While much is known regarding morphogenetic factors involved in specification and differentiation of Rathke’s pouch, less attention has been given to extracellular matrix (ECM) interactions involved in its formation. The present research investigated localization of two different chondroitin sulfate glycosaminoglycans (CS-GAGs), TC2 and d1C4, and versican CS-proteoglycan (PG) to identify additional ECM molecules involved in formation of the pituitary rudiment. Immunohistochemical evaluation of anterior pituitary primordia between HH15 and HH28 showed these ECM molecules prevalent in basement membrane and surrounding ECM underlying Rathke’s epithelia and to a lesser extent between pouch epithelial cells. TC2/d1C4 CS-GAGs and versican showed changing and heterogeneous localization during pouch development that suggested specific roles in cell-ECM interaction during pituitary morphogenesis. TC2 antigen colocalized with versican at early stages in an asymmetric pattern, with particularly strong staining between ventral diencephalon and roof of Rathke’s pouch while d1C4 CS-GAG encompassed the entire pouch by HH22 indicating association with a different CSPG. The heparan sulfate proteoglycan, perlecan, used to verify basement membrane structure, was a consistent component of Rathke’s pouch. Data show a dynamic and heterogeneous pattern of CS-GAG and versican expression during early chick Rathke’s pouch development that suggests new possibilities for ECM function in its establishment and growth. 1. Introduction The pituitary gland is a small, lobed organ located at the base of the brain behind the optic chiasm in a concavity of the sphenoid bone. The anterior lobe or adenohypophysis derives from oral ectoderm and originates from Rathke’s pouch [1], a hollow diverticulum that extends upwards from the stomodeum to underlie the diencephalon in the region of the infundibulum. An outpocketing of the infundibulum forms the primordium of the posterior lobe or neurohypophysis. In the chick, it has also been suggested that formation of Rathke’s pouch may include a neuroectodermal contribution along with its stomodeal origin [2], with evagination and expansion toward the prechordal plate and anterior tip of the notochord underway by Hamburger and Hamilton stage 14 (HH14) [3]. Formation of lateral lobes at the lower end of Rathke’s pouch by HH17/18 indicates beginning of the pars tuberalis and by HH25–28 developing glandular tissue of the pars distalis is evident during which time the proximal aspects of Rathke’s pouch have become progressively constricted [4]. Over the
References
[1]
H. Rathke, “Uber die entstehung der glandula pituitaria,” Archives of Anatomy and Physiology (Müller’s Archives), vol. 5, pp. 482–485, 1838.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[22]
L. Zhang, “Glycosaminoglycan (GAG) biosynthesis and GAG-binding proteins,” Progress in Molecular Biology and Translational Science, vol. 93, pp. 1–17, 2010.
[23]
R. V. Iozzo, “Matrix proteoglycans: from molecular design to cellular function,” Annual Review of Biochemistry, vol. 67, pp. 609–652, 1998.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.