Prenatal retinoid deficiency leads to airway hyperresponsiveness in adult mice

Journal of Clinical Investigation

Volumn 124, Issue 2, 2014, Pages 801-811

  Chen, Felicia ^a   Marquez, Hector ^a   Kim, Youn Kyung ^b   Qian, Jun ^c   Shao, Fengzhi ^a   Fine, Alan ^a   Cruikshank, William W ^a   Quadro, Loredana ^b   Cardoso, Wellington V ^c  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOCONSTRICTOR AGENTS; CELL DIFFERENTIATION; DIET; DISEASE MODELS, ANIMAL; FEMALE; LUNG; METHACHOLINE CHLORIDE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PREGNANCY; SIGNAL TRANSDUCTION; TRETINOIN; VITAMIN A; VITAMIN A DEFICIENCY;

EID: 84893863604     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI70291     Document Type: Article

References (67)

1. West KP, Howard GR, Sommer A. Vitamin A and infection: public health implications. Annu Rev Nutr. 1989;9:63-86.
2. West KP Jr. Extent of vitamin A deficiency among preschool children and women of reproductive age. J Nutr. 2002;132(9 Suppl):2857S-2866S.
3. Williams SR. Nutrition and Diet Therapy: Instructor's Manual and Text Book. Maryland Heights, Missouri, USA: Mosby; 1997.
4. Chambon P. The retinoid signaling pathway: molecular and genetic analyses. Semin Cell Biol. 1994;5(2):115-125.
5. Clagett-Dame M, DeLuca HF. The role of vitamin a in mammalian reproduction and embryonic development. Annu Rev Nutr. 2002;22:347-381.
6. Wilson JG, Roth CB, Warkany J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat. 1953;92(2):189-217.
7. Spears K, Cheney C, Zerzan J. Low plasma retinol concentrations increase the risk of developing bronchopulmonary dysplasia and long-term respiratory disability in very-low-birth-weight infants. Am J Clin Nutr. 2004;80(6):1589-1594.
8. Babu TA, Sharmila V. Vitamin A supplementation in late pregnancy can decrease the incidence of bronchopulmonary dysplasia in newborns. J Matern Fetal Neonatal Med. 2010;23(12):1468-1469.
9. Kling DE, Schnitzer JJ. Vitamin A deficiency (VAD), teratogenic, and surgical models of congenital diaphragmatic hernia (CDH). Am J Med Genet C Semin Med Genet. 2007; 145C(2):139-157.
10. Golzio C, et al. Matthew-Wood syndrome is caused by truncating mutations in the retinol-binding protein receptor gene STRA6. Am J Hum Genet. 2007; 80(6):1179-1187.
11. Arora P, Kumar V, Batra S. Vitamin A status in children with asthma. Pediatr Allergy Immunol. 2002;13(3):223-226.
12. Luo Z-X, et al. Vitamin A deficiency and wheezing. World J Pediatr. 2010;6(1):81-84.
13. Allen S, Britton JR, Leonardi-Bee JA. Association between antioxidant vitamins and asthma outcome measures: systematic review and meta-analysis. Thorax. 2009;64(7):610-619.
14. Al Senaidy AM. Serum vitamin A and beta-carotene levels in children with asthma. J Asthma. 2009; 46(7):699-702.
15. Checkley W, et al. Maternal vitamin A supplementation and lung function in offspring. N Engl J Med. 2010;362(19):1784-1794.
16. Patelarou E, et al. Association between biomarker-quantified antioxidant status during pregnancy and infancy and allergic disease during early childhood: a systematic review. Nutr Rev. 2011; 69(11):627-641.
17. Badri KR, Zhou Y, Schuger L. Embryological origin of airway smooth muscle. Proc Am Thorac Soc. 2008;5(1):4-10.
18. Tollet J, Everett AW, Sparrow MP. Spatial and temporal distribution of nerves, ganglia, and smooth muscle during the early pseudoglandular stage of fetal mouse lung development. Dev Dyn. 2001;221(1):48-60.
19. Sparrow MP, Lamb JP. Ontogeny of airway smooth muscle: structure, innervation, myogenesis and function in the fetal lung. Respir Physiol Neurobiol. 2003;137(2-3):361-372.
20. Peng T, et al. Coordination of heart lung co-development by a multipotent cardiopulmonary progenitor. Nature. 2013;500(7464):589-592.
21. Schittny JC, Miserocchi G, Sparrow MP. Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants. Am J Respir Cell Mol Biol. 2000; 23(1):11-18.
22. Jesudason EC, et al. Developing rat lung has a sided pacemaker region for morphogenesis-related airway peristalsis. Am J Respir Cell Mol Biol. 2005; 32(2):118-127.
23. Hirota JA, Nguyen TT, Schaafsma D, Sharma P, Tran T. Airway smooth muscle in asthma: phenotype plasticity and function. Pulm Pharmacol Ther. 2009;22(5):370-378.
24. Zuyderduyn S, Sukkar MB, Fust A, Dhaliwal S, Burgess JK. Treating asthma means treating airway smooth muscle cells. Eur Respir J. 2008;32(2):265-274.
25. Mizuno Y, Furusho T, Yoshida A, Nakamura H, Matsuura T, Eto Y. Serum vitamin A concentrations in asthmatic children in Japan. Pediatr Int. 2006;48(3):261-264.
26. DiCosmo BF, et al. Airway epithelial cell expression of interleukin-6 in transgenic mice. Uncoupling of airway inflammation and bronchial hyperreactivity. J Clin Invest. 1994;94(5):2028-2035.
27. Plant PJ, et al. Hypertrophic airway smooth muscle mass correlates with increased airway responsiveness in a murine model of asthma. Am J Respir Cell Mol Biol. 2012;46(4):532-540.
28. Niederreither K, Subbarayan V, Dollé P, Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet. 1999;21(4):444-448.
29. Dickman ED, Thaller C, Smith SM. Temporally-regulated retinoic acid depletion produces specific neural crest, ocular and nervous system defects. Dev Camb Engl. 1997;124(16):3111-3121.
30. Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV. Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Dev Biol. 2004;273(2):402-415.
31. Desai TJ, et al. Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol. 2006;291(1):12-24.
32. Chen F, Desai TJ, Qian J, Niederreither K, Lü J, Cardoso WV. Inhibition of Tgfβsignaling by endoge-nous retinoic acid is essential for primary lung bud induction. Development. 2007;134(16):2969-2979.
33. Chen F, Cao Y, Qian J, Shao F, Niederreither K, Cardoso WV. A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J Clin Invest. 2010;120(6):2040-2048.
34. Manabe I, Nagai R. Regulation of smooth muscle phenotype. Curr Atheroscler Rep. 2003;5(3):214-222.
35. Rossant J, Zirngibl R, Cado D, Shago M, Giguère V. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 1991;5(8):1333-1344.
36. Malpel S, Mendelsohn C, Cardoso WV. Regulation of retinoic acid signaling during lung morphogenesis. Development. 2000;127(14):3057-3067.
37. Kong SK, Halayko AJ, Stephens NL. Increased myosin phosphorylation in sensitized canine tracheal smooth muscle. Am J Physiol - Lung Cell Mol Physiol. 1990;259(2):L53-L56.
38. Jean J-C, Lü J, Joyce-Brady M, Cardoso WV. Regulation of Fgf10 gene expression in murine mesenchymal cells. J Cell Biochem. 2008;103(6):1886-1894.
39. Chazaud C, Dollé P, Rossant J, Mollard R. Retinoic acid signaling regulates murine bronchial tubule formation. Mech Dev. 2003;120(6):691-700.
40. Mailleux AA, et al. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development. 2005;132(9):2157-2166.
41. Cardoso WV, Lü J. Regulation of early lung morphogenesis: questions, facts and controversies. Development. 2006;133(9):1611-1624.
42. Warburton D, et al. Lung organogenesis. Curr Top Dev Biol. 2010;90:73-158.
43. Wang D, et al. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell. 2001;105(7):851-862.
44. Goss AM, et al. Wnt2 signaling is necessary and sufficient to activate the airway smooth muscle program in the lung by regulating myocardin/Mrtf-B and Fgf10 expression. Dev Biol. 2011;356(2):541-552.
45. Wang D-Z, et al. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A. 2002; 99(23):14855-14860.
46. Ghosh S, et al. Activation dynamics and signaling properties of Notch3 receptor in the developing pulmonary artery. J Biol Chem. 2011; 286(25):22678-22687.
47. Kim Y-K, et al. Retinyl ester formation by lecithin: retinol acyltransferase is a key regulator of retinoid homeostasis in mouse embryogenesis. J Biol Chem. 2008;283(9):5611-5621.
48. Morrisey EE, Hogan BLM. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell. 2010;18(1):8-23.
49. Kim Y-K, Quadro L. Reverse-phase high-performance liquid chromatography (HPLC) analysis of retinol and retinyl esters in mouse serum and tissues. Methods Mol Biol. 2010;652:263-275.
50. Tompkins DH, et al. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. PLoS One. 2009;4(12):e8248.
51. Que J, Luo X, Schwartz RJ, Hogan BLM. Multiple roles for Sox2 in the developing and adult mouse trachea. Dev Camb Engl. 2009;136(11):1899-1907.
52. Lu Y, Okubo T, Rawlins E, Hogan BLM. Epithelial progenitor cells of the embryonic lung and the role of microRNAs in their proliferation. Proc Am Thorac Soc. 2008;5(3):300-304.
53. Little FF, de Bie J, van Oosterhout A, Kornfeld H, Center DM, Cruikshank WW. Immunomodulatory effect of interleukin-16 on allergic airway inflammation. Chest. 2003;123(3 Suppl):431S-432S.
54. Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J. 2007; 15(3):100-108.
55. Azambuja AP, et al. Retinoic acid and VEGF delay smooth muscle relative to endothelial differentiation to coordinate inner and outer coronary vessel wall morphogenesis. Circ Res. 2010;107(2):204-216.
56. Weaver M, Batts L, Hogan BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol. 2003;258(1):169-184.
57. Litingtung Y, Lei L, Westphal H, Chiang C. Sonic hedgehog is essential to foregut development. Nat Genet. 1998;20(1):58-61.
58. Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol. 1998;8(19):1083-1086.
59. Cohen ED, Ihida-Stansbury K, Lu MM, Panettieri RA, Jones PL, Morrisey EE. Wnt signaling regulates smooth muscle precursor development in the mouse lung via a tenascin C/PDGFR pathway. J Clin Invest. 2009;119(9):2538-2549.
60. Yi L, Domyan ET, Lewandoski M, Sun X. Fibroblast growth factor 9 signaling inhibits airway smooth muscle differentiation in mouse lung. Dev Dyn. 2009;238(1):123-137.
61. McGowan SE, et al. Vitamin A deficiency promotes bronchial hyperreactivity in rats by altering muscarinic M(2) receptor function. Am J Physiol Lung Cell Mol Physiol. 2002;282(5):L1031-L1039.
62. Barker DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998;95(2):115-128.
63. Håland G, et al. Reduced lung function at birth and the risk of asthma at 10 years of age. N Engl J Med. 2006;355(16):1682-1689.
64. Demarini DM, Preston RJ. Smoking while pregnant: Transplacental mutagenesis of the fetus by tobacco smoke. JAMA. 2005;293(10):1264-1265.
65. Lü J, Qian J, Izvolsky KI, Cardoso WV. Global analysis of genes differentially expressed in branching and non-branching regions of the mouse embryonic lung. Dev Biol. 2004;273(2):418-435.
66. Quadro L, et al. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 1999;18(17):4633-4644.
67. Kotlikoff MI, et al. Methodologic advancements in the study of airway smooth muscle. J Allergy Clin Immunol. 2004;114(2 suppl):S18-S31.