Advertisement

Decreased surfactant protein B expression in mice derived completely from embryonic stem cells

  • Shumin Gao
  • Xiaohui Wen
  • Rongrong Yang
  • Keqian Di
  • Jun Tong
  • Xiangyun Li
Article

Abstract

ES mice that are derived completely from embryonic stem (ES) cells can be obtained by tetraploid embryo complementation. Many neonate ES mice die because of respiratory distress, but it is not clear what contributes to the phenomenon. Using five microsatellite DNA markers, we confirmed that our ES mice were completely derived from ES cells and contained no tetraploid component. The neonatal ES mice that exhibited respiratory distress were tested for surfactant protein B (SP-B) expression by Western blotting. These mice had no SP-B expression, and even apparently healthy adult ES mice had decreased SP-B levels and aberrant SP-B phenotypes. These data suggest that the expression of SP-B protein is an important factor in the survival of ES mice to term and adulthood.

Keywords

ES mice Respiratory distress Pulmonary surfactant protein B Tetraploid embryo complementation 

Notes

Acknowledgements

We thank Prof. Zhijie Chang for kindly providing the BCATM Protein Assay Kit (PIERCE) and assisting in the Western blotting. We also thank Dr. Man Hu, Dr. Yuzhong Ma, Mrs. Xianrui Gu, Mrs. Rongyan Zhou, Mr. Jie Tang, and Mr. Lei Ju for the many suggestions and help. In particular, we would like to thanks Mrs. Eileen Rattner for her critical remarks and editing this manuscript. This work was supported by the National Natural Science Foundation of China (No.30571336) and the President Foundation from Agricultural University of Hebei.

References

  1. Clark, J.C.; Wert, S.E.; Bachurski, C.J.; Stahlman, M.T.; Stripp, B.R.; Weaver, T.E.; Whitsett, J.A. Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice. Proc. Natl. Acad. Sci. USA 92:7794–7798; 1995PubMedCrossRefGoogle Scholar
  2. Dean, W.; Bowden, L.; Aitchison, A.; Klose, J.; Moore, T.; Meneses, J.J.; Reik, W.; Feil, R. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 125:2273–2282; 1998PubMedGoogle Scholar
  3. Deng, T.; Kuang, Y.; Zhang, D.; Wang, L.; Sun, R.; Xu, G.; Wang, Z.; Fei, J. Disruption of imprinting and aberrant embryo development in completely inbred embryonic stem cell-derived mice. Dev. Growth Differ. 49:603–610; 2007PubMedCrossRefGoogle Scholar
  4. Eakin, G.S.; Hadjantonakis, A.K.; Papaioannou, V.E.; Behringer, R.R. Developmental potential and behavior of tetraploid cells in the mouse embryo. Dev. Biol. 288:150–159; 2005PubMedCrossRefGoogle Scholar
  5. Eggan, K.; Akutsu, H.; Loring, J.; Jackson-Grusby, L.; Klemm, M.; Rideout, W.M. 3rd; Yanagimachi, R.; Jaenisch, R.; Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc. Natl. Acad. Sci. USA 98:5949–5951; 2001CrossRefGoogle Scholar
  6. Fisher, J.H.; Sheftelyevich, V.; Ho, Y.S.; Fligiel, S.; McCormack, F.X.; Korfhagen, T.R.; Whitsett, J.A.; Ikegami, M. Pulmonary-specific expression of SP-D corrects pulmonary lipid accumulation in SP-D gene-targeted mice. Am. J. Physiol. Lung. Cell. Mol. Physiol. 278: L365–L373; 2000PubMedGoogle Scholar
  7. Floros, J.; Thomas, N.J.; Liu, W.; Papagaroufalis, C.; Xanthou, M.; Pereira, S.; Fan, R.; Guo, X.; Diangelo, S.; Pavlovic, J. Family-based association tests suggest linkage between surfactant protein B (SP-B) (and flanking region) and respiratory distress syndrome (RDS): SP-B haplotypes and alleles from SP-B-linked loci are risk factors for RDS. Pediatr. Res. 59:616–621, 2006PubMedCrossRefGoogle Scholar
  8. Glasser, S.W.; Burhans, M.S.; Korfhagen, T.R.; Na, C.L.; Sly, P.D.; Ross, G.F.; Ikegami, M.; Whitsett, J.A.; Altered stability of pulmonary surfactant in SP-C-deficient mice. Proc. Natl. Acad. Sci. USA 98:6366–6371; 2001PubMedCrossRefGoogle Scholar
  9. Glasser, S.W.; Detmer, E.A.; Ikegami, M.; Na, C.L.; Stahlman, M.T.; Whitsett, J.A. Pneumonitis and emphysema in SP-C gene targeted mice. J. Biol. Chem. 278:14291–14298; 2003PubMedCrossRefGoogle Scholar
  10. Goerke, J. Pulmonary surfactant: functions and molecular composition. Biochim. Biophys. Acta. 1408:79–89; 1998PubMedGoogle Scholar
  11. Humpherys, D.; Eggan, K.; Akutsu, H.; Friedman, A.; Hochedlinger, K.; Yanagimachi, R.; Lander, E.S.; Golub, T.R.; Jaenisch, R. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc. Natl. Acad. Sci. USA 99:12889–12894; 2002PubMedCrossRefGoogle Scholar
  12. Humpherys, D.; Eggan, K.; Akutsu, H.; Hochedlinger, K.; Rideout, W.M. 3rd; Biniszkiewicz, D.; Yanagimachi, R.; Jaenisch, R. Epigenetic instability in ES cells and cloned mice. Science 293:95–97; 2001PubMedCrossRefGoogle Scholar
  13. Ikegami, M.; Korfhagen, T.R.; Whitsett, J.A.; Bruno, M.D.; Wert, S.E.; Wada, K.; Jobe, A.H. Characteristics of surfactant from SP-A-deficient mice. Am. J. Physiol. 275:L247–L254; 1998PubMedGoogle Scholar
  14. Ikegami, M.; Whitsett, J.A.; Jobe, A.; Ross, G.; Fisher, J.; Korfhagen, T. Surfactant metabolism in SP-D gene-targeted mice. Am. J. Physiol. Lung Cell Mol. Physiol. 279:L468–L476; 2000PubMedGoogle Scholar
  15. Inoue, K.; Kohda, T.; Lee, J.; Ogonuki, N.; Mochida, K.; Noguchi, Y.; Tanemura, K.; Kaneko-Ishino, T.; Ishino, F.; Ogura, A. Faithful expression of imprinted genes in cloned mice. Science 295:297; 2002PubMedCrossRefGoogle Scholar
  16. James, R.M.; Klerkx, A.H.; Keighren, M.; Flockhart, J.H.; West, J.D. Restricted distribution of tetraploid cells in mouse tetraploid–diploid chimaeras. Dev. Biol. 167:213–226; 1995PubMedCrossRefGoogle Scholar
  17. Korfhagen, T.R.; Bruno, M.D.; Ross, G.F.; Huelsman, K.M.; Ikegami, M.; Jobe, A.H.; Wert, S.E.; Stripp, B.R.; Morris, R.E.; Glasser, S.W.; Bachurski, C.J.; Iwamoto, H.S.; Whitsett, J.A. Altered surfactant function and structure in SP-A gene targeted mice. Proc. Natl. Acad. Sci. USA 93:9594–9599; 1996PubMedCrossRefGoogle Scholar
  18. Li, X.Y.; Jia, Q.; Di, K.Q.; Gao, S.M.; Wen, X.H.; Zhou, R.Y.; Wei, W.; Wang, L.Z. Passage number affects the pluripotency of mouse embryonic stem cells as judged by tetraploid embryo aggregation. Cell Tissue Res. 327:607–614; 2007PubMedCrossRefGoogle Scholar
  19. Li, X.Y.; Yu, Y.S.; Wei, W.; Yong, J.; Yang, J.; You, J.F.; Xiong, X.R.; Qing, T.T.; Deng, H.K. Simple and efficient production of mice derived from embryonic stem cells aggregated with tetraploid embryos. Mol. Reprod. Dev. 71:154–158; 2005PubMedCrossRefGoogle Scholar
  20. Melton, K.R.; Nesslein, L.L.; kegami, M.; Tichelaar, J.W.; Clark, J.C.; Whitsett, J.A.; Weaver, T.E. SP-B deficiency causes respiratory failure in adult mice. Am. J. Physiol. Lung Cell Mol. Physiol. 285:L543–L549; 2003PubMedGoogle Scholar
  21. Nagy, A.; Gócza, E.; Diaz, E.M.; Prideaux, V.R.; Iványi, E.; Markkula, M.; Rossant, J. Embryonic stem cells alone are able to support fetal development in the mouse. Development 110(3):815–21; 1990PubMedGoogle Scholar
  22. Nagy, A.; Rossant, J.; Nagy, R.; Abramow-Newerly, W.; Roder, J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90:8424–8428; 1993PubMedCrossRefGoogle Scholar
  23. Nesslein, L.L.; Melton, K.R.; Ikegami, M.; Na, C.L.; Wert, S.E.; Rice, W.R.; Whitsett, J.A.; Weaver, T.E. Partial SP-B deficiency perturbs lung function and causes air space abnormalities. Am. J. Physiol. Lung Cell Mol. Physiol. 288:L1154–L1161; 2005PubMedCrossRefGoogle Scholar
  24. Schumacher, A.; Doerfler, W. Influence of in vitro manipulation on the stability of methylation patterns in the Snurf/Snrpn-imprinting region in mouse embryonic stem cells. Nucleic. Acids. Res. 32:1566–1576; 2004PubMedCrossRefGoogle Scholar
  25. Schwenk, F.; Zevnik, B.; Bruning, J.; Rohl, M.; Willuweit, A.; Rode, A.; Hennek, T.; Kauselmann, G.; Jaenisch, R.; Kuhn, R. Hybrid embryonic stem cell-derived tetraploid mice show apparently normal morphological, physiological, and neurological characteristics. Mol. Cell Biol. 23:3982–3989; 2003PubMedCrossRefGoogle Scholar
  26. Sui, L.; Cheng, L.N.; Akinbi, H.T.; Apsley, K.S.; Whitsett, J.A.; Weaver, T.E. Surfactant protein B (SP-B) −/− mice are rescued by restoration of SP-B expression in alveolar type II cells but not Clara cells. J. Biol. Chem. 274:19168–19174; 1999CrossRefGoogle Scholar
  27. Tokieda, K.; Whitsett, J.A.; Clark, J.C.; Weaver, T.E.; Ikeda, K.; McConnell, K.B.; Jobe, A.H.; Ikegami, M.; Iwamoto, H.S. Pulmonary dysfunction in neonatal SP-B-deficient mice. Am. J. Physiol. 273:L875–L882; 1997PubMedGoogle Scholar
  28. Wang, Z.; Jaenisch, R. At most three ES cells contribute to the somatic lineages of chimeric mice and of mice produced by ES-tetraploid complementation. Dev. Biol. 275:192–201; 2004PubMedCrossRefGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2007

Authors and Affiliations

  • Shumin Gao
    • 1
    • 2
  • Xiaohui Wen
    • 1
    • 2
  • Rongrong Yang
    • 1
    • 2
  • Keqian Di
    • 1
    • 2
  • Jun Tong
    • 3
  • Xiangyun Li
    • 1
    • 2
  1. 1.College of Animal Science and TechnologyAgricultural University of HebeiBaodingChina
  2. 2.Cattle and Sheep Embryo Engineering Center of HebeiBaodingChina
  3. 3.College of Chinese Traditional VeterinaryAgricultural University of HebeiBaodingChina

Personalised recommendations