The Ptch1DL mouse: A new model to study lambdoid craniosynostosis and basal cell nevus syndrome-associated skeletal defects

Genesis

Volumn 51, Issue 10, 2013, Pages 677-689

  Feng, Weiguo ^a,c   Choi, Irene ^a   Clouthier, David E ^a   Niswander, Lee ^b   Williams, Trevor ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c STANFORD CANCER INSTITUTE   (United States)

Author keywords

Craniofacial defects; Craniosynostosis; Hedgehog; Omphalocele; Polydactyly

Indexed keywords

ETHYLNITROSOUREA; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL CELL NEVUS SYNDROME; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL SYNOSTOSIS; DISEASE ASSOCIATION; EMBRYO; EXENCEPHALY; GENE MAPPING; GENETIC COMPLEMENTATION; GENOTYPE; HYPOPLASIA; LIMB DEVELOPMENT; MALE; MOUSE; MOUSE MODEL; MOUSE STRAIN; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PTCH1 MOUSE; SCAPULA; SECONDARY PALATE; SIGNAL TRANSDUCTION; SKULL BASE; SKULL SUTURE; THORAX;

ERINACEIDAE; MUS;

CRANIOFACIAL DEFECTS; CRANIOSYNOSTOSIS; HEDGEHOG; OMPHALOCELE; POLYDACTYLY;

ANIMALS; BASAL CELL NEVUS SYNDROME; BONE AND BONES; CRANIOSYNOSTOSES; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; HEDGEHOG PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POINT MUTATION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SKULL;

EID: 84886293015     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22416     Document Type: Article

References (61)

1. Abzhanov A, Rodda SJ, McMahon AP, Tabin CJ. 2007. Regulation of skeletogenic differentiation in cranial dermal bone. Development 134:3133-3144.
2. Babbs C, Furniss D, Morriss-Kay GM, Wilkie AO. 2008. Polydactyly in the mouse mutant Doublefoot involves altered Gli3 processing and is caused by a large deletion in cis to Indian hedgehog. Mech Dev 125:517-526.
3. Balczerski B, Zakaria S, Tucker AS, Borycki AG, Koyama E, Pacifici M, Francis-West P. 2012. Distinct spatiotemporal roles of hedgehog signalling during chick and mouse cranial base and axial skeleton development. Dev Biol 371:203-214.
4. Barnes EA, Kong M, Ollendorff V, Donoghue DJ. 2001. Patched1 interacts with cyclin B1 to regulate cell cycle progression. EMBO J 20:2214-2223.
5. Brewer S, Feng W, Huang J, Sullivan S, Williams T. 2004. Wnt1-Cre-mediated deletion of AP-2alpha causes multiple neural crest-related defects. Dev Biol 267:135-152.
6. Bruce SJ, Butterfield NC, Metzis V, Town L, McGlinn E, Wicking C. 2010. Inactivation of Patched1 in the mouse limb has novel inhibitory effects on the chondrogenic program. J Biol Chem 285:27967-27981.
7. Butterfield NC, Metzis V, Mcglinn E, Bruce SJ, Wainwright BJ, Wicking C. 2009. Patched 1 is a crucial determinant of asymmetry and digit number in the vertebrate limb. Development 136:3515-3524.
8. Caparros-Martin JA, Valencia M, Reytor E, Pacheco M, Fernandez M, Perez-Aytes A, Gean E, Lapunzina P, Peters H, Goodship JA, Ruiz-Perez VL. 2013. The ciliary Evc/Evc2 complex interacts with Smo and controls Hedgehog pathway activity in chondrocytes by regulating Sufu/Gli3 dissociation and Gli3 trafficking in primary cilia. Hum Mol Genet 22:124-139.
9. Caspary T, Anderson KV. 2006. Uncovering the uncharacterized and unexpected: Unbiased phenotype-driven screens in the mouse. Dev Dyn 235:2412-2423.
10. Christopher KJ, Wang B, Kong Y, Weatherbee SD. 2012. Forward genetics uncovers transmembrane protein 107 as a novel factor required for ciliogenesis and Sonic hedgehog signaling. Dev Biol 368:382-392.
11. Cobourne MT, Xavier GM, Depew M, Hagan L, Sealby J, Webster Z, Sharpe PT. 2009. Sonic hedgehog signalling inhibits palatogenesis and arrests tooth development in a mouse model of the nevoid basal cell carcinoma syndrome. Dev Biol 331:38-49.
12. Cui C, Chatterjee B, Francis D, Yu Q, SanAgustin JT, Francis R, Tansey T, Henry C, Wang B, Lemley B, Pazour GJ, Lo CW. 2011. Disruption of Mks1 localization to the mother centriole causes cilia defects and developmental malformations in Meckel-Gruber syndrome. Dis Model Mech 4:43-56.
13. Dudas M, Kim J, Li W-Y, Nagy A, Larsson J, Karlsson S, Chai Y, Kaartinen V. 2006. Epithelial and ectomesenchymal role of the type I TGF-beta receptor ALK5 during facial morphogenesis and palatal fusion. Dev Biol 296:298-314.
14. Ellis T, Smyth I, Riley E, Graham S, Elliot K, Narang M, Kay GF, Wicking C, Wainwright B. 2003. Patched 1 conditional null allele in mice. Genesis 36:158-161.
15. Evans GD, Farndon PA. 2010. Nevoid basal cell carcinoma syndrome. 2002 Jun 20 [Updated 2013 Mar 7]. In: Pagon RA, Adam MP, Bird TD, editors. GeneReviews™ [Internet]. Seattle (WA): University of Washington, Seattle 1993-2013. Available from: http://www.ncbi.nlm.nih.gov/books/NBK1151/.
16. Feng W, Williams T. 2003. Cloning and characterization of the mouse AP-2 epsilon gene: A novel family member expressed in the developing olfactory bulb. Mol Cell Neurosci 24:460-475.
17. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109-1113.
18. Gritli-Linde A. 2008. The etiopathogenesis of cleft lip and cleft palate: Usefulness and caveats of mouse models. Curr Top Dev Biol 84:37-138.
19. Hahn H, Wojnowski L, Zimmer AM, Hall J, Miller G, Zimmer A. 1998. Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nat Med 4:619-622.
20. Hayes C, Lyon MF, Morriss-Kay GM. 1998. Morphogenesis of Doublefoot (Dbf), a mouse mutant with polydactyly and craniofacial defects. J Anat 193 (Part 1):81-91.
21. Holmes G. 2012. The role of vertebrate models in understanding craniosynostosis. Childs Nerv Syst 28:1471-1481.
22. Hurst JA, Jenkins D, Vasudevan PC, Kirchhoff M, Skovby F, Rieubland C, Gallati S, Rittinger O, Kroisel PM, Johnson D, Biesecker LG, Wilkie AO. 2011. Metopic and sagittal synostosis in Greig cephalopolysyndactyly syndrome: Five cases with intragenic mutations or complete deletions of GLI3. Eur J Hum Genet 19:757-762.
23. Iwanaga S, Shimoura H, Shimizu M, Numaguchi Y. 1998. Gorlin syndrome: Unusual manifestations in the sella turcica and the sphenoidal sinus. AJNR Am J Neuroradiol 19:956-958.
24. Jax. 2011. Protocol for genotyping. Available at: http://jaxmice.jax.org/protocolsdb/f?p=116:2:1406893156903556::NO:2:P2_MASTER_PROTOCOL_ID, P2_JRS_CODE:1687, 003081. Last accessed 12th August 2013.
25. Jenkins D, Seelow D, Jehee FS, Perlyn CA, Alonso LG, Bueno DF, Donnai D, Josifova D, Mathijssen IM, Morton JE, Orstavik KH, Sweeney E, Wall SA, Marsh JL, Nurnberg P, Passos-Bueno MR, Wilkie AO. 2007. RAB23 mutations in Carpenter syndrome imply an unexpected role for hedgehog signaling in cranial-suture development and obesity. Am J Hum Genet 80:1162-1170.
26. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. 2002. Tissue origins and interactions in the mammalian skull vault. Dev Biol 241:106-116.
27. Johnson DR. 1967. Extra-toes: A new mutant gene causing multiple abnormalities in the mouse. J Embryol Exp Morphol 17:543-581.
28. Kimonis VE, Goldstein AM, Pastakia B, Yang ML, Kase R, DiGiovanna JJ, Bale AE, Bale SJ. 1997. Clinical manifestations in 105 persons with nevoid basal cell carcinoma syndrome. Am J Med Genet 69:299-308.
29. Kimonis VE, Singh KE, Zhong R, Pastakia B, Digiovanna JJ, Bale SJ. 2013. Clinical and radiological features in young individuals with nevoid basal cell carcinoma syndrome. Genet Med 15:79-83.
30. Klopocki E, Lohan S, Brancati F, Koll R, Brehm A, Seemann P, Dathe K, Stricker S, Hecht J, Bosse K, Betz RC, Garaci FG, Dallapiccola B, Jain M, Muenke M, Ng VC, Chan W, Chan D, Mundlos S. 2011. Copy-number variations involving the IHH locus are associated with syndactyly and craniosynostosis. Am J Hum Genet 88:70-75.
31. Kuijper S, Beverdam A, Kroon C, Brouwer A, Candille S, Barsh G, Meijlink F. 2005. Genetics of shoulder girdle formation: Roles of Tbx15 and aristaless-like genes. Development 132:1601-1610.
32. Lenton K, James AW, Manu A, Brugmann SA, Birker D, Nelson ER, Leucht P, Helms JA, Longaker MT. 2011. Indian hedgehog positively regulates calvarial ossification and modulates bone morphogenetic protein signaling. Genesis 49:784-796.
33. Leonardi R, Caltabiano M, Lo Muzio L, Gorlin RJ, Bucci P, Pannone G, Canfora M, Sorge G. 2002. Bilateral hyperplasia of the mandibular coronoid processes in patients with nevoid basal cell carcinoma syndrome: An undescribed sign. Am J Med Genet 110:400-403.
34. Lindstrom E, Shimokawa T, Toftgard R, Zaphiropoulos PG. 2006. PTCH mutations: Distribution and analyses. Hum Mutat 27:215-219.
35. Lo Muzio L. 2008. Nevoid basal cell carcinoma syndrome (Gorlin syndrome). Orphanet J Rare Dis 3:32.
36. Mai S, Wei K, Flenniken A, Adamson SL, Rossant J, Aubin JE, Gong SG. 2010. The missense mutation W290R in Fgfr2 causes developmental defects from aberrant IIIb and IIIc signaling. Dev Dyn 239:1888-1900.
37. Mak KK, Bi Y, Wan C, Chuang PT, Clemens T, Young M, Yang Y. 2008. Hedgehog signaling in mature osteoblasts regulates bone formation and resorption by controlling PTHrP and RANKL expression. Dev Cell 14:674-688.
38. Mak KK, Chen MH, Day TF, Chuang PT, Yang Y. 2006. Wnt/beta-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 133:3695-3707.
39. Makino S, Masuya H, Ishijima J, Yada Y, Shiroishi T. 2001. A spontaneous mouse mutation, mesenchymal dysplasia (mes), is caused by a deletion of the most C-terminal cytoplasmic domain of patched (ptc). Dev Biol 239:95-106.
40. Matsumaru D, Haraguchi R, Miyagawa S, Motoyama J, Nakagata N, Meijlink F, Yamada G. 2011. Genetic analysis of Hedgehog signaling in ventral body wall development and the onset of omphalocele formation. PloS One 6:e16260.
41. McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM. 2008. Development and tissue origins of the mammalian cranial base. Dev Biol 322:121-132.
42. Meester-Smoor MA, Vermeij M, van Helmond MJL, Molijn AC, van Wely KHM, Hekman ACP, Vermey-Keers C, Riegman PHJ, Zwarthoff EC. 2005. Targeted disruption of the Mn1 oncogene results in severe defects in development of membranous bones of the cranial skeleton. Mol Cell Biol 25:4229-4236.
43. Milenkovic L, Goodrich LV, Higgins KM, Scott MP. 1999. Mouse patched1 controls body size determination and limb patterning. Development 126:4431-4440.
44. Nagayama M, Iwamoto M, Hargett A, Kamiya N, Tamamura Y, Young B, Morrison T, Takeuchi H, Pacifici M, Enomoto-Iwamoto M, Koyama E. 2008. Wnt/beta-catenin signaling regulates cranial base development and growth. J Dent Res 87:244-249.
45. Ngan ES, Garcia-Barcelo MM, Yip BH, Poon HC, Lau ST, Kwok CK, Sat E, Sham MH, Wong KK, Wainwright BJ, Cherny SS, Hui CC, Sham PC, Lui VC, Tam PK. 2011. Hedgehog/Notch-induced premature gliogenesis represents a new disease mechanism for Hirschsprung disease in mice and humans. J Clin Invest 121:3467-3478.
46. Ohba S, Kawaguchi H, Kugimiya F, Ogasawara T, Kawamura N, Saito T, Ikeda T, Fujii K, Miyajima T, Kuramochi A, Miyashita T, Oda H, Nakamura K, Takato T, Chung U-i. 2008. Patched1 haploinsufficiency increases adult bone mass and modulates Gli3 repressor activity. Dev Cell 14:689-699.
47. Pacheco M, Valencia M, Caparros-Martin JA, Mulero F, Goodship JA, Ruiz-Perez VL. 2012. Evc works in chondrocytes and osteoblasts to regulate multiple aspects of growth plate development in the appendicular skeleton and cranial base. Bone 50:28-41.
48. Quijada L, Callejo A, Torroja C, Guerrero I. 2006. The patched receptor: Switching on/off the Hedgehog signaling pathway. In: Madame Curie Bioscience Database [Internet]. Austin (TX): Landes Bioscience; 2000. Available from: http://www.ncbi.nlm.nih.gov/books/NBK6164/.
49. Reid BS, Yang H, Melvin VS, Taketo MM, Williams T. 2011. Ectodermal Wnt/beta-catenin signaling shapes the mouse face. Dev Biol 349:261-269.
50. Rice DP, Connor EC, Veltmaat JM, Lana-Elola E, Veistinen L, Tanimoto Y, Bellusci S, Rice R. 2010. Gli3Xt-J/Xt-J mice exhibit lambdoid suture craniosynostosis which results from altered osteoprogenitor proliferation and differentiation. Hum Mol Genet 19:3457-3467.
51. Robbins DJ, Fei DL, Riobo NA. 2012. The Hedgehog signal transduction network. Sci Signal 5:re6.
52. Roberts RB, Hu Y, Albertson RC, Kocher TD. 2011. Craniofacial divergence and ongoing adaptation via the hedgehog pathway. Proc Natl Acad Sci USA 108:13194-13199.
53. St-Jacques B, Hammerschmidt M, McMahon AP. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:2072-2086.
54. Sweet HO, Bronson RT, Donahue LR, Davisson MT. 1996. Mesenchymal dysplasia: A recessive mutation on chromosome 13 of the mouse. J Hered 87:87-95.
55. Wakabayashi Y, Mao JH, Brown K, Girardi M, Balmain A. 2007. Promotion of Hras-induced squamous carcinomas by a polymorphic variant of the Patched gene in FVB mice. Nature 445:761-765.
56. Weatherbee SD, Niswander LA, Anderson KV. 2009. A mouse model for Meckel syndrome reveals Mks1 is required for ciliogenesis and Hedgehog signaling. Hum Mol Genet 18:4565-4575.
57. Wicking C, Shanley S, Smyth I, Gillies S, Negus K, Graham S, Suthers G, Haites N, Edwards M, Wainwright B, Chenevix-Trench G. 1997. Most germ-line mutations in the nevoid basal cell carcinoma syndrome lead to a premature termination of the PATCHED protein, and no genotype-phenotype correlations are evident. Am J Hum Genet 60:21-26.
58. Winnier GE, Hargett L, Hogan BL. 1997. The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev 11:926-940.
59. Yang Y, Guillot P, Boyd Y, Lyon MF, McMahon AP. 1998. Evidence that preaxial polydactyly in the Doublefoot mutant is due to ectopic Indian Hedgehog signaling. Development 125:3123-3132.
60. Young B, Minugh-Purvis N, Shimo T, St-Jacques B, Iwamoto M, Enomoto-Iwamoto M, Koyama E, Pacifici M. 2006. Indian and sonic hedgehogs regulate synchondrosis growth plate and cranial base development and function. Dev Biol 299:272-282.
61. Yuksel-Apak M, Bogershausen N, Pawlik B, Li Y, Apak S, Uyguner O, Milz E, Nurnberg G, Karaman B, Gulgoren A, Grzeschik KH, Nurnberg P, Kayserili H, Wollnik B. 2012. A large duplication involving the IHH locus mimics acrocallosal syndrome. Eur J Hum Genet 20:639-644.