Bone development in the femoral epiphysis of mice: The role of cartilage canals and the fate of resting chondrocytes

Developmental Dynamics

Volumn 236, Issue 8, 2007, Pages 2077-2088

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

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cartilage canals; Endochondral bone formation; Long bones; Mammals; Secondary ossification centre; Type I collagen

Indexed keywords

COLLAGEN TYPE 1;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE; CARTILAGE CELL; CELL FATE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; FEMUR EPIPHYSIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BONE DEVELOPMENT; CARTILAGE; CHONDROCYTES; DIHYDROPYRIDINES; EPIPHYSES; FEMUR; MICE;

MAMMALIA; MUS;

EID: 34548077823     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21228     Document Type: Article

References (47)

1. Agrawal P, Kulkarni DS, Atre PR. 1986. The participation of cartilage canals in the ossification of the human fetal calcaneum. J Anat 147:135-142.
2. 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 Min Res 20:1011-1021.
3. 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.
4. 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.
5. Blumer MJF, Fritsch H, Pfaller K, Brenner E. 2004a. Cartilage canals in the chicken embryo: ultrastructure and function. Anat Embryo 207:453-462.
6. 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.
7. 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.
8. 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.
9. 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.
10. Chandraraj S, Briggs CA. 1988. Role of cartilage canals in the osteogenesis and growth of the vertebral centra. J Anat 158:121-136.
11. Chappard D, Alexandre C, Riffat G. 1986 Uncalcified cartilage resorption in human fetal cartilage canals. Tissue Cell 18:701-707.
12. Cole AA, Cole MB. 1989. Are perivascular cells in cartilage canals chondrocytes? J Anat 165:1-8.
13. Cole AA, Wezeman FH. 1985. Perivascular cells in cartilage canals of the developing mouse epiphysis. Am J Anat 174:119-129.
14. Davoli MA, Lamplugh L, Beauchemin A, Chan K, Mordier S, Mort JS, Murphy G, Docherty AJP, Leblond CP, Lee ER. 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.
15. 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
16. Doschak MR, Cooper DML, Huculak CN, Matyas JR, Hart DA, Hallgrimsson B, Zernicke RF, Bray RC. 2003. Angiogenesis in the distal femoral chondroepiphysis of the rabbit during the development of the secondary centre of ossification. J Anat 203:223-233.
17. Eslaminejad MRB, Valojerdi MR, Yazdi PE. 2006. Computerized three-dimensional reconstruction of cartilage canals in chick tibial chondroepiphysis. Anat Hist Embryol 35:247-252.
18. Franz-Odendall TA, Hall BK, Witten PE. 2006. Buried alive: how osteoblasts become osteocytes. Dev Dyn 235:176-190.
19. Fritsch H, Eggers R. 1999. Ossification of the calcaneus in the normal foot and in the clubfoot. J Pediatr Orthop 19:22-26.
20. Fritsch H, Brenner E, Debbage P. 2001. Ossification in the human calcaneus: a model for spatial bone development and ossification. J Anat 199:609-616.
21. Galatto M, Campanile G, Robino G, Cancedda FD, Bianco P, Cancedda R. 1994. Hypertrophic chondrocytes undergo further differentiation to osteoblast-like cells and participate in the initial bone formation in the developing chick embryo. J Bone Min Res 9:1239-1249.
22. 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.
23. Gilbert JA, Roach HI, Clarke NMP. 2001. Histological abnormalities of the calcaneum in congential talipes equinovarus. J Orthop Sci 6:519-526.
24. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Pole AR, Pidoux I, Ward JM, Birkedal-Hansen H. 1999. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis and connective tissue disease due to inadequate collagen turnover. Cell 99:81-92.
25. 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.
26. Lee ER, Lamplugh L, Davoli MA, Beauchemin A, Chan K, Mort JS, Leblond CP. 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.
27. Lutfi AM. 1970. Mode of growth, fate and functions of cartilage canals. J Anat 106:135-145.
28. 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.
29. Mizoguchi I, Nakamura M, Takahashi I, Kagayama M, Mitani H. 1992. A comparison of the immunohistochemical localization of type I and Type II collagens in craniofacial cartilages of the rat. Acta Anat 144:59-64.
30. Morini S, Pannarale L, Franchitto A, Donati S, Gaudio E. 1999. Microvascular features and ossification process in the femoral head of growing rats. J Anat 195:225-233.
31. 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.
32. Reno PL, McBurney D, Lovejoy CO, Horton WE. 2006. Ossification of the mouse metatarsal: differentiation and proliferation in the presence/absence of a defined growth plate. Anat Rec 288A:104-118.
33. 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:85-100.
34. 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 12:795-805.
35. Roach HI. 1999. Association of matrix acid and alkaline phosphatases with mineralization of cartilage and endochondral bone. Histochem J 31:53-61.
36. Roach HI, Clarke NMP. 1999. "Cell paralysis" as an intermediate stage in the programmed cell death of epiphyseal chondrocytes during development. J Bone Min Res 14:1367-1378.
37. Roach HI, Shearer JR. 1989. Cartilage resorption and endochondral bone formation during the development of long bones in chick embryos. Bone Mineral 6:289-309.
38. Roach Hi, Erenpreisa J, Aigner T. 1995. Osteogenic differentiation of hypertrophic chondrocytes involves asymmetric cell division and apoptosis. J Cell Biol 131:483-494
39. Roach HI, Baker JE, Clarke NMP. 1998. Initiation of the bony epiphysis in long bones: chronology of interactions between the vascular system and chondrocytes. J Bone Min Res 13:950-961.
40. Roach HI, Aigner T, Kouri JB. 2004. Chondroptosis: A variant of apoptotic cell death in chondrocytes? Apoptosis 9:265-277.
41. Stockwell RA. 1971. The ultrastructure of cartilage canals and the surrounding cartilage in the sheep fetus. J Anat 109:397-410.
42. Thorp BH. 1990. Absence of cartilage canals in the long bone extremities of four species of skeletally immature marsupials. Anat Rec 226:440-446.
43. 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.
44. Wilsman NJ, Van Sickle DC. 1972. Cartilage canals, their morphology and distribution. Anat Rec 173:79-93.
45. Ytrehus B, Carlson CS, Lundeheim N, Mathisen L, Reinholt FP, Teige J, Ekman S. 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.
46. 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.
47. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K. 2000. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. PNAS 97:4052-4057.