To investigate the role of the nervous system of bone in steroid-induced osteonecrosis in rabbits

Osteoporosis International

Volumn 21, Issue 12, 2010, Pages 2057-2066

  Wang, L ^a   Wang, N ^b   Li, M ^a   Wang, K ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Bidirectional regulation; Bone tissue; Neural factors; Osteonecrosis; Rabbit; Steroid

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY; NERVE GROWTH FACTOR ANTIBODY; NEUROPEPTIDE Y; SUBSTANCE P; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE NECROSIS; BONE PLATE; CONTROLLED STUDY; DISEASE MODEL; FEMALE; FEMUR HEAD; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE FIBER; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; STEROID INDUCED OSTEONECROSIS;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FEMUR HEAD; FEMUR HEAD NECROSIS; GLUCOCORTICOIDS; METHYLPREDNISOLONE; NERVE FIBERS; NEUROPEPTIDES; RABBITS;

EID: 78549247787     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-009-1159-8     Document Type: Article

References (77)

1. DE Fisher WH Bickel 1971 Corticosteroid-induced avascular necrosis J Bone Joint Surg 53A 859 873
2. MA Mont DS Hungerford 1995 Non-traumatic avascular necrosis of the femoral head J Bone Joint Surg 77A 459 474
3. HJ Mankin 1992 Nontraumatic necrosis of bone (osteonecrosis) N Engl J Med 326 1473 1479 10.1056/NEJM199205283262206 1574093
4. CC Chang A Greenspan ME Gershwin 1993 Osteonecrosis: current perspectives on pathogenesis and treatment Semin Arthritis Rheum 23 47 69 10.1016/S0049-0172(05)80026-5 8235665
5. K Ono T Tohjima T Komazawa 1992 Risk factors of avascular necrosis of the femoral head in patients with systemic lupus erythematosus under high-dose corticosteroid therapy Clin Orthop 277 89 97 1555361
6. DL Veenstra JH Best J Hornberger SD Sullivan DE Hricik 1999 Incidence and long-term cost of steroid-related side effects after renal transplantation Am J Kidney Dis 33 829 839 10.1016/S0272-6386(99)70414-2 10213637 (Pubitemid 29214678)
7. W Drescher KP Weigert MH Bunger J Ingerslev C Bunger ES Hansen 2004 Femoral head blood flow reduction and hypercoagulability under 24 h megadose steroid treatment in pigs J Orthop Res 22 501 508 10.1016/j.orthres.2003.10.002 15099627 (Pubitemid 38489725)
8. TM Zizic C Marcoux DS Hungerford MB Stevens 1986 The early diagnosis of ischemic necrosis of bone Arthritis Rheum 29 1177 1186 10.1002/art.1780291001 3768054
9. DE Fisher 1978 The role of fat embolism in the etiology of corticosteroid-induced avascular necrosis: clinical and experimental results Clin Orthop 130 68 80 639408
10. JP Jones Jr 1993 Fat embolism, intravascular coagulation, and osteonecrosis Clin Orthop 292 294 308 8519124
11. JP Jones Jr 1992 Intravascular coagulation and osteonecrosis Clin Orthop Relat Res 277 41 53 1532547
12. C Zalavras Z Dailiana M Elisaf E Bairaktari P Vlachogiannopoulos A Katsaraki KN Malizos 2000 Potential aetiological factors concerning the development of osteonecrosis of the femoral head Eur J Clin Invest 30 215 221 10.1046/j.1365-2362.2000.00621.x 10691998 (Pubitemid 30153662)
13. GJ Wang DE Sweet SI Reger RC Thompson 1977 Fat-cell changes as a mechanism of avascular necrosis of the femoral head in cortisone-treated rabbits J Bone Joint Surg Am 59 729 735 908695
14. K Miyanishi T Yamamoto T Irisa A Yamashita S Jingushi Y Noguchi Y Iwamoto 2002 Bone marrow fat cell enlargement and a rise in intraosseous pressure in steroid-treated rabbits with osteonecrosis Bone (NY) 30 185 190
15. EL Hill R Elde 1991 Distribution of CGRP-, VIP-, D beta H-,SP-, and NPY-immunoreactive nerves in the periosteum of the rat Cell Tissue Res 264 469 480 10.1007/BF00319037 1714353
16. EL Hohmann RP Elde JA Rysavy S Einzig RL Gebhard 1986 Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibers Science 232 868 871 10.1126/science.3518059 3518059
17. Y Konttinen S Imai A Suda 1996 Neuropeptides and the puzzle of bone remodeling. State of the art Acta Orthop Scand 67 632 639 10.3109/ 17453679608997772 9065083
18. P Lundberg A Lie A Bjurholm PP Lehenkari MA Horton UH Lerner M Ransjo 2000 Vasoactive intestinal peptide regulates osteoclast activity via specific binding sites on both osteoclasts and osteoblasts Bone 27 803 810 10.1016/S8756-3282(00)00394-X 11113391
19. T Goto T Yamaza MA Kido T Tanaka 1998 Light- and electron-microscopic study of the distribution of axons containing substance P and the localization of neurokinin-1 receptor in bone Cell Tissue Res 293 87 93 10.1007/s004410051100 9634600 (Pubitemid 28331977)
20. F Hara-Irie N Amizuka H Ozawa 1996 Immunohistochemical and ultrastructural localization of CGRP-positive nerve fibers at the epiphyseal trabecules facing the growth plate of rat femurs Bone 18 29 39 10.1016/8756-3282(95)00425-4 8717534 (Pubitemid 26047530)
21. CM Serre D Farlay PD Delmas C Chenu 1999 Evidence for a dense and intimate innervation of the bone tissue, including glutamate-containing fibers Bone 25 623 629 10.1016/S8756-3282(99)00215-X 10593406 (Pubitemid 29525427)
22. M Cherruau P Facchinetti B Baroukh JL Saffar 1999 Chemical sympathectomy impairs bone resorption in rats: a role for the sympathetic system on bone metabolism Bone 25 545 551 10.1016/S8756-3282(99)00211-2 10574574 (Pubitemid 29469460)
23. K Edoff J Hellman J Persliden C Hildebrand 1997 The developmental skeletal growth in the rat foot is reduced after denervation Anat Embryol (Berl) 195 531 538 10.1007/s004290050073 (Pubitemid 27271733)
24. EL Hill R Turner R Elde 1991 Effects of neonatal sympathectomy and capsaicin treatment on bone remodeling in rats Neuroscience 44 747 755 10.1016/0306-4522(91)90094-5 1721689
25. M Hukkanen YT Konttinen S Santavirta L Nordsletten JE Madsen R Almaas AB Oestreicher T Rootwelt JM Polak 1995 Effect of sciatic nerve section on neural ingrowth into the rat tibial fracture callus Clin Orthop 311 247 257 7634582
26. J Li T Ahmad M Spetea M Ahmed A Kreicbergs 2001 Bone reinnervation after fracture: a study in the rat J Bone Miner Res 16 1505 1510 10.1359/jbmr.2001.16. 8.1505 11499873
27. A Ramnemark L Nyberg R Lorentzon U Englund Y Gustafson 1999 Progressive hemiosteoporosis on the paretic side and increased bone mineral density in the nonparetic arm the first year after severe stroke Osteoporos Int 9 269 275 10.1007/s001980050147 10450417 (Pubitemid 29182379)
28. Levi-Montalcini R (1975) NGF: an unchartered route. In: Worden FG, Swazey JP, Adelman G (eds) The neurosciences: paths of discovery. MIT Press, Cambridge, pp 245-265
29. R Levi-Montalcini 1987 The nerve growth factor 35 years later Science 237 1154 1162 10.1126/science.3306916 3306916
30. T Kabata T Kubo T Matsumoto, et al. 2000 Apoptotic cell death in steroid-induced osteonecrosis: an experimental study in rabbits J Rheumatol 27 166 171
31. T Kabata T Kubo T Matsumoto, et al. 2005 Onset of steroid-induced osteonecrosis in rabbits and its relationship to hyperlipaemia and increased free fatty acids Rheumatology 44 1233 1237 10.1093/rheumatology/keh721 15972352 (Pubitemid 41487955)
32. T Ichiseki T Matsumoto M Nishino, et al. 2004 Oxidative stress and vascular permeability in steroid-induced osteonecrosis model J Orthop Sci 9 509 515 10.1007/s00776-004-0816-1 15449127 (Pubitemid 39410181)
33. T Ichiseki A Kaneuji S Katsuda, et al. 2005 DNA oxidation injury in bone early after steroid administration is involved in the pathogenesis of steroid-induced osteonecrosis Rheumatology 44 456 460 10.1093/rheumatology/ keh518 15598705 (Pubitemid 41511133)
34. T Yamamoto T Irisa Y Sugioka, et al. 1997 Effects of pulse methylprednisolone on bone and marrow tissues Arthritis Rheum 40 2055 2064 10.1002/art.1780401119 9365096 (Pubitemid 27494667)
35. K Miyanishi T Yamamoto T Irisa, et al. 2006 Effects of cyclosporin A on the development of osteonecrosis in rabbits Acta Orthop 77 813 819 10.1080/17453670610013042 17068716 (Pubitemid 44521925)
36. T Asada T Kushida M Umeda, et al. 2008 Prevention of corticosteroid- induced osteonecrosis in rabbits by intra-bone marrow injection of autologous bone marrow cells Rheumatology 47 591 596 10.1093/rheumatology/ken037 18326537 (Pubitemid 351619195)
37. G Zhang L Qin H Sheng, et al. 2009 A novel semisynthesized small molecule icaritin reduces incidence of steroid-associated osteonecrosis with inhibition of both thrombosis and lipid-deposition in a dose-dependent manner Bone 44 345 356 10.1016/j.bone.2008.10.035 19015051
38. DM Mendonca L Chimelli AM Martinez 2005 Quantitative evidence for neurofilament heavy subunit aggregation in motor neurons of spinal cords of patients with amyotrophic lateral sclerosis Braz J Med Biol Res 38 925 933 10.1590/S0100-879X2005000600015 15933787
39. T Kubo S Yamazoe N Sugano, et al. 1997 Initial MRI findings of nontraumatic osteonecrosis of the femoral head in renal allograft recipients Magn Reson Imaging 9 1017 1023 10.1016/S0730-725X(97)00159-8 (Pubitemid 27451310)
40. N Sugano K Ohzono K Masuhara, et al. 1994 Prognostication of osteonecrosis of the femoral head in patients with systemic lupus erythematosus by magnetic resonance imaging Clin Orthop 305 190 199 8050228
41. N Sugano K Masuhara N Nakamura, et al. 1996 MRI of early osteonecrosis of the femoral head after transcervical fracture J Bone Joint Surg Br 78 253 257 8666637
42. LF Bonewald 2002 Osteocytes: a proposed multifunctional bone cell J Musculoskelet Neuronal Interact 2 239 241 15758443
43. GA Rodan TJ Martin 2000 Therapeutic approaches to bone diseases Science 289 1508 1514 10.1126/science.289.5484.1508 10968781
44. A Bjurholm 1991 Neuroendocrine peptides in bone Int Orthop 15 4 325 329 10.1007/BF00186871 1725676
45. A Suzuki G Palmer JP Bonjour J Caverzasio 1998 Catecholamines stimulate the proliferation and alkaline phosphatase activity of MC3T3-E1 osteoblast-like cells Bone 23 197 203 10.1016/S8756-3282(98)00099-4 9737341 (Pubitemid 28434663)
46. C Chenu CM Serre C Raynal B Burt-Pichat PD Delmas 1998 Glutamate receptors are expressed by bone cells and are involved in bone resorption Bone 22 295 299 10.1016/S8756-3282(97)00295-0 9556127 (Pubitemid 28177180)
47. A Letic-Gavrilvic A Piattelli K Abe 2003 Nerve growth factorβ (NGFβ) delivery via a collagen/hydroxyapatite (Col/HAp) composite and its effects on new bone ingrowth J Mater Sci 14 95 102
48. M Zaidi AS Alam BE Bax VS Shankar CM Bax JS Gill, et al. 1993 Role of the endothelial cell in osteoclast control: new perspectives Bone 14 2 97 102 10.1016/8756-3282(93)90234-2 8392855 (Pubitemid 23098955)
49. J Cornish KE Callon U Bava SA Kamona GJ Cooper IR Reid 2001 Effects of calcitonin, amylin, and calcitonin gene-related peptide on osteoclast development Bone 29 2 162 168 10.1016/S8756-3282(01)00494-X 11502478 (Pubitemid 32737190)
50. J Cornish KE Callon CQ Lin CL Xiao GD Gamble GJ Cooper, et al. 1999 Comparison of the effects of calcitonin gene-related peptide and amylin on osteoblasts J Bone Miner Res 14 8 1302 1309 10.1359/jbmr.1999.14.8.1302 10457262 (Pubitemid 29368292)
51. T Mori T Ogata H Okumura T Shibata Y Nakamura K Kataoka 1999 Substance P regulates the function of rabbit cultured osteoclast; increase of intracellular free calcium concentration and enhancement of bone resorption Biochem Biophys Res Commun 262 2 418 422 10.1006/bbrc.1999.1220 10462490 (Pubitemid 29429883)
52. BE Sherman RA Chole 1995 A mechanism for sympathectomy-induced bone resorption in the middle ear Otolaryngol Head Neck Surg 113 5 569 581 10.1016/S0194-5998(95)70048-X 7478647
53. A Bjurholm A Kreicbergs L Terenius M Goldstein M Schultzberg 1988 Neuropeptide Y-, tyrosine hydroxylase- and vasoactive intestinal polypeptide-immunoreactive nerves in bone and surrounding tissues J Auton Nerv Syst 25 119 125 10.1016/0165-1838(88)90016-1 2906951 (Pubitemid 19057144)
54. EL Hohmann L Levine AH Tashjian Jr 1983 Vasoactive intestinal peptide stimulates bone resorption via a cyclic adenosine 3′,5′- monophosphate-dependent mechanism Endocrinology 112 1233 1239 10.1210/endo-112-4-1233 6187560
55. C Lundstedt T Linjawi T Amin 1994 Liver VIPoma: report of two cases and literature review Abdom Imag 19 433 437 10.1007/BF00206933
56. PA Baldock A Sainsbury M Couzens RF Enriquez GP Thomas EM Gardiner, et al. 2002 Hypothalamic Y2 receptors regulate bone formation J Clin Invest 109 7 915 921 11927618
57. S Takeda F Elefteriou R Levasseur X Liu L Zhao KL Parker, et al. 2002 Leptin regulates bone formation via the sympathetic nervous system Cell 111 3 305 317 10.1016/S0092-8674(02)01049-8 12419242 (Pubitemid 35345151)
58. BE Sherman RA Chole 1996 In vivo effects of surgical sympathectomy on intramembranous bone resorption Am J Otol 17 2 343 346 8723974
59. A Bjurholm A Kreicbergs M Schultzberg UH Lerner 1992 Neuroendocrine regulation of cyclic AMP formation in osteoblastic cell lines(UMR-106-01, ROS 17/2.8, MC3T3-E1, and Saos-2) and primary bone cells J Bone Miner Res 7 9 1011 1019 10.1002/jbmr.5650070903 1384276
60. A Bjurholm A Kreicbergs M Schultzberg UH Lerner 1988 Parathyroid hormone and noradrenaline-induced enhancement of cyclic AMP in a cloned osteogenic sarcoma cell line (UMR 106) is inhibited by neuropeptide Y Acta Physiol Scand 134 3 451 452 10.1111/j.1748-1716.1988.tb08515.x 2852449
61. SD Brain AD Grant 2004 Vascular actions of calcitonin gene-related Peptide and adrenomedullin Physiol Rev 84 903 934 10.1152/physrev.00037.2003 15269340 (Pubitemid 38823770)
62. SD Brain TJ Williams 1985 Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability Br J Pharmacol 86 855 860 2416378
63. SD Brain 1997 Sensory neuropeptides: their role in inflammation and wound healing Immunopharmacology 37 133 152 10.1016/S0162-3109(97)00055-6 9403332 (Pubitemid 27471030)
64. BE Lindblad LB Nielsen SM Jespersen A Bjurholm C Bunger ES Hansen 1994 Vasoconstrictive action of neuropeptide Y in bone. The porcine tibia perfused in vivo Acta Orthop Scand 65 6 629 634 10.3109/17453679408994619 7839850
65. TS Gross AA Damji S Judex RC Bray RF Zernicke 1999 Bone hyperemia precedes disuse-induced intracortical bone resorption J Appl Physiol 86 1 230 235 10.1063/1.370721 9887135
66. M Laroche 2002 Intraosseous circulation from physiology to disease Joint Bone Spine 69 3 262 269 10.1016/S1297-319X(02)00391-3 12102272 (Pubitemid 34654360)
67. Aaron RK (1998) Osteonecrosis: etiology, pathophysiology and diagnosis. In: Callaghan JJ, Rosenberg AG, Rubash HE (eds) The adult hip. Lippincott-Raven, Philadelphia, pp 451-466
68. B Bax M Blaber G Ferguson MJ Sternberg PH Walls 1993 Prediction of the three-dimensional structures of the nerve growth factor and epidermal growth factor binding proteins (kallikreins) and an hypothetical structure of the high molecular weight complex of epidermal growth factor with its binding protein Protein Sci 2 1229 1241 10.1002/pro.5560020805 8401208
69. M Fahnestock 1991 Structure and biosynthesis of nerve growth factor Curr Top Microbiol Immunol 165 1 26 2032463
70. C Ibanez 1998 Emerging themes in structural biology of neurotrophic factors Trends Neurosci 21 438 444 10.1016/S0166-2236(98)01266-1 9786342 (Pubitemid 28449074)
71. NQ McDonald R Lapatto J Murray-Rust J Gunning A Wlodawer TL Blundell 1991 New protein fold revealed by a 2.3-A resolution crystal structure of nerve growth factor Nature 354 411 414 10.1038/354411a0 1956407
72. RM Lindsay AJ Harmar 1989 Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurones Nature 337 362 364 10.1038/337362a0 2911387 (Pubitemid 19043498)
73. J Donnerer R Schuligoi C Stein 1992 Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo Neuroscience 49 693 698 10.1016/0306-4522(92)90237-V 1380138
74. DD Hunter AC Myers BJ Undem 2000 Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons Am J Respir Crit Care Med 161 1985 1990 10852778
75. A Coutaux F Adam J-C Willer D Le Bars 2005 Hyperalgesia and allodynia: peripheral mechanisms Joint Bone Spine 72 359 371 10.1016/j.jbspin.2004.01.010 16214069 (Pubitemid 41415822)
76. K Freeland YZ Liu DS Latchman 2000 Distinct signalling pathways mediate the cAMP response element (CRE)-dependent activation of the calcitonin gene-related peptide gene promoter by cAMP and nerve growth factor Biochem J 345 233 238 10.1042/0264-6021:3450233 10620499 (Pubitemid 30077162)
77. PL Durham AF Russo 2003 Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons J Neurosci 23 807 815 12574409