COLLAGENS AND COLLAGENASE-3 IN GROWTH PLATES OF UREMIC RATS
523
16. Johansson N, Saarialho-Kere U, Airola C, Herva R, Nissinen
L, Westermarck J, Vuorio E, Heino J, Ka¨ha¨ri V-M 1997
bearing growth plate chondrocytes. J Cell Biochem 65:209–
230.
Collagenase-3 (MMP-13) is expressed by hypertrophic chon- 34. O’Keefe RJO, Loveys LS, Hicks DG, Reynolds PR, Crabb ID,
drocytes, periosteal cells, and osteoblast during human fetal
bone development. Dev Dyn 208:387–397.
17. Ståhle-Ba¨ckdahl M, Sandstedt B, Bruce K, Lindahl A, Jime´nez
Puzas JE, Rosier RN 1997 Differential regulation of type-II
and type-X collagen synthesis by PTHrP in chick growth plate
chondrocytes. J Orthop Res 15:162–174.
MJ, Vega JA, Lo´pez-Ot´ın C 1997 Collagenase-3 (MMP-13) is 35. Kirsch T, Ishikawa Y, Mwale F, Wuthier RE 1994 Roles of the
expressed during human fetal ossification and re-expressed in
postnatal bone remodeling and rheumatoid arthritis. Lab Invest
76:717–728.
nucleational core complex and collagens (types II and X) in
calcification of growth plate cartilage matrix vesicles. J Biol
Chem 269:20103–20109.
18. Alvarez J, Balbin M, Santos F, Fernandez M, Ferrando S, 36. Kirsch T, Wuthier RE 1994 Stimulation of calcification of
Lopez JM 2000 Different bone growth rates are associated
with changes in the expression pattern of types II and X
growth plate cartilage matrix vesicles by binding to type II and
X collagens. J Biol Chem 269:11462–11469.
collagens and collagenase 3 in proximal growth plates of the 37. Sa´nchez CP, Kuizon BD, Abdella PA, Ju¨ppner H, Salusky IB,
rat tibia. J Bone Miner Res 15:82–94.
Goodman WG 2000 Impaired growth, delayed ossification,
and reduced osteoclastic activity in the growth plate of
calcium-supplemented rats with renal failure. Endocrinology
141:1536–1544.
19. Cruz-Orive LM, Hunziker EB 1986 Stereology for anisotropic
cells: Application to growth cartilage. J Microsc 113:47–80.
20. Hunziker EB, Schenk RK 1989 Physiological mechanisms
adopted by chondrocytes in regulating longitudinal bone 38. Dean DD, Mun˜iz OE, Berman I, Pita JC, Carren˜o MR, Woess-
growth in rats. J Physiol 414:55–71.
ner JF, Howell DS 1984 Localization of collagenase in the
21. Breur GJ, Turgai BA, VanEnkevort CE, Farnum CE, Wilsman
growth plate of rachitic rats. J Clin Invest 76:716–722.
´
NJ 1994 Stereological and serial section analysis of chondro- 39. Jime´nez MJG, Balb´ın M, Lo´pez JM, Alvarez J, Komori T,
cytic enlargement in the proximal tibial growth plate of the rat.
Anat Rec 239:255–268.
22. Balb´ın M, Fueyo A, Lopez JM, D´ıez-Itza I, Velasco G, Lopez-
Lo´pez-Ot´ın C 1999 Collagenase-3 is a target of Cbfa1, a
transcription factor of the runt gene family involved in bone
formation. Mol Cell Biol 19:4431–4442.
Ot´ın C 1996 Expression of collagenase-3 in the rat ovary 40. Meikle MC, Bord S, Hembry RM, Reynolds JJ 1995 The
during the ovulatory process. J Endocrinol 149:405–415.
23. Kohno K, Martin GR, Yamada Y 1984 Isolation and charac-
terization of a cDNA clone for the amino-terminal portion of
synthesis of collagenase, gelatinase-A (72kDA) and -B (95
kDa), and TIMP-1 and -2 by human osteoblasts from normal
and arthritic bone. Bone 17:255–260.
the pro-alpha 1(II) chain of cartilage collagen. J Biol Chem 41. Bord S, Horner A, Hembry RM, Compston JE 1998 Stromelysin-1
259:13668–13673.
24. Apte SS, Seldin MF, Hayashi M, Olsen BR 1992 Cloning of
the human and mouse type-X collagen genes and mapping of
(MMP-3) and stromelysin-2 (MMP-10) expression in develop-
ing human bone: Potential roles in skeletal development. Bone
23:7–12.
the mouse type-X collagen gene to chromosome 10. Eur J Bio- 42. Reponen P, Sahlberg C, Munaut C, Thesleff I, Tryggvason K
chem 206:217–224.
1994 High expression of 92-kD type IV collagenase (gelati-
nase B) in osteoclast lineage during mouse development. J Cell
Biol 124:1091–1102.
25. Svoboda KK 1998 Chondrocyte-matrix attachment complexes
mediate survival and differentiation. Microsc Res Tech 43:
111–122.
26. Cao L, Lee V, Adams ME, Kiani C, Zhang Y, Hu W, Yang BB
1999 Beta-integrin-collagen interaction reduces chondrocyte
apoptosis. Matrix Biol 18:343–355.
43. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hana-
han D, Shapiro SD, Senior RM, Werb Z 1998 MMP-9/
Gelatinase B is a key regulator of growth plate angiogenesis
and apoptosis of hypertrophic chondrocytes. Cell 93:411–422.
27. Sandell LJ, Dudek EJ, Bielaga B, Wight TN 1989 Regulation 44. Sato T, Ovejero MC, Hou P, Heegaard AM, Kumegawa M,
of cartilage collagen and proteoglycan synthesis by transform-
ing growth factor-beta. Trans Orthop Res Soc 14:280.
28. Erdmann S, Muller W, Bahrami S, Vornehm SI, Mayer H,
Foged NT, Delaisse JM 1997 Identification of the membrane-
type matrix metallo-proteinase MT1-MMP in osteoclasts.
J Cell Sci 110:589–596.
Bruckner P, von der Mark K, Burkhardt H 1996 Differential 45. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M,
effects of parathyroid hormone fragments on collagen gene
expression in chondrocytes. J Cell Biol 135:1179–1191.
29. Yaeger PC, Masi TL, de Ortiz JL, Binette F, Tubo R, McPher-
son JM 1997 Synergistic action of transforming growth factor-
beta and insulin-like growth factor-I induces expression of
Kuznetsov SA, Mankani M, Robey PG, Poole 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.
type II collagen and aggrecan genes in adult human articular 46. Lee ER, Lamplugh L, Shepard NL, Mort JS 1995 The septo-
chondrocytes. Exp Cell Res 237:318–325.
clast, a cathepsin B-rich cell involved in the resorption of
30. Galera P, Vivien D, Pronost S, Bonaventure J, Redini F, Loyau
growth plate cartilage. J Histochem Cytochem 43:525–536.
G, Pujol JP 1992 Transforming growth factor-beta 1 (TGF- 47. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M,
beta 1) up-regulation of collagen type II in primary cultures of
rabbit articular chondrocytes (RAC) involves increased mRNA
levels without affecting mRNA stability and procollagen pro-
cessing. J Cell Physiol 153:596–606.
Bertoncello I, Drake F, Zavarselk S, Tellis I, Hertzog P,
Debouck C, Kola I 1999 Cathepsin K knockout mice develop
osteopetrosis due to a deficit in matrix degradation but not
demineralization. J Bone Miner Res 14:1654–1663.
31. Oettinger HF, Pacifici M 1990 Type X collagen gene expres- 48. Ho N, Punturieri A, Wilkin D, Szabo J, Johnson M, Whaley J,
sion is transiently up-regulated by retinoic acid treatment in
chick chondrocyte cultures. Exp Cell Res 191:292–298.
32. Iwamoto M, Golden EB, Adams SL, Noji S, Pacifici M 1993
Davis J, Clark A, Weiss S, Francomano C 1999 Mutations of
CTSK result in pycnodysostosis via a reduction in cathepsin K
protein. J Bone Miner Res 14:1649–1653.
Responsiveness to retinoic acid changes during chondrocyte 49. Chan W, Valeri K, Chan JCM 1993 Expression of insulin-like
maturation. Exp Cell Res 205:153–161.
growth factor-I in uremic rats: Growth hormone resistance and
33. Wu LNY, Ishikawa Y, Nie D, Genge BR, Wuthier RE 1997
nutritional intake. Kidney Int 43:790–795.
Retinoic acid stimulates matrix calcification and initiates type 50. Tonshoff B, Ede´n S, Weiser E, Carlsson B, Robinson ICAF,
I collagen synthesis in primary cultures of avian weight- Blum W, Mehls O 1994 Reduced hepatic growth hormone