Uterine inactivation of muscle segment homeobox (Msx) genes alters epithelial cell junction proteins during embryo implantation

FASEB Journal

Volumn 30, Issue 4, 2016, Pages 1425-1435

  Sun, Xiaofei ^a   Park, Craig B ^a   Deng, Wenbo ^a   Potter, S Steven ^a   Dey, Sudhansu K ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Adhesion; Claudin; Receptivity; Sprr2; Uterus

Indexed keywords

ADRENOMEDULLIN; ALPHA 2 MACROGLOBULIN; BONE MORPHOGENETIC PROTEIN 2; CLAUDIN 1; COLLAGEN TYPE 1; COLLAGEN TYPE 6; ELASTIN; FIBRILLIN 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HOMEODOMAIN PROTEIN; JUNCTIONAL ADHESION MOLECULE; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA; MESSENGER RNA; MICROFIBRILLAR ASSOCIATED PROTEIN 4; MUSCLE SEGMENT HOMEOBOX PROTEIN 1; MUSCLE SEGMENT HOMEOBOX PROTEIN 2; OCCLUDIN; OSTEOGLYCIN; PROLINE RICH PROTEIN; PROSTAGLANDIN SYNTHASE; PROTEIN LYSINE 6 OXIDASE; PROTEIN ZO1; SMALL PROLINE RICH 2 PROTEIN; SONIC HEDGEHOG PROTEIN; SPONDIN 2; STAT3 PROTEIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG; WNT5A PROTEIN; CORNIFIED ENVELOPE LIKE PROLINE RICH PROTEIN; MSX1 PROTEIN, MOUSE; SPRR2A PROTEIN, MOUSE; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENDOMETRIUM; ENDOMETRIUM CELL; EPIDERMIS; EXON; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; INTRACELLULAR SPACE; KERATINIZATION; LASER CAPTURE MICRODISSECTION; MOUSE; NIDATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOPREGNANCY; RNA SEQUENCE; STROMA CELL; TIGHT JUNCTION; UPREGULATION; ANIMAL; C57BL MOUSE; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENETICS; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; MALE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; UTERUS;

ANIMALS; CLAUDIN-1; CORNIFIED ENVELOPE PROLINE-RICH PROTEINS; EMBRYO IMPLANTATION; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MSX1 TRANSCRIPTION FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UTERUS;

EID: 84963956064     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-282798     Document Type: Article

References (43)

1. Carson, D. D., Bagchi, I., Dey, S. K., Enders, A. C., Fazleabas, A. T., Lessey, B. A., and Yoshinaga, K. (2000) Embryo implantation. Dev. Biol. 223, 217-237
2. Wang, H., and Dey, S. K. (2006) Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7, 185-199
3. Dey, S. K. (2004) Focus on implantation. Reproduction 128, 655-656
4. Paria, B. C., Reese, J., Das, S. K., and Dey, S. K. (2002) Deciphering the cross-talk of implantation: advances and challenges. Science 296, 2185-2188
5. Murphy, C. R. (2004) Uterine receptivity and the plasmamembrane transformation. Cell Res. 14, 259-267
6. Daikoku, T., Cha, J., Sun, X., Tranguch, S., Xie, H., Fujita, T., Hirota, Y., Lydon, J., DeMayo, F., Maxson, R., and Dey, S. K. (2011) Conditional deletion of Msx homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev. Cell 21, 1014-1025
7. Cha, J., Sun, X., and Dey, S.K. (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat. Med. 18, 1754-1767
8. Finnerty, J. R., Mazza, M. E., and Jezewski, P. A. (2009) Domain duplication, divergence, and loss events in vertebrate Msx paralogs reveal phylogenomically informed disease markers. BMC Evol. Biol. 9, 18
9. Satokata, I., and Maas, R. (1994) Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356
10. Satokata, I., Ma, L., Ohshima, H., Bei, M., Woo, I., Nishizawa, K., Maeda, T., Takano, Y., Uchiyama, M., Heaney, S., Peters, H., Tang, Z., Maxson, R., and Maas, R. (2000) Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 24, 391-395
11. Zhong, Y. F., and Holland, P.W. (2011) The dynamics of vertebrate homeobox gene evolution: gain and loss of genes in mouse and human lineages. BMC Evol. Biol. 11, 169
12. Alappat, S., Zhang, Z. Y., and Chen, Y. P. (2003) Msx homeobox gene family and craniofacial development. Cell Res. 13, 429-442
13. Zhang, H., Catron, K. M., and Abate-Shen, C. (1996) A role for the Msx-1 homeodomain in transcriptional regulation: residues in the N-terminal arm mediate TATA binding protein interaction and transcriptional repression. Proc. Natl. Acad. Sci. USA 93, 1764-1769
14. Daikoku, T., Song, H., Guo, Y., Riesewijk, A., Mosselman, S., Das, S. K., and Dey, S. K. (2004) Uterine Msx-1 and Wnt4 signaling becomes aberrant inmice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox-Wnt signaling in implantation. Mol. Endocrinol. 18, 1238-1250
15. Cha, J., Bartos, A., Park, C., Sun, X., Li, Y., Cha, S.W., Ajima, R., Ho, H. Y., Yamaguchi, T. P., and Dey, S. K. (2014) Appropriate crypt formation in the uterus for embryo homing and implantation requires Wnt5a-ROR signaling. Cell Reports 8, 382-392
16. Soyal, S.M., Mukherjee, A., Lee, K. Y., Li, J., Li, H., DeMayo, F. J., and Lydon, J. P. (2005) Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 41, 58-66
17. Sun, X., Bartos, A., Whitsett, J. A., and Dey, S. K. (2013) Uterine deletion of Gp130 or Stat3 shows implantation failure with increased estrogenic responses. Mol. Endocrinol. 27, 1492-1501
18. Sun, X., Zhang, L., Xie, H., Wan, H., Magella, B., Whitsett, J. A., and Dey, S. K. (2012) Kruppel-like factor 5 (KLF5) is critical for conferring uterine receptivity to implantation. Proc. Natl. Acad. Sci. USA 109, 1145-1150
19. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578
20. Simmons, D. G., Rawn, S., Davies, A., Hughes, M., and Cross, J. C. (2008) Spatial and temporal expression of the 23murine prolactin/placental lactogen-related genes is not associated with their position in the locus. BMC Genomics 9, 352
21. Das, S. K., Yano, S., Wang, J., Edwards, D. R., Nagase, H., and Dey, S. K. (1997) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in themouse uterus during the periimplantation period. Dev. Genet. 21, 44-54
22. Borth, W. (1992) Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J. 6, 3345-3353
23. Frantz, C., Stewart, K.M., and Weaver, V.M. (2010) The extracellular matrix at a glance. J. Cell Sci. 123, 4195-4200
24. Maier, S., Paulsson, M., and Hartmann, U. (2008) The widely expressed extracellular matrix protein SMOC-2 promotes keratinocyte attachment and migration. Exp. Cell Res. 314, 2477-2487
25. Song, H., Lim, H., Paria, B. C., Matsumoto, H., Swift, L. L., Morrow, J., Bonventre, J. V., and Dey, S. K. (2002) Cytosolic phospholipase A2alpha is crucial [correction of A2alpha deficiency is crucial] for 'on-time' embryo implantation that directs subsequent development. Development 129, 2879-2889
26. Stewart, C. L., Kaspar, P., Brunet, L. J., Bhatt, H., Gadi, I., Köntgen, F., and Abbondanzo, S. J. (1992) Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79
27. Tsukita, S., Furuse, M., and Itoh, M. (2001) Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293
28. Furuse, M. (2010) Molecular basis of the core structure of tight junctions. Cold Spring Harb. Perspect. Biol. 2, a002907
29. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A., and Tsukita, S. (2002) Claudin-based tight junctions are crucial for themammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 156, 1099-1111
30. Tan, Y. F., Sun, X. Y., Li, F. X., Tang, S., Piao, Y. S., and Wang, Y. L. (2006) Gene expression pattern and hormonal regulation of small proline-rich protein 2 family members in the female mouse reproductive system during the estrous cycle and pregnancy. Reprod. Nutr. Dev. 46, 641-655
31. Reese, J., Das, S. K., Paria, B. C., Lim, H., Song, H., Matsumoto, H., Knudtson, K. L., DuBois, R. N., and Dey, S. K. (2001) Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J. Biol. Chem. 276, 44137-44145
32. Cha, J., Sun, X., Bartos, A., Fenelon, J., Lefèvre, P., Daikoku, T., Shaw, G., Maxson, R., Murphy, B.D., Renfree, M.B., and Dey, S.K. (2013) A new role for muscle segment homeobox genes in mammalian embryonic diapause. Open Biol. 3, 130035
33. Franco, H. L., Lee, K. Y., Rubel, C. A., Creighton, C. J., White, L. D., Broaddus, R. R., Lewis, M.T., Lydon, J.P., Jeong, J.W., and DeMayo, F. J. (2010) Constitutive activation of smoothened leads to female infertility and altered uterine differentiation in the mouse. Biol. Reprod. 82, 991-999
34. Madara, J. L. (1988) Tight junction dynamics: is paracellular transport regulated? Cell 53, 497-498
35. Gumbiner, B.M. (1993) Breaking through the tight junctionbarrier. J. Cell Biol. 123, 1631-1633
36. Furuse, M., Sasaki, H., Fujimoto, K., and Tsukita, S. (1998) A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell Biol. 143, 391-401
37. Enders, A. C. (1975) The implantation chamber, blastocyst and blastocyst imprint of the rat: a scanning electron microscope study. Anat. Rec. 182, 137-149
38. Candi, E., Schmidt, R., and Melino, G. (2005) The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6, 328-340
39. Kartasova, T., and van de Putte, P. (1988) Isolation, characterization, and UV-stimulated expression of two families of genes encoding polypeptides of related structure in human epidermal keratinocytes. Mol. Cell. Biol. 8, 2195-2203
40. Hong, S.H., Nah, H. Y., Lee, J. Y., Lee, Y. J., Lee, J.W., Gye, M.C., Kim, C. H., Kang, B. M., and Kim, M. K. (2004) Estrogen regulates the expression of the small proline-rich 2 gene family in the mouse uterus. Mol. Cells 17, 477-484
41. Hong, S.H., Lee, J.E., Jeong, J. J., Hwang, S. J., Bae, S.N., Choi, J. Y., and Song, H. (2010) Small proline-rich protein 2 family is a cluster of genes induced by estrogenic compounds through nuclear estrogen receptors in the mouse uterus. Reprod. Toxicol. 30, 469-476
42. Wang, J., Kumar, R. M., Biggs, V. J., Lee, H., Chen, Y., Kagey, M. H., Young, R. A., and Abate-Shen, C. (2011) The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development. Dev. Cell 21, 575-588
43. Catron, K. M., Wang, H., Hu, G., Shen, M. M., and Abate-Shen, C. (1996) Comparison of MSX-1 and MSX-2 suggests amolecular basis for functional redundancy. Mech. Dev. 55, 185-199