A Grhl2-dependent gene network controls trophoblast branching morphogenesis

Development (Cambridge)

Volumn 142, Issue 6, 2015, Pages 1125-1136

  Walentin, Katharina ^a,b   Hinze, Christian ^a,b   Werth, Max ^a,b,c   Haase, Nadine ^b   Varma, Saaket ^d   Morell, Robert ^e   Aue, Annekatrin ^a,b   Pötschke, Elisabeth ^a   Warburton, David ^d   Qiu, Andong ^c   Barasch, Jonathan ^c   Purfürst, Bettina ^a   Dieterich, Christoph ^f   Popova, Elena ^a   Bader, Michael ^a   Dechend, Ralf ^b   Staff, Anne Cathrine ^g   Yurtdas, Zeliha Yesim ^a,h,i   Kilic, Ergin ^h   Schmidt Ott, Kai M ^a,b,h  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b Experimental and Clinical Research Center   (Germany)

^c Columbia University College of Physicians and Surgeons ^*  (United States)

^d CHILDREN S HOSPITAL LOS ANGELES   (United States)

^e NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^f MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^g OSLO UNIVERSITY HOSPITAL   (Norway)

^h CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

ⁱ Berlin Institute for Urologic Research   (Germany)

Author keywords

Basement membrane defects; Epithelial differentiation; Epithelial morphogenesis; Placenta defects; Spint1

Indexed keywords

GRAINYHEAD LIKE 2 TRANSCRIPTION FACTOR; KUNITZ TYPE 1 PROTEIN; SERINE PROTEINASE INHIBITOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; GRHL2 PROTEIN, HUMAN; LEUKOCYTE ELASTASE INHIBITOR; SPINT1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BASAL CHORIONIC TROPHOBLAST; BASEMENT MEMBRANE; BINDING SITE; BRANCHING MORPHOGENESIS; CELL POLARITY; CONTROLLED STUDY; DOWN REGULATION; ECTODERM; EMBRYO; FEMALE; GENE ACTIVITY; GENE DELETION; GENE EXPRESSION; GENE IDENTIFICATION; GENE INACTIVATION; GENOMICS; HUMAN; HUMAN TISSUE; INNER EAR; MALE; MORPHOGENESIS; MOUSE; MOUSE EMBRYO; NONHUMAN; ORTHOLOGY; PHENOTYPE; PLACENTA; PLACENTA DEVELOPMENT; PLACENTA DISORDER; PRIORITY JOURNAL; TROPHOBLAST; CHROMATIN IMMUNOPRECIPITATION; ELECTRON MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROARRAY ANALYSIS; PHYSIOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION;

MURINAE;

BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE REGULATORY NETWORKS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; MICROSCOPY, ELECTRON; MORPHOGENESIS; PLACENTA; PREGNANCY; PROTEINASE INHIBITORY PROTEINS, SECRETORY; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 84929515787     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113829     Document Type: Article

References (64)

1. Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C. and Cross, J. C. (2002). Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev. Biol. 250, 358-373.
2. Anson-Cartwright, L., Dawson, K., Holmyard, D., Fisher, S. J., Lazzarini, R. A. and Cross, J. C. (2000). The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25, 311-314.
3. Auden, A., Caddy, J., Wilanowski, T., Ting, S. B., Cunningham, J. M. and Jane, S. M. (2006). Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development. Gene Expr. Patterns 6, 964-970.
4. Bailey, T. L. and Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36.
5. Bray, S. J. and Kafatos, F. C. (1991). Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev. 5, 1672-1683.
6. Brouns, M. R., De Castro, S. C. P., Terwindt-Rouwenhorst, E. A., Massa, V., Hekking, J. W., Hirst, C. S., Savery, D., Munts, C., Partridge, D., Lamers, W. et al. (2011). Over-expression of Grhl2 causes spina bifida in the Axial defects mutant mouse. Hum. Mol. Genet. 20, 1536-1546.
7. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J. et al. (2008). Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117.
8. Cox, B., Kotlyar, M., Evangelou, A. I., Ignatchenko, V., Ignatchenko, A., Whiteley, K., Jurisica, I., Adamson, S. L., Rossant, J. and Kislinger, T. (2009). Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol. Syst. Biol. 5, 279.
9. Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H. and Kingdom, J. C. P. (2003a). Genes, development and evolution of the placenta. Placenta 24, 123-130.
10. Cross, J. C., Simmons, D. G. and Watson, E. D. (2003b). Chorioallantoic morphogenesis and formation of the placental villous tree. Ann. N. Y. Acad. Sci. 995, 84-93.
11. Durbeej, M. and Ekblom, P. (1997). Dystroglycan and laminins: glycoconjugates involved in branching epithelial morphogenesis. Exp. Lung Res. 23, 109-118.
12. Egbor, M., Ansari, T., Morris, N., Green, C. J. and Sibbons, P. D. (2006). Morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction. BJOG 113, 580-589.
13. Fan, C. B., He, J. L., Wang, Y. X., Liu, X. Q., Chen, X. M., Li, H. M., and Ding, Y. B., (2006). HAI-1 expression in villous tissue of early gestational period in women. Sichuan Da Xue Xue Bao Yi Xue Ban 37, 602-605.
14. Fan, B., Brennan, J., Grant, D., Peale, F., Rangell, L. and Kirchhofer, D. (2007). Hepatocyte growth factor activator inhibitor-1 (HAI-1) is essential for the integrity of basement membranes in the developing placental labyrinth. Dev. Biol. 303, 222-230.
15. Founds, S. A., Conley, Y. P., Lyons-Weiler, J. F., Jeyabalan, A., Hogge, W. A. and Conrad, K. P. (2009). Altered global gene expression in first trimester placentas of women destined to develop preeclampsia. Placenta 30, 15-24.
16. Gao, X., Vockley, C. M., Pauli, F., Newberry, K. M., Xue, Y., Randell, S. H., Reddy, T. E. and Hogan, B. L. M. (2013). Evidence for multiple roles for grainyheadlike 2 in the establishment and maintenance of human mucociliary airway epithelium. Proc. Natl. Acad. Sci. USA 110, 9356-9361.
17. Georgiades, P., Ferguson-Smith, A. C. and Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3-19.
18. Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L. and Noble, W. S. (2007). Quantifying similarity between motifs. Genome Biol. 8, R24.
19. Hallikas, O. K., Aaltonen, J. M., von Koskull, H., Lindberg, L.-A., Valmu, L., Kalkkinen, N., Wahlström, T., Kataoka, H., Andersson, L., Lindholm, D. et al. (2006). Identification of antibodies against HAI-1 and integrin alpha6beta4 as immunohistochemical markers of human villous cytotrophoblast. J. Histochem. Cytochem. 54, 745-752.
20. Han, Y., Mu, Y., Li, X., Xu, P., Tong, J., Liu, Z., Ma, T., Zeng, G., Yang, S., Du, J. et al. (2011). Grhl2 deficiency impairs otic development and hearing ability in a zebrafish model of the progressive dominant hearing loss DFNA28. Hum. Mol. Genet. 20, 3213-3226.
21. Hayashi, S., Lewis, P., Pevny, L. and McMahon, A. P. (2002). Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 119 Suppl. 1, S97-S101.
22. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H. and Glass, C. K. (2010). Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589.
23. Huuskonen, P., Storvik, M., Reinisalo, M., Honkakoski, P., Rysä, J., Hakkola, J. and Pasanen, M. (2008). Microarray analysis of the global alterations in the gene expression in the placentas from cigarette-smoking mothers. Clin. Pharmacol. Ther. 83, 542-550.
24. Jackman, S. M., Kong, X. and Fant, M. E. (2012). Plac1 (placenta-specific 1) is essential for normal placental and embryonic development. Mol. Reprod. Dev. 79, 564-572.
25. Kataoka, H., Meng, J. Y., Itoh, H., Hamasuna, R., Shimomura, T., Suganuma, T. and Koono, M. (2000). Localization of hepatocyte growth factor activator inhibitor type 1 in Langhans’ cells of human placenta. Histochem. Cell Biol. 114, 469-475.
26. Kawaguchi, M., Takeda, N., Hoshiko, S., Yorita, K., Baba, T., Sawaguchi, A., Nezu, Y., Yoshikawa, T., Fukushima, T. and Kataoka, H. (2011). Membranebound serine protease inhibitor HAI-1 is required for maintenance of intestinal epithelial integrity. Am. J. Pathol. 179, 1815-1826.
27. Klein, G., Langegger, M., Timpl, R. and Ekblom, P. (1988). Role of laminin A chain in the development of epithelial cell polarity. Cell 55, 331-341.
28. Li, Z., Van Calcar, S., Qu, C., Cavenee, W. K., Zhang, M. Q. and Ren, B. (2003). A global transcriptional regulatory role for c-Myc in Burkitt’s lymphoma cells. Proc. Natl. Acad. Sci. USA 100, 8164-8169.
29. Lin, C.-Y., Anders, J., Johnson, M. and Dickson, R. B. (1999). Purification and characterization of a complex containing matriptase and a Kunitz-type serine protease inhibitor from human milk. J. Biol. Chem. 274, 18237-18242.
30. Mace, K. A., Pearson, J. C. and McGinnis, W. (2005). An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 308, 381-385.
31. Mikheev, A. M., Nabekura, T., Kaddoumi, A., Bammler, T. K., Govindarajan, R., Hebert, M. F. and Unadkat, J. D. (2008). Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study. Reprod. Sci. 15, 866-877.
32. Millar, I. D., Taylor, H. C., Cooper, G. J., Kibble, J. D., Barhanin, J. and Robson, L. (2006). Adaptive downregulation of a quinidine-sensitive cation conductance in renal principal cells of TWIK-1 knockout mice. Pflugers Arch. 453, 107-116.
33. Narasimha, M., Uv, A., Krejci, A., Brown, N. H. and Bray, S. J. (2008). Grainy head promotes expression of septate junction proteins and influences epithelial morphogenesis. J. Cell Sci. 121, 747-752.
34. Oberst, M. D., Chen, L.-Y. L., Kiyomiya, K.-I., Williams, C. A., Lee, M.-S., Johnson, M. D., Dickson, R. B. and Lin, C.-Y. (2005). HAI-1 regulates activation and expression of matriptase, a membrane-bound serine protease. Am. J. Physiol. Cell Physiol. 289, C462-C470.
35. Pöschl, E., Schlötzer-Schrehardt, U., Brachvogel, B., Saito, K., Ninomiya, Y. and Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131, 1619-1628.
36. Pyrgaki, C., Liu, A. and Niswander, L. (2011). Grainyhead-like 2 regulates neural tube closure and adhesion molecule expression during neural fold fusion. Dev. Biol. 353, 38-49.
37. Raffel, G. D., Chu, G. C., Jesneck, J. L., Cullen, D. E., Bronson, R. T., Bernard, O. A. and Gilliland, D. G. (2009). Ott1 (Rbm15) is essential for placental vascular branching morphogenesis and embryonic development of the heart and spleen. Mol. Cell. Biol. 29, 333-341.
38. Rifat, Y., Parekh, V., Wilanowski, T., Hislop, N. R., Auden, A., Ting, S. B., Cunningham, J. M. and Jane, S. M. (2010). Regional neural tube closure defined by the Grainy head-like transcription factors. Dev. Biol. 345, 237-245.
39. Schmidt, D., Wilson, M. D., Spyrou, C., Brown, G. D., Hadfield, J. and Odom, D. T. (2009). ChIP-seq: using high-throughput sequencing to discover proteinDNA interactions. Methods 48, 240-248.
40. Schorle, H., Meier, P., Buchert, M., Jaenisch, R. and Mitchell, P. J. (1996). Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381, 235-238.
41. Senga, K., Mostov, K. E., Mitaka, T., Miyajima, A. and Tanimizu, N. (2012). Grainyhead-like 2 regulates epithelial morphogenesis by establishing functional tight junctions through the organization of a molecular network among claudin3, claudin4, and Rab25. Mol. Biol. Cell 23, 2845-2855.
42. Shimomura, T., Denda, K., Kitamura, A., Kawaguchi, T., Kito, M., Kondo, J., Kagaya, S., Qin, L., Takata, H., Miyazawa, K. et al. (1997). Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. J. Biol. Chem. 272, 6370-6376.
43. Simmons, D. G., Natale, D. R. C., Begay, V., Hughes, M., Leutz, A. and Cross, J. C. (2008). Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135, 2083-2091.
44. Sorokin, L., Sonnenberg, A., Aumailley, M., Timpl, R. and Ekblom, P. (1990). Recognition of the laminin E8 cell-binding site by an integrin possessing the alpha 6 subunit is essential for epithelial polarization in developing kidney tubules. J. Cell Biol. 111, 1265-1273.
45. Stemmler, M. P. and Bedzhov, I. (2010). A Cdh1HA knock-in allele rescues the Cdh1-/- phenotype but shows essential Cdh1 function during placentation. Dev. Dyn. 239, 2330-2344.
46. Stemmler, M. P., Hecht, A. and Kemler, R. (2005). E-cadherin intron 2 contains cisregulatory elements essential for gene expression. Development 132, 965-976.
47. Szabo, R., Molinolo, A., List, K. and Bugge, T. H. (2007). Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene 26, 1546-1556.
48. Szabo, R., Uzzun Sales, K., Kosa, P., Shylo, N. A., Godiksen, S., Hansen, K. K., Friis, S., Gutkind, J. S., Vogel, L. K., Hummler, E. et al. (2012). Reduced prostasin (CAP1/PRSS8) activity eliminates HAI-1 and HAI-2 deficiencyassociated developmental defects by preventing matriptase activation. PLoS Genet. 8, e1002937.
49. Takahashi, Y., Carpino, N., Cross, J. C., Torres, M., Parganas, E. and Ihle, J. N. (2003). SOCS3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J. 22, 372-384.
50. Tanaka, H., Nagaike, K., Takeda, N., Itoh, H., Kohama, K., Fukushima, T., Miyata, S., Uchiyama, S., Uchinokura, S., Shimomura, T. et al. (2005). Hepatocyte growth factor activator inhibitor type 1 (HAI-1) is required for branching morphogenesis in the chorioallantoic placenta. Mol. Cell. Biol. 25, 5687-5698.
51. Tang, T., Li, L., Tang, J., Li, Y., Lin, W. Y., Martin, F., Grant, D., Solloway, M., Parker, L., Ye, W. et al. (2010). A mouse knockout library for secreted and transmembrane proteins. Nat. Biotechnol. 28, 749-755.
52. Tao, J., Kuliyev, E., Wang, X., Li, X., Wilanowski, T., Jane, S. M., Mead, P. E. and Cunningham, J. M. (2005). BMP4-dependent expression of Xenopus Grainyhead-like 1 is essential for epidermal differentiation. Development 132, 1021-1034.
53. Tarabay, Y., Kieffer, E., Teletin, M., Celebi, C., Van Montfoort, A., Zamudio, N., Achour, M., El Ramy, R., Gazdag, E., Tropel, P. et al. (2013). The mammalianspecific Tex19.1 gene plays an essential role in spermatogenesis and placentasupported development. Hum. Reprod. 28, 2201-2214.
54. Uhlen, M., Oksvold, P., Fagerberg, L., Lundberg, E., Jonasson, K., Forsberg, M., Zwahlen, M., Kampf, C., Wester, K., Hober, S. et al. (2010). Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250.
55. Valouev, A., Johnson, D. S., Sundquist, A., Medina, C., Anton, E., Batzoglou, S., Myers, R. M. and Sidow, A. (2008). Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods 5, 829-834.
56. Varma, S., Cao, Y., Tagne, J.-B., Lakshminarayanan, M., Li, J., Friedman, T. B., Morell, R. J., Warburton, D., Kotton, D. N. and Ramirez, M. I. (2012). The transcription factors Grainyhead-like 2 and NK2-homeobox 1 form a regulatory loop that coordinates lung epithelial cell morphogenesis and differentiation. J. Biol. Chem. 287, 37282-37295.
57. Werth, M., Walentin, K., Aue, A., Schönheit, J., Wuebken, A., Pode-Shakked, N., Vilianovitch, L., Erdmann, B., Dekel, B., Bader, M. et al. (2010). The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137, 3835-3845.
58. Wilanowski, T., Tuckfield, A., Cerruti, L., O’Connell, S., Saint, R., Parekh, V., Tao, J., Cunningham, J. M. and Jane, S. M. (2002). A highly conserved novel family of mammalian developmental transcription factors related to Drosophila grainyhead. Mech. Dev. 114, 37-50.
59. Wilanowski, T., Caddy, J., Ting, S. B., Hislop, N. R., Cerruti, L., Auden, A., Zhao, L.-L., Asquith, S., Ellis, S., Sinclair, R. et al. (2008). Perturbed desmosomal cadherin expression in grainy head-like 1-null mice. EMBO J. 27, 886-897.
60. Yamauchi, M., Kataoka, H., Itoh, H., Seguchi, T., Hasui, Y. and Osada, Y. (2004). Hepatocyte growth factor activator inhibitor types 1 and 2 are expressed by tubular epithelium in kidney and down-regulated in renal cell carcinoma. J. Urol. 171, 890-896.
61. Yu, Z., Lin, K. K., Bhandari, A., Spencer, J. A., Xu, X., Wang, N., Lu, Z., Gill, G. N., Roop, D. R., Wertz, P. et al. (2006). The Grainyhead-like epithelial transactivator Get-1/Grhl3 regulates epidermal terminal differentiation and interacts functionally with LMO4. Dev. Biol. 299, 122-136.
62. Yu, Z., Mannik, J., Soto, A., Lin, K. K. and Andersen, B. (2009). The epidermal differentiation-associated Grainyhead gene Get1/Grhl3 also regulates urothelial differentiation. EMBO J. 28, 1890-1903.
63. Zhang, J., Hagopian-Donaldson, S., Serbedzija, G., Elsemore, J., Plehn Dujowich, D., McMahon, A. P., Flavell, R. A. and Williams, T. (1996). Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381, 238-241.
64. Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W. et al. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137.