title: Evolution of a developmental mechanism: Species-specific regulation of the cell cycle and the timing of events during craniofacial osteogenesis.
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.
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: Jane
authors.initials: J
authors.lastname: Hall
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: Andrew H
authors.initials: AH
authors.lastname: Jheon
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: Erin L
authors.initials: EL
authors.lastname: Ealba
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: B Frank
authors.initials: BF
authors.lastname: Eames
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: Kristin D
authors.initials: KD
authors.lastname: Butcher
authors.affiliation: RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minami, Chuo-ku Kobe 650-0047, Japan.
authors.forename: Siu-Shan
authors.initials: SS
authors.lastname: Mak
authors.affiliation: RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minami, Chuo-ku Kobe 650-0047, Japan.
authors.forename: Raj
authors.initials: R
authors.lastname: Ladher
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA.
authors.forename: Tamara
authors.initials: T
authors.lastname: Alliston
authors.affiliation: University of California at San Francisco, Department of Orthopaedic Surgery, 513 Parnassus Avenue, S-1161, San Francisco, CA 94143-0514, USA. Electronic address: rich.schneider@ucsf.edu.
authors.forename: Richard A
authors.initials: RA
authors.lastname: Schneider
mesh_terms: D000818:Animals; D001483:Base Sequence; D001808:Blood Vessels / Q000254:growth & development; D015153:Blotting, Western; D002453:Cell Cycle / Q000235:genetics*; D003370:Coturnix; D017931:DNA Primers; D004372:Ducks; D019143:Evolution, Molecular; D005145:Face; D010012:Osteogenesis / Q000235:genetics*; D012886:Skull / Q000254:growth & development*; D013045:Species Specificity
chemical_list: D017931:DNA Primers
keywords: Cell cycle regulation; Cranial neural crest; Craniofacial osteogenesis; Evolutionary developmental biology; Quail–duck and quail–emu chimeras; Runx2