Loss of cilia causes embryonic lung hypoplasia, liver fibrosis, and cholestasis in the talpid³ ciliopathy mutant

References

• Fliegauf M, Benzing T, Omran H. When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 2007; 8:880 - 93; http://dx.doi.org/10.1038/nrm2278; PMID: 17955020
   PubMed Web of Science ®Google Scholar
• Hildebrandt F, Benzing T, Katsanis N. Ciliopathies. N Engl J Med 2011; 364:1533 - 43; http://dx.doi.org/10.1056/NEJMra1010172; PMID: 21506742
   PubMed Web of Science ®Google Scholar
• Goetz SC, Anderson KV. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 2010; 11:331 - 44; http://dx.doi.org/10.1038/nrg2774; PMID: 20395968
   PubMed Web of Science ®Google Scholar
• Ho NC, Francomano CA, van Allen M. Jeune asphyxiating thoracic dystrophy and short-rib polydactyly type III (Verma-Naumoff) are variants of the same disorder. Am J Med Genet 2000; 90:310 - 4; http://dx.doi.org/10.1002/(SICI)1096-8628(20000214)90:4<310::AID-AJMG9>3.0.CO;2-N; PMID: 10710229
   PubMed Web of Science ®Google Scholar
• Rix S, Calmont A, Scambler PJ, Beales PL. An Ift80 mouse model of short rib polydactyly syndromes shows defects in hedgehog signalling without loss or malformation of cilia. Hum Mol Genet 2011; 20:1306 - 14; http://dx.doi.org/10.1093/hmg/ddr013; PMID: 21227999
   PubMed Web of Science ®Google Scholar
• Dagoneau N, Goulet M, Geneviève D, Sznajer Y, Martinovic J, Smithson S, Huber C, Baujat G, Flori E, Tecco L, et al. DYNC2H1 mutations cause asphyxiating thoracic dystrophy and short rib-polydactyly syndrome, type III. Am J Hum Genet 2009; 84:706 - 11; http://dx.doi.org/10.1016/j.ajhg.2009.04.016; PMID: 19442771
   PubMed Web of Science ®Google Scholar
• Beales PL, Bland E, Tobin JL, Bacchelli C, Tuysuz B, Hill J, Rix S, Pearson CG, Kai M, Hartley J, et al. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat Genet 2007; 39:727 - 9; http://dx.doi.org/10.1038/ng2038; PMID: 17468754
   PubMed Web of Science ®Google Scholar
• Bredrup C, Saunier S, Oud MM, Fiskerstrand T, Hoischen A, Brackman D, Leh SM, Midtbø M, Filhol E, Bole-Feysot C, et al. Ciliopathies with skeletal anomalies and renal insufficiency due to mutations in the IFT-A gene WDR19. Am J Hum Genet 2011; 89:634 - 43; http://dx.doi.org/10.1016/j.ajhg.2011.10.001; PMID: 22019273
   PubMed Web of Science ®Google Scholar
• Shokeir MH, Houston CS, Awen CF. Asphyxiating thoracic chondrodystrophy. Association with renal disease and evidence for possile heterozygous expression. [Internet] J Med Genet 1971; 8:107 - 12; http://dx.doi.org/10.1136/jmg.8.1.107; PMID: 5098065
   PubMed Web of Science ®Google Scholar
• Whitley CB, Schwarzenberg SJ, Burke BA, Freese DK, Gorlin RJ. Direct hyperbilirubinemia and hepatic fibrosis: a new presentation of Jeune syndrome (asphyxiating thoracic dystrophy). Am J Med Genet Suppl 1987; 3:211 - 20; http://dx.doi.org/10.1002/ajmg.1320280525; PMID: 3130856
   PubMedGoogle Scholar
• Yerian LM, Brady L, Hart J. Hepatic manifestations of Jeune syndrome (asphyxiating thoracic dystrophy). Semin Liver Dis 2003; 23:195 - 200; http://dx.doi.org/10.1055/s-2003-39950; PMID: 12800072
   PubMed Web of Science ®Google Scholar
• Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 1998; 8:1083 - 6; http://dx.doi.org/10.1016/S0960-9822(98)70446-4; PMID: 9768363
   PubMed Web of Science ®Google Scholar
• Miller L-AD, Wert SE, Clark JC, Xu Y, Perl A-KT, Whitsett JA. Role of Sonic hedgehog in patterning of tracheal-bronchial cartilage and the peripheral lung. Dev Dyn 2004; 231:57 - 71; http://dx.doi.org/10.1002/dvdy.20105; PMID: 15305287
   PubMed Web of Science ®Google Scholar
• Loscertales M, Mikels AJ, Hu JK-H, Donahoe PK, Roberts DJ. Chick pulmonary Wnt5a directs airway and vascular tubulogenesis. Development 2008; 135:1365 - 76; http://dx.doi.org/10.1242/dev.010504; PMID: 18305003
   PubMed Web of Science ®Google Scholar
• Ashe A, Butterfield NC, Town L, Courtney AD, Cooper AN, Ferguson C, Barry R, Olsson F, Liem KF Jr., Parton RG, et al. Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies. Hum Mol Genet 2012; 21:1808 - 23; http://dx.doi.org/10.1093/hmg/ddr613; PMID: 22228095
   PubMed Web of Science ®Google Scholar
• Deutsch G, Jung J, Zheng M, Lóra J, Zaret KS. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001; 128:871 - 81; PMID: 11222142
   PubMed Web of Science ®Google Scholar
• Hirose Y, Itoh T, Miyajima A. Hedgehog signal activation coordinates proliferation and differentiation of fetal liver progenitor cells. Exp Cell Res 2009; 315:2648 - 57; http://dx.doi.org/10.1016/j.yexcr.2009.06.018; PMID: 19559697
   PubMed Web of Science ®Google Scholar
• Sicklick JK, Li Y-X, Melhem A, Schmelzer E, Zdanowicz M, Huang J, Caballero M, Fair JH, Ludlow JW, McClelland RE, et al. Hedgehog signaling maintains resident hepatic progenitors throughout life. Am J Physiol Gastrointest Liver Physiol 2006; 290:G859 - 70; http://dx.doi.org/10.1152/ajpgi.00456.2005; PMID: 16322088
   PubMed Web of Science ®Google Scholar
• Ochoa B, Syn W-K, Delgado I, Karaca GF, Jung Y, Wang J, Zubiaga AM, Fresnedo O, Omenetti A, Zdanowicz M, et al. Hedgehog signaling is critical for normal liver regeneration after partial hepatectomy in mice. Hepatology 2010; 51:1712 - 23; http://dx.doi.org/10.1002/hep.23525; PMID: 20432255
   PubMed Web of Science ®Google Scholar
• Grzelak CA, Martelotto LG, Sigglekow ND, Patkunanathan B, Ajami K, Calabro SR, Dwyer BJ, Tirnitz-Parker JEE, Neil Watkins D, Warner FJ, et al. The Intrahepatic Signalling Niche of Hedgehog is Defined by Primary Cilia Positive Cells During Chronic Liver Injury. J Hepatol 2014; 60:143 - 51; PMID: 23978713
   PubMed Web of Science ®Google Scholar
• Philips GM, Chan IS, Swiderska M, Schroder VT, Guy C, Karaca GF, Moylan C, Venkatraman T, Feuerlein S, Syn W-K, et al. Hedgehog signaling antagonist promotes regression of both liver fibrosis and hepatocellular carcinoma in a murine model of primary liver cancer. PLoS One 2011; 6:e23943; http://dx.doi.org/10.1371/journal.pone.0023943; PMID: 21912653
   PubMed Web of Science ®Google Scholar
• Omenetti A, Diehl AM. The adventures of sonic hedgehog in development and repair. II. Sonic hedgehog and liver development, inflammation, and cancer. Am J Physiol Gastrointest Liver Physiol 2008; 294:G595 - 8; http://dx.doi.org/10.1152/ajpgi.00543.2007; PMID: 18218671
   PubMedGoogle Scholar
• Omenetti A, Diehl AM. Hedgehog signaling in cholangiocytes. Curr Opin Gastroenterol 2011; 27:268 - 75; http://dx.doi.org/10.1097/MOG.0b013e32834550b4; PMID: 21423008
   PubMed Web of Science ®Google Scholar
• Syn W-K, Jung Y, Omenetti A, Abdelmalek M, Guy CD, Yang L, Wang J, Witek RP, Fearing CM, Pereira TA, et al. Hedgehog-mediated epithelial-to-mesenchymal transition and fibrogenic repair in nonalcoholic fatty liver disease. Gastroenterology 2009; 137:1478 - , e8; http://dx.doi.org/10.1053/j.gastro.2009.06.051; PMID: 19577569
   PubMed Web of Science ®Google Scholar
• Masyuk AI, Masyuk TV, Splinter PL, Huang BQ, Stroope AJ, LaRusso NF. Cholangiocyte cilia detect changes in luminal fluid flow and transmit them into intracellular Ca2+ and cAMP signaling. Gastroenterology 2006; 131:911 - 20; http://dx.doi.org/10.1053/j.gastro.2006.07.003; PMID: 16952559
   PubMed Web of Science ®Google Scholar
• Bergmann C, Weiskirchen R. It’s not all in the cilium, but on the road to it: genetic interaction network in polycystic kidney and liver diseases and how trafficking and quality control matter. J Hepatol 2012; 56:1201 - 3; http://dx.doi.org/10.1016/j.jhep.2011.10.014; PMID: 22133568
   PubMed Web of Science ®Google Scholar
• Davey MG, Paton IR, Yin Y, Schmidt M, Bangs FK, Morrice DR, Smith TG, Buxton P, Stamataki D, Tanaka M, et al. The chicken talpid3 gene encodes a novel protein essential for Hedgehog signaling. Genes Dev 2006; 20:1365 - 77; http://dx.doi.org/10.1101/gad.369106; PMID: 16702409
   PubMed Web of Science ®Google Scholar
• Yin Y, Bangs F, Paton IR, Prescott A, James J, Davey MG, Whitley P, Genikhovich G, Technau U, Burt DW, et al. The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation. Development 2009; 136:655 - 64; http://dx.doi.org/10.1242/dev.028464; PMID: 19144723
   PubMed Web of Science ®Google Scholar
• Macrae VE, Davey MG, McTeir L, Narisawa S, Yadav MC, Millan JL, Farquharson C. Inhibition of PHOSPHO1 activity results in impaired skeletal mineralization during limb development of the chick. Bone 2010; 46:1146 - 55; http://dx.doi.org/10.1016/j.bone.2009.12.018; PMID: 20053388
   PubMed Web of Science ®Google Scholar
• Cruz C, Ribes V, Kutejova E, Cayuso J, Lawson V, Norris D, Stevens J, Davey M, Blight K, Bangs F, et al. Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 2010; 137:4271 - 82; http://dx.doi.org/10.1242/dev.051714; PMID: 21098568
   PubMed Web of Science ®Google Scholar
• Bangs F, Antonio N, Thongnuek P, Welten M, Davey MG, Briscoe J, Tickle C. Generation of mice with functional inactivation of talpid3, a gene first identified in chicken. Development 2011; 138:3261 - 72; http://dx.doi.org/10.1242/dev.063602; PMID: 21750036
   PubMed Web of Science ®Google Scholar
• Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 2003; 426:570 - 4; http://dx.doi.org/10.1038/nature02166; PMID: 14654843
   PubMed Web of Science ®Google Scholar
• Stephen LA, Davis GM, McTeir KE, James J, McTeir L, Kierans M, Bain A, Davey MG. Failure of centrosome migration causes a loss of motile cilia in talpid(3) mutants. Dev Dyn 2013; 242:923 - 31; http://dx.doi.org/10.1002/dvdy.23980; PMID: 23613203
   PubMed Web of Science ®Google Scholar
• Maina JN, Madan AK, Alison B. Expression of fibroblast growth factor-2 (FGF-2) in early stages (days 3-11) of the development of the avian lung, Gallus gallus variant domesticus: an immunocytochemical study. J Anat 2003; 203:505 - 12; http://dx.doi.org/10.1046/j.1469-7580.2003.00236.x; PMID: 14635803
   PubMed Web of Science ®Google Scholar
• Vähätalo R, Asikainen TM, Karikoski R, Kinnula VL, White CW, Andersson S, Heikinheimo M, Myllärniemi M. Expression of Transcription Factor GATA-6 in Alveolar Epithelial Cells Is Linked to Neonatal Lung Disease. Neonatology 2011; 99:231 - 40; http://dx.doi.org/10.1159/000317827; PMID: 21071980
   PubMed Web of Science ®Google Scholar
• Clotman F, Libbrecht L, Killingsworth MC, Loo CCK, Roskams T, Lemaigre FP. Lack of cilia and differentiation defects in the liver of human foetuses with the Meckel syndrome. Liver Int 2008; 28:377 - 84; http://dx.doi.org/10.1111/j.1478-3231.2007.01617.x; PMID: 17976156
   PubMed Web of Science ®Google Scholar
• Gleghorn JP, Kwak J, Pavlovich AL, Nelson CM. Inhibitory morphogens and monopodial branching of the embryonic chicken lung. Dev Dyn 2012; 241:852 - 62; http://dx.doi.org/10.1002/dvdy.23771; PMID: 22410853
   PubMed Web of Science ®Google Scholar
• Sakiyama J, Yokouchi Y, Kuroiwa A. Coordinated expression of Hoxb genes and signaling molecules during development of the chick respiratory tract. [Available from] Dev Biol 2000; 227:12 - 27; http://dx.doi.org/10.1006/dbio.2000.9880; PMID: 11076673
   PubMed Web of Science ®Google Scholar
• Cardoso WV, Lü J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 2006; 133:1611 - 24; http://dx.doi.org/10.1242/dev.02310; PMID: 16613830
   PubMed Web of Science ®Google Scholar
• Maeda Y, Davé V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev 2007; 87:219 - 44; http://dx.doi.org/10.1152/physrev.00028.2006; PMID: 17237346
   PubMed Web of Science ®Google Scholar
• Davey MG, Tickle C. The chicken as a model for embryonic development. Cytogenet Genome Res 2007; 117:231 - 9; http://dx.doi.org/10.1159/000103184; PMID: 17675864
   PubMed Web of Science ®Google Scholar
• Miller LA, Wert SE, Whitsett JA. Immunolocalization of sonic hedgehog (Shh) in developing mouse lung. J Histochem Cytochem 2001; 49:1593 - 604; http://dx.doi.org/10.1177/002215540104901213; PMID: 11724907
   PubMed Web of Science ®Google Scholar
• Weaver M, Batts L, Hogan BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 2003; 258:169 - 84; http://dx.doi.org/10.1016/S0012-1606(03)00117-9; PMID: 12781691
   PubMed Web of Science ®Google Scholar
• Zhang M, Wang H, Teng H, Shi J, Zhang Y. Expression of SHH signaling pathway components in the developing human lung. Histochem Cell Biol 2010; 134:327 - 35; http://dx.doi.org/10.1007/s00418-010-0738-2; PMID: 20821230
   PubMed Web of Science ®Google Scholar
• Litingtung Y, Lei L, Westphal H, Chiang C. Sonic hedgehog is essential to foregut development. Nat Genet 1998; 20:58 - 61; http://dx.doi.org/10.1038/1717; PMID: 9731532
   PubMed Web of Science ®Google Scholar
• Motoyama J, Liu J, Mo R, Ding Q, Post M, Hui CC. Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat Genet 1998; 20:54 - 7; http://dx.doi.org/10.1038/1711; PMID: 9731531
   PubMed Web of Science ®Google Scholar
• Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 1995; 121:3163 - 74; PMID: 7588051
   PubMed Web of Science ®Google Scholar
• Li C, Hu L, Xiao J, Chen H, Li JT, Bellusci S, Delanghe S, Minoo P. Wnt5a regulates Shh and Fgf10 signaling during lung development. Dev Biol 2005; 287:86 - 97; http://dx.doi.org/10.1016/j.ydbio.2005.08.035; PMID: 16169547
   PubMed Web of Science ®Google Scholar
• Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998; 12:3156 - 61; http://dx.doi.org/10.1101/gad.12.20.3156; PMID: 9784490
   PubMed Web of Science ®Google Scholar
• Lewis KE, Drossopoulou G, Paton IR, Morrice DR, Robertson KE, Burt DW, Ingham PW, Tickle C. Expression of ptc and gli genes in talpid3 suggests bifurcation in Shh pathway. Development 1999; 126:2397 - 407; PMID: 10225999
   PubMed Web of Science ®Google Scholar
• Buxton P, Davey MG, Paton IR, Morrice DR, Francis-West PH, Burt DW, Tickle C. Craniofacial development in the talpid3 chicken mutant. Differentiation 2004; 72:348 - 62; http://dx.doi.org/10.1111/j.1432-0436.2004.07207006.x; PMID: 15554946
   PubMed Web of Science ®Google Scholar
• Mill P, Lockhart PJ, Fitzpatrick E, Mountford HS, Hall EA, Reijns MA, Keighren M, Bahlo M, Bromhead CJ, Budd P, et al. Human and mouse mutations in WDR35 cause short-rib polydactyly syndromes due to abnormal ciliogenesis. Am J Hum Genet 2011; 88:508 - 15; http://dx.doi.org/10.1016/j.ajhg.2011.03.015; PMID: 21473986
   PubMed Web of Science ®Google Scholar
• Kajantie E, Andersson S, Kaitila I. Familial asphyxiating thoracic dysplasia: clinical variability and impact of improved neonatal intensive care. J Pediatr 2001; 139:130 - 3; http://dx.doi.org/10.1067/mpd.2001.114701; PMID: 11445806
   PubMed Web of Science ®Google Scholar
• Gunay-Aygun M. Liver and kidney disease in ciliopathies. Am J Med Genet C Semin Med Genet 2009; 151C:296 - 306; http://dx.doi.org/10.1002/ajmg.c.30225; PMID: 19876928
   PubMed Web of Science ®Google Scholar
• de Vries J, Yntema JL, van Die CE, Crama N, Cornelissen EA, Hamel BC. Jeune syndrome: description of 13 cases and a proposal for follow-up protocol. Eur J Pediatr 2010; 169:77 - 88; http://dx.doi.org/10.1007/s00431-009-0991-3; PMID: 19430947
   PubMed Web of Science ®Google Scholar
• Oberklaid F, Danks DM, Mayne V, Campbell P. Asphyxiating thoracic dysplasia. Clinical, radiological, and pathological information on 10 patients. Arch Dis Child 1977; 52:758 - 65; http://dx.doi.org/10.1136/adc.52.10.758; PMID: 931421
   PubMed Web of Science ®Google Scholar
• Waters AM, Beales P. Bardet–Biedl and Jeune Syndromes. Fibrocystic Diseases of the Liver. 2010: 257-285.
   Google Scholar
• Doherty D. Joubert syndrome: insights into brain development, cilium biology, and complex disease. Semin Pediatr Neurol 2009; 16:143 - 54; http://dx.doi.org/10.1016/j.spen.2009.06.002; PMID: 19778711
   PubMed Web of Science ®Google Scholar
• Sokol RJ, Mack CL. Biliary atresia and the ductal plate. In: Gastroenterology: Fibrocystic Diseases of the Liver, Murray KF and Larson AM (eds.). Humana Press: 2010, 179-200
   Google Scholar
• Norris DP. Cilia, calcium and the basis of left-right asymmetry. BMC Biol 2012; 10:102; http://dx.doi.org/10.1186/1741-7007-10-102; PMID: 23256866
   PubMed Web of Science ®Google Scholar
• Omenetti A, Bass LM, Anders RA, Clemente MG, Francis H, Guy CD, McCall S, Choi SS, Alpini G, Schwarz KB, et al. Hedgehog activity, epithelial-mesenchymal transitions, and biliary dysmorphogenesis in biliary atresia. Hepatology 2011; 53:1246 - 58; http://dx.doi.org/10.1002/hep.24156; PMID: 21480329
   PubMed Web of Science ®Google Scholar
• Shimadera S, Iwai N, Deguchi E, Kimura O, Fumino S, Yokoyama T. The inv mouse as an experimental model of biliary atresia. J Pediatr Surg 2007; 42:1555 - 60; http://dx.doi.org/10.1016/j.jpedsurg.2007.04.018; PMID: 17848248
   PubMed Web of Science ®Google Scholar
• Cui S, Leyva-Vega M, Tsai EA, EauClaire SF, Glessner JT, Hakonarson H, Devoto M, Haber BA, Spinner NB, Matthews RP. Evidence from human and zebrafish that GPC1 is a biliary atresia susceptibility gene. Gastroenterology 2013; 144:1107 - , e3; http://dx.doi.org/10.1053/j.gastro.2013.01.022; PMID: 23336978
   PubMed Web of Science ®Google Scholar
• Huang BQ, Masyuk TV, Muff MA, Tietz PS, Masyuk AI, Larusso NF. Isolation and characterization of cholangiocyte primary cilia. Am J Physiol Gastrointest Liver Physiol 2006; 291:G500 - 9; http://dx.doi.org/10.1152/ajpgi.00064.2006; PMID: 16899714
   PubMedGoogle Scholar
• Strazzabosco M, Somlo S. Polycystic liver diseases: congenital disorders of cholangiocyte signaling. Gastroenterology 2011; 140:1855 - 9, e1; http://dx.doi.org/10.1053/j.gastro.2011.04.030; PMID: 21515270
   PubMed Web of Science ®Google Scholar
• Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol 1951; 88:49 - 92; http://dx.doi.org/10.1002/jmor.1050880104; PMID: 24539719
   PubMed Web of Science ®Google Scholar
• Acloque H, Wilkinson DG, Nieto MA. In Situ Hybridization Analysis of Chick Embryos in Whole Mount and Tissue Sections. Methods Cell Biol 2008; 87:169 - 85; http://dx.doi.org/10.1016/S0091-679X(08)00209-4; PMID: 18485297
   PubMed Web of Science ®Google Scholar
• Dunn IC, Paton IR, Clelland AK, Sebastian S, Johnson EJ, McTeir L, Windsor D, Sherman A, Sang H, Burt DW, et al. The chicken polydactyly (Po) locus causes allelic imbalance and ectopic expression of Shh during limb development. Dev Dyn 2011; 240:1163 - 72; http://dx.doi.org/10.1002/dvdy.22623; PMID: 21465618
   PubMed Web of Science ®Google Scholar
• Boardman PE, Sanz-Ezquerro J, Overton IM, Burt DW, Bosch E, Fong WT, Tickle C, Brown WR, Wilson SA, Hubbard SJ. A comprehensive collection of chicken cDNAs. Curr Biol 2002; 12:1965 - 9; http://dx.doi.org/10.1016/S0960-9822(02)01296-4; PMID: 12445392
   PubMed Web of Science ®Google Scholar