Hyperactivation of mTOR critically regulates abnormal osteoclastogenesis in neurofibromatosis type 1

Journal of Orthopaedic Research

Volumn 30, Issue 1, 2012, Pages 144-152

  Ma, Junrong ^a   Li, Mi ^a   Hock, Janet ^b   Yu, Xijie ^a  

^a SICHUAN UNIVERSITY   (China)

^b Maine Institute for Human Genetics & Health   (United States)

Author keywords

mTOR; Nf1; osteoclasts

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; NEUROFIBROMIN; RAPAMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BONE MARROW CELLS; BONE RESORPTION; CELL DIVISION; CELLS, CULTURED; GENOTYPE; MALE; MICE; MICE, MUTANT STRAINS; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; OSTEOCLASTS; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 81555209713     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.21497     Document Type: Article

References (51)

1. Friedman JM,. 1999. Epidemiology of neurofibromatosis type 1. Am J Med Genet 89 (1): 1-6. (Pubitemid 30033170)
2. Vitale MG, Guha A, Skaggs DL,. 2002. Orthopaedic manifestations of neurofibromatosis in children: an update. Clin Orthop Relat Res (401): 107-118. (Pubitemid 34832841)
3. Gilbert A, Brockman R,. 1995. Congenital pseudarthrosis of the tibia. Long-term followup of 29 cases treated by microvascular bone transfer. Clin Orthop Relat Res (314): 37-44.
4. Crawford AH, Schorry EK,. 1999. Neurofibromatosis in children: the role of the orthopaedist. J Am Acad Orthop Surg 7 (4): 217-230.
5. Kuorilehto T, Poyhonen M, Bloigu R, et al. 2005. Decreased bone mineral density and content in neurofibromatosis type 1: lowest local values are located in the load-carrying parts of the body. Osteoporos Int 16 (8): 928-936. (Pubitemid 41127102)
6. Lammert M, Kappler M, Mautner VF, et al. 2005. Decreased bone mineral density in patients with neurofibromatosis 1. Osteoporos Int 16 (9): 1161-1166. (Pubitemid 41225104)
7. Stevenson DA, Moyer-Mileur LJ, Murray M, et al. 2007. Bone mineral density in children and adolescents with neurofibromatosis type 1. J Pediatr 150 (1): 83-88. (Pubitemid 44937722)
8. Yilmaz K, Ozmen M, Bora Goksan S, et al. 2007. Bone mineral density in children with neurofibromatosis 1. Acta Paediatr 96 (8): 1220-1222. (Pubitemid 47106537)
9. Dulai S, Briody J, Schindeler A, et al. 2007. Decreased bone mineral density in neurofibromatosis type 1: results from a pediatric cohort. J Pediatr Orthop 27 (4): 472-475. (Pubitemid 46868318)
10. Kuorilehto T, Nissinen M, Koivunen J, et al. 2004. NF1 tumor suppressor protein and mRNA in skeletal tissues of developing and adult normal mouse and NF1-deficient embryos. J Bone Miner Res 19 (6): 983-989. (Pubitemid 41103455)
11. Stevenson DA, Schwarz EL, Viskochil DH, et al. 2008. Evidence of increased bone resorption in neurofibromatosis Type 1 using urinary pyridinium crosslink analysis. Pediatr Res.
12. Tucker T, Schnabel C, Hartmann M, et al. 2009. Bone health and fracture rate in individuals with neurofibromatosis 1 (NF1). J Med Genet 46 (4): 259-265.
13. Seitz S, Schnabel C, Busse B, et al. 2010. High bone turnover and accumulation of osteoid in patients with neurofibromatosis 1. Osteoporos Int 21 (1): 119-127.
14. Heerva E, Alanne MH, Peltonen S, et al. 2010. Osteoclasts in neurofibromatosis type 1 display enhanced resorption capacity, aberrant morphology, and resistance to serum deprivation. Bone 47 (3): 583-590.
15. Fieber LA, Gonzalez DM, Wallace MR, et al. 2003. Delayed rectifier K currents in NF1 Schwann cells. Pharmacological block inhibits proliferation. Neurobiol Dis 13 (2): 136-146. (Pubitemid 36793978)
16. Barkan B, Starinsky S, Friedman E, et al. 2006. The Ras inhibitor farnesylthiosalicylic acid as a potential therapy for neurofibromatosis type 1. Clin Cancer Res 12 (18): 5533-5542. (Pubitemid 44497271)
17. Kim HA, Ling B, Ratner N,. 1997. Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: reversion of some phenotypes by an inhibitor of farnesyl protein transferase. Mol Cell Biol 17 (2): 862-872. (Pubitemid 27044386)
18. Packer RJ, Gutmann DH, Rubenstein A, et al. 2002. Plexiform neurofibromas in NF1: toward biologic-based therapy. Neurology 58 (10): 1461-1470. (Pubitemid 34552949)
19. Johannessen CM, Reczek EE, James MF, et al. 2005. The NF1 tumor suppressor critically regulates TSC2 and mTOR. Proc Natl Acad Sci USA 102 (24): 8573-8578. (Pubitemid 40862777)
20. Dasgupta B, Yi Y, Chen DY, et al. 2005. Proteomic analysis reveals hyperactivation of the mammalian target of rapamycin pathway in neurofibromatosis 1-associated human and mouse brain tumors. Cancer Res 65 (7): 2755-2760. (Pubitemid 40490077)
21. Kneissel M, Luong-Nguyen NH, Baptist M, et al. 2004. Everolimus suppresses cancellous bone loss, bone resorption, and cathepsin K expression by osteoclasts. Bone 35 (5): 1144-1156. (Pubitemid 39487361)
22. Glantschnig H, Fisher JE, Wesolowski G, et al. 2003. M-CSF, TNFalpha and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ 10 (10): 1165-1177. (Pubitemid 37258582)
23. Sugatani T, Hruska KA,. 2005. Akt1/Akt2 and mammalian target of rapamycin/Bim play critical roles in osteoclast differentiation and survival, respectively, whereas Akt is dispensable for cell survival in isolated osteoclast precursors. J Biol Chem 280 (5): 3583-3589. (Pubitemid 40223824)
24. Brannan CI, Perkins AS, Vogel KS, et al. 1994. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 8 (9): 1019-1029. (Pubitemid 24145666)
25. John V, Hock JM, Short LL, et al. 1996. A role for CD8+ T lymphocytes in osteoclast differentiation in vitro. Endocrinology 137 (6): 2457-2463. (Pubitemid 26155782)
26. Yang FC, Ingram DA, Chen S, et al. 2003. Neurofibromin-deficient Schwann cells secrete a potent migratory stimulus for Nf1+/- mast cells. J Clin Invest 112 (12): 1851-1861. (Pubitemid 38063708)
27. Livak KJ, Schmittgen TD,. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (4): 402-408. (Pubitemid 34164012)
28. Johannessen CM, Johnson BW, Williams SM, et al. 2008. TORC1 is essential for NF1-associated malignancies. Curr Biol 18 (1): 56-62.
29. Boissy P, Saltel F, Bouniol C, et al. 2002. Transcriptional activity of nuclei in multinucleated osteoclasts and its modulation by calcitonin. Endocrinology 143 (5): 1913-1921. (Pubitemid 34415907)
30. Lorget F, Kamel S, Mentaverri R, et al. 2000. High extracellular calcium concentrations directly stimulate osteoclast apoptosis. Biochem Biophys Res Commun 268 (3): 899-903. (Pubitemid 30150888)
31. Parfitt AM, Drezner MK, Glorieux FH, et al. 1987. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2 (6): 595-610.
32. Papapoulos SE,. 1997. Paget's disease of bone: clinical, pathogenetic and therapeutic aspects. Baillieres Clin Endocrinol Metab 11 (1): 117-143. (Pubitemid 27309772)
33. Yang FC, Chen S, Robling AG, et al. 2006. Hyperactivation of p21ras and PI3K cooperate to alter murine and human neurofibromatosis type 1-haploinsufficient osteoclast functions. J Clin Invest 116 (11): 2880-2891. (Pubitemid 44684473)
34. Bjornsti MA, Houghton PJ,. 2004. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 4 (5): 335-348. (Pubitemid 38579480)
35. Fingar DC, Blenis J,. 2004. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23 (18): 3151-3171. (Pubitemid 38638827)
36. Takuwa N, Fukui Y, Takuwa Y,. 1999. Cyclin D1 expression mediated by phosphatidylinositol 3-kinase through mTOR-p70(S6K)-independent signaling in growth factor-stimulated NIH 3T3 fibroblasts. Mol Cell Biol 19 (2): 1346-1358. (Pubitemid 29046876)
37. Wullschleger S, Loewith R, Hall MN,. 2006. TOR signaling in growth and metabolism. Cell 124 (3): 471-484. (Pubitemid 43199434)
38. Pouyssegur J, Dayan F, Mazure NM,. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441 (7092): 437-443. (Pubitemid 44050138)
39. Kim HA, Ratner N, Roberts TM, et al. 2001. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J Neurosci 21 (4): 1110-1116. (Pubitemid 32128756)
40. Fang Y, Elahi A, Denley RC, et al. 2009. Molecular characterization of permanent cell lines from primary, metastatic and recurrent malignant peripheral nerve sheath tumors (MPNST) with underlying neurofibromatosis-1. Anticancer Res 29 (4): 1255-1262.
41. Hirokawa Y, Nheu T, Grimm K, et al. 2006. Sichuan pepper extracts block the PAK1/cyclin D1 pathway and the growth of NF1-deficient cancer xenograft in mice. Cancer Biol Ther 5 (3): 305-309.
42. Singha UK, Jiang Y, Yu S, et al. 2008. Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J Cell Biochem 103 (2): 434-446. (Pubitemid 351171915)
43. Ogawa T, Tokuda M, Tomizawa K, et al. 1998. Osteoblastic differentiation is enhanced by rapamycin in rat osteoblast-like osteosarcoma (ROS 17/2.8) cells. Biochem Biophys Res Commun 249 (1): 226-230. (Pubitemid 28418724)
44. Martin SK, Fitter S, Bong LF, et al. 2010. NVP-BEZ235, a dual pan class I PI3 kinase and mTOR inhibitor, promotes osteogenic differentiation in human mesenchymal stromal cells. J Bone Miner Res 25 (10): 2126-2137.
45. Lee KW, Yook JY, Son MY, et al. Rapamycin promotes the osteoblastic differentiation of human embryonic stem cells by blocking the mTOR pathway and stimulating the BMP/Smad pathway. Stem Cells Dev 19 (4): 557-568.
46. Yu X, Chen S, Potter OL, et al. 2005. Neurofibromin and its inactivation of Ras are prerequisites for osteoblast functioning. Bone 36 (5): 793-802. (Pubitemid 40616014)
47. Abraham RT, Wiederrecht GJ,. 1996. Immunopharmacology of rapamycin. Annu Rev Immunol 14: 483-510. (Pubitemid 26130192)
48. Blagosklonny MV,. 2007. An anti-aging drug today: from senescence-promoting genes to anti-aging pill. Drug Discov Today 12 (5-6): 218-224.
49. Law BK,. 2005. Rapamycin: an anti-cancer immunosuppressant? Crit Rev Oncol Hematol 56 (1): 47-60. (Pubitemid 41278645)
50. Romero DF, Buchinsky FJ, Rucinski B, et al. 1995. Rapamycin: a bone sparing immunosuppressant? J Bone Miner Res 10 (5): 760-768.
51. Ory B, Moriceau G, Redini F, et al. 2007. mTOR inhibitors (rapamycin and its derivatives) and nitrogen containing bisphosphonates: bi-functional compounds for the treatment of bone tumours. Curr Med Chem 14 (13): 1381-1387. (Pubitemid 46902220)