Tetracyclines inhibit rat osteoclast formation and activity in vitro and affect bone turnover in young rats in vivo

Calcified Tissue International

Volumn 86, Issue 2, 2010, Pages 163-171

  Zhou, Xiaoxiao ^a,b   Zhang, Peng ^c   Zhang, Chao ^d   An, Bingchen ^a   Zhu, Zhen'An ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Tai Zhou Central Hospital   (China)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Bone histomorphometry; Osteoclastogenesis; Oxytetracycline; Tetracycline; Tetracyclines

Indexed keywords

ALIZARIN RED S; CALCEIN; OXYTETRACYCLINE; SODIUM CHLORIDE; TETRACYCLINE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DENSITY; BONE MINERALIZATION; BONE TURNOVER; CELL CULTURE; CELL MATURATION; CELL STIMULATION; CONTROLLED STUDY; FLUOROCHROME STAINING; GROWTH INHIBITION; HISTOPATHOLOGY; IN VITRO STUDY; MACROPHAGE; MALE; METAPHYSIS; NONHUMAN; OSSIFICATION; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; RAT; SURFACE PROPERTY; TIBIA; TRABECULAR BONE;

EID: 76649093268     PISSN: 0171967X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00223-009-9328-5     Document Type: Article

References (46)

1. LM Golub K Soummalainen T Sorsa 1992 Host modulation with tetracyclines and their chemically modified analogues Curr Opin Dent 2 80 90 1:STN:280:DyaK38zptlWrsQ%3D%3D 1325849
2. L Shapira WA Soskolne Y Houri V Barak A Halabi A Stabholz 1996 Protection against endotoxic shock and lipopolysaccharide induced local inflammation by tetracycline: correlation with inhibition of cytokine secretion Infect Immun 64 3 5 8
3. LM Golub HM Lee ME Ryan WV Giannobile J Payne T Sorsa 1998 Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms Adv Dent Res 12 12 26 10.1177/08959374980120010501 1:STN:280:DyaK1M7jvVSltg%3D%3D 9972117
4. BR Rifkin AT Vernillo LM Golub NS Ramamurthy 1994 Modulation of bone resorption by tetracyclines Ann NY Acad Sci 732 165 180 10.1111/j.1749-6632. 1994.tb24733.x 1:CAS:528:DyaK2MXjvFWqt74%3D 7978789
5. LM Golub RT Evans TF McNamara HM Lee NS Ramamurthy 1994 A non-antimicrobial tetracycline inhibits gingival matrix metalloproteinases and bone loss in Porphyromonas gingivalis-induced periodontitis in rats Ann NY Acad Sci 732 96 111 10.1111/j.1749-6632.1994.tb24728.x 1:CAS:528:DyaK2MXjvFWqtrg%3D 7978855
6. L Lambs M Venturini B Decock-Le Révérend H Kozlowski G Berthon 1988 Metal ion-tetracycline interactions in biological fluids. Part 8. Potentiometric and spectroscopic studies on the formation of Ca(II) and Mg(II) complexes with 4-dedimethylamino-tetracycline and 6-desoxy-6-demethyl- tetracycline J Inorg Biochem 33 193 210 10.1016/0162-0134(88)80049-7 1:CAS:528:DyaL1cXlt1ajtr4%3D 3418341 (Pubitemid 18169730)
7. I Chopra M Roberts 2001 Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance Microbiol Mol Biol Rev 65 232 260 10.1128/MMBR.65.2.232-260.2001 1:CAS:528:DC%2BD3MXkvVKmu7Y%3D 11381101 (Pubitemid 32538179)
8. BL Lokeshwar MG Selzer BQ Zhu NL Block LM Golub 2002 Inhibition of cell proliferation, invasion, tumor growth and metastasis by an oral non-antimicrobial tetracycline analog (COL-3) in a metastatic prostate cancer model Int J Cancer 98 297 309 10.1002/ijc.10168 1:CAS:528:DC%2BD38XhsVSku78%3D 11857423 (Pubitemid 34150817)
9. Amin AR, Attur MG, Thakker GD, Patel PD, Vyas PR, Patel RN, Patel IR, Abramson SB (1996) A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc Natl Acad Sci USA 93:14,014-14,019
10. JT Bettany NM Peet RG Wolowacz TM Skerry PS Grabowski 2000 Tetracyclines induce apoptosis in osteoclasts Bone 27 75 80 10.1016/S8756-3282(00)00297-0 1:CAS:528:DC%2BD3cXktFSisL0%3D 10865212 (Pubitemid 30365080)
11. C Zhang TT Tang WP Ren XL Zhang KR Dai 2007 Inhibiting wear particles-induced osteolysis with doxycycline Acta Pharmacol Sin 28 10 1603 1610 10.1111/j.1745-7254.2007.00638.x 1:CAS:528:DC%2BD2sXhtFKjtr3J 17883947 (Pubitemid 47493289)
12. TC Sun S Mori J Roper C Brown T Hooser DB Burr 1992 Do different fluorochrome labels give equivalent histomorphometric information? Bone 13 443 446 10.1016/8756-3282(92)90088-E 1:CAS:528:DyaK3sXlt1KmtrY%3D 1476823
13. BY Lin WS Jee YF Ma HZ Ke DB Kimmel XJ Li 1994 Effects of prostaglandin E2 and risedronate administration on cancellous bone in older female rats Bone 15 489 496 10.1016/8756-3282(94)90272-0 1:CAS:528:DyaK2cXlvFKltbs%3D 7980959 (Pubitemid 24249206)
14. N Takahashi T Akatsu T Sasaki GC Nicholson JM Moseley TJ Martin T Suda 1988 Induction of calcitonin receptors by 1, 25-dihydroxyvitamin D in osteoclast-like multinucleated cells formed from mouse bone marrow cells Endocrinology 123 1504 1510 10.1210/endo-123-3-1504 1:CAS:528:DyaL1cXlsVeht7k%3D 2841098
15. S Takeshita K Kaji A Kudo 2000 Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts J Bone Miner Res 15 1477 1488 10.1359/jbmr.2000.15.8.1477 1:CAS:528:DC%2BD3cXlvVSjsLg%3D 10934646
16. WP Ren SY Yang PH Wooley 2004 A novel murine model of orthopaedic wear debris-associated osteolysis Scand J Immunol 33 1 10 1:CAS:528: DC%2BD2cXjtlGitb4%3D
17. IE el-Hakim 1999 The effect of fibrin stabilizing factor (F.XIII) on healing of bone defects in normal and uncontrolled diabetic rats Int J Oral Maxillofac Surg 28 304 308 10.1034/j.1399-0020.1999.284280413.x 1:STN:280:DyaK1Mzktlejuw%3D%3D 10416901
18. AM Parfitt MK Drezner FH Glorieux JA Kanis H Malluche PJ Meunier SM Ott RR Recker 1987 Bone histomorphometry: standardization of nomenclature, symbols and units. Report of the ASMBR histomorphometry nomenclature committee J Bone Miner Res 2 595 610 1:STN:280:DyaL1czjvVemsQ%3D%3D 3455637
19. LM Golub NS Ramamurthy TF McNamara RA Greenwald BR Rifkin 1991 Tetracyclines inhibit connective tissue breakdown: new therapeutic implications for an old family of drugs Crit Rev Oral Biol Med 2 3 297 321 1:STN:280:DyaK3MzntVWqtA%3D%3D 1654139
20. KM Chang NS Ramamurthy TF McNamara RT Evans B Klausen PA Murray LM Golub 1994 Tetracyclines inhibit Porphyromonas gingivalis-induced alveolar bone loss in rats by a non-antimicrobial mechanism J Periodont Res 29 4 242 249 10.1111/j.1600-0765.1994.tb01218.x 1:CAS:528:DyaK2cXmsVGhsrc%3D 7932017
21. ME Ryan A Usman NS Ramamurthy LM Golub RA Greenwald 2001 Excessive matrix metalloproteinase activity in diabetes: inhibition by tetracycline analogues with zinc reactivity Curr Med Chem 8 3 305 316 1:CAS:528:DC%2BD3MXhs1Krtrc%3D 11172685
22. JA Curci D Petrinec S Liao LM Golub RW Thompson 1998 Pharmacologic suppression of experimental abdominal aortic aneurysms: a comparison of doxycycline and four chemically modified tetracyclines J Vasc Surg 28 6 1082 1093 10.1016/S0741-5214(98)70035-7 1:STN:280:DyaK1M%2FmtFyqsg%3D%3D 9845660
23. LM Golub TF McNamara G D'Angelo RA Greenwald NS Ramamurthy 1987 A non-antibacterial chemically-modified tetracycline inhibits mammalian collagenase activity J Dent Res 66 8 1310 1314 1:CAS:528:DyaL2sXlvFSqtLo%3D 3040832
24. RA Greenwald LM Golub NS Ramamurthy M Chowdhury SA Moak T Sorsa 1998 In vitro sensitivity of the three mammalian collagenases to tetracycline inhibition: relationship to bone and cartilage degradation Bone 22 1 33 38 10.1016/S8756-3282(97)00221-4 9437511 (Pubitemid 28033650)
25. H Trachtman S Futterweit R Greenwald S Moak P Singhal N Franki AR Amin 1996 Chemically modified tetracyclines inhibit inducible nitric oxide synthase expression and nitric oxide production in cultured rat mesangial cells Biochem Biophys Res Commun 229 1 243 248 10.1006/bbrc.1996.1787 1:CAS:528: DyaK28Xnt12quro%3D 8954113 (Pubitemid 27013738)
26. RN Patel MG Attur MN Dave IV Patel SA Stuchin SB Abramson AR Amin 1999 A novel mechanism of action of chemically modified tetracyclines: inhibition of COX-2-mediated prostaglandin E2 production J Immunol 163 6 3459 3467 1:CAS:528:DyaK1MXlvV2lt7w%3D 10477618
27. P D'Agostino V Ferlazzo S Milano M La Rosa G Di Bella R Caruso S Grimaudo M Tolomeo S Feo E Cillari 2001 Anti-inflammatory effects of chemically modified tetracyclines by the inhibition of nitric oxide and interleukin-12 synthesis in J774 cell line Int Immunopharmacol 1 9-10 1765 1776 10.1016/S1567-5769(01) 00100-X 11562068 (Pubitemid 32772647)
28. KL Kirkwood LM Golub PG Bradford 1999 Non-antimicrobial and antimicrobial tetracyclines inhibit IL-6 expression in murine osteoblasts Ann NY Acad Sci 878 667 670 10.1111/j.1749-6632.1999.tb07757.x 1:CAS:528:DyaK1MXkslemsbc%3D 10415803 (Pubitemid 29353643)
29. AT Vernillo NS Ramamurthy LM Golub BR Rifkin 1994 The antimicrobial properties of tetracycline for the treatment of periodontal disease Curr Opin Periodontol 2 111 118
30. LM Golub S Ciancio NS Ramamamurthy M Leung TF McNamara 1990 Low dose doxycycline therapy: effect on gingival and crevicular fluid collagenase in humans J Periodont Res 25 321 330 10.1111/j.1600-0765.1990.tb00923.x 1:STN:280:DyaK3M7hs1Ckuw%3D%3D 2177499
31. JK Woodward I Holen RE Coleman DJ Buttle 2007 The roles of proteolytic enzymes in the development of tumour-induced bone disease in breast and prostate cancer Bone 41 6 912 917 10.1016/j.bone.2007.07.024 1:CAS:528: DC%2BD2sXhtlGjtr3J 17945547 (Pubitemid 350116741)
32. JT Bettany RG Wolowacz 1998 Tetracycline derivatives induce apoptosis selectively in cultured monocytes and macrophages but not in mesenchymal cells Adv Dent Res 12 136 143 10.1177/08959374980120010901 1:STN:280: DyaK1M7jvVSrtw%3D%3D 9972138
33. R Baron L Neff P Tran Van JR Nefussi A Vignery 1986 Kinetic and cytochemical identification of osteoclast precursors and their differentiation into multinucleated osteoclasts Am J Pathol 122 363 378 1:STN:280: DyaL287islKgsg%3D%3D 3946557
34. SG Holmes K Still DJ Buttle NJ Bishop PS Grabowski 2004 Chemically modified tetracyclines act through multiple mechanisms directly on osteoclast precursors Bone 35 2 471 478 10.1016/j.bone.2004.02.028 1:CAS:528: DC%2BD2cXmtVWit7g%3D 15268899 (Pubitemid 38953195)
35. S Holmes S Smith L Borthwick J Dunford M Rogers N Bishop PS Grabowski 2008 CMT3 alters mitochondrial function in murine osteoclast lineage cells Biochem Biophys Res Commun 365 4 840 845 10.1016/j.bbrc.2007.11.054 1:CAS:528:DC%2BD2sXhsVCks7bJ 18036558 (Pubitemid 350234868)
36. AT Vernillo BR Rifkin 1998 Effects of tetracyclines on bone metabolism Adv Dent Res 12 56 62 10.1177/08959374980120012101 1:STN:280: DyaK1M7jvVSksg%3D%3D 9972123
37. TC Lee FJ O'Brien D Taylor 2000 The nature of fatigue damage in bone Int J Fatigue 22 10 847 853 10.1016/S0142-1123(00)00054-2 1:CAS:528: DC%2BD3cXptVemsr0%3D (Pubitemid 32030233)
38. HM Myers HJ Tochon-Danguy CA Baud 1983 IR absorption spectrophotometric analysis of the complex formed by tetracycline and synthetic hydroxyapatite Calcif Tissue Int 35 745 749 10.1007/BF02405117 1:CAS:528:DyaL2cXivFaktQ%3D%3D 6652549
39. D Stepensky L Kleinberg A Hoffman 2003 Bone as an effect compartment: models for uptake and release of drugs Clin Pharmacokinet 42 863 881 10.2165/00003088-200342100-00001 1:CAS:528:DC%2BD3sXntlKiu7c%3D 12885262 (Pubitemid 36995259)
40. JR White FL Pearce 1982 Characterization of chlortetracycline (aureomycin) as a calcium ionophore Biochemistry 21 6309 6312 10.1021/bi00267a041 1:CAS:528:DyaL38XlvFClt74%3D 7150561
41. ML Nelson 1998 Chemical and biological dynamics of tetracyclines Adv Dent Res 12 5 11 10.1177/08959374980120011901 1:STN:280:DyaK1M7jvVSlsQ%3D%3D 9972116
42. S Williams A Wakisaka QQ Zeng J Barnes G Martin WJ Wechter CT Liang 1996 Minocycline prevents the decrease in bone mineral density and trabecular bone in ovariectomized aged rats Bone 19 6 637 644 10.1016/S8756-3282(96)00302-X 1:CAS:528:DyaK2sXpt1Wkuw%3D%3D 8968031 (Pubitemid 27035844)
43. T Sasaki NS Ramamurthy LM Golub 1998 Long-term therapy with a new chemically modified tetracycline (CMT-8) inhibits bone loss in femurs of ovariectomized rats Adv Dent Res 12 2 76 81 10.1177/08959374980120012501 1:STN:280:DyaK1M7jvVSksQ%3D%3D 9972126
44. J Folwarczna M Pytlik W Janiec 2003 Effects of doxycycline on development of changes in histomorphometric parameters of bones induced by bilateral ovariectomy in rats Pol J Pharmacol 55 3 433 441 1:CAS:528:DC%2BD3sXotlemurY%3D 14506323
45. P Garnero M Ferreras MA Karsdal R Nicamhlaoibh J Risteli O Borel 2003 The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation J Bone Miner Res 18 5 859 867 10.1359/jbmr.2003.18.5. 859 1:CAS:528:DC%2BD3sXjslahsrY%3D 12733725 (Pubitemid 37294969)
46. F Chopin P Garnero A le Henanff F Debiais A Daragon C Roux 2008 Long term effects of Infliximab on bone and cartilage turnover markers in patients with rheumatoid arthritis Ann Rheum Dis 67 3 353 357 10.1136/ard.2007.076604 1:CAS:528:DC%2BD1cXjs1ejs7w%3D 17644538 (Pubitemid 351281270)