Multiscale, converging defects of macro-porosity, microstructure and matrix mineralization impact long bone fragility in NF1

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Kühnisch, Jirko ^a,b   Seto, Jong ^c,d   Lange, Claudia ^c,e   Schrof, Susanne ^a   Stumpp, Sabine ^a   Kobus, Karolina ^b   Grohmann, Julia ^b   Kossler, Nadine ^b   Varga, Peter ^a   Osswald, Monika ^b   Emmerich, Denise ^a,b   Tinschert, Sigrid ^f,g   Thielemann, Falk ^g   Duda, Georg ^a,h   Seifert, Wenke ^a   El Khassawna, Thaqif ⁱ   Stevenson, David A ^j   Elefteriou, Florent ^k   Kornak, Uwe ^a,b   Raum, Kay ^a   Fratzl, Peter ^c,h   Mundlos, Stefan ^a,b,h   Kolanczyk, Mateusz ^a,b   more..

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^d UNIVERSITY OF KONSTANZ   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^f INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^g DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^h Institut für Klinische Genetik Medizinische Fakultät Carl Gustav Carus Technische Universität Dresden ^*  (Germany)

ⁱ JUSTUS LIEBIG UNIVERSITY   (Germany)

^j UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^k VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER; MATRIX PROTEIN; NEUROFIBROMIN;

ADULT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; BONE DEMINERALIZATION; BONE DYSPLASIA; BONE FRAGILITY; BONE STRENGTH; BONE STRUCTURE; CASE REPORT; CELL VOLUME; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; HUMAN; MECHANICAL STRESS; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; OSTEOCYTE; TENSILE STRENGTH; TIBIA;

ANIMALS; BIOMECHANICAL PHENOMENA; BLOOD VESSELS; BONE AND BONES; BONE DENSITY; BONE MATRIX; CALCIFICATION, PHYSIOLOGIC; COLLAGEN; DIAPHYSES; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; OSTEOCYTES; POROSITY; TIBIA;

EID: 84903475113     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086115     Document Type: Article

References (54)

1. Alwan S, Tredwell SJ, Friedman JM (2005) Is osseous dysplasia a primary feature of neurofibromatosis 1 (NF1)? Clin Genet 67: 378-390. (Pubitemid 40561488)
2. Stevenson DA, Carey JC, Viskochil DH, Moyer-Mileur LJ, Slater H, et al. (2009) Analysis of radiographic characteristics of anterolateral bowing of the leg before fracture in neurofibromatosis type 1. Jô Pediatr Orthop 29: 385-392.
3. Tucker T, Schnabel C, Hartmann M, Friedrich RE, Frieling I, et al. (2009) Bone health and fracture rate in individuals with neurofibromatosis 1 (NF1). Jô Med Genet 46: 259-265.
4. Wallace MR, Marchuk DA, Andersen LB, Letcher R, Odeh HM, et al. (1990) Type 1 neurofibromatosis gene: identification of a large transcript disrupted in three NF1 patients. Science 249: 181-186.
5. Cully M, Downward J (2008) SnapShot: Ras Signaling. Cell 133: 1292-1292 e1291.
6. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Montalto G, et al. (2012) Mutations and deregulation of Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascades which alter therapy response. Oncotarget 3: 954-987.
7. Larizza L, Gervasini C, Natacci F, Riva P (2009) Developmental abnormalities and cancer predisposition in neurofibromatosis type 1. Curr Mol Med 9: 634-653.
8. Dang I, De Vries GH (2011) Aberrant cAMP metabolism in NF1 malignant peripheral nerve sheath tumor cells. Neurochem Res 36: 1697-1705.
9. Ozawa T, Araki N, Yunoue S, Tokuo H, Feng L, et al. (2005) The neurofibromatosis type 1 gene product neurofibromin enhances cell motility by regulating actin filament dynamics via the Rho-ROCK-LIMK2-cofilin pathway. Jô Biol Chem 280: 39524-39533. (Pubitemid 41713911)
10. Starinsky-Elbaz S, Faigenbloom L, Friedman E, Stein R, Kloog Y (2009) The pre-GAP-related domain of neurofibromin regulates cell migration through the LIM kinase/cofilin pathway. Mol Cell Neurosci 42: 278-287.
11. Kolanczyk M, Kossler N, Kuhnisch J, Lavitas L, Stricker S, et al. (2007) Multiple roles for neurofibromin in skeletal development and growth. Hum Mol Genet 16: 874-886. (Pubitemid 47062733)
12. Kossler N, Stricker S, Rodelsperger C, Robinson PN, Kim J, et al. (2011) Neurofibromin (Nf1) is required for skeletal muscle development. Hum Mol Genet 20: 2697-2709.
13. Elefteriou F, Benson MD, Sowa H, Starbuck M, Liu X, et al. (2006) ATF4 mediation of NF1 functions in osteoblast reveals a nutritional basis for congenital skeletal dysplasiae. Cell Metab 4: 441-451. (Pubitemid 44817348)
14. Lammert M, Kappler M, Mautner VF, Lammert K, Storkel S, et al. (2005) Decreased bone mineral density in patients with neurofibromatosis 1. Osteoporos Int 16: 1161-1166. (Pubitemid 41225104)
15. Seitz S, Schnabel C, Busse B, Schmidt HU, Beil FT, et al. (2010) High bone turnover and accumulation of osteoid in patients with neurofibromatosis 1. Osteoporos Int 21: 119-127.
16. Chappard D, Basle MF, Legrand E, Audran M (2011) New laboratory tools in the assessment of bone quality. Osteoporos Int 22: 2225-2240.
17. Weiner S, Traub W (1992) Bone structure: from angstroms to microns. Fasebô J 6: 879-885.
18. Ritchie RO (2011) The conflicts between strength and toughness. Nat Mater 10: 817-822.
19. Shapiro F (2008) Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur Cell Mater 15: 53-76.
20. Clarke B (2008) Normal bone anatomy and physiology. Clinô Jô Am Soc Nephrol 3 Suppl 3: S131-139.
21. Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, et al. (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19: 329-344.
22. Maes C, Stockmans I, Moermans K, Van Looveren R, Smets N, et al. (2004) Soluble VEGF isoforms are essential for establishing epiphyseal vascularization and regulating chondrocyte development and survival. Jô Clin Invest 113: 188-199. (Pubitemid 38544204)
23. Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, et al. (2006) Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sciô Uô Sô A 103: 17741-17746. (Pubitemid 44852230)
24. Currey JD (1988) The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. Jô Biomech 21: 131-139.
25. Schaffler MB, Burr DB (1988) Stiffness of compact bone: effects of porosity and density. Jô Biomech 21: 13-16. (Pubitemid 17165212)
26. Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, et al. (2007) Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. Jô Bone Miner Res 22: 1557-1570. (Pubitemid 351229326)
27. Turner CH (2006) Bone strength: current concepts. Annô Nô Yô Acad Sci 1068: 429-446. (Pubitemid 43824172)
28. Kolanczyk M, Kuhnisch J, Kossler N, Osswald M, Stumpp S, et al. (2008) Modelling neurofibromatosis type 1 tibial dysplasia and its treatment with lovastatin. BMC Med 6: 21.
29. Pascaretti-Grizon F, Gaudin-Audrain C, Gallois Y, Retaillaud-Gaborit N, Basle MF, et al. (2007) Osteopontin is an argentophilic protein in the bone matrix and in cells of kidney convoluted tubules. Morphologie 91: 180-185. (Pubitemid 350235276)
30. Junqueira LC, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochemô J 11: 447-455. (Pubitemid 9238595)
31. Dayan D, Hiss Y, Hirshberg A, Bubis JJ, Wolman M (1989) Are the polarization colors of picrosirius red-stained collagen determined only by the diameter of the fibers? Histochemistry 93: 27-29. (Pubitemid 19272698)
32. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. Jô Bone Miner Res 2: 595-610.
33. Kawamoto T, Shimizu M (2000) A method for preparing 2- to 50-micron-thick fresh-frozen sections of large samples and undecalcified hard tissues. Histochem Cell Biol 113: 331-339.
34. Gupta HS, Wagermaier W, Zickler GA, Raz-Ben Aroush D, Funari SS, et al. (2005) Nanoscale deformation mechanisms in bone. Nano Lett 5: 2108-2111. (Pubitemid 41546347)
35. Lakshmanan S, Bodi A, Raum K (2007) Assessment of anisotropic tissue elasticity of cortical bone from high-resolution, angular acoustic measurements. IEEE Trans Ultrason Ferroelectr Freq Control 54: 1560-1570. (Pubitemid 47295134)
36. Granke M, Gourrier A, Rupin F, Raum K, Peyrin F, et al. (2013) Microfibril orientation dominates the microelastic properties of human bone tissue at the lamellar length scale. PLoS One 8: e58043.
37. Preininger B, Checa S, Molnar FL, Fratzl P, Duda GN, et al. (2011) Spatial-temporal mapping of bone structural and elastic properties in a sheep model following osteotomy. Ultrasound Med Biol 37: 474-483.
38. Raum K, Cleveland RO, Peyrin F, Laugier P (2006) Derivation of elastic stiffness from site-matched mineral density and acoustic impedance maps. Phys Med Biol 51: 747-758. (Pubitemid 43139116)
39. Lange C, Li C, Manjubala I, Wagermaier W, Kuhnisch J, et al. (2011) Fetal and postnatal mouse bone tissue contains more calcium than is present in hydroxyapatite. Jô Struct Biol 176: 159-167.
40. Tanck E, Hannink G, Ruimerman R, Buma P, Burger EH, et al. (2006) Cortical bone development under the growth plate is regulated by mechanical load transfer. Jô Anat 208: 73-79.
41. Kyono A, Avishai N, Ouyang Z, Landreth GE, Murakami S (2012) FGF and ERK signaling coordinately regulate mineralization-related genes and play essential roles in osteocyte differentiation. Jô Bone Miner Metab 30: 19-30.
42. Ono K, Karolak MR, Ndong JD, Wang W, Yang X, et al. (2013) The RasGTPase activity of neurofibromin restrains ERK-dependent FGFR signaling during endochondral bone formation. Hum Mol Genet.
43. Kono SJ, Oshima Y, Hoshi K, Bonewald LF, Oda H, et al. (2007) Erk pathways negatively regulate matrix mineralization. Bone 40: 68-74. (Pubitemid 44839341)
44. Xiao L, Esliger A, Hurley MM (2013) Nuclear fibroblast growth factor 2 (FGF2) isoforms inhibit bone marrow stromal cell mineralization through FGF23/FGFR/MAPK in vitro. Jô Bone Miner Res 28: 35-45.
45. Ge C, Xiao G, Jiang D, Franceschi RT (2007) Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. Jô Cell Biol 176: 709-718. (Pubitemid 46333984)
46. El-Hoss J, Sullivan K, Cheng T, Yu NY, Bobyn JD, et al. (2011) A murine model of neurofibromatosis type 1 tibial pseudarthrosis featuring proliferative fibrous tissue and osteoclast-like cells. Jô Bone Miner Res.
47. Franceschi RT, Ge C, Xiao G, Roca H, Jiang D (2009) Transcriptional regulation of osteoblasts. Cells Tissues Organs 189: 144-152.
48. He G, George A (2004) Dentin matrix protein 1 immobilized on type I collagen fibrils facilitates apatite deposition in vitro. Jô Biol Chem 279: 11649-11656. (Pubitemid 38401667)
49. Martin A, Liu S, David V, Li H, Karydis A, et al. (2011) Bone proteins PHEX and DMP1 regulate fibroblastic growth factor Fgf23 expression in osteocytes through a common pathway involving FGF receptor (FGFR) signaling. Fasebô J 25: 2551-2562.
50. Dudley AC (2012) Tumor endothelial cells. Cold Spring Harb Perspect Med 2: a006536.
51. Kornak U (2011) Animal models with pathological mineralization phenotypes. Joint Bone Spine 78: 561-567.
52. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, et al. (2007) Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 5: 464-475. (Pubitemid 46825494)
53. Seeman E, Delmas PD (2006) Bone quality - the material and structural basis of bone strength and fragility. Nô Englô Jô Med 354: 2250-2261.
54. Ascenzi MG, Liao VP, Lee BM, Billi F, Zhou H, et al. (2012) Parathyroid Hormone Treatment Improves the Cortical Bone Microstructure by Improving the Distribution of Type I Collagen in Postmenopausal Women With Osteoporosis. Journal of Bone and Mineral Research 27: 702-712.