Cited by 67Developmental Biology and Gene RegulationRenal and related cancersThyroid Disorders and Treatments

Gene expression profiling at early organogenesis reveals both common and diverse mechanisms in foregut patterning

Open access
Fagman, Henrik, Amendola, Elena, Parrillo, Luca, Zoppoli, Pietro, Marotta, Pina, Scarfò, Marzia, De Luca, Pasquale, de Carvalho, Denise Pires +3 more·2011·Developmental Biology

Abstract

The thyroid and lungs originate as neighboring bud shaped outgrowths from the midline of the embryonic foregut. When and how organ specific programs regulate development into structures of distinct shapes, positions and functions is incompletely understood. To characterize, at least in part, the genetic basis of these events, we have employed laser capture microdissection and microarray analysis to define gene expression in the mouse thyroid and lung primordia at E10.5. By comparing the transcriptome of each bud to that of the whole embryo as well as to each other, we broadly describe the genes that are preferentially expressed in each developing organ as well as those with an enriched expression common to both. The results thus obtained provide a valuable resource for further analysis of genes previously unrecognized to participate in thyroid and lung morphogenesis and to discover organ specific as well as common developmental mechanisms. As an initial step in this direction we describe a regulatory pathway involving the anti-apoptotic gene Bcl2 that controls cell survival in early thyroid development.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.ydbio.2011.08.015

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Tbx3 is a thyroid bud-specific factor as early as E10.5.

    “previous microarray combined with laser capture microdissection analysis identifies Tbx3 as a thyroid bud-specific factor at early as E10.548.”

    From Proteostatic reactivation of the developmental transcription factor TBX3 drives BRAF/MAPK-mediated tumorigenesis (2024) · cites this paper as [48]

    In “Genes enriched in the E10.5 thyroid bud” (page not provided), the paper reports Tbx3 expression in the thyroid bud at E10.5. It also reports Tbx3 in the first pharyngeal arch and mesenchyme surrounding the lung bud and trachea, so “thyroid bud-specific” overstates its distribution. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 69

  1. Al Taji E. Biebermann H. Limanova Z. Hnikova O. Zikmund J. Dame C. Gruters A. Lebl J. Krude H. Screening for mutations in transcription factors in a Czech cohort of 170 patients with congenital and early-onset hypothyroidism: identification of a novel PAX8 mutation in dominantly inherited early-onset non-autoimmune hypothyroidism Eur. J. Endocrinol. 156 2007 521 529 17468187
  2. Auden A. Caddy J. Wilanowski T. Ting S.B. Cunningham J.M. Jane S.M. Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development Gene Expr. Patterns 6 2006 964 970 16831572
  3. Berrocal T. Madrid C. Novo S. Gutierrez J. Arjonilla A. Gomez-Leon N. Congenital anomalies of the tracheobronchial tree, lung, and mediastinum: embryology, radiology, and pathology Radiographics 24 2004 e17 14610245
  4. Bouchard M. Souabni A. Mandler M. Neubuser A. Busslinger M. Nephric lineage specification by Pax2 and Pax8 Genes Dev. 16 22 2002 2958 2970 12435636 PMC187478
  5. Bouchard M. Souabni A. Busslinger M. Tissue-specific expression of cre recombinase from the Pax8 locus Genesis 38 2004 105 109 15048807
  6. Brown J.D. Dutta S. Bharti K. Bonner R.F. Munson P.J. Dawid I.B. Akhtar A.L. Onojafe I.F. Alur R.P. Gross J.M. Hejtmancik J.F. Jiao X. Chan W.Y. Brooks B.P. Expression profiling during ocular development identifies 2 Nlz genes with a critical role in optic fissure closure Proc. Natl. Acad. Sci. U.S.A. 106 2009 1462 1467 19171890 PMC2631080
  7. Brunelle J.K. Letai A. Control of mitochondrial apoptosis by the Bcl-2 family J. Cell Sci. 122 2009 437 441 19193868 PMC2714431
  8. Brunskill E.W. Aronow B.J. Georgas K. Rumballe B. Valerius M.T. Aronow J. Kaimal V. Jegga A.G. Yu J. Grimmond S. McMahon A.P. Patterson L.T. Little M.H. Potter S.S. Atlas of gene expression in the developing kidney at microanatomic resolution Dev. Cell 15 2008 781 791 19000842 PMC2653061
  9. Cardoso W.V. Lu J. Regulation of early lung morphogenesis: questions, facts and controversies Development (Cambridge, England) 133 2006 1611 1624 16613830
  10. Castrillon D.H. Miao L. Kollipara R. Horner J.W. DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a Science 301 2003 215 218 12855809
  11. Chapman D.L. Garvey N. Hancock S. Alexiou M. Agulnik S.I. Gibson-Brown J.J. Cebra-Thomas J. Bollag R.J. Silver L.M. Papaioannou V.E. Expression of the T-box family genes, Tbx1–Tbx5, during early mouse development Dev. Dyn. 206 1996 379 390 8853987
  12. Corbetta C. Weber G. Cortinovis F. Calebiro D. Passoni A. Vigone M.C. Beck-Peccoz P. Chiumello G. Persani L. A 7-year experience with low blood TSH cutoff levels for neonatal screening reveals an unsuspected frequency of congenital hypothyroidism (CH) Clin. Endocrinol. (Oxf.) 71 2009 739 745 19486019
  13. Correia-Pinto J. Gonzaga S. Huang Y. Rottier R. Congenital lung lesions—underlying molecular mechanisms Semin. Pediatr. Surg. 19 2010 171 179 20610189
  14. De Felice M. Di Lauro R. Thyroid development and its disorders: genetics and molecular mechanisms Endocr. Rev. 25 2004 722 746 15466939
  15. De Felice M. Ovitt C. Biffali E. Rodriguez-Mallon A. Arra C. Anastassiadis K. Macchia P.E. Mattei M.G. Mariano A. Scholer H. Macchia V. Di Lauro R. A mouse model for hereditary thyroid dysgenesis and cleft palate Nat. Genet. 19 1998 395 398 9697704
  16. De Moerlooze L. Spencer-Dene B. Revest J.M. Hajihosseini M. Rosewell I. Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal–epithelial signalling during mouse organogenesis Development (Cambridge, England) 127 2000 483 492 10631169
  17. Dennis G. Jr. Sherman B.T. Hosack D.A. Yang J. Gao W. Lane H.C. Lempicki R.A. DAVID: Database for Annotation, Visualization, and Integrated Discovery Genome Biol. 4 2003 P3 12734009
  18. Fagman H. Grande M. Gritli-Linde A. Nilsson M. Genetic deletion of sonic hedgehog causes hemiagenesis and ectopic development of the thyroid in mouse Am. J. Pathol. 164 2004 1865 1872 15111333 PMC1615667
  19. Fagman H. Nilsson M. Morphogenesis of the thyroid gland Mol. Cell. Endocrinol. 323 2010 35 54 20026174
  20. Freedom R.M. Yoo S.J. Goo H.W. Mikailian H. Anderson R.H. The bronchopulmonary foregut malformation complex Cardiol. Young 16 2006 229 251 16725062
  21. Fuchtbauer E.M. Expression of M-twist during postimplantation development of the mouse Dev. Dyn. 204 1995 316 322 8573722
  22. Gu G. Wells J.M. Dombkowski D. Preffer F. Aronow B. Melton D.A. Global expression analysis of gene regulatory pathways during endocrine pancreatic development Development 131 2004 165 179 14660441
  23. Guazzi S. Price M. De Felice M. Damante G. Mattei M.G. Di Lauro R. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity EMBO J. 9 1990 3631 3639 1976511 PMC552115
  24. Hewitt S.M. Hamada S. Monarres A. Kottical L.V. Saunders G.F. McDonnell T.J. Transcriptional activation of the bcl-2 apoptosis suppressor gene by the paired box transcription factor PAX8 Anticancer Res. 17 1997 3211 3215 9413150
  25. Hilberg F. Aguzzi A. Howells N. Wagner E.F. c-jun is essential for normal mouse development and hepatogenesis Nature 365 1993 179 181 8371760
  26. Irizarry R.A. Hobbs B. Collin F. Beazer-Barclay Y.D. Antonellis K.J. Scherf U. Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 4 2003 249 264 12925520
  27. Ishii Y. Rex M. Scotting P.J. Yasugi S. Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial–mesenchymal interactions Dev. Dyn. 213 1998 464 475 9853967
  28. Jiang X. Rowitch D.H. Soriano P. McMahon A.P. Sucov H.M. Fate of the mammalian cardiac neural crest Development 127 2000 1607 1616 10725237
  29. Keijzer R. van Tuyl M. Meijers C. Post M. Tibboel D. Grosveld F. Koutsourakis M. The transcription factor GATA6 is essential for branching morphogenesis and epithelial cell differentiation during fetal pulmonary development Development (Cambridge, England) 128 2001 503 511 11171334
  30. Kimura S. Hara Y. Pineau T. Fernandez-Salguero P. Fox C.H. Ward J.M. Gonzalez F.J. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary Genes Dev. 10 1996 60 69 8557195
  31. Kratzsch J. Pulzer F. Thyroid gland development and defects Best Pract. Res. Clin. Endocrinol. Metab. 22 2008 57 75 18279780
  32. Lazzaro D. Price M. de Felice M. Di Lauro R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain Development (Cambridge, England) 113 1991 1093 1104 1811929
  33. Little M.H. Brennan J. Georgas K. Davies J.A. Davidson D.R. Baldock R.A. Beverdam A. Bertram J.F. Capel B. Chiu H.S. Clements D. Cullen-McEwen L. Fleming J. Gilbert T. Herzlinger D. Houghton D. Kaufman M.H. Kleymenova E. Koopman P.A. Lewis A.G. McMahon A.P. Mendelsohn C.L. Mitchell E.K. Rumballe B.A. Sweeney D.E. Valerius M.T. Yamada G. Yang Y. Yu J. A high-resolution anatomical ontology of the developing murine genitourinary tract Gene Expr. Patterns 7 2007 680 699 17452023 PMC2117077
  34. Liu Y. Jiang H. Crawford H.C. Hogan B.L. Role for ETS domain transcription factors Pea3/Erm in mouse lung development Dev. Biol. 261 2003 10 24 12941618
  35. Lo C.W. Cohen M.F. Huang G.Y. Lazatin B.O. Patel N. Sullivan R. Pauken C. Park S.M. Cx43 gap junction gene expression and gap junctional communication in mouse neural crest cells Dev. Genet. 20 1997 119 132 9144923
  36. Lonergan W. Whistler T. Vernon S.D. Comparison of target labeling methods for use with Affymetrix GeneChips BMC Biotechnol. 7 2007 24 17511875 PMC1885795
  37. Mansouri A. Chowdhury K. Gruss P. Follicular cells of the thyroid gland require Pax8 gene function Nat. Genet. 19 1998 87 90 9590297
  38. Martinez Barbera J.P. Clements M. Thomas P. Rodriguez T. Meloy D. Kioussis D. Beddington R.S. The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation Development (Cambridge, England) 127 2000 2433 2445 10804184
  39. Masuda T. Kai N. Sakuma C. Kobayashi K. Koga H. Yaginuma H. Laser capture microdissection and cDNA array analysis for identification of mouse KIAA/FLJ genes differentially expressed in the embryonic dorsal spinal cord Brain Res. 1249 2009 61 67 19026994
  40. Metzger D.E. Xu Y. Shannon J.M. Elf5 is an epithelium-specific, fibroblast growth factor-sensitive transcription factor in the embryonic lung Dev. Dyn. 236 2007 1175 1192 17394208
  41. Metzger R.J. Klein O.D. Martin G.R. Krasnow M.A. The branching programme of mouse lung development Nature 453 2008 745 750 18463632 PMC2892995
  42. Minoo P. Hu L. Xing Y. Zhu N.L. Chen H. Li M. Borok Z. Li C. Physical and functional interactions between homeodomain NKX2.1 and winged helix/forkhead FOXA1 in lung epithelial cells Mol. Cell. Biol. 27 2007 2155 2165 17220277 PMC1820505
  43. Mitchell P.J. Timmons P.M. Hebert J.M. Rigby P.W. Tjian R. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis Genes Dev. 5 1991 105 119 1989904
  44. Monaghan A.P. Kaestner K.H. Grau E. Schutz G. Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm Development (Cambridge, England) 119 1993 567 578 8187630
  45. Morrisey E.E. Hogan B.L. Preparing for the first breath: genetic and cellular mechanisms in lung development Dev. Cell 18 2010 8 23 20152174 PMC3736813
  46. Narumi S. Muroya K. Asakura Y. Adachi M. Hasegawa T. Transcription factor mutations and congenital hypothyroidism: systematic genetic screening of a population-based cohort of Japanese patients J. Clin. Endocrinol. Metab. 95 2010 1981 1985 20157192
  47. Ohuchi H. Hori Y. Yamasaki M. Harada H. Sekine K. Kato S. Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development Biochem. Biophys. Res. Commun. 277 2000 643 649 11062007
  48. Orr-Urtreger A. Lonai P. Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo Development 115 1992 1045 1058 1451656
  49. Park D. Jia H. Rajakumar V. Chamberlin H.M. Pax2/5/8 proteins promote cell survival in C. elegans Development (Cambridge, England) 133 2006 4193 4202 17021039
  50. Parlato R. Rosica A. Rodriguez-Mallon A. Affuso A. Postiglione M.P. Arra C. Mansouri A. Kimura S. Di Lauro R. De Felice M. An integrated regulatory network controlling survival and migration in thyroid organogenesis Dev. Biol. 276 2004 464 475 15581879
  51. Purcell P. Joo B.W. Hu J.K. Tran P.V. Calicchio M.L. O'Connell D.J. Maas R.L. Tabin C.J. Temporomandibular joint formation requires two distinct hedgehog-dependent steps Proc. Natl. Acad. Sci. U.S.A. 106 2009 18297 18302 19815519 PMC2775291
  52. Que J. Okubo T. Goldenring J.R. Nam K.T. Kurotani R. Morrisey E.E. Taranova O. Pevny L.H. Hogan B.L. Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm Development 134 2007 2521 2531 17522155 PMC3625644
  53. Rapley R. Enhancing PCR amplification and sequencing using DNA-binding proteins Mol. Biotechnol. 2 1994 295 298 7866882
  54. Rifat Y. Parekh V. Wilanowski T. Hislop N.R. Auden A. Ting S.B. Cunningham J.M. Jane S.M. Regional neural tube closure defined by the Grainy head-like transcription factors Dev. Biol. 345 2010 237 245 20654612
  55. Sado T. Nakajima N. Tada M. Takagi N. A novel mesoderm-specific cDNA isolated from a mouse embryonal carcinoma cell line Develop Growth Differ 35 1993 551 560 37281168
  56. Scheidl S.J. Nilsson S. Kalen M. Hellstrom M. Takemoto M. Hakansson J. Lindahl P. mRNA expression profiling of laser microbeam microdissected cells from slender embryonic structures Am. J. Pathol. 160 2002 801 813 11891179 PMC1867164
  57. Sekine K. Ohuchi H. Fujiwara M. Yamasaki M. Yoshizawa T. Sato T. Yagishita N. Matsui D. Koga Y. Itoh N. Kato S. Fgf10 is essential for limb and lung formation Nat. Genet. 21 1999 138 141 9916808
  58. Sherwood R.I. Jitianu C. Cleaver O. Shaywitz D.A. Lamenzo J.O. Chen A.E. Golub T.R. Melton D.A. Prospective isolation and global gene expression analysis of definitive and visceral endoderm Dev. Biol. 304 2007 541 555 17328885
  59. Shu W. Lu M.M. Zhang Y. Tucker P.W. Zhou D. Morrisey E.E. Foxp2 and Foxp1 cooperatively regulate lung and esophagus development Development (Cambridge, England) 134 2007 1991 2000 17428829
  60. Simonneau L. Kitagawa M. Suzuki S. Thiery J.P. Cadherin 11 expression marks the mesenchymal phenotype: towards new functions for cadherins? Cell Adhes. Commun. 3 1995 115 130 7583005
  61. Stoppa-Vaucher S. Lapointe A. Turpin S. Rydlewski C. Vassart G. Deladoey J. Ectopic thyroid gland causing dysphonia: imaging and molecular studies J. Clin. Endocrinol. Metab. 95 2010 4509 4510 20926539
  62. Thorwarth A. Mueller I. Biebermann H. Ropers H.H. Grueters A. Krude H. Ullmann R. Screening chromosomal aberrations by array comparative genomic hybridization in 80 patients with congenital hypothyroidism and thyroid dysgenesis J. Clin. Endocrinol. Metab. 2010 20427504
  63. van Tuyl M. Liu J. Groenman F. Ridsdale R. Han R.N. Venkatesh V. Tibboel D. Post M. Iroquois genes influence proximo-distal morphogenesis during rat lung development Am. J. Physiol. Lung Cell. Mol. Physiol. 290 2006 L777 L789 16299054
  64. Vassart G. Dumont J.E. Thyroid dysgenesis: multigenic or epigenetic … or both? Endocrinology 146 2005 5035 5037 16291637
  65. Veis D.J. Sorenson C.M. Shutter J.R. Korsmeyer S.J. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair Cell 75 1993 229 240 8402909
  66. Wells J.M. Melton D.A. Vertebrate endoderm development Annu. Rev. Cell Dev. Biol. 15 1999 393 410 10611967
  67. Werth M. Walentin K. Aue A. Schonheit J. Wuebken A. Pode-Shakked N. Vilianovitch L. Erdmann B. Dekel B. Bader M. Barasch J. Rosenbauer F. Luft F.C. Schmidt-Ott K.M. The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex Development (Cambridge, England) 137 2010 3835 3845 20978075
  68. Young P.E. Baumhueter S. Lasky L.A. The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development Blood 85 1995 96 105 7528578
  69. Zaret K.S. Grompe M. Generation and regeneration of cells of the liver and pancreas Science 322 2008 1490 1494 19056973 PMC2641009

Cited by

Sorted by citations

Authors
Fagman, H., Amendola, E., Parrillo, L., Zoppoli, P., Marotta, P., Scarfò, M., De Luca, P., de Carvalho, D. P., Ceccarelli, M., De Felice, M., & Di Lauro, R.
Affiliations
  • Biogem (IT)
  • Stazione Zoologica Anton Dohrn (IT)
  • University of Sannio (IT)
Venue
Developmental Biology
Publisher
Elsevier BV
Published
2011-11
Volume
359
Issue
2
Pages
163-175
ISSN
0012-1606 (ISSN-L)
OpenAlex
W2002737460
Cited by
67
References
4
Citations by year
2026: 3 · 2025: 2 · 2024: 4 · 2022: 5 · 2021: 5 · 2020: 2 · 2019: 4 · 2018: 6 · 2017: 8 · 2016: 4 · 2015: 5 · 2014: 7 · 2013: 5 · 2012: 5
FWCI
2.21
Type
journal article
Language
en
Open access
Locations
  • Developmental Biology (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • EMBO
  • Västra Götalandsregionen
  • Assar Gabrielssons Foundation
  • Telethon (GGP05161)
  • European Community (LSHM-CT-2005-01865)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Renal and related cancers
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
Keywords
thyroid development, lung development, organogenesis, gene expression profiling, Bcl-2, anti-apoptotic genes, cell survival, mouse embryo
MeSH terms
Animals, Digestive System, Embryo, Mammalian, Female, Lung, Male, Mice, Inbred C57BL, Thyroid Gland, Time Factors, In Situ Hybridization, Mice, Knockout, Gene Expression Regulation, Developmental, Body Patterning, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Organogenesis, Mice, Transcriptome, Laser Capture Microdissection

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review