Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-13T02:37:21.494Z Has data issue: false hasContentIssue false

2 - The Contribution of Angiogenesis to Variation in Bone Development and Evolution

Published online by Cambridge University Press:  25 March 2017

Christopher J. Percival
Affiliation:
University of Calgary
Joan T. Richtsmeier
Affiliation:
Pennsylvania State University
Get access
Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abzhanov, A., Rodda, S. J., McMahon, A. P. and Tabin, C. J. (2007). Regulation of skeletogenic differentiation in cranial dermal bone. Development, 134, 31333144.CrossRefGoogle ScholarPubMed
Aldridge, K., Hill, C. A., Austin, J. R., et al. (2010). Brain phenotypes in two FGFR2 mouse models for Apert syndrome. Developmental Dynamics, 239, 987997.Google Scholar
Amizuka, N., Hasegawa, T., Oda, K., et al. (2012). Histology of epiphyseal cartilage calcification and endochondral ossification. Frontiers in Bioscience, 4, 20852100.CrossRefGoogle ScholarPubMed
Athreya, S. (2009). A comparative study of frontal bone morphology among Pleistocene hominin fossil groups. Journal of Human Evolution, 57, 786804.CrossRefGoogle ScholarPubMed
Auguste, P., Gürsel, D. B., Lemière, S., et al. (2001). Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and-independent mechanisms. Cancer Research, 61, 17171726.Google ScholarPubMed
Bates, C. M. (2007). Role of fibroblast growth factor receptor signaling in kidney development. Pediatric Nephrology, 22, 343349.Google Scholar
Beals, K. L., Smith, C. L. and Dodd, S. M. (1984). Brain size, cranial morphology, climate, and time machines. Current Anthropology, 25, 301330.Google Scholar
Bloom, W. and Fawcett, D. W. (1994). A Textbook of Histology. New York, NY: Chapman & Hall.Google Scholar
Carmody, R. N., Weintraub, G. S. and Wrangham, R. W. (2011). Energetic consequences of thermal and nonthermal food processing. Proceedings of the National Academy of Sciences, 108, 1919919203.Google Scholar
Carroll, S. B., Grenier, J. K. and Weatherbee, S. D. (2001). From DNA to Diversity. London: Blackwell Science.Google Scholar
Cobb, S. N. and O’Higgins, P. (2004). Hominins do not share a common postnatal facial ontogenetic shape trajectory. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 302, 302321.CrossRefGoogle ScholarPubMed
Cohen Jr, M. M. and Maclean, R. E. (2000). Craniosynostosis: Diagnosis, Evaluation and Management, 2nd ed. New York, NY: Oxford University Press.Google Scholar
Colnot, C., Lu, C., Hu, D. and Helms, J. A. (2004). Distinguishing the contributions of the perichondrium, cartilage, and vascular endothelium to skeletal development. Developmental Biology, 269, 5569.CrossRefGoogle ScholarPubMed
Dean, C., Leakey, M. G., Reid, D., et al. (2001). Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature, 414, 628631.Google Scholar
Drake, A. G. and Klingenberg, C. P. (2008). The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proceedings of the Royal Society B: Biological Sciences, 275, 7176.CrossRefGoogle Scholar
Drushel, R. F., Pechak, D. G. and Caplan, A. I. (1985). The anatomy, ultrastructure and fluid dynamics of the developing vasculature of the embryonic chick wing bud. Cell Differentiation, 16, 1328.Google Scholar
Dufton, M. and Franz-Odendaal, T. A. (2015). Morphological diversity in the orbital bones of two teleosts with experimental and natural variation in eye size. Developmental Dynamics, 244, 11091120.CrossRefGoogle ScholarPubMed
Dufton, M., Hall, B. K. and Franz-Odendaal, T. A. (2012). Early lens ablation causes dramatic long-term effects on the shape of bones in the craniofacial skeleton of Astyanax mexicanus. PLoS ONE, 7, e50308.Google Scholar
Eames, B. F. and Helms, J. A. (2004). Conserved molecular program regulating cranial and appendicular skeletogenesis. Developmental Dynamics, 231, 413.Google Scholar
Eames, B. F., De La Fuente, L. and Helms, J. A. (2003). Molecular ontogeny of the skeleton. Birth Defects Research Part A: Clinical and Molecular Teratology, 69, 93101.Google Scholar
Eshkar-Oren, I., Viukov, S. V., Salameh, S., et al. (2009). The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation of Vegf. Development, 136, 12631272.Google Scholar
Eswarakumar, V. P., Monsonego-Ornan, E., Pines, M., et al. (2002). The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development, 129, 37833793.Google Scholar
Falk, D. (1992). Evolution of the Brain and Cognition in Hominids. New York, NY: American Museum of Natural History.Google Scholar
Fleagle, J. G., Babbitt, C. C. and Baden, A. L. (2010). Primate cranial diversity. American Journal of Physical Anthropology, 142, 565578.Google Scholar
Franz-Odendaal, T. A. (2011). Induction and patterning of intramembranous bone. Frontiers in Bioscience, 16, 27342746.CrossRefGoogle ScholarPubMed
Gould, S. J. (1977). Ontogeny and Phylogeny. Cambridge, MA: Belknap Press.Google Scholar
Gregory, W. K. (1947). The monotremes and the palimpsest theory. Bulletin of the American Museum of Natural History, 88, 152.Google Scholar
Hall, B. K. (1999). Evolutionary Developmental Biology. Dodrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Hall, B. K. (2003). Evo–Devo: evolutionary developmental mechanisms. International Journal of Developmental Biology, 47, 491496.Google Scholar
Hallgrímsson, B., Jamniczky, H., Young, N. M., et al. (2009). Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36, 355376.Google Scholar
Herring, S. (2008). Mechanical influences on suture development and patency. Frontiers of Oral Biology, 12, 4156.CrossRefGoogle ScholarPubMed
Heuzé, Y., Holmes, G., Peter, I., Richtsmeier, J. T. and Jabs, E. W. (2014). Closing the gap: genetic and genomic continuum from syndromic to nonsyndromic craniosynostoses. Current Genetic Medicine Reports 2, 135145.Google Scholar
Holloway, J. R. L. (1969). Culture: a human domain. Current Anthropology, 10, 395412.CrossRefGoogle Scholar
Iseki, S., Wilkie, A. O. and Morriss-Kay, G. M. (1999). Fgfr1 and Fgfr2 have distinct differentiation- and proliferation-related roles in the developing mouse skull vault. Development, 126, 56115620.Google Scholar
Isler, K., Christopher Kirk, E., Miller, J., et al. (2008). Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. Journal of Human Evolution, 55, 967978.Google Scholar
Jabalee, J. and Franz-Odendaal, T. A. (2015). Vascular endothelial growth factor signaling affects both angiogenesis and osteogenesis during the development of scleral ossicles. Developmental Biology, 406, 5262.Google Scholar
Javerzat, S., Auguste, P. and Bikfalvi, A. (2002). The role of fibroblast growth factors in vascular development. Trends in Molecular Medicine, 8, 483489.Google Scholar
Jeffery, N. and Spoor, F. (2002). Brain size and the human cranial base: a prenatal perspective. American Journal of Physical Anthropology, 118, 324340.Google Scholar
Jourdeuil, K. and Franz-Odendaal, T. A. (2012). Vasculogenesis and the induction of skeletogenic condensations in the avian eye. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 295, 691698.CrossRefGoogle ScholarPubMed
Kanda, S., Landgren, E., Ljungström, M. and Claesson-Welsh, L. (1996). Fibroblast growth factor receptor 1-induced differentiation of endothelial cell line established from tsA58 large T transgenic mice. Cell Growth & Differentiation, 7, 383395.Google Scholar
Karaplis, A. C. (2008). Embryonic development of bone and regulation of intramembranous and endochondral bone formation. In: Bilezikian, J. P., Raisz, L. G. and Martin, T. J. (eds.) Principles of Bone Biology. 3rd ed. New York, NY: Academic Press, pp. 5384.Google Scholar
Kay, R. F., Cartmill, M. and Balow, M. (1998). The hypoglossal canal and the origin of human vocal behavior. Proceedings of the National Academy of Sciences, 95, 54175419.CrossRefGoogle ScholarPubMed
Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., et al. (2001). Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Developmental Biology, 230, 230242.CrossRefGoogle ScholarPubMed
Kish, P. E., Bohnsack, B. L., Gallina, D., Kasprick, D. S. and Kahana, A. (2011). The eye as an organizer of craniofacial development. Genesis, 49, 222230.Google Scholar
Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353357.Google Scholar
Kronenberg, H. M. (2003). Developmental regulation of the growth plate. Nature, 423: 332336.Google Scholar
Krovitz, G. (2000). Three-dimensional comparisons of craniofacial morphology and growth patterns in Neanderthals and modern humans. PhD Dissertation, Johns Hopkins University.Google Scholar
Lahr, M. M. (1996). The Evolution of Modern Human Diversity: A Study of Cranial Variation. Cambridge: Cambridge University Press.Google Scholar
Lambert, J. E., Chapman, C. A., Wrangham, R. W. and Conklin-Brittain, N. L. (2004). Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125, 363368.Google Scholar
Leigh, S. R. (2004). Brain growth, life history, and cognition in primate and human evolution. American Journal of Primatology, 62, 139164.Google Scholar
Lele, S. and Richtsmeier, J. T. (1991). Euclidean distance matrix analysis: a coordinate-free approach for comparing biological shapes using landmark data. American Journal of Physical Anthropology, 86, 415427.CrossRefGoogle ScholarPubMed
Lieberman, D. E., Ross, C. F. and Ravosa, M. J. (2000). The primate cranial base: ontogeny, function, and integration. American Journal of Physical Anthropology, 113, 117169.Google Scholar
Lieberman, D. E., McBratney, B. M. and Krovitz, G. (2002). The evolution and development of cranial form in Homosapiens. Proceedings of the National Academy of Science, 99, 11341139.Google Scholar
Lieberman, D. E., Hallgrímsson, B., Liu, W., Parsons, T. E. and Jamniczky, H. A. (2008). Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. Journal of Anatomy, 212, 720735.Google Scholar
Lovejoy, C. O., McCollum, M. A., Reno, P. L. and Rosenman, B. A. (2003). Developmental biology and human evolution. Annual Review of Anthropology, 32, 85109.CrossRefGoogle Scholar
Mackie, E. J., Ahmed, Y. A., Tatarczuch, L., Chen, K. S. and Mirams, M. (2008). Endochondral ossification: how cartilage is converted into bone in the developing skeleton. The International Journal of Biochemistry & Cell Biology, 40, 4662.Google Scholar
MacLarnon, A. M. and Hewitt, G. P. (1999). The evolution of human speech: the role of enhanced breathing control. American Journal of Physical Anthropology, 109, 341363.Google Scholar
Marcucio, R. S., Young, N. M., Hu, D. and Hallgrimsson, B. (2011). Mechanisms that underlie co-variation of the brain and face. Genesis, 49, 177189.Google Scholar
Martínez-Abadías, N., Percival, C., Aldridge, K., et al. (2010). Beyond the closed suture in Apert mouse models: evidence of primary effects of FGFR2 signaling on facial shape at P0. Developmental Dynamics, 239, 30583071.Google Scholar
Martínez-Abadías, N., Motch, S. M., Pankratz, T. L., et al. (2013). Tissue-specific responses to aberrant FGF signaling in complex head phenotypes. Developmental Dynamics, 242, 8094.Google Scholar
Menegaz, R. A., Sublett, S. V., Figueroa, S. D., et al. (2010). Evidence for the influence of diet on cranial form and robusticity. The Anatomical Record, 293, 630641.Google Scholar
Moss, M. L. and Young, R. W. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281292.Google Scholar
Nakamura, T., Mochizuki, Y., Kanetake, H. and Kanda, S. (2001). Signals via FGF receptor 2 regulate migration of endothelial cells. Biochemical and Biophysical Research Communications, 289, 801806.Google Scholar
Opperman, L. A. (2000). Cranial sutures as intramembranous bone growth sites. Developmental Dynamics, 219, 472485.Google Scholar
Ornitz, D. M. and Marie, P. J. (2002). FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes & Development, 16, 14461465.Google Scholar
Ornitz, D. M. and Marie, P. J. (2015). Fibroblast growth factor signlaing in skeletal development and disease. Genes & Development, 29, 14631486.Google Scholar
Percival, C. J. (2013). The influence of angiogenesis on craniofacial development and evolution. Dissertation, The Pennsylvania State University. Available at: https://etda.libraries.psu.edu/paper/16838/ [Accessed: 9 July 2013].Google Scholar
Percival, C. and Richtsmeier, J. T. (2011). The epigenetics of dysmorphology: craniosynostosis as an example. In: Hallgrímsson, B. and Hall, B. K. (eds.) Epigenetics: Linking Genotype and Phenotype in Development and Evolution. San Fransisco, CA: University of California Press.Google Scholar
Percival, C. J. and Richtsmeier, J. T. (2013). Angiogenesis and intramembranous osteogenesis. Developmental Dynamics, 242, 909922.Google Scholar
Percival, C. J., Wang, Y., Zhou, X., Jabs, E. W. and Richtsmeier, J. T. (2012). The effect of a Beare–Stevenson syndrome Fgfr2 Y394C mutation on early craniofacial bone volume and relative bone mineral density in mice. Journal of Anatomy, 221, 434442.Google Scholar
Percival, C. J., Huang, Y., Jabs, E. W., Li, R. and Richtsmeier, J. T. (2014). Embryonic craniofacial bone volume and bone mineral density in Fgfr2+/P253R and nonmutant mice. Developmental Dynamics, 243, 541551.Google Scholar
Plavcan, J. M. (2001). Sexual dimorphism in primate evolution. American Journal of Physical Anthropology, 116, 2553.Google Scholar
Ponce de León, M. S. P. and Zollikofer, C. P. E. (2001). Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature, 412, 534538.Google Scholar
Raff, R. A. (1996). The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago, IL: University of Chicago Press.Google Scholar
Ramsay, J. O., Hooker, G. and Graves, S. (2009). Functional Data Analysis with R and MATLAB. New York, NY: Springer.Google Scholar
Ravosa, M. J., Noble, V. E., Hylander, W. L., Johnson, K. R. and Kowalski, E. M. (2000). Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. Journal of Human Evolution, 38, 667693.CrossRefGoogle ScholarPubMed
R Developmental Core Team (2008). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at: http://www.R-project.org.Google Scholar
Reeves, R. H., Baxter, L. L. and Richtsmeier, J. T. (2001). Too much of a good thing: mechanisms of gene action in Down syndrome. Trends in Genetics, 17, 8388.Google Scholar
Reno, P. L., McCollum, M. A., Cohn, M. J., et al. (2008). Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories. Journal of Experimental Zoology (Mol Dev Evol), 310, 240258.Google Scholar
Richtsmeier, J. T. and Flaherty, K. (2013). Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathologica, 125, 469489.Google Scholar
Richtsmeier, J. T. and Walker, A. (1993). A morphometric study of facial growth. In: Walker, A. and Leakey, R. (eds.) The Nariokotome Homo erectus Skeleton. Cambridge, MA: Harvard University Press, pp. 391410.Google Scholar
Richtsmeier, J. T., Corner, B. D., Grausz, H. M., Cheverud, J. M. and Danahey, S. E. (1993). The role of postnatal growth pattern in the production of facial morphology. Systematic Biology, 42, 307330.Google Scholar
Richtsmeier, J. T., Aldridge, K., DeLeon, V. B., et al. (2006). Phenotypic integration of neurocranium and brain. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 306, 360378.Google Scholar
Robson, S. L. and Wood, B. (2008). Hominin life history: reconstruction and evolution. Journal of Anatomy, 212, 394425.Google Scholar
Roseman, C. C., Kenny-Hunt, J. P. and Cheverud, J. M. (2009). Phenotypic integration without modularity: testing hypotheses about the distribution of pleiotropic quantitative trait loci in a continuous space. Evolutionary Biology, 36, 282291.Google Scholar
Ross, C. F. (1995). Allometric and functional influences on primate orbit orientation and the origins of the Anthropoidea. Journal of Human Evolution, 29, 201227.Google Scholar
Saarimäki-Vire, J., Peltopuro, P., Lahti, L., et al. (2007). Fibroblast growth factor receptors cooperate to regulate neural progenitor properties in the developing midbrain and hindbrain. The Journal of Neuroscience, 27, 85818592.Google Scholar
Schwartz, J. H. and Tattersall, I. (2003). The Human Fossil Record: Craniodental Morphology of Genus Homo (Africa and Asia). Hoboken, NJ: John Wiley and Sons.Google Scholar
Serrat, M. A., King, D. and Lovejoy, C. O. (2008). Temperature regulates limb length in homeotherms by directly modulating cartilage growth. Proceedings of the National Academy of Sciences, 105, 1934819353.Google Scholar
Sherwood, C. C., Subiaul, F. and Zawidzki, T. W. (2008). A natural history of the human mind: tracing evolutionary changes in brain and cognition. Journal of Anatomy, 212, 426454.Google Scholar
Smith, S. L. (2004). Skeletal age, dental age, and the maturation of KNM-WT 15000. American Journal of Physical Anthropology, 125, 105120.Google Scholar
Smith, T. D., DeLeon, V. B. and Rosenberger, A. L. (2013). At birth, tarsiers lack a postorbital bar or septum. The Anatomical Record, 296, 365377.Google Scholar
Smith, T. D., Kentzel, E. S., Cunningham, J. M., et al. (2014). Mapping bone cell distributions to assess ontogenetic origin of primate midfacial form. American Journal of Physical Anthropology, 154, 424435.Google Scholar
Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics, 21, 7071.Google Scholar
Spoor, F., Garland, T., Krovitz, G., et al. (2007). The primate semicircular canal system and locomotion. Proceedings of the National Academy of Sciences, 104, 1080810812.Google Scholar
Suhardja, A. and Hoffman, H. (2003). Role of growth factors and their receptors in proliferation of microvascular endothelial cells. Microscopy Research and Technique, 60, 7075.Google Scholar
Suwa, G., Kono, R. T., Simpson, S. W., et al. (2009). Paleobiological implications of the Ardipithecus ramidus dentition. Science, 326, 69.Google Scholar
Takimoto, A., Nishizaki, Y., Hiraki, Y. and Shukunami, C. (2009). Differential actions of VEGF-A isoforms on perichondrial angiogenesis during endochondral bone formation. Developmental Biology, 332, 196211.Google Scholar
Tholpady, S. S., Abdelaal, M. M., Dufresne, C. R., et al. (2004). Aberrant bony vasculature associated with activating fibroblast growth factor receptor mutations accompanying Crouzon syndrome. Journal of Craniofacial Surgery, 15, 431435.Google Scholar
Thompson, T. J., Owens, P. D. and Wilson, D. J. (1989). Intramembranous osteogenesis and angiogenesis in the chick embryo. Journal of Anatomy, 166, 5565.Google Scholar
Tillier, A. M. (1995). Neanderthal ontogeny: a new source for critical analysis. Anthropologie, 33, 6368.Google Scholar
Twigg, S. R. and Wilkie, A. O. (2015). A genetic–pathophysiological framework for craniosynostosis. The American Journal of Human Genetics, 97, 359377.Google Scholar
Wang, Y., Sun, M., Uhlhorn, V. L., et al. (2010). Activation of p38 MAPK pathway in the skull abnormalities of Apert syndrome Fgfr2+/P253R mice. BMC Developmental Biology, 10, 22.CrossRefGoogle ScholarPubMed
Warburton, D., Schwarz, M., Tefft, D., et al. (2000). The molecular basis of lung morphogenesis. Mechanisms of Development, 92, 5582.Google Scholar
Weaver, T. D. (2009). The meaning of Neanderthal skeletal morphology. Proceedings of the National Academy of Sciences, 106, 1602816033.Google Scholar
Yang, Y. Q., Tan, Y. Y., Wong, R., et al. (2012). The role of vascular endothelial growth factor in ossification. International Journal of Oral Science, 4, 6468.Google Scholar
Young, N. M. and Devlin, M. J. (2012). Finding our inner animal: understanding human evolutionary variation via experimental model systems. Curated Podium Session at the American Association of Physical Anthropologists Annual Meeting, Portland, OR.Google Scholar
Zelzer, E., McLean, W., Ng, Y. S., et al. (2002). Skeletal defects in VEGF120/120 mice reveal multiple roles for VEGF in skeletogenesis. Development, 129, 18931904.Google Scholar
Zernik, J., Twarog, K. and Upholt, W. B. (1990). Regulation of alkaline phosphatase and alpha2 (I) procollagen synthesis during early intramembranous bone formation in the rat mandible. Differentiation, 44, 207215.CrossRefGoogle Scholar
Zhang, Y., Singh, M. K., Degenhardt, K. R., et al. (2009). Tie2Cre-mediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects. Developmental Biology, 325, 8293.Google Scholar
Zollikofer, C. P. E. and Ponce de León, M. S. (2010). The evolution of hominin ontogenies. Seminars in Cell & Developmental Biology, 21, 441452.Google Scholar
Zumpano, M. P. and Richtsmeier, J. T. (2003). Growth-related shape changes in the fetal craniofacial complex of humans (Homo sapiens) and pigtailed macaques (Macaca nemestrina): a 3D-CT comparative analysis. American Journal of Physical Anthropology, 120, 339351.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×