Alterations in alveolar epithelium differentiation and vasculogenesis in lungs of LIF/IGF-I double deficient embryos

Developmental Dynamics

Volumn 235, Issue 8, 2006, Pages 2040-2050

  Moreno Barriuso, Nuria ^a   López Malpartida, Ana V ^a   De Pablo, Flora ^b   Pichel, José G ^a,c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c Salamanca Spain   (Spain)

Author keywords

Alveolum; Development; Differentiation; Epithelium; Insulin like growth factor; Knockout mice; Leukemia inhibitory factor; Lung; Proliferation; Vasculogenesis

Indexed keywords

AQUAPORIN 5; BROXURIDINE; CD31 ANTIGEN; CYCLINE; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SOMATOMEDIN C; THYROID TRANSCRIPTION FACTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO DEATH; ENZYME PHOSPHORYLATION; FETUS LUNG; GENOTYPE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LUNG ALVEOLUS CELL TYPE 1; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; LUNG HYPOPLASIA; MORPHOMETRICS; MOUSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY FAILURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; EPITHELIUM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN-LIKE GROWTH FACTOR I; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; LUNG; MICE; PHOSPHORYLATION; PROLIFERATING CELL NUCLEAR ANTIGEN; RNA, MESSENGER;

EID: 33747026685     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20842     Document Type: Article

References (65)

1. Aitola M, Carlsson P, Mahlapuu M, Enerback S, Pelto-Huikko M. 2000. Forkhead transcription factor FoxF2 is expressed in mesodermal tissues involved in epithelio-mesenchymal interactions. Dev Dyn 218:136-149.
2. Argetsinger LS, Hsu GW, Myers MG Jr, Billestrup N, White MF, Carter-Su C. 1995. Growth hormone, interferon-gamma, and leukemia inhibitory factor promoted tyrosyl phosphorylation of insulin receptor substrate-1. J Biol Chem 270:14685-14692.
3. Auernhammer CJ, Melmed S. 2000. Leukemia-inhibitory factor: neuroimmune modulator of endocrine function. Endocr Rev 21:313-345.
4. Bohinski RJ, Di Lauro R, Whitsett JA. 1994. The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol Cell Biol 14: 5671-5681.
5. Chinoy MR. 2003. Lung growth and development. Front Biosci 8:d392-415.
6. Coleman C, Zhao J, Gupta M, Buckley S, Tefft JD, Wuenschell CW, Minoo P, Anderson KD, Warburton D. 1998. Inhibition of vascular and epithelial differentiation in murine nitrofen-induced diaphragmatic hernia. Am J Physiol 274: L636-646.
7. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D, Carmeliet P. 2002. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8:702-710.
8. Costa RH, Kalinichenko W, Lim L. 2001. Transcription factors in mouse lung development and function. Am J Physiol Lung Cell Mol Physiol 280:L823-838.
9. De Pablo F, Banner LR, Patterson PH. 2000. IGF-I expression is decreased in LIF-deficient mice after peripheral nerve injury. Neuroreport 11:1365-1368.
10. Fernandez-Moreno C, Pichel JG, Chesnokova V, De Pablo F. 2004. Increased leptin and white adipose tissue hypoplasia are sexually dimorphic in Lif null/Igf-I haplo-insufficient mice. FEBS Lett 557:64-68.
11. Ferrell JE Jr. 1996. MAP kinases in mitogenesis and development. Curr Top Dev Biol 33:1-60.
12. Frankel SK, Moats-Staats BM, Cool CD, Wynes MW, Stiles AD, Riches DW. 2005. Human insulin-like growth factor-IA expression in transgenic mice promotes adenomatous hyperplasia but not pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 288:L805-812.
13. Frost RA, Nystrom GJ, Lang CH. 2002. Regulation of IGF-I mRNA and signal transducers and activators of transcription-3 and -5 (Stat-3 and -5) by GH in C2C12 myoblasts. Endocrinology 143:492-503.
14. Fukada K, Korsching S, Towle MF. 1997. Tissue-specific and ontogenetic regulation of LIF protein levels determined by quantitative enzyme immunoassay. Growth Factors 14:279-295.
15. Funaki H, Yamamoto T, Koyama Y, Kondo D, Yaoita E, Kawasaki K, Kobayashi H, Sawaguchi S, Abe H, Kihara I. 1998. Localization and expression of AQP5 in cornea, serous salivary glands, and pulmonary epithelial cells. Am J Physiol 275: C1151-1157.
16. Han RN, Post M, Tanswell AK, Lye SJ. 2003. Insulin-like growth factor-I receptor-mediated vasculogenesis/angiogenesis in human lung development. Am J Respir Cell Mol Biol 28:159-169.
17. Hellqvist M, Mahlapuu M, Samuelsson L, Enerback S, Carlsson P. 1996. Differential activation of lung-specific genes by two forkhead proteins, FREAC-1 and FREAC-2. J Biol Chem 271:4482-4490.
18. Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, LeRoith D, Senger DR, Smith LE. 2001. Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci USA 98:5804-5808.
19. Hwa V, Little B, Kofoed EM, Rosenfeld RG. 2004. Transcriptional regulation of insulin-like growth factor-I by interferon-gamma requires STAT-5b. J Biol Chem 279:2728-2736.
20. Ikeda K, Clark JC, Shaw-White JR, Stahlman MT, Boutell CJ, Whitsett JA. 1995. Gene structure and expression of human thyroid transcription factor-1 in respiratory epithelial cells. J Biol Chem 270: 8108-8114.
21. Inanlou MR, Kablar B. 2005a. Abnormal development of the intercostal muscles and the rib cage in Myf5-/- embryos leads to pulmonary hypoplasia. Dev Dyn 232: 43-54.
22. Inanlou MR, Kablar B. 2005b. Contractile activity of skeletal musculature involved in breathing is essential for normal lung cell differentiation, as revealed in Myf5-/-: MyoD-/- embryos. Dev Dyn 233:772-782.
23. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. 2000. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279:L600-607.
24. Kalina M, Mason RJ, Shannon JM. 1992. Surfactant protein C is expressed in alveolar type II cells but not in Clara cells of rat lung. Am J Respir Cell Mol Biol 6:594-600.
25. Kalinichenko VV, Lim L, Stolz DB, Shin B, Rausa FM, Clark J, Whitsett JA, Watkins SC, Costa RH. 2001. Defects in pulmonary vasculature and perinatal lung hemorrhage in mice heterozygous null for the Forkhead Box f1 transcription factor. Dev Biol 235:489-506.
26. Kauffman SL. 1975. Kinetics of pulmonary epithelial proliferation during prenatal growth of the mouse lung. Anat Rec 183: 393-403.
27. Klempt M, Hutchins AM, Gluckman PD, Skinner SJ. 1992. IGF binding protein-2 gene expression and the location of IGF-I and IGF-II in fetal rat lung. Development 115:765-772.
28. Kling DE, Lorenzo HK, Trbovich AM, Kinane TB, Donahoe PK, Schnitzer JJ. 2002. MEK-1/2 inhibition reduces branching morphogenesis and causes mesenchymal cell apoptosis in fetal rat lungs. Am J Physiol Lung Cell Mol Physiol 282:L370-378.
29. Knight DA, Lydell CP, Zhou D, Weir TD, Robert Schellenberg R, Bai TR. 1999. Leukemia inhibitory factor (LIF) and LIF receptor in human lung. Distribution and regulation of LIF release. Am J Respir Cell Mol Biol 20:834-841.
30. Lee GH, Nishimori H, Sasaki Y, Matsushita H, Kitagawa T, Tokino T. 2003. Analysis of lung tumorigenesis in chimeric mice indicates the Pulmonary adenoma resistance 2 (Par2) locus to operate in the tumor-initiation stage in a cell-autonomous manner: detection of polymorphisms in the Poli gene as a candidate for Par2. Oncogene 22:2374-2382.
31. Lee JH, Johnson PR, Roth M, Hunt NH, Black JL. 2001. ERK activation and mitogenesis in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 280:L1019-1029.
32. Lim L, Kalinichenko W, Whitsett JA, Costa RH. 2002. Fusion of lung lobes and vessels in mouse embryos heterozygous for the forkhead box f1 targeted allele. Am J Physiol Lung Cell Mol Physiol 282: L1012-1022.
33. Liu C, Glasser SW, Wan H, Whitsett JA. 2002. GATA-6 and thyroid transcription factor-1 directly interact and regulate surfactant protein-C gene expression. J Biol Chem 277:4519-4525.
34. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59-72.
35. Lopez-Lopez C, LeRoith D, Torres-Aleman I. 2004. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci USA 101: 9833-9838.
36. Mahlapuu M, Enerback S, Carlsson P. 2001. Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development 128:2397-2406.
37. Mendelson CR. 2000. Role of transcription factors in fetal lung development and surfactant protein gene expression. Annu Rev Physiol 62:875-915.
38. Metcalf D. 2003. The unsolved enigmas of leukemia inhibitory factor. Stem Cells 21:5-14.
39. Metcalf D, Willson TA, Hilton DJ, Di Rago L, Mifsud S. 1995. Production of hematopoietic regulatory factors in cultures of adult and fetal mouse organs: measurement by specific bioassays. Leukemia 9: 1556-1564.
40. Muglia LJ, Bae DS, Brown TT, Vogt SK, Alvarez JG, Sunday ME, Majzoub JA. 1999. Proliferation and differentiation defects during lung development in corticotropin-releasing hormone-deficient mice. Am J Respir Cell Mol Biol 20:181-188.
41. Oh H, Fujio Y, Kunisada K, Hirota H, Matsui H, Kishimoto T, Yamauchi-Takihara K. 1998. Activation of phosphatidylinositol 3-kinase through glycoprotein 130 induces protein kinase B and p70 S6 kinase phosphorylation in cardiac myocytes. J Biol Chem 273:9703-9710.
42. Park JI, Strock CJ, Ball DW, Nelkin BD. 2003. The Ras/Raf/MEK/ extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway. Mol Cell Biol 23:543-554.
43. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
44. Pichel JG, Fernandez-Moreno C, Vicario-Abejon C, Testillano PS, Patterson PH, De Pablo F. 2003. Developmental cooperation of leukemia inhibitory factor and insulin-like growth factor I in mice is tissue-specific and essential for lung maturation involving the transcription factors Sp3 and TTF-1. Mech Dev 120:349-361.
45. Powell-Braxton L, Hollingshead P, Warburton C, Dowd M, Pitts-Meek S, Dalton D, Gillett N, Stewart TA. 1993. IGF-I is required for normal embryonic growth in mice. Genes Dev 7:2609-2617.
46. Ramirez MI, Rishi AK, Cao YX, Williams MC. 1997. TGT3, thyroid transcription factor I, and Sp1 elements regulate transcriptional activity of the 1.3-kilobase pair promoter of T1alpha, a lung alveolar type I cell gene. J Biol Chem 272:26285-26294.
47. Ramirez MI, Millien G, Hinds A, Cao Y, Seldin DC, Williams MC. 2003. T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev Biol 256:61-72.
48. Retsch-Bogart GZ, Moats-Staats BM, Howard K, D'Ercole AJ, Stiles AD. 1996. Cellular localization of messenger RNAs for insulin-like growth factors (IGFs), their receptors and binding proteins during fetal rat lung development. Am J Respir Cell Mol Biol 14:61-69.
49. Rishi AK, Joyce-Brady M, Fisher J, Dobbs LG, Floros J, VanderSpek J, Brody JS, Williams MC. 1995. Cloning, characterization, and development expression of a rat lung alveolar type I cell gene in embryonic endodermal and neural derivatives. Dev Biol 167:294-306.
50. Robertson M, Chambers I, Rathjen P, Nichols J, Smith A. 1993. Expression of alternative forms of differentiation inhibiting activity (DIA/LIF) during murine embryogenesis and in neonatal and adult tissues. Dev Genet 14:165-173.
51. Ruberte J, Ayuso E, Navarro M, Carretero A, Nacher V, Haurigot V, George M, Llombart C, Casellas A, Costa C, Bosch A, Bosch F. 2004. Increased ocular levels of IGF-1 in transgenic mice lead to diabetes-like eye disease. J Clin Invest 113: 1149-1157.
52. Schuller AG, van Neck JW, Beukenholdt RW, Zwarthoff EC, Drop SL. 1995. IGF, type I IGF receptor and IGF-binding protein mRNA expression in the developing mouse lung. J Mol Endocrinol 14:349-355.
53. Shapiro P, Absher PM, Posada JP, Evans JN. 1997. Activation of ERK and JNK1 MAP kinases in cultured lung tissue. Am J Physiol 273:L459-467.
54. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359:76-79.
55. Thrane EV, Schwarze PE, Thoresen GH, Lag M, Refsnes M. 2001. Persistent versus transient map kinase (ERK) activation in the proliferation of lung epithelial type 2 cells. Exp Lung Res 27:387-400.
56. Turnley AM, Bartlett PF. 2000. Cytokines that signal through the leukemia inhibitory factor receptor-beta complex in the nervous system. J Neurochem 74:889-899.
57. Varela-Nieto I, Chowen JA, editors. 2005. The growth hormone/Insulin-like growth factor axis during development. Adv Exp Med Biol, vol. 567. Springer. 410 p.
58. Vicario-Abejon C, Fernandez-Moreno C, Pichel JG, De Pablo F. 2004. Mice lacking IGF-I and LIF have motoneuron deficits in brain stem nuclei. Neuroreport 15:2769-2772.
59. Wang J, Zhou J, Powell-Braxton L, Bondy C. 1999. Effects of Igf1 gene deletion on postnatal growth patterns. Endocrinology 140:3391-3394.
60. Wang J, Chen Q, Corne J, Zhu Z, Lee CG, Bhandari V, Homer RJ, Elias JA. 2003. Pulmonary expression of leukemia inhibitory factor induces B cell hyperplasia and confers protection in hyperoxia. J Biol Chem 278:31226-31232.
61. Warburton D, Schwarz M, Tefft D, Flores-Delgado G, Anderson KD, Cardoso WV. 2000. The molecular basis of lung morphogenesis. Mech Dev 92:55-81.
62. Williams MC. 2003. Alveolar type I cells: molecular phenotype and development. Annu Rev Physiol 65:669-695.
63. Yang L, Lian X, Cowen A, Xu H, Du H, Yan C. 2004. Synergy between signal transducer and activator of transcription 3 and retinoic acid receptor-alpha in regulation of the surfactant protein B gene in the lung. Mol Endocrinol 18:1520-1532.
64. Zhou L, Lim L, Costa RH, Whitsett JA. 1996. Thyroid transcription factor-1, hepatocyte nuclear factor-3beta, surfactant protein B, C, and Clara cell secretory protein in developing mouse lung. J Histochem Cytochem 44:1183-1193.
65. Zong CS, Chan J, Levy DE, Horvath C, Sadowski HB, Wang LH. 2000. Mechanism of STAT3 activation by insulin-like growth factor I receptor. J Biol Chem 275:15099-15105.