Villification in the mouse: Bmp signals control intestinal villus patterning

Development (Cambridge)

Volumn 143, Issue 3, 2016, Pages 427-436

  Walton, Katherine D ^a   Whidden, Mark ^a   Kolterud, Åsa ^b   Shoffner, Suzanne K ^a   Czerwinski, Michael J ^a   Kushwaha, Juhi ^a   Parmar, Nishita ^a   Chandhrasekhar, Deepa ^a   Freddo, Andrew M ^a   Schnell, Santiago ^a   Gumucio, Deborah L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Activator inhibitor patterning model Turing field; Epithelial mesenchymal crosstalk; Intestinal development; Mathematical model; Morphogenesis; Villus formation

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SONIC HEDGEHOG PROTEIN; BMPR1A PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; LIGAND;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EXPLANT; FEMALE; GENE EXPRESSION; IN VIVO STUDY; INTESTINE EPITHELIUM; INTESTINE VILLUS; MATHEMATICAL MODEL; MESENCHYME; MESENCHYME CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; TENSILE STRENGTH; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; EMBRYOLOGY; EPITHELIUM; IN SITU HYBRIDIZATION; INTESTINE; MESODERM; METABOLISM; MICROVILLUS; MORPHOGENESIS; ORGAN SIZE;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; EPITHELIUM; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; INTESTINES; LIGANDS; MESODERM; MICE, INBRED C57BL; MICROVILLI; MODELS, BIOLOGICAL; MUSCLE, SMOOTH; ORGAN SIZE; SIGNAL TRANSDUCTION; TENSILE STRENGTH;

EID: 84956686374     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.130112     Document Type: Article

References (52)

1. Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D. and Joyner, A. L. (2002). Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761.
2. Baker, R. E., Schnell, S. and Maini, P. K. (2009). Waves and patterning in developmental biology: vertebrate segmentation and feather bud formation as case studies. Int. J. Dev. Biol. 53, 783-794.
3. Coulombre, A. J. and Coulombre, J. L. (1958). Intestinal development. I. Morphogenesis of the villi and musculature. J. Embryol. Exp. Morphol. 6, 403-411.
4. de Castro, A. M. M. G., Alvares, E. P., Zocoller-Seno, M. C., Neves, M. F. and Passipieri, M. (2001). Morphological study of the small intestine of moura pigs (Sus scrofa- Lineaus, 1758) during fetal development. Braz. J. Morphol. Sci. 18, 95-101.
5. Dekaney, C. M., Bazer, F. W. and Jaeger, L. A. (1997). Mucosal morphogenesis and cytodifferentiation in fetal porcine small intestine. Anat. Rec. 249, 517-523.
6. Dillon, R. and Othmer, H. G. (1993). Control of gap junction permeability can control pattern formation in limb development. Exp. Theor. Adv. Biol. Pattern Format. 259, 65-81.
7. Dunn, J. S. (1967). The fine structure of the absorptive epithelial cells of the developing small intestine of the rat. J. Anat. 101, 57-68.
8. Economou, A. D., Ohazama, A., Porntaveetus, T., Sharpe, P. T., Kondo, S., Basson, M. A., Gritli-Linde, A., Cobourne, M. T. and Green, J. B. (2012). Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 44, 348-351.
9. Eom, D. S., Amarnath, S., Fogel, J. L. and Agarwala, S. (2011). Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway. Development 138, 3179-3188.
10. Eom, D. S., Inoue, S., Patterson, L. B., Gordon, T. N., Slingwine, R., Kondo, S., Watanabe, M. and Parichy, D. M. (2012). Melanophore migration and survival during zebrafish adult pigment stripe development require the immunoglobulin superfamily adhesion molecule Igsf11. PLoS Genet. 8, e1002899.
11. Fekete, E., Benedeczky, I., Timmermans, J. P., Resch, B. A. and Scheuermann, D.W. (1996). Sequential pattern of nerve-muscle contacts in the small intestine of developing human fetus. An ultrastructural and immunohistochemical study. Histol. Histopathol. 11, 845-850.
12. Garfinkel, A., Tintut, Y., Petrasek, D., Bostrom, K. and Demer, L. L. (2004). Pattern formation by vascular mesenchymal cells. Proc. Natl. Acad. Sci. USA 101, 9247-9250.
13. Georgieva, R. and Gerov, K. (1975). The morphological and functional differentiation of the alimentary canal of the pig during ontogeny. II. Development and differentiation of the jejunum. Anat. Anz. 137, 16-20.
14. Gibson, M. C. and Perrimon, N. (2005). Extrusion and death of DPP/BMPcompromised epithelial cells in the developing Drosophila wing. Science 307, 1785-1789.
15. Gierer, A. and Meinhardt, H. (1972). Theory of biological pattern formation. Kybernetik 12, 30-39.
16. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
17. Hamilton, T. G., Klinghoffer, R. A., Corrin, P. D. and Soriano, P. (2003). Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol. Cell. Biol. 23, 4013-4025.
18. Harfe, B., Scherz, P., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
19. Harris, M. P., Williamson, S., Fallon, J. F., Meinhardt, H. and Prum, R. O. (2005). Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc. Natl. Acad. Sci. USA 102, 11734-11739.
20. Hogan, B. L. M. (1996). Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6, 432-438.
21. Johnson, F. P. (1910). The development of the mucous membrane of the oesophagus, stomach and small intestine in the human embryo. Am. J. Anat. 10, 521-575.
22. Karlsson, L., Lindahl, P., Heath, J. K. and Betsholtz, C. (2000). Abnormal gastrointestinal development in PDGF-A and PDGFR-(alpha) deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis. Development 127, 3457-3466.
23. Kedinger, M., Simon-Assmann, P., Bouziges, F., Arnold, C., Alexandra, E. and Haffen, K. (1990). Smooth muscle actin expression during rat gut development and induction in fetal skin fibroblastic cells associated with intestinal embryonic epithelium. Differentiation 43, 87-97.
24. Keibel, F. and Mall, F. P. (1910). Manual of Human Embryology. Philadelphia: J. B. Lippincott Company.
25. Kolterud, A., Grosse, A. S., Zacharias, W. J., Walton, K., Kretovich, K. E., Madison, B. B., Waghray, M., Ferris, J. E., Hu, C., Merchant, J. L. et al. (2009). Paracrine Hedgehog signaling in stomach and intestine: new roles for hedgehog in gastrointestinal patterning. Gastroenterology 137, 618-628.
26. Kondo, S. and Miura, T. (2010). Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616-1620.
27. Lacroix, B., Kedinger, M., Simon-Assmann, P. and Haffen, K. (1984). Early organogenesis of human small intestine: scanning electron microscopy and brush border enzymology. Gut 25, 925-930.
28. Li, X., Madison, B. B., Zacharias, W., Kolterud, A., States, D. and Gumucio, D. L. (2007). Deconvoluting the intestine: molecular evidence for a major role of the mesenchymein themodulationof signalingcrosstalk.Physiol.Genomics 29, 290-301.
29. Madison, B. B., Braunstein, K., Kuizon, E., Portman, K., Qiao, X. T. and Gumucio, D. L. (2005). Epithelial hedgehog signals pattern the intestinal cryptvillus axis. Development 132, 279-289.
30. Maini, P. K. (2004). The impact of Turing’s work on pattern fomation in biology. Math. Today 40, 73-92.
31. Maini, P. K., Baker, R. E. and Chuong, C.-M. (2006). Developmental biology: the Turing model comes of molecular age. Science 314, 1397-1398.
32. Mathan, M., Moxey, P. C. and Trier, J. S. (1976). Morphogenesis of fetal rat duodenal villi. Am. J. Anat. 146, 73-92.
33. Matsumoto, A., Hashimoto, K., Yoshioka, T. and Otani, H. (2002). Occlusion and subsequent re-canalization in early duodenal development of human embryos: integrated organogenesis and histogenesis through a possible epithelialmesenchymal interaction. Anat. Embryol. 205, 53-65.
34. Meinhardt, H. (2012). Turing’s theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and longrange inhibition. Interface Focus 2, 407-416.
35. Mishina, Y., Hanks, M. C., Miura, S., Tallquist, M. D. and Behringer, R. R. (2002). Generation of Bmpr/Alk3 conditional knockout mice. Genesis 32, 69-72.
36. Mou, C., Pitel, F., Gourichon, D., Vignoles, F., Tzika, A., Tato, P., Yu, L., Burt, D.W., Bed’hom, B., Tixier-Boichard, M. et al. (2011). Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering. PLoS Biol. 9, e1001028.
37. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
38. Nakamura, K. and Komuro, T. (1983). A three-dimensional study of the embryonic development and postnatal maturation of rat duodenal villi. J. Electron Microsc. 32, 338-347.
39. Rajagopal, R., Huang, J., Dattilo, L. K., Kaartinen, V., Mishina, Y., Deng, C.-X., Umans, L., Zwijsen, A., Roberts, A. B. and Beebe, D. C. (2009). The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev. Biol. 335, 305-316.
40. Raspopovic, J., Marcon, L., Russo, L. and Sharpe, J. (2014). Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 345, 566-570.
41. Roberts, D. J., Johnson, R. L., Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121, 3163-3174.
42. Sbarbati, R. (1982). Morphogenesis of the intestinal villi of the mouse embryo: chance and spatial necessity. J. Anat. 135, 477-499.
43. Shen, J. and Dahmann, C. (2005). Extrusion of cells with inappropriate Dpp signaling from Drosophila wing disc epithelia. Science 307, 1789-1790.
44. Shyer, A. E., Tallinen, T., Nerurkar, N. L., Wei, Z., Gil, E. S., Kaplan, D. L., Tabin, C. J. and Mahadevan, L. (2013). Villification: how the gut gets its villi. Science 342, 212-218.
45. Shyer, A. E., Huycke, T. R., Lee, C., Mahadevan, L. and Tabin, C. J. (2015). Bending gradients: how the intestinal stem cell gets its home. Cell 161, 569-580.
46. Sick, S., Reinker, S., Timmer, J. and Schlake, T. (2006).WNTandDKKdetermine hair follicle spacing through a reaction-diffusion mechanism. Science 314, 1447-1450.
47. Trahair, J. and Robinson, P. (1986). The development of the ovine small intestine. Anat. Rec. 214, 294-303.
48. Turing, A. M. (1952). The chemical basis of morphogenesis. Philos. Trans. R. Soc. B Biol. Sci. 237, 37-72.
49. Walton, K. D. and Kolterud, A. (2014). Mouse fetal whole intestine culture system for ex vivo manipulation of signaling pathways and three-dimensional live imaging of villus development. J. Vis. Exp. 91, e51817.
50. Walton, K. D., Kolterud, A., Czerwinski, M. J., Bell, M. J., Prakash, A., Kushwaha, J., Grosse, A. S., Schnell, S. and Gumucio, D. L. (2012). Hedgehog-responsive mesenchymal clusters direct patterning and emergence of intestinal villi. Proc. Natl. Acad. Sci. USA 109, 15817-15822.
51. Wells, J. M. and Spence, J. R. (2014). How to make an intestine. Development 141, 752-760.
52. Zhou, Y., Liu, H.-X. and Mistretta, C. M. (2006). Bone morphogenetic proteins and noggin: inhibiting and inducing fungiform taste papilla development. Dev. Biol. 297, 198-213.