BMP-9-induced muscle heterotopic ossification requires changes to the skeletal muscle microenvironment

Journal of Bone and Mineral Research

Volumn 26, Issue 6, 2011, Pages 1166-1177

  Leblanc, Elisabeth ^a,c   Trensz, Frédéric ^a,c   Haroun, Sonia ^a,c   Drouin, Geneviève ^a,c   Bergeron, Éric ^d   Penton, Christopher M ^e   Montanaro, Federica ^e,f   Roux, Sophie ^b,c   Faucheux, Nathalie ^b,d   Grenier, Guillaume ^a,b,c  

^a Research Centre on Aging   (Canada)

^b tienne Lebel Clinical Research Centre   (Canada)

^c UNIVERSITY OF SHERBROOKE   (Canada)

^d UNIVERSITÉ DE SHERBROOKE   (Canada)

^e THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^f THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

ALK1; MUSCLE DAMAGE; MUSCLE RESIDENT STROMAL CELLS; SCA1; CT SCAN

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ALKALINE PHOSPHATASE; BETA GALACTOSIDASE; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 9; BONE MORPHOGENETIC PROTEIN RECEPTOR; OSTEOCALCIN; OSTEOGENIC PROTEIN 1; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MATRIX; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CONTROLLED STUDY; CRUSH TRAUMA; ENZYME ACTIVITY; ENZYME SUBSTRATE; FLUORESCENCE ACTIVATED CELL SORTING; GASTROCNEMIUS MUSCLE; HETEROTOPIC OSSIFICATION; HISTOPATHOLOGY; INHIBITION KINETICS; MALE; MICROENVIRONMENT; MOUSE; MUSCLE INJURY; NONHUMAN; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STROMA CELL; TIBIALIS ANTERIOR MUSCLE; UPREGULATION;

EID: 79958836135     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.311     Document Type: Article

References (55)

1. Vanden Bossche L, Vanderstraeten G,. Heterotopic ossification: a review. J Rehabil Med. 2005; 37: 129-136. (Pubitemid 40775150)
2. Kaplan FS, Shen Q, Lounev V, et al. Skeletal metamorphosis in fibrodysplasia ossificans progressiva (FOP). J Bone Miner Metab. 2008; 26: 521-530.
3. Shore EM, Xu M, Feldman GJ, et al. A recurrent mutation in the BMP type 1 receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet. 2006; 38: 525-527.
4. Shehab D, Elgazzar AH, Collier BD,. Heterotopic ossification. J Nucl Med. 2002; 43: 346-353. (Pubitemid 34208096)
5. Mollan RA,. Serum alkaline phosphatase in heterotopic para-articular ossification after total hip replacement. J Bone Joint Surg Br. 1979; 61B: 432-434. (Pubitemid 10201803)
6. Newman RJ, Stone MH, Mukherjee SK,. Accelerated fracture union in association with severe head injury. Injury. 1987; 18: 241-246. (Pubitemid 17102292)
7. van Kuijk AA, Geurts AC, van Kuppevelt HJ,. Neurogenic heterotopic ossification in spinal cord injury. Spinal Cord. 2002; 40: 313-326. (Pubitemid 34756209)
8. Reddi AH,. Marshall R. Urist: a renaissance scientist and orthopaedic surgeon. J Bone Joint Surg Am. 2003; 85-A (Suppl 3): 3-7. (Pubitemid 36951111)
9. Craven PL, Urist MR,. Osteogenesis by radioisotope labelled cell populations in implants of bone matrix under the influence of ionizing radiation. Clin Orthop Relat Res. 1971; 76: 231-243.
10. Chalmers J, Gray DH, Rush J,. Observations on the induction of bone in soft tissues. J Bone Joint Surg Br. 1975; 57: 36-45.
11. Chen D, Zhao M, Mundy GR,. Bone morphogenetic proteins. Growth Factors. 2004; 22: 233-241. (Pubitemid 40136452)
12. Kitisin K, Saha T, Blake T, et al. Tgf-Beta signaling in development. Sci STKE. 2007; 399.
13. Kang Q, Sun MH, Cheng H, et al. Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther. 2004; 11: 1312-1320. (Pubitemid 39213996)
14. Miyazono K, Maeda S, Imamura T,. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005; 16: 251-263. (Pubitemid 40910315)
15. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S,. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood. 2007; 109: 1953-1961. (Pubitemid 46348192)
16. Attisano L, Carcamo J, Ventura F, Weis FM, Massague J, Wrana JL,. Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell. 1993; 75: 671-680. (Pubitemid 23346366)
17. Lopez-Coviella I, Mellott TM, Kovacheva VP, et al. Developmental pattern of expression of BMP receptors and Smads and activation of Smad1 and Smad5 by BMP9 in mouse basal forebrain. Brain Res. 2006; 1088: 49-56. (Pubitemid 43729407)
18. Scime A, Desrosiers J, Trensz F, et al. Transcriptional profiling of skeletal muscle reveals factors that are necessary to maintain satellite cell integrity during ageing. Mech Ageing Dev. 2010; 131: 9-20.
19. Charge SB, Rudnicki MA,. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004; 84: 209-238. (Pubitemid 38049880)
20. Mauro A,. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961; 9: 493-495.
21. Grenier G, Scime A, Le Grand F, et al. Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells. 2007; 25: 3101-3110. (Pubitemid 350294436)
22. Christov C, Chretien F, Abou-Khalil R, et al. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell. 2007; 18: 1397-1409. (Pubitemid 46626634)
23. Joe AW, Yi L, Natarajan A, et al. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol. 2010; 12: 153-163.
24. Scime A, Grenier G, Huh MS, et al. Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. Cell Metab. 2005; 2: 283-295.
25. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA,. Myogenic specification of side population cells in skeletal muscle. J Cell Biol. 2002; 159: 123-134. (Pubitemid 35191524)
26. Trensz F, Haroun S, Cloutier A, Richter MV, Grenier G,. A Muscle Resident Cell Population Promotes Fibrosis in Hindlimb Skeletal Muscles of Mdx Mice Through the Wnt Canonical Pathway. Am J Physiol Cell Physiol. 2010; 299: c939-c947.
27. Walker MR, Patel KK, Stappenbeck TS,. The stem cell niche. J Pathol. 2009; 217: 169-180.
28. Caron AZ, Drouin G, Desrosiers J, Trensz F, Grenier G,. A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. J Appl Physiol. 2009; 106: 2049-2059.
29. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE,. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol. 1998; 194: 114-128. (Pubitemid 28115263)
30. Campeau E, Ruhl VE, Rodier F, et al. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS ONE. 2009; 4: e6529.
31. Kablar B, Krastel K, Ying C, Asakura A, Tapscott SJ, Rudnicki MA,. MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development. 1997; 124: 4729-38. (Pubitemid 28014376)
32. Abramoff MD, Magelhaes PJ, Ram SJ,. Image Processing with ImageJ. Biophotonics International. 2004; 11: 36-42.
33. Depew MJ,. Analysis of skeletal ontogenesis through differential staining of bone and cartilage. Methods Mol Biol. 2008; 461: 37-45.
34. Bergeron E, Marquis ME, Chretien I, Faucheux N,. Differentiation of preosteoblasts using a delivery system with BMPs and bioactive glass microspheres. J Mater Sci Mater Med. 2007; 18: 255-263. (Pubitemid 46332846)
35. Beiner JM, Jokl P,. Muscle contusion injury and myositis ossificans traumatica. Clin Orthop Relat Res. 2002; (403 Suppl): S110-9. (Pubitemid 35345996)
36. Karsenty G,. Transcriptional control of skeletogenesis. Annu Rev Genomics Hum Genet. 2008; 9: 183-196.
37. Senta H, Park H, Bergeron E, et al. Cell responses to bone morphogenetic proteins and peptides derived from them: biomedical applications and limitations. Cytokine Growth Factor Rev. 2009; 20: 213-222.
38. Walton M, Rothwell AG,. Reactions of thigh tissues of sheep to blunt trauma. Clin Orthop Relat Res. 1983; 273-281. (Pubitemid 13064879)
39. Gautschi OP, Cadosch D, Frey SP, Skirving AP, Filgueira L, Zellweger R,. Serum-mediated osteogenic effect in traumatic brain-injured patients. ANZ J Surg. 2009; 79: 449-455.
40. Hosoyama T, Ishiguro N, Yamanouchi K, Nishihara M,. Degenerative muscle fiber accelerates adipogenesis of intramuscular cells via RhoA signaling pathway. Differentiation. 2009; 77: 350-359.
41. Rothwell AG,. Quadriceps Hematoma. A prospective clinical study. Clin Orthop Relat Res. 1982; 97-103. (Pubitemid 13217493)
42. King JB,. Post-traumatic ectopic calcification in the muscles of athletes: a review. Br J Sports Med. 1998; 32: 287-290. (Pubitemid 28534873)
43. Forsberg JA, Potter BK,. Heterotopic ossification in wartime wounds. J Surg Orthop Adv. 2010; 19: 54-61.
44. Egermann M, Baltzer AW, Adamaszek S, et al. Direct adenoviral transfer of bone morphogenetic protein-2 cDNA enhances fracture healing in osteoporotic sheep. Hum Gene Ther. 2006; 17: 507-517. (Pubitemid 43794490)
45. Kan L, Hu M, Gomes WA, Kessler JA,. Transgenic mice overexpressing BMP4 develop a fibrodysplasia ossificans progressiva (FOP)-like phenotype. Am J Pathol. 2004; 165: 1107-1115. (Pubitemid 39297718)
46. Gautschi OP, Toffoli AM, Joesbury KA, Skirving AP, Filgueira L, Zellweger R,. Osteoinductive effect of cerebrospinal fluid from brain-injured patients. J Neurotrauma. 2007; 24: 154-162. (Pubitemid 46214421)
47. Chantraine A, Minaire P,. Para-osteo-arthropathies. A new theory and mode of treatment. Scand J Rehabil Med. 1981; 13: 31-37. (Pubitemid 11039442)
48. Wick L, Berger M, Knecht H, Glucker T, Ledermann HP,. Magnetic resonance signal alterations in the acute onset of heterotopic ossification in patients with spinal cord injury. Eur Radiol. 2005; 15: 1867-1875. (Pubitemid 41222893)
49. Kozlowski P,. Could hypoxia of connective tissue lead to heterotopic ossification?. Chir Narzadow Ruchu Ortop Pol. 2004; 69: 241-244.
50. Blackwell KA, Raisz LG, Pilbeam CC,. Prostaglandins in bone: bad cop, good cop? Trends Endocrinol Metab. 2010; 21: 294-301.
51. Banovac K, Williams JM, Patrick LD, Haniff YM,. Prevention of heterotopic ossification after spinal cord injury with indomethacin. Spinal Cord. 2001; 39: 370-374. (Pubitemid 32758622)
52. Romano CL, Duci D, Romano D, Mazza M, Meani E,. Celecoxib versus indomethacin in the prevention of heterotopic ossification after total hip arthroplasty. J Arthroplasty. 2004; 19: 14-18. (Pubitemid 38112326)
53. Teasell RW, Mehta S, Aubut JL, et al. A systematic review of the therapeutic interventions for heterotopic ossification after spinal cord injury. Spinal Cord. 2010; 48: 512-521.
54. Chen L, Jiang W, Huang J, et al. Insulin-like growth factor 2 (IGF2) potentiates BMP9-induced osteogenic differentiation and bone formation. J Bone Miner Res. 2010; 25: 2447-2459.
55. Zhang W, Deng ZL, Chen L, et al. Retinoic acids potentiate BMP9-induced osteogenic differentiation of mesenchymal progenitor cells. PLoS ONE. 2010; 5: e11917.