Differential effects between the loss of MMP-2 and MMP-9 on structural and tissue-level properties of bone

Journal of Bone and Mineral Research

Volumn 26, Issue 6, 2011, Pages 1252-1260

  Nyman, Jeffry S ^a,b,c,h   Lynch, Conor C ^d   Perrien, Daniel S ^b   Thiolloy, Sophie ^e   O'Quinn, Elizabeth C ^b   Patil, Chetan A ^c   Bi, Xiaohong ^b,c   Pharr, George M ^f,g   Mahadevan Jansen, Anita ^c   Mundy, Gregory R ^a,b,e  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f University of Tennessee Knoxville   (United States)

^g OAK RIDGE NATIONAL LABORATORY   (United States)

^h Medical Center East   (United States)

Author keywords

Collagen; Matrix Metalloproteinase; MCT; Mineral; Nanoindentation; Raman

Indexed keywords

COLLAGEN; GELATINASE A; GELATINASE B;

ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE DENSITY; BONE MINERAL; BONE MINERALIZATION; BONE STRENGTH; BONE STRUCTURE; BONE TISSUE; COMPRESSION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; FEMALE; FEMUR; FRACTURE; HARDNESS; LUMBAR VERTEBRA; METAPHYSIS; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAMAN SPECTROMETRY; TIBIA; TRABECULAR BONE; WILD TYPE;

ANIMALS; BIOMECHANICS; BONE AND BONES; BONE DENSITY; DIAPHYSES; FEMALE; FEMUR; GENOTYPE; LUMBAR VERTEBRAE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; ORGAN SPECIFICITY; POROSITY; SPECTRUM ANALYSIS, RAMAN; X-RAY MICROTOMOGRAPHY;

EID: 79958859696     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.326     Document Type: Article

References (45)

1. Burr DB,. The contribution of the organic matrix to bone's material properties. Bone. 2002; 31: 8-11. (Pubitemid 34754418)
2. Krane SM, Inada M,. Matrix metalloproteinases and bone. Bone. 2008; 43: 7-18.
3. Reponen P, Sahlberg C, Munaut C, Thesleff I, Tryggvason K,. High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development. J Cell Biol. 1994; 124: 1091-1102. (Pubitemid 24109410)
4. Blavier L, Delaisse JM,. Matrix metalloproteinases are obligatory for the migration of preosteoclasts to the developing marrow cavity of primitive long bones. J Cell Sci. 1995; 108: 3649-3659. (Pubitemid 26004028)
5. Lu M, Rabie AB,. Matrix metalloproteinase-9 regulates graft bone resorption. Angle Orthod. 2006; 76: 598-604. (Pubitemid 44066014)
6. Vu TH, Shipley JM, Bergers G, et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 1998; 93: 411-422. (Pubitemid 28232085)
7. Bonfil RD, Osenkowski P, Fridman R, Cher ML,. Matrix metalloproteinaes and bone metastasis. Cancer Treat Res. 2004; 118: 173-195.
8. Perez-Amodio S, Beertsen W, Everts V,. (Pre-)osteoclasts induce retraction of osteoblasts before their fusion to osteoclasts. J Bone Miner Res. 2004; 19: 1722-1731. (Pubitemid 41094336)
9. Boumah CE, Selvamurugan N, Partridge NC,. Transcription in the osteoblast: regulatory mechanisms utilized by parathyroid hormone and transforming growth factor-beta. Prog Nucleic Acid Res Mol Biol. 2005; 80: 287-321. (Pubitemid 43574886)
10. Zhao W, Byrne MH, Boyce BF, Krane SM,. Bone resorption induced by parathyroid hormone is strikingly diminished in collagenase-resistant mutant mice. J Clin Invest. 1999; 103: 517-524. (Pubitemid 29094052)
11. Inoue K, Mikuni-Takagaki Y, Oikawa K, et al. A crucial role for matrix metalloproteinase 2 in osteocytic canalicular formation and bone metabolism. J Biol Chem. 2006; 281: 33814-33824. (Pubitemid 46036758)
12. Bi X, Patil CA, Lynch CC, Pharr GM, Mahadevan-Jansen A, Nyman JS,. Raman and mechanical properties correlate at whole bone- and tissue-levels in a genetic mouse model. J Biomech. 2011; 44: 297-303.
13. Dallas SL, Miyazono K, Skerry TM, Mundy GR, Bonewald LF,. Dual role for the latent transforming growth factor-beta binding protein in storage of latent TGF-beta in the extracellular matrix and as a structural matrix protein. J Cell Biol. 1995; 131: 539-549.
14. Maeda S, Dean DD, Gomez R, Schwartz Z, Boyan BD,. The first stage of transforming growth factor beta1 activation is release of the large latent complex from the extracellular matrix of growth plate chondrocytes by matrix vesicle stromelysin-1 (MMP-3). Calcif Tissue Int. 2002; 70: 54-65. (Pubitemid 36934737)
15. Balooch G, Balooch M, Nalla RK, et al. TGF-beta regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci U S A. 2005; 102: 18813-18818. (Pubitemid 43049527)
16. Mohammad KS, Chen CG, Balooch G, et al. Pharmacologic inhibition of the tgf-Beta type I receptor kinase has anabolic and anti-catabolic effects on bone. PLoS ONE. 2009; 4: e5275.
17. Saeki K, Hilton JF, Alliston T, et al. Elevated TGF-beta2 signaling in dentin results in sex related enamel defects. Arch Oral Biol. 2007; 52: 814-821. (Pubitemid 47125839)
18. Erben RG,. Embedding of bone samples in methylmethacrylate: an improved method suitable for bone histomorphometry, histochemistry, and immunohistochemistry. J Histochem Cytochem. 1997; 45: 307-313. (Pubitemid 27114500)
19. Jepsen KJ, Akkus OJ, Majeska RJ, Nadeau JH,. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm Genome. 2003; 14: 97-104. (Pubitemid 36241337)
20. Turner CH, Burr DB,. Basic biomechanical measurements of bone: a tutorial. Bone. 1993; 14: 595-608. (Pubitemid 23198821)
21. Lieber CA, Mahadevan-Jansen A,. Automated method for subtraction of fluorescence from biological Raman spectra. Appl Spectrosc. 2003; 57: 1363-1367.
22. Kazanci M, Roschger P, Paschalis EP, Klaushofer K, Fratzl P,. Bone osteonal tissues by Raman spectral mapping: orientation-composition. J Struct Biol. 2006; 156: 489-496. (Pubitemid 44781298)
23. Awonusi A, Morris MD, Tecklenburg MM,. Carbonate assignment and calibration in the Raman spectrum of apatite. Calcif Tissue Int. 2007; 81: 46-52. (Pubitemid 47030206)
24. Akkus O, Adar F, Schaffler MB,. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone. 2004; 34: 443-453. (Pubitemid 38314909)
25. Schriefer JL, Robling AG, Warden SJ, Fournier AJ, Mason JJ, Turner CH,. A comparison of mechanical properties derived from multiple skeletal sites in mice. J Biomech. 2005; 38: 467-475. (Pubitemid 40126457)
26. Oliver W, Pharr G,. Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology. J Mater Res. 2004; 19: 3-20.
27. Legrand E, Audran M, Guggenbuhl P, et al. Trabecular bone microarchitecture is related to the number of risk factors and etiology in osteoporotic men. Microsc Res Tech. 2007; 70: 952-959. (Pubitemid 350127325)
28. Akhter MP, Lappe JM, Davies KM, Recker RR,. Transmenopausal changes in the trabecular bone structure. Bone. 2007; 41: 111-116. (Pubitemid 46891901)
29. Genant HK, Delmas PD, Chen P, et al. Severity of vertebral fracture reflects deterioration of bone microarchitecture. Osteoporos Int. 2007; 18: 69-76. (Pubitemid 44885497)
30. Nazarian A, Stauber M, Zurakowski D, Snyder BD, Muller R,. The interaction of microstructure and volume fraction in predicting failure in cancellous bone. Bone. 2006; 39: 1196-1202. (Pubitemid 44827930)
31. Nyman JS, Reyes M, Wang X,. Effect of ultrastructural changes on the toughness of bone. Micron. 2005; 36: 566-582. (Pubitemid 41745022)
32. Colnot C, Thompson Z, Miclau T, Werb Z, Helms JA,. Altered fracture repair in the absence of MMP9. Development. 2003; 130: 4123-4133. (Pubitemid 37063429)
33. Delaisse JM, Andersen TL, Engsig MT, Henriksen K, Troen T, Blavier L,. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc Res Tech. 2003; 61: 504-513. (Pubitemid 36890583)
34. Engsig MT, Chen QJ, Vu TH, et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol. 2000; 151: 879-889.
35. Mosig RA, Dowling O, DiFeo A, et al. Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum Mol Genet. 2007; 16: 1113-1123. (Pubitemid 47062731)
36. Zioupos P, Currey JD, Hamer AJ,. The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res. 1999; 45: 108-116. (Pubitemid 29114158)
37. Wang X, Puram S,. The toughness of cortical bone and its relationship with age. Ann Biomed Eng. 2004; 32: 123-135.
38. Gok F, Crettol LM, Alanay Y, et al. Clinical and radiographic findings in two brothers affected with a novel mutation in matrix metalloproteinase 2 gene. Eur J Pediatr. 2009; 169: 363-367.
39. Yamada Y, Ando F, Niino N, Shimokata H,. Association of a polymorphism of the matrix metalloproteinase-9 gene with bone mineral density in Japanese men. Metabolism. 2004; 53: 135-137. (Pubitemid 38168880)
40. Zhao H, Cai G, Du J, Xia Z, Wang L, Zhu T,. Expression of matrix metalloproteinase-9 mRNA in osteoporotic bone tissues. J Tongji Med Univ. 1997; 17: 28-31.
41. Williams S, Wakisaka A, Zeng QQ, et al. Minocycline prevents the decrease in bone mineral density and trabecular bone in ovariectomized aged rats. Bone. 1996; 19: 637-644. (Pubitemid 27035844)
42. Williams S, Barnes J, Wakisaka A, Ogasa H, Liang CT,. Treatment of osteoporosis with MMP inhibitors. Ann N Y Acad Sci. 1999; 878: 191-200. (Pubitemid 29353570)
43. Bain S, Ramamurthy NS, Impeduglia T, Scolman S, Golub LM, Rubin C,. Tetracycline prevents cancellous bone loss and maintains near-normal rates of bone formation in streptozotocin diabetic rats. Bone. 1997; 21: 147-153. (Pubitemid 27395402)
44. Wang M, Zhao D, Spinetti G, et al. Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol. 2006; 26: 1503-1509. (Pubitemid 44288975)
45. Tang Y, Wu X, Lei W, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med. 2009; 15: 757-765.