Lrp4 and Wise interplay controls the formation and patterning of mammary and other skin appendage placodes by modulating Wnt signaling

Development (Cambridge)

Volumn 140, Issue 3, 2013, Pages 583-593

  Ahn, Youngwook ^a   Sims, Carrie ^a   Logue, Jennifer M ^a   Weatherbee, Scott D ^b   Krumlauf, Robb ^a,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Limb; Lrp4; Mammary placodes; Skin appendages; Sostdc1; Vibrissae; Wnt antagonists; Wnt catenin signaling

Indexed keywords

BETA CATENIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; LRP4 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; WISE PROTEIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BREAST DEVELOPMENT; CELL COUNT; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; FEMALE; GENE INACTIVATION; GENETIC EPISTASIS; HAIR FOLLICLE; HAIR GROWTH; IN VIVO STUDY; LIMB DEFECT; MAMMARY GLAND; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SKIN APPENDAGE; STEM CELL; VIBRISSA; WNT SIGNALING PATHWAY;

ANIMALS; BETA CATENIN; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EPISTASIS, GENETIC; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR FOLLICLE; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-5; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREGNANCY; PROTEIN INTERACTION MAPPING; RECEPTORS, LDL; SKIN; VIBRISSAE; WNT SIGNALING PATHWAY;

MUS;

EID: 84872062607     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.085118     Document Type: Article

References (58)

1. Ahn, Y., Sanderson, B. W., Klein, O. D. and Krumlauf, R. (2010). Inhibition of Wnt signaling by Wise (Sostdc1) and negative feedback from Shh controls tooth number and patterning. Development 137, 3221-3231.
2. Balemans, W., Ebeling, M., Patel, N., Van Hul, E., Olson, P., Dioszegi, M., Lacza, C., Wuyts, W., Van Den Ende, J., Willems, P. et al. (2001). Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum. Mol. Genet. 10, 537-543.
3. Balinsky, B. I. (1950). On the prenatal growth of the mammary gland rudiment in the mouse. J. Anat. 84, 227-235.
4. Boras-Granic, K., Chang, H., Grosschedl, R. and Hamel, P. A. (2006). Lef1 is required for the transition of Wnt signaling from mesenchymal to epithelial cells in the mouse embryonic mammary gland. Dev. Biol. 295, 219-231.
5. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O. and Kemler, R. (2001). Inactivation of the beta- catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264.
6. Choi, H. Y., Dieckmann, M., Herz, J. and Niemeier, A. (2009). Lrp4, a novel receptor for Dickkopf 1 and sclerostin, is expressed by osteoblasts and regulates bone growth and turnover in vivo. PLoS ONE 4, e7930.
7. Chu, E. Y., Hens, J., Andl, T., Kairo, A., Yamaguchi, T. P., Brisken, C., Glick, A., Wysolmerski, J. J. and Millar, S. E. (2004). Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 131, 4819-4829.
8. Cowin, P. and Wysolmerski, J. (2010). Molecular mechanisms guiding embryonic mammary gland development. Cold Spring Harb. Perspect. Biol. 2, a003251.
9. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
10. Dassule, H. R., Lewis, P., Bei, M., Maas, R. and McMahon, A. P. (2000). Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785.
11. Dietrich, M. F., van der Weyden, L., Prosser, H. M., Bradley, A., Herz, J. and Adams, D. J. (2010). Ectodomains of the LDL receptor-related proteins LRP1b and LRP4 have anchorage independent functions in vivo. PLoS ONE 5, e9960.
12. Fernandez-Teran, M. and Ros, M. A. (2008). The Apical Ectodermal Ridge: morphological aspects and signaling pathways. Int. J. Dev. Biol. 52, 857-871.
13. Ferrer-Vaquer, A., Piliszek, A., Tian, G., Aho, R. J., Dufort, D. and Hadjantonakis, A. K. (2010). A sensitive and bright single-cell resolution live imaging reporter of Wnt/β-catenin signaling in the mouse. BMC Dev. Biol. 10, 121.
14. Fliniaux, I., Mikkola, M. L., Lefebvre, S. and Thesleff, I. (2008). Identification of dkk4 as a target of Eda-A1/Edar pathway reveals an unexpected role of ectodysplasin as inhibitor of Wnt signalling in ectodermal placodes. Dev. Biol. 320, 60-71.
15. Gossen, M. and Bujard, H. (1992). Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89, 5547-5551.
16. He, J., Ma, L., Kim, S., Nakai, J. and Yu, C. R. (2008). Encoding gender and individual information in the mouse vomeronasal organ. Science 320, 535-538.
17. Herz, J. and Bock, H. H. (2002). Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71, 405-434.
18. Holmen, S. L., Giambernardi, T. A., Zylstra, C. R., Buckner-Berghuis, B. D., Resau, J. H., Hess, J. F., Glatt, V., Bouxsein, M. L., Ai, M., Warman, M. L. et al. (2004). Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J. Bone Miner. Res. 19, 2033-2040.
19. Itasaki, N., Jones, C. M., Mercurio, S., Rowe, A., Domingos, P. M., Smith, J. C. and Krumlauf, R. (2003). Wise, a context-dependent activator and inhibitor of Wnt signalling. Development 130, 4295-4305.
20. Iwatsuki, K., Liu, H. X., Grónder, A., Singer, M. A., Lane, T. F., Grosschedl, R., Mistretta, C. M. and Margolskee, R. F. (2007). Wnt signaling interacts with Shh to regulate taste papilla development. Proc. Natl. Acad. Sci. USA 104, 2253-2258.
21. Jamora, C., DasGupta, R., Kocieniewski, P. and Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322.
22. Johnson, E. B., Hammer, R. E. and Herz, J. (2005). Abnormal development of the apical ectodermal ridge and polysyndactyly in Megf7-deficient mice. Hum. Mol. Genet. 14, 3523-3538.
23. Karner, C. M., Dietrich, M. F., Johnson, E. B., Kappesser, N., Tennert, C., Percin, F., Wollnik, B., Carroll, T. J. and Herz, J. (2010). Lrp4 regulates initiation of ureteric budding and is crucial for kidney formation - a mouse model for Cenani-Lenz syndrome. PLoS ONE 5, e10418.
24. Kato, M., Patel, M. S., Levasseur, R., Lobov, I., Chang, B. H., Glass, D. A., II, Hartmann, C., Li, L., Hwang, T. H., Brayton, C. F. et al. (2002). Cbfa1- independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157, 303-314.
25. Kim, N., Stiegler, A. L., Cameron, T. O., Hallock, P. T., Gomez, A. M., Huang, J. H., Hubbard, S. R., Dustin, M. L. and Burden, S. J. (2008). Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 135, 334-342.
26. Laurikkala, J., Kassai, Y., Pakkasjärvi, L., Thesleff, I. and Itoh, N. (2003). Identification of a secreted BMP antagonist, ectodin, integrating BMP, FGF, and SHH signals from the tooth enamel knot. Dev. Biol. 264, 91-105.
27. Lee, E. C., Yu, D., Martinez de Velasco, J., Tessarollo, L., Swing, D. A., Court, D. L., Jenkins, N. A. and Copeland, N. G. (2001). A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65.
28. Lee, M. Y., Racine, V., Jagadpramana, P., Sun, L., Yu, W., Du, T., Spencer-Dene, B., Rubin, N., Le, L., Ndiaye, D. et al. (2011). Ectodermal influx and cell hypertrophy provide early growth for all murine mammary rudiments, and are differentially regulated among them by Gli3. PLoS ONE 6, e26242.
29. Leupin, O., Piters, E., Halleux, C., Hu, S., Kramer, I., Morvan, F., Bouwmeester, T., Schirle, M., Bueno-Lozano, M., Fuentes, F. J. et al. (2011). Bone overgrowth-associated mutations in the LRP4 gene impair sclerostin facilitator function. J. Biol. Chem. 286, 19489-19500.
30. Li, X., Zhang, Y., Kang, H., Liu, W., Liu, P., Zhang, J., Harris, S. E. and Wu, D. (2005). Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J. Biol. Chem. 280, 19883-19887.
31. Li, Y., Pawlik, B., Elcioglu, N., Aglan, M., Kayserili, H., Yigit, G., Percin, F., Goodman, F., Nürnberg, G., Cenani, A. et al. (2010). LRP4 mutations alter Wnt/ -catenin signaling and cause limb and kidney malformations in Cenani- Lenz syndrome. Am. J. Hum. Genet. 86, 696-706.
32. Lindvall, C., Evans, N. C., Zylstra, C. R., Li, Y., Alexander, C. M. and Williams, B. O. (2006). The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J. Biol. Chem. 281, 35081-35087.
33. Lindvall, C., Zylstra, C. R., Evans, N., West, R. A., Dykema, K., Furge, K. A. and Williams, B. O. (2009). The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS ONE 4, e5813.
34. Lintern, K. B., Guidato, S., Rowe, A., Saldanha, J. W. and Itasaki, N. (2009). Characterization of wise protein and its molecular mechanism to interact with both Wnt and BMP signals. J. Biol. Chem. 284, 23159-23168.
35. MacDonald, B. T., Adamska, M. and Meisler, M. H. (2004). Hypomorphic expression of Dkk1 in the doubleridge mouse: dose dependence and compensatory interactions with Lrp6. Development 131, 2543-2552.
36. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
37. May, P., Woldt, E., Matz, R. L. and Boucher, P. (2007). The LDL receptor-related protein (LRP) family: an old family of proteins with new physiological functions. Ann. Med. 39, 219-228.
38. Mikkola, M. L. and Millar, S. E. (2006). The mammary bud as a skin appendage: unique and shared aspects of development. J. Mammary Gland Biol. Neoplasia 11, 187-203.
39. Morvan, F., Boulukos, K., Clément-Lacroix, P., Roman Roman, S., Suc-Royer, I., Vayssière, B., Ammann, P., Martin, P., Pinho, S., Pognonec, P. et al. (2006). Deletion of a single allele of the Dkk1 gene leads to an increase in bone formation and bone mass. J. Bone Miner. Res. 21, 934-945.
40. Munne, P. M., Tummers, M., Järvinen, E., Thesleff, I. and Jernvall, J. (2009). Tinkering with the inductive mesenchyme: Sostdc1 uncovers the role of dental mesenchyme in limiting tooth induction. Development 136, 393-402.
41. Närhi, K., Tummers, M., Ahtiainen, L., Itoh, N., Thesleff, I. and Mikkola, M. L. (2012). Sostdc1 defines the size and number of skin appendage placodes. Dev. Biol. 364, 149-161.
42. Ohazama, A., Johnson, E. B., Ota, M. S., Choi, H. Y., Porntaveetus, T., Oommen, S., Itoh, N., Eto, K., Gritli-Linde, A., Herz, J. et al. (2008). Lrp4 modulates extracellular integration of cell signaling pathways in development. PLoS ONE 3, e4092.
43. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J. and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538.
44. Pispa, J. and Thesleff, I. (2003). Mechanisms of ectodermal organogenesis. Dev. Biol. 262, 195-205.
45. Propper, A. Y. (1978). Wandering epithelial cells in the rabbit embryo milk line. A preliminary scanning electron microscope study. Dev. Biol. 67, 225-231.
46. Robinson, G. W. (2007). Cooperation of signalling pathways in embryonic mammary gland development. Nat. Rev. Genet. 8, 963-972.
47. Schmidt-Ullrich, R. and Paus, R. (2005). Molecular principles of hair follicle induction and morphogenesis. Bioessays 27, 247-261.
48. Semënov, M. V., Tamai, K., Brott, B. K., Kühl, M., Sokol, S. and He, X. (2001). Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11, 951-961.
49. Semënov, M., Tamai, K. and He, X. (2005). SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J. Biol. Chem. 280, 26770-26775.
50. Simon-Chazottes, D., Tutois, S., Kuehn, M., Evans, M., Bourgade, F., Cook, S., Davisson, M. T. and Guénet, J. L. (2006). Mutations in the gene encoding the low-density lipoprotein receptor LRP4 cause abnormal limb development in the mouse. Genomics 87, 673-677.
51. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
52. van Genderen, C., Okamura, R. M., Fariñas, I., Quo, R. G., Parslow, T. G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1- deficient mice. Genes Dev. 8, 2691-2703.
53. Veltmaat, J. M., Van Veelen, W., Thiery, J. P. and Bellusci, S. (2004). Identification of the mammary line in mouse by Wnt10b expression. Dev. Dyn. 229, 349-356.
54. Weatherbee, S. D., Anderson, K. V. and Niswander, L. A. (2006). LDL-receptor- related protein 4 is crucial for formation of the neuromuscular junction. Development 133, 4993-5000.
55. Willnow, T. E., Hammes, A. and Eaton, S. (2007). Lipoproteins and their receptors in embryonic development: more than cholesterol clearance. Development 134, 3239-3249.
56. Yamakado, M. and Yohro, T. (1979). Subdivision of mouse vibrissae on an embryological basis, with descriptions of variations in the number and arrangement of sinus hairs and cortical barrels in BALB/c (nu/+; nude, nu/nu) and hairless (hr/hr) strains. Am. J. Anat. 155, 153-173.
57. Zhang, B., Luo, S., Wang, Q., Suzuki, T., Xiong, W. C. and Mei, L. (2008). LRP4 serves as a coreceptor of agrin. Neuron 60, 285-297.
58. Zhou, C. J., Wang, Y. Z., Yamagami, T., Zhao, T., Song, L. and Wang, K. (2010). Generation of Lrp6 conditional gene-targeting mouse line for modeling and dissecting multiple birth defects/congenital anomalies. Dev. Dyn. 239, 318-326.