Localization of tartrate-resistant acid phosphatase (TRAP), membrane type-1 matrix metalloproteinases (MT1-MMP) and macrophages during early endochondral bone formation

Journal of Anatomy

Volumn 213, Issue 4, 2008, Pages 431-441

  Blumer, Michael J F ^a   Longato, Stefano ^a   Fritsch, Helga ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cartilage canals; Endochondral bone formation; Macrophages; Membrane type 1 matrix metalloproteinases (MT1 MMP); Tartrate resistant acid phosphatase (TRAP)

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; INTERSTITIAL COLLAGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE MATRIX; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIAPHYSIS; ENCHONDRAL OSSIFICATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; EPIPHYSIS; FEMUR; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ACID PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; BONE DEVELOPMENT; CARTILAGE; CHONDROCYTES; FEMUR; HISTOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MACROPHAGES; MATRIX METALLOPROTEINASE 14; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OSTEOBLASTS; OSTEOGENESIS;

ANIMALIA; MUS;

EID: 53149110818     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2008.00958.x     Document Type: Article

References (61)

1. Álvarez J, Costales L, Serra R, Balbin M, López JM (2005a) Expression patterns of matrix metalloproteinases and vascular endothelial growth factor during epiphyseal ossification. J Bone Miner Res 20, 1011-1021.
2. Álvarez J, Costales L, López-Muñiz A, López JM (2005b) Chondrocytes are released as viable cells during cartilage resorption associated with the formation of intrachondral canals in the rat tibial epiphysis. Cell Tissue Res 320, 501-507.
3. Blumer MJF, Gahleitner P, Narzt T, Handl C, Ruthensteiner B (2002) Ribbons of semithin sections: An advanced method with a new type of diamond knife. J Neurosci Methods 120, 11-16.
4. Blumer MJF, Fritsch H, Pfaller K, Brenner E (2004a) Cartilage canals in the chicken embryo: Ultrastructure and function. Anat Embryo 207, 453-462.
5. Blumer MJF, Longato S, Fritsch H (2004b) Cartilage canals in the chicken embryo are involved in the process of endochondral bone formation within the epiphyseal growth plate. Anat Rec 279A, 692-700.
6. Blumer MJF, Longato S, Richter E, Pérez MT, Konakci KZ, Fritsch H (2005) The role of cartilage canals in endochondral and perichondral bone formation: Are there similarities between these two processes? J Anat 206, 359-372.
7. Blumer MJF, Schwarzer C, Pérez MT, Konakci KZ, Fritsch H (2006) Identification and location of bone forming cells within cartilage canals on their course into the secondary ossification centre (SOC). J Anat 208, 695-707.
8. Blumer MJF, Longato S, Schwarzer C, Fritsch H (2007) Bone development in the femoral epiphysis of mice: The role of cartilage canals and the fate of resting chondrocytes. Dev Dyn 236, 2077-2088.
9. Blumer MJF, Longato S, Fritsch H (2008) Structure, formation and role of cartilage canals in the developing bone. Ann Anat (in press).
10. Burkus KJ, Ganey TM, Ogden JA (1993) Development of the cartilage canals and the secondary center of ossification in the distal chondroepiphysis of the prenatal human femur. Yale J Biol Med 66, 193-202.
11. Carlevaro MF, Cermelli S, Cancedda R, Descalzi Cancedda F (2000) Vascular endothelial growth factor (VEGF) in cartilage neovascularization and chondrocyte differentiation: Auto-paracrine role during endochondral bone formation. J Cell Sci 113, 59-69.
12. Chappard D, Alexandre C, Riffat G (1986) Uncalcified cartilage resorption in human fetal cartilage canals. Tissue Cell 18, 701-707.
13. Cole AA, Cole MB (1989) Are perivascular cells in cartilage canals chondrocytes? J Anat 165, 1-8.
14. Cole AA, Wezeman FH (1985) Perivascular cells in cartilage canals of the developing mouse epiphysis. Am J Anat 174, 119-129.
15. Cole AA, Wezeman FH (1987) Cytochemical localization of tartrate-resistant acid phosphatase, alkaline phosphatase and non-specific esterase in perivascular cells of cartilage canals in the developing mouse epiphysis. Am J Anat 180, 237-242.
16. Davoli MA, Lamplugh L, Beauchemin A, et al. (2001) Enzymes active in the areas undergoing cartilage resorption during the development of the secondary ossification center in the tibiae of rats ages 0-21.days: II. Two proteinases, gelatinase B and collagenase-3, are implicated in the lysis of collagen fibrils. Dev Dyn 222, 71-88.
17. Delgado-Baeza E, Giménez-Ribotta M, Miralles-Flores C, Nieto-Chaguaceda A, Santos-Alvarez I (1991) Relationship between the cartilage canal and the perichondrium in the rat proximal tibial epiphysis. Acta Anat 141, 31-35.
18. Doménech-Ratto G, Fernández-Villacañas Marín M, Ballester-Moreno A, Doménech-Asensi P (1999) Development and segments of cartilage canals in the chick embryo. A light microscope study. Eur J Anat 3, 121-126.
19. Doschak MR, Cooper DML, Huculak CN, et al. (2003) Angiogenesis in the distal femoral chondroepiphysis of the rabbit during the development of the secondary centre of ossification. J Anat 203, 223-233.
20. Erenpreisa J, Roach HI (1998) Aberrant death in dark chondrocytes of the avian growth plate. Cell Death Differ 5, 60-66.
21. Eslaminejad MRB, Valojerdi MR, Yazdi PE (2006) Computerized three-dimensional reconstruction of cartilage canals in chick tibial chondroepiphysis. Anat Hist Embryol 35, 247-252.
22. Filanti C, Dickson GR, Di Martino D, et al. (2000) The expression of metalloproteinase-2, -9, and -14, and of tissue inhibitors-1 and -2 is developmentally modulated during ontogenesis in vitro, the mature osteoblastic phenotype expressing metalloproteinase-14. J Bone Miner Res 15, 2154-2168.
23. Franz-Odendaal TA, Hall BK, Witten PE (2006) Buried alive: How osteoblasts become osteocytes. Dev Dyn 235, 176-190.
24. Ganey TM, Ogden JA, Sasse J, Neame PJ, Hilbelink DR (1995) Basement membrane composition of cartilage canals during development and ossification of the epiphysis. Anat Rec 241, 425-437.
25. Haines RW (1933) Cartilage canals. J Anat 68, 45-64.
26. Hayman AR, Cox TM (2003) Tartrate-resistant acid phosphatase knockout mice. J Bone Miner Res 18, 1905-1907.
27. Hayman AR, Bune AJ, Cox TM (2000) Widespread expression of tartrate-resistant acid phosphatase (Acp 5) in the mouse embryo. J Anat 196, 433-441.
28. Hayman AR, Jones SJ, Boyde A, et al. (1996) Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis. Development 122, 3151-3162.
29. Hollberg K, Hultenby K, Hayman AR, Cox TM, Andersson G (2002) Osteoclasts from mice deficient in tartrate-resistant acid phosphatase have altered ruffled borders and disturbed intracellular vesicular transport. Exp Cell Res 279, 227-238.
30. Holmbeck K, Szabova L (2006) Aspects of extracellular matrix remodeling in development and disease. Birth Defects Res C Embryo Today 78, 11-23.
31. Holmbeck K, Bianco P, Caterina J, et al. (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
32. Holmbeck K, Bianco P, Pidoux I, et al. (2005) The metalloproteinase MT1-MMP is required for normal development and maintenance of osteocyte processes in bone. J Cell Sci 118, 147-156.
33. Irie K, Tsugura E, Sakakura Y, Muto T, Yajima T (2001) Immunohistochemical localization of membrane type1-matrix metalloproteinase (MT1-MMP) in osteoclasts in vivo. Tissue and Cell 33, 478-482.
34. Izu Y, Soeta S, Kamiya S, Saito RT, Yamamoto S, Taniguchi K (2005) Distribution of type VI collagen in the cartilaginous tissue of the proximal tibia in the domestic cat. J Vet Med Sci 67 (9), 927-933.
35. Kugler JH, Tomlinson A, Wagstaff A, Ward SM (1979) The role of cartilage canals in the formation of secondary centres of ossification. J Anat 129, 493-506.
36. Lee ER, Lamplugh L, Davoli MA, et al. (2001) Enzymes active in the areas undergoing cartilage resorption during the development of the secondary ossification center in the tibiae of rats ages 0-21.days: I. Two groups of proteinases cleave the core protein of aggrecan. Dev Dyn 222, 52-70.
37. Li M, Sasaki T, Ono K, et al. (2007) Distribution of macrophages, osteoclasts and B-lymphocyte lineage in osteolytic metastasis of mouse mammary carcinoma. Biomed Res 28, 127-137.
38. Lutfi AM (1970) Mode of growth, fate and functions of cartilage canals. J Anat 106, 135-145.
39. Malemud CJ (2006) Matrix metalloproteinase: Role in the skeletal development and growth plate disorders. Front Biosci 11, 1702-1715.
40. Melton JTK, Clarke NMP, Roach HI (2006) Matrix metalloproteinase-9 induces the formation of cartilage canals in the chondroepiphysis of the neonatal rabbit. J Bone Joint Surg 88-A, 155-161.
41. Morini S, Continenza MA, Ricciardi G, Gaudio E, Pannarale L (2004) Development of the microcirculation of the secondary ossification centre in rat humeral head. Anat Rec 278A, 419-427.
42. Olstad K, Ytrehus B, Ekman S, Carlson CS, Dolvik NI (2007) Early lesions of osteochondrosis in the distal tibia of foals. J Orthop Res 25, 1094-1105.
43. Petersen W, Tsokos M, Pufe T (2002) Expression of VEGF121 and VEGF165 in hypertrophic chondrocytes of the human growth plate and epiphyseal cartilage. J Anat 201, 153-157.
44. Rivas R, Shapiro F (2002) Structural stages in the development of the long bones and epiphyses: A study in the New Zealand white rabbit. J Bone Joint Surg 84-A (1), 85-100.
45. Roach HI (1997) New Aspects of endochondral ossification in the chick: chondrocyte apoptosis, bone formation by former chondrocytes, and acid phosphatase activity in the endochondral bone matrix. J Bone Miner Res 12 (5), 795-805.
46. Roach HI (2000) Bone anatomy and cell biology. Reviews of the European Calcified Tissue Society. http://www.ectsoc.org/reviews/011_roac.htm, 1/13-13/13.
47. Roach HI, Shearer JR (1989) Cartilage resorption and endochondral bone formation during the development of long bones in chick embryos. Bone and Mineral 6, 289-309.
48. Roach HI, Mehta G, Oreffo ROC, Clarke NMP, Cooper C (2003) Temporal analysis of rat growth plates: Cessation of growth with age despite presence of a physis. J Histochem Cytochem 51 (3), 373-383.
49. Roberts HC, Knott L, Avery NC, Cox TM, Evans MJ, Hayman AR (2007) Altered collagen in tartrate-resistant acid phosphatase (TRAP)-deficient mice: A role for TRAP in collagen metabolism. Calcif Tissue Int 80, 400-410.
50. Rodríguez JI, Delgado E, Paniagua R (1985) Multivacuolated cells in human cartilage canals. Acata Anat 124, 54-57.
51. Sinha DN, Varma (1982) Cartilage canal and chondroepiphysis of the lower end of the femur of human fetus. Anat Anz Jena 152, 461-466.
52. Stickens D, Behonick D, Ortega N, et al. (2004) Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131, 5883-5895.
53. Suter A, Everts V, Boyde A, et al. (2001) Overlapping functions of lysosomal acid phosphatase (LAP) and tartrate-resistant acid phosphatase (Acp5) revealed by doubly deficient mice. Development 128, 4899-4910.
54. Suzuki H, Amizuka N, Oda K, Noda M, Ohshima H, Maeda T (2008) Histological and elemental analyses of impaired bone mineralization in klotho- deficient mice. J Anat 212, 275-285.
55. Takahara M, Naruse T, Takagi M, Orui H, Ogino T (2004) Matrix metalloproteinase-9 expression, tartrate-resistant acid phosphatase activity, and DNA fragmentation in vascular and cellular invasion into cartilage preceding primary endochondral ossification in long bones. J Orthop Res 22, 1050-1057.
56. Visco DM, Hill MA, Van Sickle DC, Kincaid SA (1990) The development of centres of ossification of bones forming elbow joints in young swine. J Anat 171, 25-39.
57. Vu TH, Shipely JM, Bergers G, et al. (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422.
58. Wilsman NJ, Van Sickle DC (1972) Cartilage canals, their morphology and distribution. Anat Rec 173, 79-93.
59. Ytrehus B, Carlson CS, Lundeheim N, et al. (2004a) Vascularisation and osteochondrosis of the epiphyseal growth cartilage of the distal femur in pigs - development with age, growth rate, weight and joint shape. Bone 34, 454-465.
60. Ytrehus B, Ekman S, Carlson CS, Teige J, Reinholt FP (2004b) Focal changes in blood flow are central in the pathogenesis of osteochondrosis in pigs. Bone 35, 1294-1306.
61. Zhou Z, Apte SS, Soininen R, et al. (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. PNAS 97, 4052-4057.