[en] Congenital pseudarthrosis of the tibia (CPT) is a rare disease which normally presents itself during early childhood by anterolateral bowing of the tibia and spontaneous tibial fractures. Although the exact etiology of CPT is highly debated, 40-80% of CPT patients are carriers of a mutation in the Neurofibromatosis Type 1 (NF1) gene, which can potentially result in an altered phenotype of the skeletal cells and impaired bone healing. In this study we use a computational model of bone regeneration to examine the effect of the Nf1 mutation on bone fracture healing by altering the parameter values of eight key factors which describe the aberrant cellular behaviour of Nf1 haploinsufficient and Nf1 bi-allelically inactivated cells. We show that the computational model is able to predict the formation of a hamartoma as well as a wide variety of CPT phenotypes through different combinations of altered parameter values. A sensitivity analysis by "Design of Experiments" identified the impaired endochondral ossification process and increased infiltration of fibroblastic cells as key contributors to the degree of severity of CPT. Hence, the computational model results have added credibility to the experimental hypothesis of a genetic cause (i.e. Nf1 mutation) for CPT.
Disciplines :
Engineering, computing & technology: Multidisciplinary, general & others
Author, co-author :
carlier, aurelie
brems, h.
ashbourn, j.m.a.
nica, i
legius, e
Geris, Liesbet ; Université de Liège > Département d'aérospatiale et mécanique > Génie biomécanique
Language :
English
Title :
Capturing the wide variety of impaired fracture healing phenotypes in Neurofibromatosis Type 1 with eight key factors: a computational study.
Publication date :
2016
Journal title :
Scientific Reports
eISSN :
2045-2322
Publisher :
Nature Publishing Group, London, United Kingdom
Volume :
7
Pages :
20010
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
FP7 - 279100 - BRIDGE - Biomimetic process design for tissue regeneration: from bench to bedside via in silico modelling
Schindeler, A., Little, D. G. Recent insights into bone development, homeostasis, and repair in type 1 neurofibromatosis (NFI). Bone 42, 616-622 (2008).
Pannier, S. Congenital pseudarthrosis of the tibia. Orthopaedics & Traumatology-Surgery & Research 97, 750-761 (2011).
Crawford, A. H., Schorry, E. K. Neurofibromatosis update. Journal of Pediatric Orthopaedics 26, 413-423 (2006).
Crawford, A. H., Bagamery, N. Osseous Manifestations of Neurofibromatosis in Childhood. Journal of Pediatric Orthopaedics 6, 72-88 (1986).
Friedman, J. M., Birch, P. H. Type 1 neurofibromatosis: A descriptive analysis of the disorder in 1,728 patients. American Journal of Medical Genetics 70, 138-143 (1997).
Sant, D. W. et al. Evaluation of somatic mutations in tibial pseudarthrosis samples in neurofibromatosis type 1. Journal of Medical Genetics 52, 256-61 (2015).
Stevenson, D. A. et al. Double inactivation of NF1 in tibial pseudarthrosis. American Journal of Human Genetics 79, 143-148 (2006).
Kuorilehto, T., Nissinen, M., Koivunen, J., Benson, M. D., Peltonen, J. NF1 tumor suppressor protein and mRNA in skeletal tissues of developing and adult normal mouse and NF1-deficient embryos. Journal of Bone and Mineral Research 19, 983-989 (2004).
El-Hoss, J. et al. A murine model of neurofibromatosis type 1 tibial pseudarthrosis featuring proliferative fibrous tissue and osteoclast-like cells. Journal of Bone and Mineral Research 27, 68-78 (2012).
Kolanczyk, M. et al. Modelling neurofibromatosis type 1 tibial dysplasia and its treatment with lovastatin. Bmc Medicine 6, doi: 10.1186/1741-7015-6-21 (2008).
Carlier, A., Geris, L., Lammens, J., Van Oosterwyck, H. Bringing computational models of bone regeneration to the clinic. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 7(4), 183-194 (2015).
Geris, L. Regenerative orthopaedics: in vitro, in vivo and in silico. International Orthopaedics (SICOT) 38, 1771-1778 (2014).
Carlier, A., Geris, L., Gastel, N. V., Carmeliet, G., Oosterwyck, H. V. Oxygen as a critical determinant of bone fracture healing-A multiscale model. J Theor Biol 365C, 247-264 (2014).
Carlier, A. et al. MOSAIC: a multiscale model of osteogenesis and sprouting angiogenesis with lateral inhibition of endothelial cells. PLoS Comput. Biol. 8, doi: 10.1371/journal.pcbi.1002724 (2012).
Peiffer, V., Gerisch, A., Vandepitte, D., Van Oosterwyck, H., Geris, L. A hybrid bioregulatory model of angiogenesis during bone fracture healing. Biomech. Model. Mechanobiol. 10, 383-395 (2011).
Geris, L., Gerisch, A., Sloten, J. V., Weiner, R., Oosterwyck, H. V. Angiogenesis in bone fracture healing: a bioregulatory model. J. Theor. Biol. 251, 137-158 (2008).
Carlier, A., Geris, L., Gastel, N.v., Carmeliet, G., Oosterwyck, H. V. Oxygen as a critical determinant of bone fracture healing-a multiscale model. J. Theor. Biol. 365, 247-264 (2015).
Bentley, K., Gerhardt, H., Bates, P. A. Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. J. Theor. Biol. 250, 25-36 (2008).
Harrison, L. J., Cunningham, J. L., Stromberg, L., Goodship, A. E. Controlled induction of a pseudarthrosis: A study using a rodent model. Journal of Orthopaedic Trauma 17, 11-21 (2003).
Gerstenfeld, L. C., Cullinane, D. M., Barnes, G. L., Graves, D. T., Einhorn, T. A. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J. Cell Biochem. 88, 873-884 (2003).
Barnes, G. L., Kostenuik, P. J., Gerstenfeld, L. C., Einhorn, T. A. Growth factor regulation of fracture repair. Journal of Bone and Mineral Research 14, 1805-1815 (1999).
Dimitriou, R., Tsiridis, E., Giannoudis, P. V. Current concepts of molecular aspects of bone healing. Injury-International Journal of the Care of the Injured 36, 1392-1404 (2005).
Atit, R. P., Crowe, M. J., Greenhalgh, D. G., Wenstrup, R. J., Ratner, N. The Nf1 tumor suppressor regulates mouse skin wound healing, fibroblast proliferation, and collagen deposited fibroblasts. Journal of Investigative Dermatology 112, 835-842 (1999).
Carlier, A. et al. Designing optimal calcium phosphate scaffold-cell combinations using an integrative model-based approach. Acta Biomater. 7, 3573-3585 (2011).
Isaksson, H., van Donkelaar, C. C., Huiskes, R., Yao, J., Ito, K. Determining the most important cellular characteristics for fracture healing using design of experiments methods. J. Theor. Biol. 255, 26-39 (2008).
Leskela, H. V. et al. Congenital pseudarthrosis of neurofibromatosis type 1: Impaired osteoblast differentiation and function and altered NF1 gene expression. Bone 44, 243-250 (2009).
Cho, T. J. et al. Biologic Characteristics of Fibrous Hamartoma from Congenital Pseudarthrosis of the Tibia Associated with Neurofibromatosis Type 1. Journal of Bone and Joint Surgery-American Volume 90A, 2735-2744 (2008).
Lee, D. Y. et al. Disturbed Osteoblastic Differentiation of Fibrous Hamartoma Cell from Congenital Pseudarthrosis of the Tibia Associated with Neurofibromatosis Type I. Clin Orthop Surg 3, 230-237 (2011).
Crawford, A. H., Bagamery, N. Osseous Manifestations of Neurofibromatosis in Childhood. Journal of Pediatric Orthopaedics 6, 72-88 (1986).
Boyd, H. B. Pathology and Natural-History of Congenital Pseudarthrosis of the Tibia. Clinical Orthopaedics and Related Research 166, 5-13 (1982).
Lasater, E. A. et al. Genetic and cellular evidence of vascular inflammation in neurofibromin-deficient mice and humans. Journal of Clinical Investigation 120, 859-870 (2010).
Heerva, E. et al. Osteoclasts in neurofibromatosis type 1 display enhanced resorption capacity, aberrant morphology, and resistance to serum deprivation. Bone 47, 583-590 (2010).
Kuhnisch, J. et al. Multiscale, Converging Defects of Macro-Porosity, Microstructure and Matrix Mineralization Impact Long Bone Fragility in NF1. Plos One 9, doi: 10.1371/journal.pone.0086115 (2014).
Stevenson, D. A. et al. Peripheral muscle weakness in RASopathies. Muscle & Nerve 46, 394-399 (2012).
Histing, T. et al. Small animal bone healing models: Standards, tips, and pitfalls results of a consensus meeting. Bone 49, 591-599 (2011).
Holstein, J. H. et al. Advances in the Establishment of Defined Mouse Models for the Study of Fracture Healing and Bone Regeneration. Journal of Orthopaedic Trauma 23, S31-S38 (2009).
Kilborn, S. H., Trudel, G., Uhthoff, H. Review of growth plate closure compared with age at sexual maturity and lifespan in laboratory animals. Contemporary Topics in Laboratory Animal Science 41, 21-26 (2002).
Kolanczyk, M. et al. Multiple roles for neurofibromin in skeletal development and growth. Human Molecular Genetics 16, 874-886 (2007).
Ono, K. et al. The Ras-GTPase activity of neurofibromin restrains ERK-dependent FGFR signaling during endochondral bone formation. Human Molecular Genetics 22, 3048-3062 (2013).
Seitz, S. et al. High bone turnover and accumulation of osteoid in patients with neurofibromatosis 1. Osteoporosis International 21, 119-127 (2010).
Ndong, J. D. L. C. et al. Combined MEK inhibition and BMP2 treatment promotes osteoblast differentiation and bone healing in Nf1OSX ?/? mice. Journal of Bone and Mineral Research 30(1), 55-63 (2014).
El-Hoss, J. et al. A Combination of rhBMP-2 (Recombinant Human Bone Morphogenetic Protein-2) and MEK (MAP Kinase/ERK Kinase) Inhibitor PD0325901 Increases Bone Formation in a Murine Model of Neurofibromatosis Type I Pseudarthrosis. Journal of Bone and Joint Surgery-American Volume 96A, http://dx.doi.org/10.2106/JBJS.M.00862 (2014).