouwer A, Candille S, et al. (2005) Genetics of shoulder girdle formation: roles of Tbx15 and aristaless-like genes. Development 132: 1601-1610.
59. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, et al. (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
60. Ahn S, Joyner A (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118: 505-516.
61. Harfe B, Scherz P, Nissim S, Tian H, McMahon A, et al. (2004) Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118: 517-528.
62. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
63. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
64. Mao J, Ligon KL, Rakhlin EY, Thayer SP, Bronson RT, et al. (2006) A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res 66: 10171-10178.
65. 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.
66. Sasaki H, Hui C, Nakafuku M, Kondoh H (1997) A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124: 1313-1322.
67. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifeninducible form of Cre recombinase. Curr Biol 8: 1323-1326.
68. 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.
69. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, et al. (1996) Ligandactivated site-specific recombination in mice. Proc Natl Acad Sci U S A 93: 10887-10890.
70. Miyagawa S, Moon A, Haraguchi R, Inoue C, Harada M, et al. (2009) Dosagedependent hedgehog signals integrated with Wnt/beta-catenin signaling regulate external genitalia formation as an appendicular program. Development 136: 3969-3978.
71. Miyagawa S, Satoh Y, Haraguchi R, Suzuki K, Iguchi T, et al. (2009) Genetic interactions of the androgen and Wnt/beta-catenin pathways for the masculinization of external genitalia. Mol Endocrinol 23: 871-880.
72. Ahn S, Joyner A (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894-897.
73. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18: 937-951.
74. Haraguchi R, Mo R, Hui C, Motoyama J, Makino S, et al. (2001) Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128: 4241-4250.
75. Suzuki K, Yamaguchi Y, Villacorte M, Mihara K, Akiyama M, et al. (2009) Embryonic hair follicle fate change by augmented {beta}-catenin through Shh and Bmp signaling. Development 136: 367-372.
76. Pomikal C, Streicher J (2010) 4D-analysis of early pelvic girdle development in the mouse (Mus musculus). J Morphol 271: 116-126.
77. Indra A, Warot X, Brocard J, Bornert J, Xiao J, et al. (1999) Temporallycontrolled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 27: 4324-4327.
78. Chan KK, Wong CK, Lui VC, Tam PK, Sham MH (2003) Analysis of SOX10 mutations identified in Waardenburg-Hirschsprung patients: Differential effects on target gene regulation. J Cell Biochem 90: 573-585.
79. Chan K, Chen Y, Yau T, Fu M, Lui V, et al. (2005) Hoxb3 vagal neural crestspecific enhancer element for controlling enteric nervous system development. Dev Dyn 233: 473-483.
80. Habib H, Hatta T, Rahman O, Yoshimura Y, Otani H (2007) Fetal jaw movement affects development of articular disk in the temporomandibular joint. Congenit Anom (Kyoto) 47: 53-57.
81. Feldkamp M, Carey J, Sadler T (2007) Development of gastroschisis: review of hypotheses, a novel hypothesis, and implications for research. Am J Med Genet A 143: 639-652.
82. Williams T (2008) Animal models of ventral body wall closure defects: a personal perspective on gastroschisis. Am J Med Genet C Semin Med Genet 148C: 186-191.
83. Kolterud A, Grosse A, Zacharias W, Walton K, Kretovich K, et al. (2009) Paracrine Hedgehog signaling in stomach and intestine: new roles for hedgehog in gastrointestinal patterning. Gastroenterology 137: 618-628.
84. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, et al. (1999) Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J Biol Chem 274: 8143-8152.
85. Bai C, Auerbach W, Lee J, Stephen D, Joyner A (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129: 4753-4761.
86. Katz L, Schultz R, Semina E, Torfs C, Krahn K, et al. (2004) Mutations in PITX2 may contribute to cases of omphalocele and VATER-like syndromes. Am J Med Genet A 130A: 277-283.
87. Shih H, Gross M, Kioussi C (2007) Expression pattern of the homeodomain transcription factor Pitx2 during muscle development. Gene Expr Patterns 7: 441-451.
88. Kioussi C, Briata P, Baek S, Rose D, Hamblet N, et al. (2002) Identification of a Wnt/Dvl/beta-Catenin -. Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111: 673-685.
89. Hilton T, Gross M, Kioussi C (2010) Pitx2-dependent occupancy by histone deacetylases is associated with T-box gene regulation in mammalian abdominal tissue. J Biol Chem 285: 11129-11142.
90. Mingin G, Nguyen H, Mathias R, Shepherd J, Glidden D, et al. (2002) Growth and metabolic consequences of bladder augmentation in children with myelomeningocele and bladder exstrophy. Pediatrics 110: 1193-1198.
91. Ebert A, Reutter H, Ludwig M, Rösch W (2009) The exstrophy-epispadias complex. Orphanet J Rare Dis 4: 23.
92. Sponseller P, Bisson L, Gearhart J, Jeffs R, Magid D, et al. (1995) The anatomy of the pelvis in the exstrophy complex. J Bone Joint Surg Am 77: 177-189.
93. Kawamura DM (1997) Abdomen and superficial structures. Philadelphia: Lippincott, xv, 799.
94. Snell RS (1992) Clinical anatomy for medical students. Boston: Little, Brown, x, 1059.
95. Christ B, Jacob M, Jacob H (1983) On the origin and development of the ventrolateral abdominal muscles in the avian embryo. An experimental and ultrastructural study. Anat Embryol (Berl) 166: 87-101.
96. Malashichev Y, Christ B, Pröls F (2008) Avian pelvis originates from lateral plate mesoderm and its development requires signals from both ectoderm and paraxial mesoderm. Cell Tissue Res 331: 595-604.
97. Brugmann S, Allen N, James A, Mekonnen Z, Madan E, et al. (2010) A primary cilia-dependent etiology for midline facial disorders. Hum Mol Genet 19: 1577-1592.
98. Novick C, Grogan DP (2009) Polydactyly of the Foot. dMedicine: Medscape.