Home LiteratureArticle Details
PMID: 16998587 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Calcineurin/Nfat signaling is required for perinatal lung maturation and function.

The Journal of clinical investigation ·Vol. 116 ·No. 10 ·2006-10-00 ·Pages 2597-609

Davé V, Childs T, Xu Y, Ikegami M, Besnard V, Maeda Y, Wert SE, Neilson JR, Crabtree GR, Whitsett JA

Abstract

Pulmonary surfactant proteins and lipids are required for lung function after birth. Lung immaturity and resultant surfactant deficiency cause respiratory distress syndrome, a common disorder contributing to morbidity and mortality in preterm infants. Surfactant synthesis increases prior to birth in association with formation of the alveoli that mediate efficient gas exchange. To identify mechanisms controlling perinatal lung maturation, the Calcineurin b1 (Cnb1) gene was deleted in the respiratory epithelium of the fetal mouse. Deletion of Cnb1 caused respiratory failure after birth and inhibited the structural maturation of the peripheral lung. Synthesis of surfactant and a lamellar body-associated protein, ABC transporter A3 (ABCA3), was decreased prior to birth. Nuclear factor of activated T cells (Nfat) calcineurin-dependent 3 (Nfatc3), a transcription factor modulated by calcineurin, was identified as a direct activator of Sftpa, Sftpb, Sftpc, Abca3, Foxa1, and Foxa2 genes. The calcineurin/Nfat pathway controls the morphologic maturation of lungs prior to birth and regulates expression of genes involved in surfactant homeostasis that are critical for adaptation to air breathing.

MeSH Terms
ATP-Binding Cassette Transporters/genetics,metabolism Animals Calcineurin/genetics,metabolism Cell Line, Transformed DNA-Binding Proteins/genetics,metabolism Gene Expression Profiling Gene Expression Regulation, Developmental/genetics Hepatocyte Nuclear Factor 3-alpha/genetics,metabolism Hepatocyte Nuclear Factor 3-beta/genetics,metabolism Lung/embryology,metabolism,pathology Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Models, Biological NFATC Transcription Factors/genetics,metabolism Nuclear Proteins/genetics Oligonucleotide Array Sequence Analysis Pulmonary Surfactant-Associated Proteins/genetics,metabolism Respiratory Insufficiency/genetics,pathology Respiratory Mucosa/metabolism Signal Transduction/physiology Thyroid Nuclear Factor 1 Transcription Factors/genetics
Chemicals
ATP-Binding Cassette Transporters Abca3 protein, mouse DNA-Binding Proteins Foxa1 protein, mouse Foxa2 protein, mouse Hepatocyte Nuclear Factor 3-alpha NFATC Transcription Factors Nfatc3 protein, mouse Nuclear Proteins Pulmonary Surfactant-Associated Proteins Thyroid Nuclear Factor 1 Transcription Factors Ttf1 protein, mouse Hepatocyte Nuclear Factor 3-beta Calcineurin
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Davé Vrushank
Section of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, Ohio 45229, USA. davev0@cchmc.org
Childs Tawanna
Xu Yan
Ikegami Machiko
Besnard Valérie
Maeda Yutaka
Wert Susan E
Neilson Joel R
Crabtree Gerald R
Whitsett Jeffrey A
References (60)
60 references, click to expand
  1. Pancreatic phospholipase A2: isolation of the human gene and cDNAs from porcine pancreas and human lung.
    DNA. 1986 Dec;5(6):519-27 PMID: 3028739
  2. Dephosphorylation of microtubule-associated protein 2, tau factor, and tubulin by calcineurin.
    J Neurochem. 1985 Jul;45(1):276-83 PMID: 2987415
  3. A thyroid-specific nuclear protein essential for tissue-specific expression of the thyroglobulin promoter.
    EMBO J. 1989 Sep;8(9):2537-42 PMID: 2583123
  4. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A.
    Nature. 1991 Aug 29;352(6338):803-7 PMID: 1715516
  5. Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):9808-12 PMID: 7694293
  6. Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11029-33 PMID: 8248207
  7. Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis.
    Science. 1994 Apr 29;264(5159):713-6 PMID: 8171324
  8. Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase.
    Nature. 1994 May 19;369(6477):235-9 PMID: 7514273
  9. Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization.
    Science. 1994 Aug 12;265(5174):970-3 PMID: 8052858
  10. Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7794-8 PMID: 7644495
  11. 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. 1996 Jan 1;10(1):60-9 PMID: 8557195
  12. The calcium/calmodulin-dependent protein phosphatase calcineurin is the major Elk-1 phosphatase.
    J Biol Chem. 1997 Nov 21;272(47):29415-8 PMID: 9367995
  13. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA.
    Nature. 1998 Mar 5;392(6671):42-8 PMID: 9510247
  14. VEGF enhances pulmonary vasculogenesis and disrupts lung morphogenesis in vivo.
    Dev Dyn. 1998 Mar;211(3):215-27 PMID: 9520109
  15. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy.
    Cell. 1998 Apr 17;93(2):215-28 PMID: 9568714
  16. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD.
    Science. 1999 Apr 9;284(5412):339-43 PMID: 10195903
  17. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A.
    Science. 1999 Sep 24;285(5436):2129-33 PMID: 10497131
  18. Phosphorus assay in column chromatography.
    J Biol Chem. 1959 Mar;234(3):466-8 PMID: 13641241
  19. FGF-10 induces SP-C and Bmp4 and regulates proximal-distal patterning in embryonic tracheal epithelium.
    Am J Physiol Lung Cell Mol Physiol. 2004 Dec;287(6):L1116-26 PMID: 15531758
  20. Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues.
    Gene Expr Patterns. 2004 Dec;5(2):193-208 PMID: 15567715
  21. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis.
    J Biol Chem. 2005 Apr 8;280(14):13809-16 PMID: 15668254
  22. Calcium signalling in growth cone migration.
    Cell Calcium. 2005 May;37(5):395-402 PMID: 15820386
  23. Regulation of calcineurin through transcriptional induction of the calcineurin A beta promoter in vitro and in vivo.
    Mol Cell Biol. 2005 Aug;25(15):6649-59 PMID: 16024800
  24. ERK1/2-dependent activation of transcription factors required for acute and chronic effects of glucose on the insulin gene promoter.
    J Biol Chem. 2005 Jul 22;280(29):26751-9 PMID: 15899886
  25. In smooth muscle, FK506-binding protein modulates IP3 receptor-evoked Ca2+ release by mTOR and calcineurin.
    J Cell Sci. 2005 Dec 1;118(Pt 23):5443-51 PMID: 16278292
  26. Respiratory failure due to differentiation arrest and expansion of alveolar cells following lung-specific loss of the transcription factor C/EBPalpha in mice.
    Mol Cell Biol. 2006 Feb;26(3):1109-23 PMID: 16428462
  27. Interaction between heat shock protein 70 kDa and calcineurin in cardiovascular systems (Review).
    Int J Mol Med. 2006 Mar;17(3):419-23 PMID: 16465387
  28. C/EBPalpha is required for lung maturation at birth.
    Development. 2006 Mar;133(6):1155-64 PMID: 16467360
  29. DAVID: Database for Annotation, Visualization, and Integrated Discovery.
    Genome Biol. 2003;4(5):P3 PMID: 12734009
  30. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8164-9 PMID: 12808131
  31. Early administration of inhaled corticosteroids for preventing chronic lung disease in ventilated very low birth weight preterm neonates.
    Cochrane Database Syst Rev. 2000;(2):CD001969 PMID: 10796275
  32. Increased metalloproteinase activity, oxidant production, and emphysema in surfactant protein D gene-inactivated mice.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5972-7 PMID: 10801980
  33. Calcineurin: form and function.
    Physiol Rev. 2000 Oct;80(4):1483-521 PMID: 11015619
  34. Reconstitution of T cell-specific transcription directed by composite NFAT/Oct elements.
    J Immunol. 2000 Nov 15;165(10):5646-55 PMID: 11067921
  35. Bronchopulmonary dysplasia.
    Am J Respir Crit Care Med. 2001 Jun;163(7):1723-9 PMID: 11401896
  36. Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature.
    Cell. 2001 Jun 29;105(7):863-75 PMID: 11439183
  37. NFAT signaling in vertebrate development.
    Curr Opin Genet Dev. 2001 Oct;11(5):505-12 PMID: 11532391
  38. Conditional gene expression in the respiratory epithelium of the mouse.
    Transgenic Res. 2002 Feb;11(1):21-9 PMID: 11874100
  39. NFAT: ubiquitous regulator of cell differentiation and adaptation.
    J Cell Biol. 2002 Mar 4;156(5):771-4 PMID: 11877454
  40. Immunolocalization of surfactant protein-D (SP-D) in human fetal, newborn, and adult tissues.
    J Histochem Cytochem. 2002 May;50(5):651-60 PMID: 11967276
  41. NFAT signaling: choreographing the social lives of cells.
    Cell. 2002 Apr;109 Suppl:S67-79 PMID: 11983154
  42. Identification of LBM180, a lamellar body limiting membrane protein of alveolar type II cells, as the ABC transporter protein ABCA3.
    J Biol Chem. 2002 Jun 21;277(25):22147-55 PMID: 11940594
  43. Hydrophobic surfactant proteins in lung function and disease.
    N Engl J Med. 2002 Dec 26;347(26):2141-8 PMID: 12501227
  44. Summaries of Affymetrix GeneChip probe level data.
    Nucleic Acids Res. 2003 Feb 15;31(4):e15 PMID: 12582260
  45. Transcription cooperation by NFAT.C/EBP composite enhancer complex.
    J Biol Chem. 2003 May 2;278(18):15874-85 PMID: 12606546
  46. Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
    Biostatistics. 2003 Apr;4(2):249-64 PMID: 12925520
  47. TTF-1 phosphorylation is required for peripheral lung morphogenesis, perinatal survival, and tissue-specific gene expression.
    J Biol Chem. 2003 Sep 12;278(37):35574-83 PMID: 12829717
  48. Transcriptional regulation by calcium, calcineurin, and NFAT.
    Genes Dev. 2003 Sep 15;17(18):2205-32 PMID: 12975316
  49. Foxa2 regulates alveolarization and goblet cell hyperplasia.
    Development. 2004 Feb;131(4):953-64 PMID: 14757645
  50. The molecular genetics of lung morphogenesis and injury repair.
    Paediatr Respir Rev. 2004;5 Suppl A:S283-7 PMID: 14980285
  51. Calcineurin B1 is essential for positive but not negative selection during thymocyte development.
    Immunity. 2004 Mar;20(3):255-66 PMID: 15030770
  52. ABCA3 gene mutations in newborns with fatal surfactant deficiency.
    N Engl J Med. 2004 Mar 25;350(13):1296-303 PMID: 15044640
  53. Nuclear factor of activated T cells regulates transcription of the surfactant protein D gene (Sftpd) via direct interaction with thyroid transcription factor-1 in lung epithelial cells.
    J Biol Chem. 2004 Aug 13;279(33):34578-88 PMID: 15173172
  54. Genetic disorders influencing lung formation and function at birth.
    Hum Mol Genet. 2004 Oct 1;13 Spec No 2:R207-15 PMID: 15358727
  55. Foxa2 is required for transition to air breathing at birth.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14449-54 PMID: 15452354
  56. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants.
    Pediatrics. 1972 Oct;50(4):515-25 PMID: 4561295
  57. Isolation of disaturated phosphatidylcholine with osmium tetroxide.
    J Lipid Res. 1976 May;17(3):281-4 PMID: 932560
  58. Development of the type II cell in the fetal rat lung.
    Am Rev Respir Dis. 1977 Jun;115(6 Pt 2):37-47 PMID: 869319
  59. Fetal and postnatal development of the lung.
    Annu Rev Physiol. 1984;46:617-28 PMID: 6370120
  60. Contingent genetic regulatory events in T lymphocyte activation.
    Science. 1989 Jan 20;243(4889):355-61 PMID: 2783497
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2006-10-00
Epub
2006-00-21
Pages
2597-609
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC1570374
Subset
IM
Grants
NHLBI NIH HHS · HL 38859 · United States
NHLBI NIH HHS · R01 HL038859 · United States
NHLBI NIH HHS · P50 HL056387 · United States
NHLBI NIH HHS · R37 HL038859 · United States
NHLBI NIH HHS · HL 56387 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com