Respiratory failure due to differentiation arrest and expansion of alveolar cells following lung-specific loss of the transcription factor C/EBPα in mice

Molecular and Cellular Biology

Volumn 26, Issue 3, 2006, Pages 1109-1123

  Bassères, Daniela S ^a,d   Levantini, Elena ^a   Ji, Hongbin ^a   Monti, Stefano ^b   Elf, Shannon ^a   Dayaram, Tajhal ^a   Fenyus, Maris ^a   Kocher, Olivier ^a   Golub, Todd ^b   Wong, Kwok Kin ^a   Halmos, Balazs ^a,e   Tenen, Daniel G ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD INSTITUTES OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; DOXYCYCLINE; GENOMIC DNA; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENOTYPE; HISTOPATHOLOGY; LUNG ALVEOLUS CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY FAILURE; RNA SEQUENCE; SOUTHERN BLOTTING; TISSUE SPECIFICITY;

ANIMALS; APOPTOSIS; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELL DIFFERENTIATION; CELL PROLIFERATION; EPITHELIUM; GENE DELETION; GENE EXPRESSION PROFILING; LUNG; MALE; MICE; MICE, MUTANT STRAINS; PULMONARY ALVEOLI; RESPIRATORY INSUFFICIENCY; SEQUENCE DELETION;

ANIMALIA;

EID: 31344444129     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.3.1109-1123.2006     Document Type: Article

References (78)

1. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57:289-300.
2. Bennett, C. N., S. E. Ross, K. A. Longo, L. Bajnok, N. Hemati, K. W. Johnson, S. D. Harrison, and O. A. MacDougald. 2002. Regulation of Wnt signaling during adipogenesis. J. Biol. Chem. 277:30998-31004.
3. Bigelow, R. L., N. S. Cbari, A. B. Unden, K. B. Spurgers, S. Lee, D. R. Roop, R. Toftgard, and T. J. McDonnell. 2004. Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J. Biol. Chem. 279:1197-1205.
4. Bourbon, J. R., M. Rieutort, M. J. Engle, and P. M. Farrell. 1982. Utilization of glycogen for phospholipid synthesis in fetal rat lung. Biochim. Biophys. Acta 712:382-389.
5. Breathnach, O. S., B. Freidlin, B. Conley, M. R. Green, D. H. Johnson, D. R. Gandara, M. O'Connell, F. A. Shepherd, and B. E. Johnson. 2001. Twenty-two years of phase III trials for patients with advanced non-small-cell lung cancer: sobering results. J. Clin. Oncol. 19:1734-1742.
6. Cassel, T. N., J. A. Gustafsson, and M. Nord. 2000. CYP2B1 is regulated by C/EBP alpha and C/EBP delta inlung epithelial cells. Mol. Cell. Biol. Res. Commun. 3:42-47.
7. Cassel, T. N., L. Nordlund-Moller, O. Andersson, J. A. Gustafsson, and M. Nord. 2000. C/EBPalpha and C/EBPdelta activate the clara cell secretory protein gene through interaction with two adjacent C/EBP-binding sites. Am. J. Respir. Cell Mol. Biol. 22:469-480.
8. Clements, J. A., and M. E. Avery. 1998. Lung surfactant and neonatal respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 157:559-566.
9. Crosson, S. M., A. Khan, J. Printen, J. E. Pessin, and A. R. Saltiel. 2003. PTG gene deletion causes impaired glycogen synthesis and developmental insulin resistance. J. Clin. Investig. 111:1423-1432.
10. Dahmane, N., J. Lee, P. Robins, P. Heller, and A. Altaba. 1997. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 389:876-881.
11. Dang, T. P., S. Eichenberger, A. Gonzalez, S. Olson, and D. P. Carbone. 2003. Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene 22:1988-1997.
12. Danto, S. I., J. M. Shannon, Z. Borok, S. M. Zabski, and E. D. Crandall. 1995. Reversible transdifferentiation of alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 12:497-502.
13. Edwards, Y. S. 2001. Stretch stimulation: its effects on alveolar type II cell function in the lung. Comp. Biochem. Physiol. A 129:245-260.
14. Flodby, P., C. Barlow, H. Kylefjord, L. Hrlund-Richter, and K. G. Xanthopoulos. 1996. Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein alpha. J. Biol. Chem. 271:24753-24760.
15. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
16. Gery, S., S. Tanosaki, S. Bose, N. Bose, J. Vadgama, and H. P. Koeffler. 2005. Down-regulation and growth inhibitory role of C/EBPalpha in breast cancer. Clin. Cancer Res. 11:3184-3190.
17. Gombart, A. F., W. K. Hofmann, S. Kawano, S. Takeuchi, U. Krug, S. H. Kwok, R. J. Larsen, H. Asou, C. W. Miller, D. Hoelzer, and H. P. Koeffler. 2002. Mutations in the gene encoding the transcription factor CCAAT/ enhancer binding protein alpha in myelodysplastic syndromes and acute myeloid leukemias. Blood 99:1332-1340.
18. Greenberg, C. C., K. N. Meredith, L. Yan, and M. J. Brady. 2003. Protein targeting to glycogen overexpression results in the specific enhancement of glycogen storage in 3T3-L1 adipocytes. J. Biol. Chem. 278:30835-30842.
19. Greene, K. E., J. R. Wright, K. P. Steinberg, J. T. Ruzinski, E. Caldwell, W. B. Wong, W. Hull, J. A. Whitsett, T. Akino, Y. Kuroki, H. Nagae, L. D. Hudson, and T. R. Martin. 1999. Serial changes in surfactant-associated proteins in lung and serum before and after onset of AIDS. Am. J. Respir. Crit. Care Med. 160:1843-1850.
20. Guthmann, F., C. Hohoff, H. Fechner, P. Humbert, T. Borchers, F. Spener, and B. Rustow. 1998. Expression of fatty-acid-binding proteins in cells involved in lung-specific lipid metabolism. Eur. J. Biochem. 253:430-436.
21. Hallman, M., R. Haataja, and R. Marttila. 2002. Surfactant proteins and genetic predisposition to respiratory distress syndrome. Semin. Perinatol. 26:450-460.
22. Halmos, B., D. S. Basseres, S. Monti, F. D'Alo, T. Dayaram, K. Ferenczi, B. J. Wouters, C. S. Huettner, T. R. Golub, and D. G. Tenen. 2004. A transcriptional profiling study of CCAAT/enhancer binding protein targets identifies hepatocyte nuclear factor 3 beta as a novel tumor suppressor in lung cancer. Cancer Res. 64:4137-4147.
23. Halmos, B., C. S. Huettner, O. Kocher, K. Ferenczi, D. D. Karp, and D. G. Tenen. 2002. Down-regulation and antiproliferative role of C/EBPalpha in lung cancer. Cancer Res. 62:528-534.
24. He, Y., and E. Crouch. 2002. Surfactant protein D gene regulation. Interactions among the conserved CCAAT/enhancer-binding protein elements. J. Biol. Chem. 277:19530-19537.
25. Heath, V., H. C. Suh, M. Holman, K. Renn, J. M. Gooya, S. Parkin, K. D. Klarmann, M. Ortiz, P. Johnson, and J. Keller. 2004. C/EBPalpha deficiency results in hyperproliferation of hematopoietic progenitor cells and disrupts macrophage development in vitro and in vivo. Blood 104:1639-1647.
26. Hendricks-Taylor, L. R., and G, J. Darlington. 1995. Inhibition of cell proliferation by C/EBP alpha occurs in many cell types, does not require the presence of p53 or Rb, and is not affected by large T-antigen. Nucleic Acids Res. 23:4726-4733.
27. Iakova, P., S. S. Awad, and N. A. Timchenko. 2003. Aging reduces proliferative capacities of liver by switching pathways of C/EBPalpha growth arrest. Cell 113:495-506.
28. Jemal, A., V. E. Cokkinides, O. Shafey, and M. J. Thun. 2003. Lung cancer trends in young adults: an early indicator of progress in tobacco control (United States). Cancer Causes Control 14:579-585.
29. Johansen, L. M., A. Iwama, T. A. Lodie, K. Sasaki, D. W. Felsher, T. R. Golub, and D. G. Tenen. 2001. c-Myc is a critical target for C/EBPalpha in granulopoiesis. Mol. Cell. Biol. 21:3789-3806.
30. Lambert, J. M., Q. T. Lambert, G. W. Reuther, A. Malliri, D. P. Siderovski, J. Sondek, J. G. Collard, and C. J. Der. 2002. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat. Cell Biol. 4:621-625.
31. Li, F., E. Rosenberg, C. I. Smith, K. Notarfrancesco, S. R. Reisher, H. Shuman, and S. I. Feinstein. 1995. Correlation of expression of transcription factor C/EBP alpha and surfactant protein genes in lung cells. Am. J. Physiol. 269:L241-L247.
32. Lu, T., L. G. Burdelya, S. M. Swiatkowski, A. D. Boiko, P. H. Howe, G. R. Stark, and A. V. Gudkov. 2004. Secreted transforming growth factor beta2 activates NF-kappaB, blocks apoptosis, and is essential for the survival of some tumor cells. Proc. Natl. Acad. Sci. USA 101:7112-7117.
33. Mahloogi, H., D. E. Bassi, and A. J. Klein-Szanto. 2002. Malignant conversion of non-tumorigenic murine skin keratinocytes overexpressing PACE4. Carcinogenesis 23:565-572.
34. Malliri, A., R. A. van der Kammen, K. Clark, M. van der Valk, F. Michaels, and J. G. Collard. 2002. Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 417:867-871.
35. Mason, R. J., B. Gao, T. Pan, X. Jiang, M. Eckart, and S. Neben. 2002. Role of keratinocyte growth factor in regulating lipogenesis in alveolar type II cells: a gene-profiling approach. Chest 121:778.
36. Mason, R. J., T. Pan, K. E. Edeen, L. D. Nielsen, F. Zhang, M. Longphre, M. R. Eckart, and S. Neben. 2003. Keratinocyte growth factor and the transcription factors C/EBP alpha, C/EBP delta, and SREBP-1c regulate fatty acid synthesis in alveolar type II cells. J. Clin. Investig. 112:244-255.
37. Montgomery, R. K., E. H. Rings, J. F. Thompson, C. C. Schuijt, K. M. Aras, V. J. Wielenga, M. J. Kothe, H. A. Buller, and R. J. Grand. 1997. Increased C/EBP in fetal rat small intestine precedes initiation of differentiation marker mRNA synthesis. Am. J. Physiol. 272:G534-G544.
38. Muller, C., C. F. Calkhoven, X. Sha, and A. Leutz. 2004. The CCAAT enhancer-binding protein alpha (C/EBPalpha) requires a SWI/SNF complex for proliferation arrest. J. Biol. Chem. 279:7353-7358.
39. Nerlov, C. 2004. C/EBPalpha mutations in acute myeloid leukaemias. Nat. Rev. Cancer 4:394-400.
40. Nilsson, M., A. B. Unden, D. Krause, U. Malmqwist, K. Raza, P. G. Zaphiropoulos, and R. Toftgard. 2000. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl. Acad. Sci. USA 97:3438-3443.
41. Nord, M., M. Lag, T. N. Cassel, M. Randmark, R. Becher, H. J. Barnes, P. E. Schwarze, J. A. Gustafsson, and J. Lund. 1998. Regulation of CCSP (PCB-BP/uteroglobin) expression in primary cultures of lung cells: involvement of C/EBP. DNA Cell Biol. 17:481-492.
42. Oh, H. S., and R. C. Smart. 1998. Expression of CCAAT/enhancer binding proteins (C/EBP) is associated with squamous differentiation in epidermis and isolated primary keratinocytes and is altered in skin neoplasms. J. Investig. Dermatol. 110:939-945.
43. Okubo, T., and B. L. Hogan. 2004. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3:11.
44. Pabst, T., B. U. Mueller, N. Harakawa, C. Schoch, T. Haferlach, G. Behre, W. Hiddemann, D. E. Zhang, and D. G. Tenen. 2001. AML1-ETO down-regulates the granulocytic differentiation factor C/EBPalpha in t(8;21) myeloid leukemia. Nat. Med. 7:444-451.
45. Pabst, T., B. U. Mueller, P. Zhang, H. S. Radomska, S. Narravula, S. Schnittger, G. Behre, W. Hiddemann, and D. G. Tenen. 2001. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat. Genet. 27:263-270.
46. Perl, A. K., S. E. Wert, A. Nagy, C. G. Lobe, and J. A. Whitsett. 2002. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc. Natl. Acad. Sci. USA 99:10482-10487.
47. Perrotti, D., V. Cesi, R. Trotta, C. Guerzoni, G. Santilli, K. Campbell, A. Iervolino, F. Condorelli, C. Gambacorti-Passerini, M. A. Caligiuri, and B. Calabretta. 2002. BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nat. Genet. 30:48-58.
48. Porse, B. T., T. A. Pedersen, X. Xu, B. Lindberg, U. M. Wewer, L. Friis-Hansen, and C. Nerlov. 2001. E2F repression by C/EBPalpha is required for adipogenesis and granulopoiesis in vivo. Cell 107:247-258.
49. Printen, J. A., M. J. Brady, and A. R. Saltiel. 1997. PTG, a protein phosphatase 1-binding protein with a role in glycogen metabolism. Science 275: 1475-1478.
50. Ridsdale, R., and M. Post. 2004. Surfactant lipid synthesis and lamellar body formation in glycogen-laden type II cells. Am. J. Physiol. Lung Cell Mol. Physiol. 287:L743-L751.
51. Rosen, E. D., C. H. Hsu, X. Wang, S. Sakai, M. W. Freeman, F. J. Gonzalez, and B. M. Spiegelman. 2002. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. 16:22-26.
52. Rosenberg, E., F. Li, S. R. Reisher, M. Wang, L. W. Gonzales, J. R. Ewing, S. Malek, P. L. Ballard, K. Notarfrancesco, H. Shuman, and S. I. Feinstein. 2002. Members of the C/EBP transcription factor family stimulate expression of the human and rat surfactant protein A (SP-A) genes. Biochim. Biophys. Acta 1575:82-90.
53. Ross, D. A., P. K. Rao, and T. Kadesch. 2004. Dual roles for the Notch target gene Hes-1 in the differentiation of 3T3-L1 preadipocytes. Mol. Cell. Biol. 24:3505-3513.
54. Ross, S. E., N. Hemati, K. A. Longo, C. N. Bennett, P. C. Lucas, R. L. Erickson, and O. A. MacDougald. 2000. Inhibition of adipogenesis by Wnt signaling. Science 289:950-953.
55. Russell, L., and D. R. Forsdyke. 1991. A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated. DNA Cell Biol. 10:581-591.
56. Scholzen, T., and J. Gerdes. 2000. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182:311-322.
57. Shim, M., K. L. Powers, S. J. Ewing, S. Zhu, and R C. Smart. 2005. Diminished expression of C/EBPalpha in skin carcinomas is linked to oncogenic Ras and reexpression of C/EBPalpha in carcinoma cells inhibits proliferation. Cancer Res. 65:861-867.
58. Siderovski, D. P., S. P. Heximer, and D. R. Forsdyke. 1994. A human gene encoding a putative basic helix-loop-helix phosphoprotein whose mRNA increases rapidly in cycloheximide-treated blood mononuclear cells. DNA Cell Biol. 13:125-147.
59. Slomiany, B. A., K. L. D'Arigo, M. M. Kelly, and D. T. Kurtz. 2000. C/EBPalpha inhibits cell growth via direct repression of E2F-DP-mediated transcription. Mol. Cell. Biol. 20:5986-5997.
60. Slonim, D. K., P. Tamayo, J. P. Mesirov, T. R. Golub, and E. S. Lander. 2000. Class prediction and discovery using gene expression data, p. 263-272. In R. Shamir, S. Miyano, S. Istrail, P. Pevzner, and M. Waterman (ed.), Proceedings of the Fourth Annual Intelnational Conference on Research in Computational Molecular Biology. (RECOMB), Tokyo, Japan. ACM Press, New York, N.Y.
61. Sugahara, K., K. I. Kama, T. Kimura, K. Sano, G. J. Darlington, T. Akiba, and M. Takiguchi. 2001. Mice lacking CCAAT/enhancer-binding protein-alpha show hyperproliferation of alveolar type II cells and increased surfactant protein mRNAs. Cell Tissue Res. 306:57-63.
62. Sutherland, L. M., Y. S. Edwards, and A. W. Murray. 2001. Alveolar type II cell apoptosis. Comp. Biochem. Physiol. A 129:267-285.
63. Takai, N., N. Kawamata, C. S. Walsh, S. Gery, J. C. Desmond, S. Whittaker, J. W. Said, L. M. Popoviciu, P. A. Jones, I. Miyakawa, and H. P. Koeffler. 2005. Discovery of epigenetically masked tumor suppressor genes in endometrial cancer. Mol. Cancer Res. 3:261-269.
64. Tanimizu, N., and A. Miyajima. 2004. Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J. Cell Sci. 117:3165-3174.
65. Tichelaar, J. W., W. Lu, and J. A. Whitsett. 2000. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J. Biol. Chem. 275:11858-11864.
66. Timcbenko, N. A., T. E. Harris, M. Wilde, T. A. Bilyeu, B. L. Burgess-Beusse, M. J. Finegold, and G. J. Darlington. 1997. CCAAT/enhancer binding protein alpha regulates p21 protein and hepatocyte proliferation in newborn mice. Mol. Cell. Biol. 17:7353-7361.
67. Uhal, B. D. 1997. Cell cycle kinetics in the alveolar epithelium. Am. J. Physiol. 272:L1031-L1045.
68. Wan, H., Y. Xu, M. Ikegami, M. T. Stahlman, K. H. Kaestner, S. L. Ang, and J. A. Whitsett. 2004. Foxa2 is required for transition to air breathing at birth. Proc. Natl. Acad. Sci. USA 101:14449-14454.
69. Wang, G. L., P. Iakova, M. Wilde, S. Awad, and N. A. Timchenko. 2004. Liver tumors escape negative control of proliferation via PI3K/Akt-mediated block of C/EBP alpha growth inhibitory activity. Genes Dev. 18:912-925.
70. Wang, H., P. Iakova, M. Wilde, A. WeIm, T. Goode, W. J. Roesler, and N. A. Timchenko. 2001. C/EBPalpha arrests cell proliferation through direct inhibition of Cdk2 and Cdk4. Mol. Cell 8:817-828.
71. Wang, N. D., M. J. Finegold, A. Bradley, C. N. Ou, S. V. Abdelsayed, M. D. Wilde, L. R. Taylor, D. R. Wilson, and G. J. Darlington. 1995. Impaired energy homeostasis in C/EBP alpha knockout mice. Science 269:1108-1112.
72. Williams, M. C. 2003. Alveolar type I cells: molecular phenotype and development. Annu. Rev. Physiol. 65:669-695.
73. Williams, M. C., and R. J. Mason. 1977. Development of the type II cell in the fetal rat lung. Am. Rev. Respir. Dis. 115:37-47.
74. Young, S. L., E. K. Fram, C. L. Spain, and E. W. Larson. 1991. Development of type II pneumocytes in rat lung. Am. J. Physiol. 260:L113-L122.
75. Zhang, D. E., P. Zhang, N. D. Wang, C. J. Hetherington, G. J. Darlington, and D. G. Tenen. 1997. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc. Natl. Acad. Sci. USA 94:569-574.
76. Zhang, F., T. Pan, L. D. Nielsen, and R. J. Mason. 2004. Lipogenesis in fetal rat lung: importance of C/EBPalpha, SREBP-1c, and stearoyl-CoA desaturase. Am. J. Respir. Cell Mol. Biol. 30:174-183.
77. Zhang, P., J. Iwasaki-Arai, H. Iwasaki, M. L. Fenyus, T. Dayaram, B. M. Owens, H. Shigematsu, E. Levantini, C. S. Huettner, J. A. Lekstrom-Himes, K. Akashi, and D. G. Tenen. 2004. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity 21:853-863.
78. Zheng, R., A. D. Friedman, M. Levis, L. Li, E. G. Weir, and D. Small. 2004. Internal tandem duplication mutation of FLT3 blocks myeloid differentiation through suppression of C/EBPalpha expression. Blood 103:1883-1890.