Table of Contents
International Journal of Embryology
Volume 2014, Article ID 173256, 11 pages
http://dx.doi.org/10.1155/2014/173256
Research Article

Heterogeneous Expression of Chondroitin Sulfate Glycosaminoglycans and Versican Proteoglycan during Early Development of Rathke’s Pouch

Department of Biology, East Carolina University, N108 Howell Science Complex, Greenville, NC 27858, USA

Received 29 August 2014; Accepted 25 November 2014; Published 14 December 2014

Academic Editor: M. Michele Pisano

Copyright © 2014 Sheelah Iyengar and Anthony A. Capehart. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Rathke, “Uber die entstehung der glandula pituitaria,” Archives of Anatomy and Physiology (Müller’s Archives), vol. 5, pp. 482–485, 1838. View at Google Scholar
  2. A. G. Jacobson, D. M. Miyamoto, and S. H. Mai, “Rathke’s pouch morphogenesis in the chick embryo,” Journal of Experimental Zoology, vol. 207, pp. 351–366, 1979. View at Google Scholar
  3. V. Hamburger and H. Hamilton, “A series of normal stages in the development of the chick embryo,” Journal of Morphology, vol. 8, pp. 241–245, 1951. View at Google Scholar
  4. W. J. Atwell and I. Sitler, “The early appearance of the anlagen of the pars tuberalis in the hypophysis of the chick,” The Anatomical Record, vol. 15, no. 4, pp. 181–187, 2005. View at Google Scholar
  5. C. G. Scanes, L. E. Hart, E. Decuypere, and E. R. Kuhn, “Endocrinology of the avian embryo: an overview,” Journal of Experimental Zoology, vol. 1, pp. 253–264, 1987. View at Google Scholar · View at Scopus
  6. J. Ericson, S. Norlin, T. M. Jessell, and T. Edlund, “Integrated FGF and BMP signaling controls the progression of progenitor cell differentiation and the emergence of pattern in the embryonic anterior pituitary,” Development, vol. 125, no. 6, pp. 1005–1015, 1998. View at Google Scholar · View at Scopus
  7. Y. Maruoka, N. Ohbayashi, M. Hoshikawa, N. Itoh, B. L. M. Hogan, and Y. Furuta, “Comparison of the expression of three highly related genes, Fgf8, Fgf17 and Fgf18, in the mouse embryo,” Mechanisms of Development, vol. 74, no. 1-2, pp. 175–177, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Treier, A. S. Gleiberman, S. M. O’Connell et al., “Multistep signaling requirements for pituitary organogenesis in vivo,” Genes and Development, vol. 12, no. 11, pp. 1691–1704, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Takuma, H. Z. Sheng, Y. Furuta et al., “Formation of Rathke’s pouch requires dual induction from the diencephalon,” Development, vol. 125, no. 23, pp. 4835–4840, 1998. View at Google Scholar · View at Scopus
  10. M. Treier, S. O’Connell, A. Gleiberman et al., “Hedgehog signaling is required for pituitary gland development,” Development, vol. 128, no. 3, pp. 377–386, 2001. View at Google Scholar · View at Scopus
  11. L. E. Olson, J. Tollkuhn, C. Scafoglio et al., “Homeodomain-mediated beta-catenin-dependent switching events dictate cell-lineage determination,” Cell, vol. 125, no. 3, pp. 593–605, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Zhu, A. S. Gleiberman, and M. G. Rosenfeld, “Molecular physiology of pituitary development: signaling and transcriptional networks,” Physiological Reviews, vol. 87, no. 3, pp. 933–963, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. J. Horacek, J. C. Thompson, M. O. Dada, and L. Terracio, “The extracellular matrix components laminin, fibronectin, and collagen IV are present among the epithelial cells forming Rathke’s pouch,” Acta Anatomica, vol. 147, no. 2, pp. 69–74, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. R. E. Waterman and G. Balian, “Indirect immonufluorescent staining of fibronectin associated with the floor of the foregut during formation and rupture of the oral membrane in the chick embryo,” Anatomical Record, vol. 198, no. 4, pp. 619–635, 1980. View at Publisher · View at Google Scholar · View at Scopus
  15. V. S. LeBleu, B. MacDonald, and R. Kalluri, “Structure and function of basement membranes,” Experimental Biology and Medicine, vol. 232, no. 9, pp. 1121–1129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. A. A. Capehart, M. M. Wienecke, G. T. Kitten, M. Solursh, and E. L. Krug, “Production of a monoclonal antibody by in vitro immunization that recognizes a native chondroitin sulfate epitope in the embryonic chick limb and heart,” Journal of Histochemistry and Cytochemistry, vol. 45, no. 11, pp. 1567–1581, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. A. A. Capehart, J.-L. Scemama, C. A. Singhas, and S. Cox, “Heterogeneity of chondroitin sulfate glycosaminoglycan localization during early development of the striped bass (Morone saxatilis),” Anatomical Record, vol. 268, no. 1, pp. 47–58, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. C. H. Mjaatvedt, H. Yamamura, A. A. Capehart, D. Turner, and R. R. Markwald, “The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation,” Developmental Biology, vol. 202, no. 1, pp. 56–66, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. J. B. Shepard, D. A. Gliga, A. P. Morrow, S. Hoffman, and A. A. Capehart, “Versican knock-down compromises chondrogenesis in the embryonic chick limb,” Anatomical Record, vol. 291, no. 1, pp. 19–27, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Choocheep, S. Hatano, H. Takagi, H. Watanabe, K. Kimata, and P. Kongtawelert, “Versican facilitates chondrocyte differentiation and regulates joint morphogenesis,” The Journal of Biological Chemistry, vol. 285, no. 27, pp. 21114–21125, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. P. S. Nagchowdhuri, K. N. Andrews, S. Robart, and A. A. Capehart, “Versican knockdown reduces interzone area during early stages of chick synovial joint development,” Anatomical Record, vol. 295, no. 3, pp. 397–409, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Zhang, “Glycosaminoglycan (GAG) biosynthesis and GAG-binding proteins,” Progress in Molecular Biology and Translational Science, vol. 93, pp. 1–17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. R. V. Iozzo, “Matrix proteoglycans: from molecular design to cellular function,” Annual Review of Biochemistry, vol. 67, pp. 609–652, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. A. A. Capehart, C. H. Mjaatvedt, S. Hoffman, and E. L. Krug, “Dynamic expression of a native chondroitin sulfate epitope reveals microheterogeneity of extracellular matrix organization in the embryonic chick heart,” The Anatomical Record, vol. 254, pp. 181–195, 1999. View at Publisher · View at Google Scholar
  25. M. K. B. Zanin, J. Bundy, H. Ernst, A. Wessels, S. J. Conway, and S. Hoffman, “Distinct spatial and temporal distributions of aggrecan and versican in the embryonic chick heart,” The Anatomical Record, vol. 256, pp. 366–380, 1999. View at Google Scholar
  26. H. E. Snow, L. M. Riccio, C. H. Mjaatvedt, S. Hoffman, and A. A. Capehart, “Versican expression during skeletal/joint morphogenesis and patterning of muscle and nerve in the embryonic mouse limb,” The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology, vol. 282, no. 2, pp. 95–105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Romanoff, The Avian Embryo, The Macmillan Company, New York, NY, USA, 1960.
  28. R. Bellairs and M. Osmond, The Atlas of Chick Development, Academic Press, New York, NY, USA, 1998.
  29. J. R. Couchman, R. Kapoor, M. Sthanam, and R.-R. Wu, “Perlecan and basement membrane-chondroitin sulfate proteoglycan (bamacan) are two basement membrane chondroitin/dermatan sulfate proteoglycans in the Engelbreth-Holm-Swarm tumor matrix,” Journal of Biological Chemistry, vol. 271, no. 16, pp. 9595–9602, 1996. View at Publisher · View at Google Scholar · View at Scopus
  30. C. E. Bandtlow and D. R. Zimmermann, “Proteoglycans in the developing brain: new conceptual insights for old proteins,” Physiological Reviews, vol. 80, no. 4, pp. 1267–1290, 2000. View at Google Scholar · View at Scopus
  31. R. A. Asher, D. A. Morgenstern, M. C. Shearer, K. H. Adcock, P. Pesheva, and J. W. Fawcett, “Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells,” The Journal of Neuroscience, vol. 22, no. 6, pp. 2225–2236, 2002. View at Google Scholar · View at Scopus
  32. R. M. Landolt, L. Vaughan, K. H. Winterhalter, and D. R. Zimmermann, “Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth,” Development, vol. 121, no. 8, pp. 2303–2312, 1995. View at Google Scholar · View at Scopus
  33. B. Bode-Lesniewska, M. T. Dours-Zimmermann, B. F. Odermatt, J. Briner, P. U. Heitz, and D. R. Zimmermann, “Distribution of the large aggregating proteoglycan versican in adult human tissues,” Journal of Histochemistry & Cytochemistry, vol. 44, no. 4, pp. 303–312, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Rahmani, B. W. Wong, L. Ang et al., “Versican: signaling to transcriptional control pathways,” Canadian Journal of Physiology and Pharmacology, vol. 84, no. 1, pp. 77–92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Takagi, K. Nagashima, M. Inoue, I. Sakata, and T. Sakai, “Detailed analysis of formation of chicken pituitary primordium in early embryonic development,” Cell and Tissue Research, vol. 333, no. 3, pp. 417–426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. P. D. Yurchenco, “Basement membranes: cell scaffoldings and signaling platforms,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 2, pp. 1–12, 2011. View at Publisher · View at Google Scholar
  37. Y. J. Wu, D. P. La Pierre, J. Wu, A. J. Yee, and B. B. Yang, “The interaction of versican with its binding partners,” Cell Research, vol. 15, no. 7, pp. 483–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Iwai-Liao, S. Kumabe, M. Takeuchi, and Y. Higashi, “Immunohistochemical localisation of epidermal growth factor, transforming growth factor α and EGF receptor during organogenesis of the murine hypophysis in vivo,” Okajimas Folia Anatomica Japonica, vol. 76, no. 6, pp. 291–302, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Miyazaki, S. Miyauchi, A. Tawada, T. Anada, S. Matsuzaka, and O. Suzuki, “Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation,” Journal of Cellular Physiology, vol. 217, no. 3, pp. 769–777, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. D. M. Whalen, T. Malinauskas, R. J. C. Gilbert, and C. Siebold, “Structural insights into proteoglycan-shaped Hedgehog signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 41, pp. 16420–16425, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. S. M.-L. Smith, L. A. West, P. Govindraj, X. Zhang, D. M. Ornitz, and J. R. Hassell, “Heparan and chondroitin sulfate on growth plate perlecan mediate binding and delivery of FGF-2 to FGF receptors,” Matrix Biology, vol. 26, no. 3, pp. 175–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Kitagawa, K. Tsutsumi, Y. Tone, and K. Sugahara, “Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain,” The Journal of Biological Chemistry, vol. 272, no. 50, pp. 31377–31381, 1997. View at Publisher · View at Google Scholar · View at Scopus