Keratin 5-Cre-driven excision of nonmuscle myosin IIA in early embryo trophectoderm leads to placenta defects and embryonic lethality

Developmental Biology

Volumn 382, Issue 1, 2013, Pages 136-148

  Crish, James ^a   Conti, Mary Anne ^b   Sakai, Takao ^a   Adelstein, Robert S ^b   Egelhoff, Thomas T ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Keratin 5; Keratinocyte; MYH9; Myosin; Placenta; Trophoblast

Indexed keywords

CRE RECOMBINASE; CYTOKERATIN 5; GREEN FLUORESCENT PROTEIN; MYOSIN IIA;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; CYTOKERATIN 5 CRE GENE; DEVELOPMENTAL STAGE; ECTODERM; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; EPIDERMIS; EXTRAEMBRYONIC ECTODERM; FEMALE; GENE CONSTRUCT; GENE EXPRESSION; GENOTYPE; MALE; MOUSE; MYOSIN II HEAVY CHAIN GENE; NEWBORN; NONHUMAN; PHENOTYPE; PLACENTA DISORDER; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; TRANSGENIC MOUSE; TROPHECTODERM; TROPHOBLAST; TROPHOBLAST GIANT CELL; VASCULARIZATION; YOLK SAC;

BOVINAE; MUS; MUS MUSCULUS;

EID: 84884415944     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.07.017     Document Type: Article

References (55)

1. Alonso L., Fuchs E. Stem cells of the skin epithelium. Proc. Nat. Acad. Sci. U.S.A. 2003, 100(Suppl. 1):11830-11835.
2. Betapudi V., Rai V., Beach J.R., Egelhoff T. Novel regulation and dynamics of myosin II activation during epidermal wound responses. Exp. Cell Res. 2010, 316:980-991.
3. Blanpain C., Fuchs E. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 2009, 10:207-217.
4. Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. Development 1994, 120:2369-2383.
5. Chrostek A., Wu X., Quondamatteo F., Hu R., Sanecka A., Niemann C., Langbein L., Haase I., Brakebusch C. Rac1 is crucial for hair follicle integrity but is not essential for maintenance of the epidermis. Mol. Cell Biol. 2006, 26:6957-6970.
6. Coan P.M., Ferguson-Smith A.C., Burton G.J. Ultrastructural changes in the interhaemal membrane and junctional zone of the murine chorioallantoic placenta across gestation. J. Anat. 2005, 207:783-796.
7. Conti M.A., Adelstein R.S. Nonmuscle myosin II moves in new directions. J. Cell Sci. 2008, 121:11-18.
8. Conti M.A., Even-Ram S., Liu C., Yamada K.M., Adelstein R.S. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J. Biol. Chem. 2004, 279:41263-41266.
9. Cross J.C. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin. Cell Dev. Biol. 2000, 11:105-113.
10. Cross J.C. Placental function in development and disease. Reprod. Fertil. Dev. 2006, 18:71-76.
11. Cross J.C., Simmons D.G., Watson E.D. Chorioallantoic morphogenesis and formation of the placental villous tree. Ann. N. Y. Acad. Sci. 2003, 995:84-93.
12. Diamond I., Owolabi T., Marco M., Lam C., Glick A. Conditional gene expression in the epidermis of transgenic mice using the tetracycline-regulated transactivators tTA and rTA linked to the keratin 5 promoter. J. Invest. Dermatol. 2000, 115:788-794.
13. Eberl M., Klingler S., Mangelberger D., Loipetzberger A., Damhofer H., Zoidl K., Schnidar H., Hache H., Bauer H.C., Solca F., Hauser-Kronberger C., Ermilov A.N., Verhaegen M.E., Bichakjian C.K., Dlugosz A.A., Nietfeld W., Sibilia M., Lehrach H., Wierling C., Aberger F. Hedgehog-EGFR cooperation response genes determine the oncogenic phenotype of basal cell carcinoma and tumour-initiating pancreatic cancer cells. EMBO Mol. Med. 2012, 4:218-233.
14. Essayem S., Kovacic-Milivojevic B., Baumbusch C., McDonagh S., Dolganov G., Howerton K., Larocque N., Mauro T., Ramirez A., Ramos D.M., Fisher S.J., Jorcano J.L., Beggs H.E., Reichardt L.F., Ilic D. Hair cycle and wound healing in mice with a keratinocyte-restricted deletion of FAK. Oncogene 2006, 25:1081-1089.
15. Ferguson B.W., Gao X., Kil H., Lee J., Benavides F., Abba M.C., Aldaz C.M. Conditional Wwox deletion in mouse mammary gland by means of two Cre recombinase approaches. PLoS One 2012, 7:e36618.
16. Franke J.D., Montague R.A., Kiehart D.P. Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr. Biol. 2005, 15:2208-2221.
17. Gandarillas A., Watt F.M. The 5' noncoding region of the mouse involucrin gene: comparison with the human gene and genes encoding other cornified envelope precursors. Mamm. Genome 1995, 6:680-682.
18. Golomb E., Ma X., Jana S.S., Preston Y.A., Kawamoto S., Shoham N.G., Goldin E., Conti M.A., Sellers J.R., Adelstein R.S. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J. Biol. Chem. 2004, 279:2800-2808.
19. Grose R., Fantl V., Werner S., Chioni A.M., Jarosz M., Rudling R., Cross B., Hart I.R., Dickson C. The role of fibroblast growth factor receptor 2b in skin homeostasis and cancer development. EMBO J. 2007, 26:1268-1278.
20. Honda K., Sakaguchi T., Sakai K., Schmedt C., Ramirez A., Jorcano J.L., Tarakhovsky A., Kamisoyama H., Sakai T. Epidermal hyperplasia and papillomatosis in mice with a keratinocyte-restricted deletion of csk. Carcinogenesis 2007, 28:2074-2081.
21. Hu D., Cross J.C. Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev. Biol. 2011, 358:231-239.
22. Indra A.K., Warot X., Brocard J., Bornert J.M., Xiao J.H., Chambon P., Metzger D. Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res. 1999, 27:4324-4327.
23. Jackson B., Peyrollier K., Pedersen E., Basse A., Karlsson R., Wang Z., Lefever T., Ochsenbein A.M., Schmidt G., Aktories K., Stanley A., Quondamatteo F., Ladwein M., Rottner K., van H.J., Brakebusch C. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol. Biol. Cell 2011, 22:593-605.
24. Jacobelli J., Friedman R.S., Conti M.A., Lennon-Dumenil A.M., Piel M., Sorensen C.M., Adelstein R.S., Krummel M.F. Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nat. Immunol. 2010, 11:953-961.
25. Jorcano J.L., Magin T.M., Franke W.W. Cell type-specific expression of bovine keratin genes as demonstrated by the use of complementary DNA clones. J. Mol. Biol. 1984, 176:21-37.
26. Lenter M., Uhlig H., Hamann A., Jeno P., Imhof B., Vestweber D. A monoclonal antibody against an activation epitope on mouse integrin chain beta 1 blocks adhesion of lymphocytes to the endothelial integrin alpha 6 beta 1. Proc. Nat. Acad. Sci. U.S.A. 1993, 90:9051-9055.
27. Lu H., Hesse M., Peters B., Magin T.M. Type II keratins precede type I keratins during early embryonic development. Eur. J. Cell Biol. 2005, 84:709-718.
28. Mack J.A., Anand S., Maytin E.V. Proliferation and cornification during development of the mammalian epidermis. Birth Defects Res., Part C 2005, 75:314-329.
29. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
30. Omori E., Inagaki M., Mishina Y., Matsumoto K., Ninomiya-Tsuji J. Epithelial transforming growth factor beta-activated kinase 1 (TAK1) is activated through two independent mechanisms and regulates reactive oxygen species. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:3365-3370.
31. Omori E., Matsumoto K., Sanjo H., Sato S., Akira S., Smart R.C., Ninomiya-Tsuji J. TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J. Biol. Chem. 2006, 281:19610-19617.
32. Perez-Moreno M., Davis M.A., Wong E., Pasolli H.A., Reynolds A.B., Fuchs E. p120-catenin mediates inflammatory responses in the skin. Cell 2006, 124:631-644.
33. Ramirez A., Page A., Gandarillas A., Zanet J., Pibre S., Vidal M., Tusell L., Genesca A., Whitaker D.A., Melton D.W., Jorcano J.L. A keratin K5Cre transgenic line appropriate for tissue-specific or generalized Cre-mediated recombination. Genesis 2004, 39:52-57.
34. Rawn S.M., Cross J.C. The evolution, regulation, and function of placenta-specific genes. Annu. Rev. Cell Dev. Biol. 2008, 24:159-181.
35. Rossant J., Cross J.C. Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2001, 2:538-548.
36. Senner C.E., Hemberger M. Regulation of early trophoblast differentiation-lessons from the mouse. Placenta 2010, 31:944-950.
37. Simmons D.G., Cross J.C. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 2005, 284:12-24.
38. Simmons D.G., Fortier A.L., Cross J.C. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 2007, 304:567-578.
39. Simmons D.G., Natale D.R., Begay V., Hughes M., Leutz A., Cross J.C. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008, 135:2083-2091.
40. Simons M., Wang M., McBride O.W., Kawamoto S., Yamakawa K., Gdula D., Adelstein R.S., Weir L. Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ. Res. 1991, 69:530-539.
41. Sumigray K.D., Foote H.P., Lechler T. Noncentrosomal microtubules and type II myosins potentiate epidermal cell adhesion and barrier formation. J. Cell Biol. 2012, 199:513-525.
42. Tullio A.N., Accili D., Ferrans V.J., Yu Z.X., Takeda K., Grinberg A., Westphal H., Preston Y.A., Adelstein R.S. Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:12407-12412.
43. Tullio A.N., Bridgman P.C., Tresser N.J., Chan C.C., Conti M.A., Adelstein R.S., Hara Y. Structural abnormalities develop in the brain after ablation of the gene encoding nonmuscle myosin II-B heavy chain. J. Comp. Neurol. 2001, 433:62-74.
44. Vasioukhin V., Bauer C., Degenstein L., Wise B., Fuchs E. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin. Cell 2001, 104:605-617.
45. Vasioukhin V., Bowers E., Bauer C., Degenstein L., Fuchs E. Desmoplakin is essential in epidermal sheet formation. Nat. Cell Biol. 2001, 3:1076-1085.
46. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
47. Wang A., Ma X., Conti M.A., Adelstein R.S. Distinct and redundant roles of the non-muscle myosin II isoforms and functional domains. Biochem. Soc. Trans. 2011, 39:1131-1135.
48. Wang A., Ma X., Conti M.A., Liu C., Kawamoto S., Adelstein R.S. Nonmuscle myosin II isoform and domain specificity during early mouse development. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:14645-14650.
49. Watson E.D., Cross J.C. Development of structures and transport functions in the mouse placenta. Physiology. (Bethesda.) 2005, 20:180-193.
50. Watson E.D., Geary-Joo C., Hughes M., Cross J.C. The Mrj co-chaperone mediates keratin turnover and prevents the formation of toxic inclusion bodies in trophoblast cells of the placenta. Development 2007, 134:1809-1817.
51. Watson E.D., Hughes M., Simmons D.G., Natale D.R., Sutherland A.E., Cross J.C. Cell-cell adhesion defects in Mrj mutant trophoblast cells are associated with failure to pattern the chorion during early placental development. Dev. Dyn. 2011, 240:2505-2519.
52. Watt F.M., Lo C.C., Silva-Vargas V. Epidermal stem cells: an update. Curr. Opin. Genet. Dev. 2006, 16:518-524.
53. Welter J.F., Crish J.F., Agarwal C., Eckert R.L. Fos-related antigen (Fra-1), junB, and junD activate human involucrin promoter transcription by binding to proximal and distal AP1 sites to mediate phorbol ester effects on promoter activity. J. Biol. Chem. 1995, 270:12614-12622.
54. Yamanaka Y., Ralston A., Stephenson R.O., Rossant J. Cell and molecular regulation of the mouse blastocyst. Dev. Dyn. 2006, 235:2301-2314.
55. Zhang Y., Conti M.A., Malide D., Dong F., Wang A., Shmist Y.A., Liu C., Zerfas P., Daniels M.P., Chan C.C., Kozin E., Kachar B., Kelley M.J., Kopp J.B., Adelstein R.S. Mouse models of MYH9-related disease: mutations in nonmuscle myosin II-A. Blood 2012, 119:238-250.