Abstract
Neural crest mesenchyme (NCM) controls species-specific pattern in the craniofacial skeleton but how this cell population accomplishes such a complex task remains unclear. To elucidate mechanisms through which NCM directs skeletal development and evolution, we made chimeras from quail and duck embryos, which differ markedly in their craniofacial morphology and maturation rates. We show that quail NCM, when transplanted into duck, maintains its faster timetable for development and autonomously executes molecular and cellular programs for the induction, differentiation, and mineralization of bone, including premature expression of osteogenic genes such as Runx2 and Col1a1. In contrast, the duck host systemic environment appears to be relatively permissive and supports osteogenesis independently by providing circulating minerals and a vascular network. Further experiments reveal that NCM establishes the timing of osteogenesis by regulating cell cycle progression in a stage- and species-specific manner. Altering the time-course of D-type cyclin expression mimics chimeras by accelerating expression of Runx2 and Col1a1. We also discover higher endogenous expression of Runx2 in quail coincident with their smaller craniofacial skeletons, and by prematurely over-expressing Runx2 in chick embryos we reduce the overall size of the craniofacial skeleton. Thus, our work indicates that NCM establishes species-specific size in the craniofacial skeleton by controlling cell cycle, Runx2 expression, and the timing of key events during osteogenesis.
Highlights
The avian craniofacial skeleton exemplifies one of the most highly diversified and adapted anatomical structures across vertebrates
We examined p27 (Cdkn1b), which is a cyclin-dependent kinase inhibitors (CKIs) that decreases proliferation in a range of cell types including differentiating osteoblasts; cyclin E (Ccne1), which is required for G1/S phase transition; and cyclin B1 (Ccnb1), which is required for G2/M phase transition (Coats et al, 1996; Drissi et al, 1999; Zavitz and Zipursky, 1997)
Other work has shown that neural crest mesenchyme (NCM) relies upon and is highly responsive to signals in the local environment that affect gene expression and provide input on the axial orientation, identity, size, and shape of the beak skeleton (Abzhanov et al, 2006; Abzhanov et al, 2004; Barlow et al, 1999; Barlow and Francis-West, 1997; Couly et al, 2002; Foppiano et al, 2007; Francis-West et al, 1998; Francis-West et al, 1994; Hu and Marcucio, 2009a, b, 2012; Hu et al, 2003; Jeong et al, 2004; Shigetani et al, 2000; Wedden, 1987; Wu et al, 2006; Wu et al, 2004)
Summary
The avian craniofacial skeleton exemplifies one of the most highly diversified and adapted anatomical structures across vertebrates. Understanding how the craniofacial skeleton becomes modified through evolution requires insights on where and when species-specific changes to the osteogenic program arise during development. To this end, we employ a unique avian chimeric transplantation system that takes advantage of the divergent maturation rates and distinct species-specific beak anatomies of quail and duck. We have shown that NCM, when transplanted between quail and duck autonomously controls the species-specific patterning of the face, and produces short quail-like beaks on duck hosts (“quck”) and long duck-like bills on quail hosts (“duail”) (Jheon and Schneider, 2009; Lwigale and Schneider, 2008; Schneider, 2005, 2007; Schneider and Helms, 2003). Further investigations have uncovered mechanisms through which NCM exerts its species-specific effects on the cartilaginous skeleton (Eames and Schneider, 2008), the epidermis (Eames and Schneider, 2005), the jaw musculature and adjacent connective tissues (Solem et al, 2011; Tokita and Schneider, 2009), and the overlying epithelium during intramembranous ossification (Merrill et al, 2008), but little is known about mechanisms through which NCM directs species-specific formation of the bony skeleton
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