Changes in cell cycle and extracellular matrix gene expression during placental development in deer mouse (Peromyscus) hybrids

Amanda R. Duselis; Craig Obergfell; Jennifer A. Mack; Michael J. O’Neill; Quang K. Nguyen; Rachel J. O’Neill; Paul B. Vrana

doi:10.1071/RD07015

RESEARCH ARTICLE (Open Access)

Changes in cell cycle and extracellular matrix gene expression during placental development in deer mouse (Peromyscus) hybrids

Amanda R. Duselis ^A , Craig Obergfell ^B , Jennifer A. Mack ^B , Michael J. O’Neill ^B , Quang K. Nguyen ^A , Rachel J. O’Neill ^B and Paul B. Vrana ^A ^C

+ Author Affiliations

- Author Affiliations

^A Department of Biological Chemistry, Sprague Hall 350, School of Medicine, University of California Irvine, Irvine, CA 92799-1700, USA.

^B Department of Molecular & Cell Biology, University of Connecticut, BH 309A, 345 Mansfield Road, Unit 2131, Storrs, CT 06269-2131, USA.

^C Corresponding author. Email: pvrana@uci.edu

Reproduction, Fertility and Development 19(5) 695-708 https://doi.org/10.1071/RD07015
Submitted: 21 January 2007 Accepted: 6 May 2007 Published: 4 July 2007

Abstract

Crosses between two species of the rodent genus Peromyscus produce defects in both growth and development. The defects are pronounced in the hybrid placentas. Peromyscuys maniculatus (strain BW) females mated to P. polionotus (strain PO) males produce placentas half the size of the parental species, as well as growth-retarded embryos. In contrast, PO females mated to BW males result in defective conceptuses that display embryonic and placental overgrowth. These ‘parent-of-origin’-dependent phenotypes are consistent with previous studies that demonstrated altered expression of imprinted genes and genetic linkage of the overgrowth phenotypes to imprinted domains. In the present study, we take a broader approach in assessing perturbations in hybrid placental gene expression through the use of Mus musculus cDNA microarrays. In verifying classes of genes identified in microarray screens differentially regulated during hybrid placental development, we focused on those influencing the cell cycle and extracellular matrix (ECM). Our work suggests that cell cycle regulators at the G₁/S phase check-point are downregulated in the large hybrid placenta, whereas the small hybrid placenta is more variable. The ECM genes are typically downstream targets of cell cycle regulation and their misregulation is consistent with many of the dysmorphic phenotypes. Thus, these data suggest imbalances in proliferation and differentiation in hybrid placentation.

Acknowledgements

This research was supported by grants from the American Cancer Society (RSG-03–070–01-MGO) and March of Dimes (#5-FY03–17) to PBV, the National Science Foundation (MCB-0093250) to RJO and the University of Connecticut Research Foundation to RJO and MJO. The authors thank the Center for Applied Genetics and Technology for Affymetrix support and the Center for Molecular and Mitochondrial Medicine and Genetics for assistance with microscopy and imaging.

References

Apte, S. S. , Mattei, M. G. , and Olsen, B. R. (1994). Cloning of the cDNA encoding human tissue inhibitor of metalloproteinases-3 (TIMP-3) and mapping of the TIMP3 gene to chromosome 22. Genomics 19, 86–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Chu, L. C., Eberhart, C. G., Grossman, S. A., and Herman, J. G. (2006). Epigenetic silencing of multiple genes in primary CNS lymphoma. Int. J. Cancer 119, 2487–2491. doi:10.1002/IJC.22124

Cheung, A. N. (2003). Pathology of gestational trophoblastic diseases. Best Pract. Res. Clin. Obstet. Gynaecol. 17, 849–868.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Fan, T., Hagan, J. P., Kozlov, S. V., Stewart, C. L., and Muegge, K. (2005). Lsh controls silencing of the imprinted Cdkn1c gene. Development 132, 635–644. doi:10.1242/DEV.01612

Farnsworth, R. L. , and Talamantes, F. (1998). Calcyclin in the mouse decidua: expression and effects on placental lactogen secretion. Biol. Reprod. 59, 546–552.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Feng, H., Cheung, A. N., Xue, W. C., Wang, Y., Wang, X., Fu, S., Wang, Q., Ngan, H. Y., and Tsao, S. W. (2004). Down-regulation and promoter methylation of tissue inhibitor of metalloproteinase 3 in choriocarcinoma. Gynecol. Oncol. 94, 375–382. doi:10.1016/J.YGYNO.2004.04.019

Frank, D. , Fortino, W. , Clark, L. , Musalo, R. , Wang, W. , Saxena, A. , Li, C. M. , Reik, W. , Ludwig, T. , and Tycko, B. (2002). Placental overgrowth in mice lacking the imprinted gene Ipl. Proc. Natl Acad. Sci. USA 99, 7490–7495.
| Crossref | GoogleScholarGoogle Scholar | Loschiavo, M., Nguyen, Q. K., Duselis, A. R., and Vrana, P. B. (2007). Mapping and identification of candidate loci responsible for peromyscus hybrid overgrowth. Mamm. Genome 18, 75–85. doi:10.1007/S00335-006-0083-X

Luu, H. H. , Zhou, L. , Haydon, R. C. , Deyrup, A. T. , and Montag, A. G. , et al. (2005). Increased expression of s100a6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma. Cancer Lett. 229, 135–148.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Rehman, I., Cross, S. S., Catto, J. W., Leiblich, A., Mukherjee, A., Azzouzi, A. R., Leung, H. Y., and Hamdy, F. C. (2005). Promoter hyper-methylation of calcium binding proteins S100A6 and S100A2 in human prostate cancer. Prostate 65, 322–330. doi:10.1002/PROS.20302

Reik, W. , Collick, A. , Norris, M. L. , Barton, S. C. , and Surani, M. A. (1987). Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature 328, 248–251.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Wistuba, I. I., Gazdar, A. F., Minna, J. D. (2001). Molecular genetics of small cell lung carcinoma. Semin. Oncol. 28(Suppl.), 3–13. doi:10.1016/S0093-7754(01)90072-7

Wu, L. , de Bruin, A. , Saavedra, H. I. , Starovic, M. , and Trimboli, A. , et al. (2003). Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421, 942–947.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Yue, H. , and Jiang, H. Y. (2005). Expression of cell cycle regulator p57kip2, cyclinE protein and proliferating cell nuclear antigen in human pancreatic cancer: an immunohistochemical study. World J. Gastroenterol. 11, 5057–5060.
| PubMed |

Zechner, U. , Reule, M. , Orth, A. , Bonhomme, F. , Strack, B. , Guenet, J. L. , Hameister, H. , and Fundele, R. (1996). An X-chromosome linked locus contributes to abnormal placental development in mouse interspecific hybrids. Nat. Genet. 12, 398–403.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Zechner, U. , Shi, W. , Hemberger, M. , Himmelbauer, H. , and Otto, S. , et al. (2004). Divergent genetic and epigenetic post-zygotic isolations mechanisms in Mus and Peromyscus. J. Evol. Biol. 17, 453–460.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Zhang, P. , Wong, C. , DePinho, R. A. , Harper, J. W. , and Elledge, S. J. (1998). Cooperation between the Cdk inhibitors p27KIP1 and p57KIP2 in the control of tissue growth and development. Genes Dev. 12, 3162–3167.
| PubMed |