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Extra-Skeletal Manifestations in Osteogenesis Imperfecta Mouse Models

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Abstract

Osteogenesis imperfecta (OI) is a rare heritable connective tissue disorder of skeletal fragility with an incidence of roughly 1:15,000. Approximately 85% of the pathogenic variants responsible for OI are in the type I collagen genes, COL1A1 and COL1A2, with the remaining pathogenic OI variants spanning at least 20 additional genetic loci that often involve type I collagen post-translational modification, folding, and intracellular transport as well as matrix incorporation and mineralization. In addition to being the most abundant collagen in the body, type I collagen is an important structural and extracellular matrix signaling molecule in multiple organ systems and tissues. Thus, OI disease-causing variants result not only in skeletal fragility, decreased bone mineral density (BMD), kyphoscoliosis, and short stature, but can also result in hearing loss, dentinogenesis imperfecta, blue gray sclera, cardiopulmonary abnormalities, and muscle weakness. The extensive genetic and clinical heterogeneity in OI has necessitated the generation of multiple mouse models, the growing awareness of non-skeletal organ and tissue involvement, and OI being more broadly recognized as a type I collagenopathy.

This has driven the investigation of mutation-specific skeletal and extra-skeletal manifestations and broadened the search of potential mechanistic therapeutic strategies. The purpose of this review is to outline several of the extra-skeletal manifestations that have recently been characterized through the use of genetically and phenotypically heterogeneous mouse models of osteogenesis imperfecta, demonstrating the significant potential impact of OI disease-causing variants as a collagenopathy (affecting multiple organ systems and tissues), and its implications to overall health.

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Data Availability

Data sharing not applicable. No new data were created or analyzed in this review.

Abbreviations

OI :

Osteogenesis imperfecta

BMD :

Bone mineral density

EDS :

Ehlers-Danlos syndrome

OMIM :

Online Mendelian Inheritance in Man

WT :

Wild type

FEV :

Forced expiratory volume

FVC :

Forced vital capacity

ER :

Endoplasmic reticulum

Fmax :

Maximum circumferential breaking strength

IEM :

Incremental elastic modulus

TEM :

Transmission electron microscopy

CSA :

Cross-sectional area

ETC :

Electron transport chain

FDL :

Flexor digitorum longus

References

  1. Forlino A, Cabral WA, Barnes AM, Marini JC (2011) New perspectives on osteogenesis imperfecta. Nat Rev Endocrinol 7:540–557. https://doi.org/10.1038/nrendo.2011.81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Charlier P, Perciaccante A, Bianucci R (2017) Oldest medical description of osteogenesis imperfecta (17th Century, France). Clin Anat 30:128–129. https://doi.org/10.1002/ca.22806

    Article  PubMed  Google Scholar 

  3. Forlino A, Marini JC (2016) Osteogenesis imperfecta. Lancet 387:1657–1671. https://doi.org/10.1016/S0140-6736(15)00728-X

    Article  CAS  PubMed  Google Scholar 

  4. Marom R, Rabenhorst BM, Morello R (2020) Osteogenesis imperfecta: an update on clinical features and therapies. Eur J Endocrinol 183:R95–R106. https://doi.org/10.1530/EJE-20-0299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gremminger VL, Phillips CL (2021) Impact of intrinsic muscle weakness on muscle-bone crosstalk in osteogenesis imperfecta. Int J Mol Sci. https://doi.org/10.3390/ijms22094963

    Article  PubMed  PubMed Central  Google Scholar 

  6. Udupa P, Shrikondawar AN, Ranjan A, Ghosh DK (2023) Assessing type I collagen expression and quality in cellular models of osteogenesis imperfecta. Clin Genet 105:329–334. https://doi.org/10.1111/cge.14463

    Article  CAS  PubMed  Google Scholar 

  7. Sillence DO, Senn A, Danks DM (1979) Genetic heterogeneity in osteogenesis imperfecta. J Med Genet 16:101–116. https://doi.org/10.1136/jmg.16.2.101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhytnik L, Maasalu K, Pashenko A, Khmyzov S, Reimann E, Prans E, Koks S, Martson A (2019) COL1A1/2 pathogenic variants and phenotype characteristics in Ukrainian osteogenesis imperfecta patients. Front Genet. https://doi.org/10.3389/fgene.2019.00722

    Article  PubMed  PubMed Central  Google Scholar 

  9. Enderli TA, Burtch SR, Templet JN, Carriero A (2016) Animal models of osteogenesis imperfecta: applications in clinical research. Orthop Res Rev 8:41–55. https://doi.org/10.2147/ORR.S85198

    Article  PubMed  PubMed Central  Google Scholar 

  10. Alcorta-Sevillano N, Infante A, Macias I, Rodriguez CI (2022) Murine animal models in osteogenesis imperfecta: the quest for improving the quality of life. Int J Mol Sci. https://doi.org/10.3390/ijms24010184

    Article  PubMed  PubMed Central  Google Scholar 

  11. Forlino A, Porter FD, Lee EJ, Westphal H, Marini JC (1999) Use of the Cre/lox recombination system to develop a non-lethal knock-in murine model for osteogenesis imperfecta with an alpha1(I) G349C substitution. variability in phenotype in BrtlIV mice. J Biol Chem 274:37923–37931. https://doi.org/10.1074/jbc.274.53.37923

    Article  CAS  PubMed  Google Scholar 

  12. Lisse TS, Thiele F, Fuchs H, Hans W, Przemeck GK, Abe K, Rathkolb B, Quintanilla-Martinez L, Hoelzlwimmer G, Helfrich M, Wolf E, Ralston SH, Hrabe de Angelis M (2008) ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet. https://doi.org/10.1371/journal.pgen.0040007

    Article  PubMed  PubMed Central  Google Scholar 

  13. Chen F, Guo R, Itoh S, Moreno L, Rosenthal E, Zappitelli T, Zirngibl RA, Flenniken A, Cole W, Grynpas M, Osborne LR, Vogel W, Adamson L, Rossant J, Aubin JE (2014) First mouse model for combined osteogenesis imperfecta and Ehlers-Danlos syndrome. J Bone Miner Res 29:1412–1423. https://doi.org/10.1002/jbmr.2177

    Article  CAS  PubMed  Google Scholar 

  14. Chipman SD, Sweet HO, McBride DJ Jr, Davisson MT, Marks SC Jr, Shuldiner AR, Wenstrup RJ, Rowe DW, Shapiro JR (1993) Defective pro alpha 2(I) collagen synthesis in a recessive mutation in mice: a model of human osteogenesis imperfecta. Proc Natl Acad Sci U S A 90:1701–1705. https://doi.org/10.1073/pnas.90.5.1701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Saban J, Zussman MA, Havey R, Patwardhan AG, Schneider GB, King D (1996) Heterozygous oim mice exhibit a mild form of osteogenesis imperfecta. Bone 19:575–579. https://doi.org/10.1016/s8756-3282(96)00305-5

    Article  CAS  PubMed  Google Scholar 

  16. Daley E, Streeten EA, Sorkin JD, Kuznetsova N, Shapses SA, Carleton SM, Shuldiner AR, Marini JC, Phillips CL, Goldstein SA, Leikin S, McBride DJ Jr (2010) Variable bone fragility associated with an Amish COL1A2 variant and a knock-in mouse model. J Bone Miner Res 25:247–261. https://doi.org/10.1359/jbmr.090720

    Article  CAS  PubMed  Google Scholar 

  17. Morello R, Bertin TK, Chen Y, Hicks J, Tonachini L, Monticone M, Castagnola P, Rauch F, Glorieux FH, Vranka J, Bachinger HP, Pace JM, Schwarze U, Byers PH, Weis M, Fernandes RJ, Eyre DR, Yao Z, Boyce BF, Lee B (2006) CRTAP is required for prolyl 3- hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127:291–304. https://doi.org/10.1016/j.cell.2006.08.039

    Article  CAS  PubMed  Google Scholar 

  18. Fratzl-Zelman N, Morello R, Lee B, Rauch F, Glorieux FH, Misof BM, Klaushofer K, Roschger P (2010) CRTAP deficiency leads to abnormally high bone matrix mineralization in a murine model and in children with osteogenesis imperfecta type VII. Bone 46:820–826. https://doi.org/10.1016/j.bone.2009.10.037

    Article  CAS  PubMed  Google Scholar 

  19. McAllion SJ, Paterson CR (1996) Causes of death in osteogenesis imperfecta. J Clin Pathol 49:627–630. https://doi.org/10.1136/jcp.49.8.627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Folkestad L, Hald JD, Canudas-Romo V, Gram J, Hermann AP, Langdahl B, Abrahamsen B, Brixen K (2016) Mortality and causes of death in patients with osteogenesis imperfecta: a register-based nationwide cohort study. J Bone Miner Res 31:2159–2166. https://doi.org/10.1002/jbmr.2895

    Article  CAS  PubMed  Google Scholar 

  21. Khan SI, Yonko EA, Carter EM, Dyer D, Sandhaus RA, Raggio CL (2020) Cardiopulmonary status in adults with osteogenesis imperfecta: intrinsic lung disease may contribute more than scoliosis. Clin Orthop Relat Res 478:2833–2843. https://doi.org/10.1097/CORR.0000000000001400

    Article  PubMed  PubMed Central  Google Scholar 

  22. Thiele F, Cohrs CM, Flor A, Lisse TS, Przemeck GK, Horsch M, Schrewe A, Gailus-Durner V, Ivandic B, Katus HA, Wurst W, Reisenberg C, Chaney H, Fuchs H, Hans W, Beckers J, Marini JC, Hrabe de Angelis M (2012) Cardiopulmonary dysfunction in the osteogenesis imperfecta mouse model Aga2 and human patients are caused by bone-independent mechanisms. Hum Mol Genet 21:3535–3545. https://doi.org/10.1093/hmg/dds183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Shapiro JR, Burn VE, Chipman SD, Jacobs JB, Schloo B, Reid L, Larsen N, Louis F (1989) Pulmonary hypoplasia and osteogenesis imperfecta type II with defective synthesis of alpha I(1) procollagen. Bone 10:165–171. https://doi.org/10.1016/8756-3282(89)90049-5

    Article  CAS  PubMed  Google Scholar 

  24. Thibeault DW, Pettett G, Mabry SM, Rezaiekhaligh MM (1995) Osteogenesis imperfecta Type IIA and pulmonary hypoplasia with normal alveolar development. Pediatr Pulmonol 20:301–306. https://doi.org/10.1002/ppul.1950200508

    Article  CAS  PubMed  Google Scholar 

  25. Baglole CJ, Liang F, Traboulsi H, Rico de Souza A, Giordano C, Tauer JT, Rauch F, Petrof BJ (2018) Pulmonary and diaphragmatic pathology in collagen type I alpha1 mutant mice with osteogenesis imperfecta. Pediatr Res 83:1165–1171. https://doi.org/10.1038/pr.2018.36

    Article  CAS  PubMed  Google Scholar 

  26. Baldridge D, Lennington J, Weis M, Homan EP, Jiang MM, Munivez E, Keene DR, Hogue WR, Pyott S, Byers PH, Krakow D, Cohn DH, Eyre DR, Lee B, Morello R (2010) Generalized connective tissue disease in Crtap-/-mouse. PLoS ONE 5:e10560. https://doi.org/10.1371/journal.pone.0010560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Dimori M, Fett J, Leikin S, Otsuru S, Thostenson JD, Carroll JL, Morello R (2023) Distinct type I collagen alterations cause intrinsic lung and respiratory defects of variable severity in mouse models of osteogenesis imperfecta. J Physiol 601:355–379. https://doi.org/10.1113/JP283452

    Article  CAS  PubMed  Google Scholar 

  28. Dimori M, Heard-Lipsmeyer ME, Byrum SD, Mackintosh SG, Kurten RC, Carroll JL, Morello R (2020) Respiratory defects in the CrtapKO mouse model of osteogenesis imperfecta. Am J Physiol Lung Cell Mol Physiol 318:L592–L605. https://doi.org/10.1152/ajplung.00313.2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gentry BA, Ferreira JA, McCambridge AJ, Brown M, Phillips CL (2010) Skeletal muscle weakness in osteogenesis imperfecta mice. Matrix Biol 29:638–644. https://doi.org/10.1016/j.matbio.2010.06.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jeong Y, Carleton SM, Gentry BA, Yao X, Ferreira JA, Salamango DJ, Weis M, Oestreich AK, Williams AM, McCray MG, Eyre DR, Brown M, Wang Y, Phillips CL (2015) Hindlimb skeletal muscle function and skeletal quality and strength in +/G610C mice with and without weight-bearing exercise. J Bone Miner Res 30:1874–1886. https://doi.org/10.1002/jbmr.2518

    Article  CAS  PubMed  Google Scholar 

  31. Hansen B, Jemec GB (2002) The mechanical properties of skin in osteogenesis imperfecta. Arch Dermatol 138:909–911. https://doi.org/10.1001/archderm.138.7.909

    Article  PubMed  Google Scholar 

  32. Himakhun W, Rojnueangnit K, Prachukthum S (2012) Perinatal lethal osteogenesis imperfecta in a thai newborn: the autopsy and histopathogical findings. J Med Assoc Thai 95(Suppl 1):S190-194

    PubMed  Google Scholar 

  33. Millington-Sanders C, Meir A, Lawrence L, Stolinski C (1998) Structure of chordae tendineae in the left ventricle of the human heart. J Anat 192(Pt 4):573–581. https://doi.org/10.1046/j.1469-7580.1998.19240573.x

    Article  PubMed  PubMed Central  Google Scholar 

  34. Migliaccio S, Barbaro G, Fornari R, Di Lorenzo G, Celli M, Lubrano C, Falcone S, Fabbrini E, Greco E, Zambrano A, Brama M, Prossomariti G, Marzano S, Marini M, Conti F, D’Eufemia P, Spera G (2009) Impairment of diastolic function in adult patients affected by osteogenesis imperfecta clinically asymptomatic for cardiac disease: casuality or causality? Int J Cardiol 131:200–203. https://doi.org/10.1016/j.ijcard.2007.10.051

    Article  PubMed  Google Scholar 

  35. Thatcher K, Mattern CR, Chaparro D, Goveas V, McDermott MR, Fulton J, Hutcheson JD, Hoffmann BR, Lincoln J (2023) Temporal progression of aortic valve pathogenesis in a mouse model of osteogenesis imperfecta. J Cardiovasc Dev Dis. https://doi.org/10.3390/jcdd10080355

    Article  PubMed  PubMed Central  Google Scholar 

  36. Cheek JD, Wirrig EE, Alfieri CM, James JF, Yutzey KE (2012) Differential activation of valvulogenic, chondrogenic, and osteogenic pathways in mouse models of myxomatous and calcific aortic valve disease. J Mol Cell Cardiol 52:689–700. https://doi.org/10.1016/j.yjmcc.2011.12.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Luczak ED, Leinwand LA (2009) Sex-based cardiac physiology. Annu Rev Physiol 71:1–18. https://doi.org/10.1146/annurev.physiol.010908.163156

    Article  CAS  PubMed  Google Scholar 

  38. Du XJ (2004) Gender modulates cardiac phenotype development in genetically modified mice. Cardiovasc Res 63:510–519. https://doi.org/10.1016/j.cardiores.2004.03.027

    Article  CAS  PubMed  Google Scholar 

  39. Weis SM, Emery JL, Becker KD, McBride DJ Jr, Omens JH, McCulloch AD (2000) Myocardial mechanics and collagen structure in the osteogenesis imperfecta murine (oim). Circ Res 87:663–669. https://doi.org/10.1161/01.res.87.8.663

    Article  CAS  PubMed  Google Scholar 

  40. Bowers SLK, Meng Q, Kuwabara Y, Huo J, Minerath R, York AJ, Sargent MA, Prasad V, Saviola AJ, Galindo DC, Hansen KC, Vagnozzi RJ, Yutzey KE, Molkentin JD (2023) Col1a2-deleted mice have defective type I collagen and secondary reactive cardiac fibrosis with altered hypertrophic dynamics. Cells. https://doi.org/10.3390/cells12172174

    Article  PubMed  PubMed Central  Google Scholar 

  41. Ashournia H, Johansen FT, Folkestad L, Diederichsen AC, Brixen K (2015) Heart disease in patients with osteogenesis imperfecta-A systematic review. Int J Cardiol 196:149–157. https://doi.org/10.1016/j.ijcard.2015.06.001

    Article  PubMed  Google Scholar 

  42. Pinheiro BS, Barrios PM, Souza LT, Felix TM (2020) Echocardiographic study in children with osteogenesis imperfecta. Cardiol Young 30:1490–1495. https://doi.org/10.1017/S1047951120002474

    Article  PubMed  Google Scholar 

  43. Verdonk SJE, Storoni S, Micha D, van den Aardweg JG, Versacci P, Celli L, de Vries R, Zhytnik L, Kamp O, Bugiani M, Eekhoff EMW (2024) Is osteogenesis imperfecta associated with cardiovascular abnormalities? A systematic review of the literature. Calcif Tissue Int. https://doi.org/10.1007/s00223-023-01171-3

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wittig C, Szulcek R (2021) Extracellular matrix protein ratios in the human heart and vessels: how to distinguish pathological from physiological changes? Front Physiol 12:708656. https://doi.org/10.3389/fphys.2021.708656

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kamberi LS, Gorani DR, Hoxha TF, Zahiti BF (2013) Aortic compliance and stiffness among severe longstanding hypertensive and non-hypertensive. Acta Inform Med 21:12–15. https://doi.org/10.5455/AIM.2013.21.12-15

    Article  PubMed  PubMed Central  Google Scholar 

  46. Balasubramanian M, Verschueren A, Kleevens S, Luyckx I, Perik M, Schirwani S, Mortier G, Morisaki H, Rodrigus I, Van Laer L, Verstraeten A, Loeys B (2019) Aortic aneurysm/dissection and osteogenesis imperfecta: four new families and review of the literature. Bone 121:191–195. https://doi.org/10.1016/j.bone.2019.01.022

    Article  PubMed  Google Scholar 

  47. Hortop J, Tsipouras P, Hanley JA, Maron BJ, Shapiro JR (1986) Cardiovascular involvement in osteogenesis imperfecta. Circulation 73:54–61. https://doi.org/10.1161/01.cir.73.1.54

    Article  CAS  PubMed  Google Scholar 

  48. Gooijer K, Heidsieck G, Harsevoort A, Bout D, Janus G, Franken A (2024) Bleeding assessment in a large cohort of patients with osteogenesis imperfecta. Orphanet J Rare Dis 19:61. https://doi.org/10.1186/s13023-024-03054-8

    Article  PubMed  PubMed Central  Google Scholar 

  49. Vouyouka AG, Pfeiffer BJ, Liem TK, Taylor TA, Mudaliar J, Phillips CL (2001) The role of type I collagen in aortic wall strength with a homotrimeric. J Vasc Surg 33:1263–1270. https://doi.org/10.1067/mva.2001.113579

    Article  CAS  PubMed  Google Scholar 

  50. Pfeiffer BJ, Franklin CL, Hsieh FH, Bank RA, Phillips CL (2005) Alpha 2(I) collagen deficient oim mice have altered biomechanical integrity, collagen content, and collagen crosslinking of their thoracic aorta. Matrix Biol 24:451–458. https://doi.org/10.1016/j.matbio.2005.07.001

    Article  CAS  PubMed  Google Scholar 

  51. Pfeiffer BJ, Phillips CL (2006) Role of Proa(2)I collagen chains and collagen crosslinking in thoracic aortic biochemical integrity during aging using the OIM mouse model. In:University of Missouri-Columbia, Columbia, Mo.

  52. Persiani P, Pesce MV, Martini L, Ranaldi FM, D’Eufemia P, Zambrano A, Celli M, Villani C (2018) Intraoperative bleeding in patients with osteogenesis imperfecta type III treated by Fassier-Duval femoral rodding: analysis of risk factors. J Pediatr Orthop B 27:338–343. https://doi.org/10.1097/BPB.0000000000000483

    Article  PubMed  Google Scholar 

  53. Gooijer K, Rondeel JMM, van Dijk FS, Harsevoort AGJ, Janus GJM, Franken AAM (2019) Bleeding and bruising in osteogenesis imperfecta: international society on thrombosis and haemostasis bleeding assessment tool and haemostasis laboratory assessment in 22 individuals. Br J Haematol 187:509–517. https://doi.org/10.1111/bjh.16097

    Article  PubMed  Google Scholar 

  54. Jackson SC, Odiaman L, Card RT, van der Bom JG, Poon MC (2013) Suspected collagen disorders in the bleeding disorder clinic: a case-control study. Haemophilia 19:246–250. https://doi.org/10.1111/hae.12020

    Article  CAS  PubMed  Google Scholar 

  55. Ermolayev V, Cohrs CM, Mohajerani P, Ale A, Hrabe de Angelis M, Ntziachristos V (2013) Ex-vivo assessment and non-invasive in vivo imaging of internal hemorrhages in Aga2/+ mutant mice. Biochem Biophys Res Commun 432:389–393. https://doi.org/10.1016/j.bbrc.2013.01.011

    Article  CAS  PubMed  Google Scholar 

  56. Yousef H, Alhajj M, Sharma S. Anatomy, Skin (Integument), Epidermis. [Updated 2022 Nov 14]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK470464/

  57. Naffa R, Maidment C, Ahn M, Ingham B, Hinkley S, Norris G (2019) Molecular and structural insights into skin collagen reveals several factors that influence its architecture. Int J Biol Macromol 128:509–520. https://doi.org/10.1016/j.ijbiomac.2019.01.151

    Article  CAS  PubMed  Google Scholar 

  58. Oxlund H, Pedersen U, Danielsen CC, Oxlund I, Elbroond O (1985) Reduced strength of skin in osteogenesis imperfecta. Eur J Clin Invest 15:408–411. https://doi.org/10.1111/j.1365-2362.1985.tb00293.x

    Article  CAS  PubMed  Google Scholar 

  59. Canuto HC, Fishbein KW, Huang A, Doty SB, Herbert RA, Peckham J, Pleshko N, Spencer RG (2012) Characterization of skin abnormalities in a mouse model of osteogenesis imperfecta using high resolution magnetic resonance imaging and Fourier transform infrared imaging spectroscopy. NMR Biomed 25:169–176. https://doi.org/10.1002/nbm.1732

    Article  CAS  PubMed  Google Scholar 

  60. Forlino A, Kuznetsova NV, Marini JC, Leikin S (2007) Selective retention and degradation of molecules with a single mutant alpha1(I) chain in the Brtl IV mouse model of OI. Matrix Biol 26:604–614. https://doi.org/10.1016/j.matbio.2007.06.005

    Article  CAS  PubMed  Google Scholar 

  61. Besio R, Iula G, Garibaldi N, Cipolla L, Sabbioneda S, Biggiogera M, Marini JC, Rossi A, Forlino A (2018) 4-PBA ameliorates cellular homeostasis in fibroblasts from osteogenesis imperfecta patients by enhancing autophagy and stimulating protein secretion. Biochim Biophys Acta Mol Basis Dis 1864:1642–1652. https://doi.org/10.1016/j.bbadis.2018.02.002

    Article  CAS  PubMed  Google Scholar 

  62. Keegan MT, Whatcott BD, Harrison BA (2002) Osteogenesis imperfecta, perioperative bleeding, and desmopressin. Anesthesiology 97:1011–1013. https://doi.org/10.1097/00000542-200210000-00039

    Article  PubMed  Google Scholar 

  63. Veilleux LN, Lemay M, Pouliot-Laforte A, Cheung MS, Glorieux FH, Rauch F (2014) Muscle anatomy and dynamic muscle function in osteogenesis imperfecta type I. J Clin Endocrinol Metab 99:E356-362. https://doi.org/10.1210/jc.2013-3209

    Article  CAS  PubMed  Google Scholar 

  64. Takken T, Terlingen HC, Helders PJ, Pruijs H, Van der Ent CK, Engelbert RH (2004) Cardiopulmonary fitness and muscle strength in patients with osteogenesis imperfecta type I. J Pediatr 145:813–818. https://doi.org/10.1016/j.jpeds.2004.08.003

    Article  PubMed  Google Scholar 

  65. Pouliot-Laforte A, Veilleux LN, Rauch F, Lemay M (2015) Physical activity in youth with osteogenesis imperfecta type I. J Musculoskelet Neuronal Interact 15:171–176

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Moffatt P, Boraschi-Diaz I, Bardai G, Rauch F (2021) Muscle transcriptome in mouse models of osteogenesis imperfecta. Bone 148:115940. https://doi.org/10.1016/j.bone.2021.115940

    Article  CAS  PubMed  Google Scholar 

  67. Tauer JT, Abdullah S, Rauch F (2019) Effect of anti-TGF-beta treatment in a mouse model of severe osteogenesis imperfecta. J Bone Miner Res 34:207–214. https://doi.org/10.1002/jbmr.3617

    Article  CAS  PubMed  Google Scholar 

  68. Abdelaziz DM, Abdullah S, Magnussen C, Ribeiro-da-Silva A, Komarova SV, Rauch F, Stone LS (2015) Behavioral signs of pain and functional impairment in a mouse model of osteogenesis imperfecta. Bone 81:400–406. https://doi.org/10.1016/j.bone.2015.08.001

    Article  PubMed  Google Scholar 

  69. Veilleux LN, Trejo P, Rauch F (2017) Muscle abnormalities in osteogenesis imperfecta. J Musculoskelet Neuronal Interact 17:1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Caudill A, Flanagan A, Hassani S, Graf A, Bajorunaite R, Harris G, Smith P (2010) Ankle strength and functional limitations in children and adolescents with type I osteogenesis imperfecta. Pediatr Phys Ther 22:288–295. https://doi.org/10.1097/PEP.0b013e3181ea8b8d

    Article  PubMed  Google Scholar 

  71. Gremminger VL, Harrelson EN, Crawford TK, Ohler A, Schulz LC, Rector RS, Phillips CL (2021) Skeletal muscle specific mitochondrial dysfunction and altered energy metabolism in a murine model (oim/oim) of severe osteogenesis imperfecta. Mol Genet Metab 132:244–253. https://doi.org/10.1016/j.ymgme.2021.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Gremminger VL, Jeong Y, Cunningham RP, Meers GM, Rector RS, Phillips CL (2019) Compromised exercise capacity and mitochondrial dysfunction in the osteogenesis imperfecta murine (oim) mouse model. J Bone Miner Res 34:1646–1659. https://doi.org/10.1002/jbmr.3732

    Article  CAS  PubMed  Google Scholar 

  73. Grol MW, Haelterman NA, Lim J, Munivez EM, Archer M, Hudson DM, Tufa SF, Keene DR, Lei K, Park D, Kuzawa CD, Ambrose CG, Eyre DR, Lee BH (2021) Tendon and motor phenotypes in the Crtap(-/-) mouse model of recessive osteogenesis imperfecta. Elife. https://doi.org/10.7554/eLife.63488

    Article  PubMed  PubMed Central  Google Scholar 

  74. Youle RJ, van der Bliek AM (2012) Mitochondrial fission, fusion, and stress. Science 337:1062–1065. https://doi.org/10.1126/science.1219855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Gremminger VL, Omosule CL, Crawford TK, Cunningham R, Rector RS, Phillips CL (2022) Skeletal muscle mitochondrial function and whole-body metabolic energetics in the +/G610C mouse model of osteogenesis imperfecta. Mol Genet Metab 136:315–323. https://doi.org/10.1016/j.ymgme.2022.06.004

    Article  CAS  PubMed  Google Scholar 

  76. Seirafi M, Kozlov G, Gehring K (2015) Parkin structure and function. FEBS J 282:2076–2088. https://doi.org/10.1111/febs.13249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gorrell L, Makareeva E, Omari S, Otsuru S, Leikin S (2022) ER, Mitochondria, and ISR regulation by mt-HSP70 and ATF5 upon procollagen misfolding in osteoblasts. Adv Sci (Weinh). https://doi.org/10.1002/advs.202201273

    Article  PubMed  Google Scholar 

  78. Tresoldi I, Oliva F, Benvenuto M, Fantini M, Masuelli L, Bei R, Modesti A (2013) Tendon’s ultrastructure. Muscles Ligaments Tendons J. https://doi.org/10.11138/mltj/2013.3.1.002

    Article  PubMed  PubMed Central  Google Scholar 

  79. Sinkam L, Boraschi-Diaz I, Svensson RB, Kjaer M, Komarova SV, Bergeron R, Rauch F, Veilleux LN (2023) Tendon properties in a mouse model of severe osteogenesis imperfecta. Connect Tissue Res 64:285–293. https://doi.org/10.1080/03008207.2022.2161376

    Article  CAS  PubMed  Google Scholar 

  80. Chretien A, Couchot M, Mabilleau G, Behets C (2022) Biomechanical, microstructural and material properties of tendon and bone in the young oim mice model of osteogenesis imperfecta. Int J Mol Sci. https://doi.org/10.3390/ijms23179928

    Article  PubMed  PubMed Central  Google Scholar 

  81. Misof K, Landis WJ, Klaushofer K, Fratzl P (1997) Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J Clin Invest 100:40–45. https://doi.org/10.1172/JCI119519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. McBride DJ Jr, Choe V, Shapiro JR, Brodsky B (1997) Altered collagen structure in mouse tail tendon lacking the alpha 2(I) chain. J Mol Biol 270:275–284. https://doi.org/10.1006/jmbi.1997.1106

    Article  CAS  PubMed  Google Scholar 

  83. Chretien A, Mabilleau G, Lebacq J, Docquier PL, Behets C (2023) Beneficial effects of zoledronic acid on tendons of the osteogenesis imperfecta mouse (oim). Pharmaceuticals (Basel). https://doi.org/10.3390/ph16060832

    Article  PubMed  Google Scholar 

  84. Suydam SM, Soulas EM, Elliott DM, Silbernagel KG, Buchanan TS, Cortes DH (2015) Viscoelastic properties of healthy achilles tendon are independent of isometric plantar flexion strength and cross-sectional area. J Orthop Res 33:926–931. https://doi.org/10.1002/jor.22878

    Article  PubMed  PubMed Central  Google Scholar 

  85. Zhang ZJ, Fu SN (2013) Shear elastic modulus on patellar tendon captured from supersonic shear imaging: correlation with tangent traction modulus computed from material testing system and test-retest reliability. PLoS ONE 8:e68216. https://doi.org/10.1371/journal.pone.0068216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Berman AG, Organ JM, Allen MR, Wallace JM (2020) Muscle contraction induces osteogenic levels of cortical bone strain despite muscle weakness in a mouse model of osteogenesis imperfecta. Bone 132:115061. https://doi.org/10.1016/j.bone.2019.115061

    Article  PubMed  Google Scholar 

  87. Tosi LL, Floor MK, Dollar CM, Gillies AP, Members of the Brittle Bone Disease C, Hart TS, Cuthbertson DD, Sutton VR, Krischer JP (2019) Assessing disease experience across the life span for individuals with osteogenesis imperfecta: challenges and opportunities for patient-reported outcomes (PROs) measurement: a pilot study. Orphanet J Rare Dis 14:23. https://doi.org/10.1186/s13023-019-1004-x

    Article  PubMed  PubMed Central  Google Scholar 

  88. Beltran-Sanchez H, Soneji S, Crimmins EM (2015) Past, present, and future of healthy life expectancy. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a025957

    Article  PubMed  PubMed Central  Google Scholar 

  89. Lee KJ, Rambault L, Bou-Gharios G, Clegg PD, Akhtar R, Czanner G et al (2022) Collagen (I) homotrimer potentiates the osteogenesis imperfecta (oim) mutant allele and reduces survival in male mice. Dis Model Mech. https://doi.org/10.1242/dmm.049428

    Article  PubMed  PubMed Central  Google Scholar 

  90. Chohan K, Mittal N, McGillis L, Lopez-Hernandez L, Camacho E, Rachinsky M, Mina DS, Reid WD, Ryan CM, Champagne KA, Orchanian-Cheff A, Clarke H, Rozenberg D (2021) A review of respiratory manifestations and their management in Ehlers-Danlos syndromes and hypermobility spectrum disorders. Chron Respir Dis 18:14799731211025312. https://doi.org/10.1177/14799731211025313

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would also like to thank the following funding sources: Wayne L. Ryan Foundation Fellowship (BNL), NIH T32 Fellowship T32GM008396 (BNL), NIH T32 Fellowship T32GM135744 (TKC), and NIH/NICHD –R56HD110848 (CLP). Figure 1 created with BioRender.com.

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  1. Tara K. Crawford and Brittany N. Lafaver are Co-first authors.

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  1. Department of Biochemistry, University of Missouri-Columbia, Columbia, MO, USA

    Tara K. Crawford & Brittany N. Lafaver

  2. Departments of Biochemistry and Child Health, University of Missouri-Columbia, 117 Schweitzer Hall, Columbia, MO, 65211, USA

    Charlotte L. Phillips

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Contributions

Conceptualization: Charlotte L. Phillips (CLP), Literature Search and Data Analyses: Tara K. Crawford (TKC), Brittany N. Lafaver (BNL), and CLP, Drafting manuscript: TKC, BNL, and CLP. Design and Artwork of Fig. 1: BNL. All authors revised the manuscript critically for intellectual content and approved the final version. All authors agree to be accountable for the work and to ensure that any questions relating to the accuracy and integrity of the paper are investigated and properly resolved. CLP is the guarantor.

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Correspondence to Charlotte L. Phillips.

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Tara K. Crawford, Brittany N. Lafaver, and Charlotte L. Phillips have declared no conflict of interests.

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Crawford, T.K., Lafaver, B.N. & Phillips, C.L. Extra-Skeletal Manifestations in Osteogenesis Imperfecta Mouse Models. Calcif Tissue Int (2024). https://doi.org/10.1007/s00223-024-01213-4

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