Understanding the local actions of lipids in bone physiology

Progress in Lipid Research

Volumn 59, Issue , 2015, Pages 126-146

  During, Alexandrine ^a   Penel, Guillaume ^a   Hardouin, Pierre ^a,b  

^a Physiopathologie des Maladies Osseuses Inflammatoires   (France)

^b UNIVERSITÉ DU LITTORAL CÔTE D OPALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

26 HYDROXYCHOLESTEROL; CHOLESTEROL; ESTROGEN; FATTY ACID; LYSOPHOSPHOLIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATASE; PHOSPHATASE ORPHAN 1; PHOSPHATIDYLSERINE; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN; PROSTAGLANDIN E2; PROSTAGLANDIN J2; SPHINGOMYELIN; UNCLASSIFIED DRUG; WNT PROTEIN; UNSATURATED FATTY ACID;

APOPTOSIS; BIOACCUMULATION; BONE ANABOLISM; BONE CELL; BONE CHARACTERISTICS AND FUNCTIONS; BONE FUNCTION; BONE HOMEOSTASIS; BONE MARROW; BONE MASS; BONE METABOLISM; BONE MINERALIZATION; BONE REMODELING; CELL SURVIVAL; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; ENZYME ACTIVITY; FATTY ACID ANALYSIS; HOMEOSTASIS; HORMONE ACTION; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; LIPID ANALYSIS; LIPID COMPOSITION; LIPOLYSIS; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; REVIEW; ANIMAL; BONE; BONE DEVELOPMENT; LIPID METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE AND BONES; BONE DEVELOPMENT; BONE REMODELING; FATTY ACIDS, UNSATURATED; HUMANS; LIPID METABOLISM; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84937543851     PISSN: 01637827     EISSN: 18732194     Source Type: Journal    
DOI: 10.1016/j.plipres.2015.06.002     Document Type: Review

References (233)

1. I.R. Reid Fat and bone Arch. Biochem. Biophys. 503 2010 20 27
2. Gijsen H. Sadie-Van, N.J. Crowther, F.S. Hough, and W.F. Ferris The interrelationship between bone and fat: from cellular see-saw to endocrine reciprocity Cell. Mol. Life Sci. 70 2013 2331 2349
3. S. Bermeo, K. Gunaratnam, and G. Duque Fat and bone interactions Curr. Osteoporos. Rep. 12 2014 235 242
4. P. Hardouin, V. Pansini, and B. Cortet Bone marrow fat Joint Bone Spine 81 2014 313 319
5. M.J. Devlin, and C.J. Rosen The bone-fat interface. Basic and clinical implications of marrow adiposity Lancet Diabetes Endocrinol. 3 2015 141 147
6. D.K. Yeung, J.F. Griffith, G.E. Antonio, F.K. Lee, J. Woo, and P.C. Leung Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study J. Magn. Reson. Imaging 22 2005 279 285
7. M.A. Bredella, P.K. Fazeli, K.K. Miller, M. Misra, M. Torriani, B.J. Thomas, and et al. Increased bone marrow fat in anorexia nervosa J. Clin. Endocrinol. Metab. 94 2009 2129 2136
8. K.H. Koo, I.O. Ahn, R. Kim, H.R. Song, S.T. Jeong, J.B. Na, and et al. Bone marrow edema and associated pain in early stage osteonecrosis of the femoral head: prospective study with serial MR images Radiology 213 1999 715 722
9. J. Justesen, K. Stenderup, E.N. Ebbesen, L. Mosekilde, T. Steiniche, and M. Kassem Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis Biogerontology 2 2001 165 171
10. N. Di Iorgi, M. Rosol, S.D. Mittelman, and V. Gilsanz Reciprocal relation between marrow adiposity and the amount of bone in the axial and appendicular skeleton of young adults J. Clin. Endocrinol. Metab. 93 2008 2281 2286
11. N. Di Iorgi, A.O. Mo, K. Grimm, T.A. Wren, F. Dorey, and V. Gilsanz Bone acquisition in healthy young females is reciprocally related to marrow adiposity J. Clin. Endocrinol. Metab. 95 2010 2977 2982
12. T.A. Wren, S.A. Chung, F.J. Dorey, S. Bluml, G.B. Adams, and V. Gilsanz Bone marrow fat is inversely related to cortical bone in young and old subjects J. Clin. Endocrinol. Metab. 96 2011 782 786
13. S. Muruganandan, and C.J. Sinal The impact of bone marrow adipocytes on osteoblast and osteoclast differentiation IUBMB Life 2014
14. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, and et al. Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
15. J.N. Beresford, J.H. Bennett, C. Devlin, P.S. Leboy, and M.E. Owen Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures J. Cell Sci. 102 Pt 2 1992 341 351
16. S. Verma, J.H. Rajaratnam, J. Denton, J.A. Hoyland, and R.J. Byers Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis J. Clin. Pathol. 55 2002 693 698
17. A. Houghton, B.O. Oyajobi, G.A. Foster, R.G. Russell, and B.M. Stringer Immortalization of human marrow stromal cells by retroviral transduction with a temperature sensitive oncogene: identification of bipotential precursor cells capable of directed differentiation to either an osteoblast or adipocyte phenotype Bone 22 1998 7 16
18. M.E. Nuttall, A.J. Patton, D.L. Olivera, D.P. Nadeau, and M. Gowen Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders J. Bone Miner. Res. 13 1998 371 382
19. S.R. Park, R.O. Oreffo, and J.T. Triffitt Interconversion potential of cloned human marrow adipocytes in vitro Bone 24 1999 549 554
20. M. Kassem, B.M. Abdallah, and H. Saeed Osteoblastic cells: differentiation and trans-differentiation Arch.Biochem. Biophys. 473 2008 183 187
21. A. Clabaut, S. Delplace, C. Chauveau, P. Hardouin, and O. Broux Human osteoblasts derived from mesenchymal stem cells express adipogenic markers upon coculture with bone marrow adipocytes Differentiation 80 2010 40 45
22. M.E. Nuttall, and J.M. Gimble Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications Curr. Opin. Pharmacol. 4 2004 290 294
23. T. Negishi-Koga, and H. Takayanagi Bone cell communication factors and Semaphorins Bonekey Rep. 1 2012 183
24. M. Bruderer, R.G. Richards, M. Alini, and M.J. Stoddart Role and regulation of RUNX2 in osteogenesis Eur. Cell Mater. 28 2014 269 286
25. B.F. Boyce, Z. Yao, and L. Xing Functions of nuclear factor kappaB in bone Ann. N. Y. Acad. Sci. 1192 2010 367 375
26. T. Nakashima, M. Hayashi, and H. Takayanagi New insights into osteoclastogenic signaling mechanisms Trends Endocrinol. Metab. 23 2012 582 590
27. Y. Wan PPARgamma in bone homeostasis Trends Endocrinol. Metab. 21 2010 722 728
28. K.M. Sinha, and X. Zhou Genetic and molecular control of osterix in skeletal formation J. Cell. Biochem. 114 2013 975 984
29. B.F. Boyce, and L. Xing The RANKL/RANK/OPG pathway Curr. Osteoporos. Rep. 5 2007 98 104
30. R. Baron, and M. Kneissel WNT signaling in bone homeostasis and disease: from human mutations to treatments Nat. Med. 19 2013 179 192
31. A. Jackson, B. Vayssiere, T. Garcia, W. Newell, R. Baron, S. Roman-Roman, and et al. Gene array analysis of Wnt-regulated genes in C3H10T1/2 cells Bone 36 2005 585 598
32. W. Feng, W. Xia, Q. Ye, and W. Wu Osteoclastogenesis and osteoimmunology Front. Biosci. (Landmark Edu.) 19 2014 758 767
33. T.J. Martin Osteoblast-derived PTHrP is a physiological regulator of bone formation J. Clin. Invest. 115 2005 2322 2324
34. R. Nishimura A novel role for TGF-β1 in bone remodeling IBMS BoneKEy 6 2009 434 438
35. N. Kamiya, and Y. Mishina New insights on the roles of BMP signaling in bone-A review of recent mouse genetic studies Biofactors 37 2011 75 82
36. H. Kakoi, S. Maeda, N. Shinohara, K. Matsuyama, K. Imamura, I. Kawamura, and et al. Bone morphogenic protein (BMP) signaling up-regulates neutral sphingomyelinase 2 to suppress chondrocyte maturation via the Akt protein signaling pathway as a negative feedback mechanism J. Biol. Chem. 289 2014 8135 8150
37. N.L. Fazzalari Bone remodeling: a review of the bone microenvironment perspective for fragility fracture (osteoporosis) of the hip Semin. Cell Dev. Biol. 19 2008 467 472
38. A.M. Parfitt The cellular basis of bone turnover and bone loss: a rebuttal of the osteocytic resorption-bone flow theory Clin. Orthop. Relat. Res. 1977 236 247
39. S.K. Das, M.T. Scott, and P.K. Adhikary Effect of the nature and amount of dietary energy on lipid composition of rat bone marrow Lipids 10 1975 584 590
40. A.A. Dietz, and B. Steinberg Chemical studies of normal and leukemic bone marrow Blood 6 1951 175 182
41. A.A. Dietz Composition of normal bone marrow in rabbits J. Biol. Chem. 165 1946 505 511
42. J.L. Lamoureux, S.D. Fitzgerald, M.K. Church, and D.W. Agnew The effect of environmental storage conditions on bone marrow fat determination in three species J. Vet. Diagn. Invest. 23 2011 312 315
43. C.M. Calhoun, T.D. Schnell, and R.W. Mandigo Porcine bone marrow: extraction procedure and characterization by bone type Meat Sci. 50 1998 489 497
44. P.K. Lund, D.M. Abadi, and J.C. Mathies Lipid composition of normal human bone marrow as determined by column chromatography J. Lipid Res. 3 1962 95 98
45. R. Ostwald, O. Darwish, D. Irwin, and R. Okey Bone marrow composition of cholesterol-fed guinea pigs Proc. Soc. Exp. Biol. Med. 123 1966 220 224
46. T. Sumida Clinical and experimental study on fatty acid composition of bone marrow lipid in hematologic disorders Acta Med. Nagasaki 9 1965 222 241
47. B.Y. Lau, V.A. Fajardo, L. McMeekin, S.M. Sacco, W.E. Ward, B.D. Roy, and et al. Influence of high-fat diet from differential dietary sources on bone mineral density, bone strength, and bone fatty acid composition in rats Appl. Physiol. Nutr. Metab. 35 2010 598 606
48. J.R. Mello, R.A. Field, S. Forenza, and J.E. Kunsman Lipid characterization of bovine bone marrow J. Food Sci. 41 1976 226 230
49. E. Mulder, J. De Gier, and L. Van Deenen Phosphatide patterns of bone marrow Biochim. Biophys. Acta 59 1962 502 504
50. I. Djelouah, G. Lefevre, Y. Ozier, N. Rosencher, and F. Tallet Fat embolism in orthopedic surgery: role of bone marrow fatty acid Anesth. Analg. 85 1997 441 443
51. D.K. Yeung, S.L. Lam, J.F. Griffith, A.B. Chan, Z. Chen, P.H. Tsang, and et al. Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy Chem. Phys. Lipids 151 2008 103 109
52. J.F. Griffith, D.K. Yeung, A.T. Ahuja, C.W. Choy, W.Y. Mei, S.S. Lam, and et al. A study of bone marrow and subcutaneous fatty acid composition in subjects of varying bone mineral density Bone 44 2009 1092 1096
53. M. Wajda Lipid composition of human bone marrow Biochem. J. 95 1965 252 255
54. G.J. Miller, M.R. Frey, J.E. Kunsman, and R.A. Field Bovine bone marrow lipids J. Food Sci. 47 1982 657 660
55. B. Clarke Normal bone anatomy and physiology Clin. J. Am. Soc. Nephrol. 3 2008 S131 S139
56. T.R. Dirksen, and G.V. Marinetti Lipids of bovine enamel and dentin and human bone Calcif. Tissue Res. 6 1970 1 10
57. R.E. Prout, A.A. Odutuga, and F.C. Tring Lipid analysis of rat enamel and dentine Arch. Oral Biol. 18 1973 373 380
58. A.A. Odutuga, and R.E. Prout Lipid analysis of human enamel and dentine Arch. Oral Biol. 19 1974 729 731
59. B. Farre, J.P. Cuif, and Y. Dauphin Occurrence and diversity of lipids in modern coral skeletons Zoology (Jena) 113 2010 250 257
60. I.M. Shapiro The phospholipids of mineralized tissues. I. Mammalian compact bone Calcif. Tissue Res. 5 1970 21 29
61. D.G. Reid, C.M. Shanahan, M.J. Duer, L.G. Arroyo, M. Schoppet, R.A. Brooks, and et al. Lipids in biocalcification: contrasts and similarities between intimal and medial vascular calcification and bone by NMR J. Lipid Res. 53 2012 1569 1575
62. R.L. Cruess, and I. Clark Alterations in the lipids of bone caused by hypervitaminosis A and D Biochem. J. 96 1965 262 265
63. P. Mularchuk, and A. Boskey Lipids in bone: optimal conditions for tissue storage prior to lipid analyses Calcif. Tissue Int. 46 1990 57 59
64. A.A. Leach The lipids of ox compact bone Biochem. J. 69 1958 429 432
65. R.E. Wuthier Lipids of mineralizing epiphyseal tissues in the bovine fetus J. Lipid Res. 9 1968 68-8.
66. I.M. Shapiro The neutral lipids of bovine bone Arch. Oral Biol. 16 1971 411 421
67. A.L. Boskey, and D.M. Timchak Phospholipid changes in the bones of the vitamin D-deficient, phosphate-deficient, immature rat Metab. Bone Dis. Relat. Res. 5 1983 81 85
68. J.M. Humphries, J.S. Kuliwaba, R.J. Gibson, and N.L. Fazzalari In situ fatty acid profile of femoral cancellous subchondral bone in osteoarthritic and fragility fracture females: implications for bone remodelling Bone 51 2012 218 223
69. M.S. Plumb, and R.M. Aspden High levels of fat and (n-6) fatty acids in cancellous bone in osteoarthritis Lipids Health Dis. 3 2004 12
70. B. Dolegowska, Z. Machoy, and D. Chlubek Profiles of fatty acids in different bone structures of growing chicks Vet. Res. Commun. 30 2006 735 747
71. I. Wolinsky, and K. Guggenheim Lipid metabolism of chick epiphyseal bone and cartilage Calcif. Tissue Res. 6 1970 113 119
72. M. Kagawa, K. Matsubara, K. Kimura, H. Shiono, and Y. Fukui Species identification by the positional analysis of fatty acid composition in triacylglyceride of adipose and bone tissues Forensic Sci. Int. 79 1996 215 226
73. C.E. Elson, and S.J. Voichick Dietary induced alterations in the fatty acids of rat bone marrow Lipids 5 1970 698 701
74. B.A. Watkins, Y. Li, K.G. Allen, W.E. Hoffmann, and M.F. Seifert Dietary ratio of (n-6)/(n-3) polyunsaturated fatty acids alters the fatty acid composition of bone compartments and biomarkers of bone formation in rats J. Nutr. 130 2000 2274 2284
75. Y. Li, R.S. Greiner, N. Salem Jr., and B.A. Watkins Impact of dietary n-3 FA deficiency on rat bone tissue FA composition Lipids 38 2003 683 686
76. S.Q. Alam, P.P. Kokkinos, and B.S. Alam Fatty acid composition and arachidonic acid concentrations in alveolar bone of rats fed diets with different lipids Calcif. Tissue Int. 53 1993 330 332
77. R.C. Poulsen, P.J. Moughan, and M.C. Kruger Long-chain polyunsaturated fatty acids and the regulation of bone metabolism Exp. Biol. Med. (Maywood) 232 2007 1275 1288
78. P. Salari, A. Rezaie, B. Larijani, and M. Abdollahi A systematic review of the impact of n-3 fatty acids in bone health and osteoporosis Med. Sci. Monit. 14 2008 RA37-44
79. S.W. Ing, and M.A. Belury Impact of conjugated linoleic acid on bone physiology: proposed mechanism involving inhibition of adipogenesis Nutr. Rev. 69 2011 123 131
80. R.L. Corwin, T.J. Hartman, S.A. Maczuga, and B.I. Graubard Dietary saturated fat intake is inversely associated with bone density in humans: analysis of NHANES III J. Nutr. 136 2006 159 165
81. S. Reinwald, Y. Li, T. Moriguchi, N. Salem Jr., and B.A. Watkins Repletion with (n-3) fatty acids reverses bone structural deficits in (n-3)-deficient rats J. Nutr. 134 2004 388 394
82. B.Y. Lau, W.E. Ward, J.X. Kang, and D.W. Ma Femur EPA and DHA are correlated with femur biomechanical strength in young fat-1 mice J. Nutr. Biochem. 20 2009 453 461
83. B.Y. Lau, W.E. Ward, J.X. Kang, and D.W. Ma Fat-1 gene modulates the fatty acid composition of femoral and vertebral phospholipids Appl. Physiol. Nutr. Metab. 35 2010 447 455
84. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
85. M. Murakami Lipid mediators in life science Exp. Anim. 60 2011 7 20
86. A.C. Maurin, P.M. Chavassieux, E. Vericel, and P.J. Meunier Role of polyunsaturated fatty acids in the inhibitory effect of human adipocytes on osteoblastic proliferation Bone 31 2002 260 266
87. A. Elbaz, X. Wu, D. Rivas, J.M. Gimble, and G. Duque Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro J. Cell. Mol. Med. 14 2009 982 991
88. D. Wang, A. Haile, and L.C. Jones Dexamethasone-induced lipolysis increases the adverse effect of adipocytes on osteoblasts using cells derived from human mesenchymal stem cells Bone 53 2013 520 530
89. S. Lucas, A. Clabaut, O. Ghali, N. Haren, P. Hardouin, and O. Broux Implication of fatty acids in the inhibitory effect of human adipocytes on osteoblastic differentiation Bone 55 2013 429 430
90. J.E. Kim, M.W. Ahn, S.H. Baek, I.K. Lee, Y.W. Kim, J.Y. Kim, and et al. AMPK activator, AICAR, inhibits palmitate-induced apoptosis in osteoblast Bone 43 2008 394 404
91. K. Gunaratnam, C. Vidal, R. Boadle, C. Thekkedam, and G. Duque Mechanisms of palmitate-induced cell death in human osteoblasts Biol. Open 2 2013 1382 1389
92. B.A. Watkins, Y. Li, H.E. Lippman, and S. Feng Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism Prostaglandins Leukot. Essent. Fatty Acids 68 2003 387 398
93. M. Coetzee, M. Haag, A.M. Joubert, and M.C. Kruger Effects of arachidonic acid, docosahexaenoic acid and prostaglandin E(2) on cell proliferation and morphology of MG-63 and MC3T3-E1 osteoblast-like cells Prostaglandins Leukot. Essent. Fatty Acids 76 2007 35 45
94. D.D. Diascro Jr., R.L. Vogel, T.E. Johnson, K.M. Witherup, S.M. Pitzenberger, S.J. Rutledge, and et al. High fatty acid content in rabbit serum is responsible for the differentiation of osteoblasts into adipocyte-like cells J. Bone Miner. Res. 13 1998 96 106
95. S. Cusack, C. Jewell, and K.D. Cashman The effect of conjugated linoleic acid on the viability and metabolism of human osteoblast-like cells Prostaglandins Leukot. Essent. Fatty Acids 72 2005 29 39
96. I. Platt, L.G. Rao, and A. El-Sohemy Isomer-specific effects of conjugated linoleic acid on mineralized bone nodule formation from human osteoblast-like cells Exp. Biol. Med. (Maywood) 232 2007 246 252
97. J. Cornish, A. MacGibbon, J.M. Lin, M. Watson, K.E. Callon, P.C. Tong, and et al. Modulation of osteoclastogenesis by fatty acids Endocrinology 149 2008 5688 5695
98. S.R. Oh, O.J. Sul, Y.Y. Kim, H.J. Kim, R. Yu, J.H. Suh, and et al. Saturated fatty acids enhance osteoclast survival J. Lipid Res. 51 2010 892 899
99. M.M. Rahman, A. Bhattacharya, and G. Fernandes Conjugated linoleic acid inhibits osteoclast differentiation of RAW264.7 cells by modulating RANKL signaling J. Lipid Res. 47 2006 1739 1748
100. J. Steinhauer, and J.E. Treisman Lipid-modified morphogens: functions of fats Curr. Opin. Genet. Dev. 19 2009 308 314
101. X. Franch-Marro, F. Wendler, J. Griffith, M.M. Maurice, and J.P. Vincent In vivo role of lipid adducts on Wingless J. Cell Sci. 121 2008 1587 1592
102. O. Laneuville, D.K. Breuer, N. Xu, Z.H. Huang, D.A. Gage, J.T. Watson, and et al. Fatty acid substrate specificities of human prostaglandin-endoperoxide H synthase-1 and -2. Formation of 12-hydroxy-(9Z, 13E/Z, 15Z)-octadecatrienoic acids from alpha-linolenic acid J. Biol. Chem. 270 1995 19330 19336
103. R.W. Norrdin, W.S. Jee, and W.B. High The role of prostaglandins in bone in vivo Prostaglandins Leukot. Essent. Fatty Acids 41 1990 139 149
104. H. Kawaguchi, C.C. Pilbeam, J.R. Harrison, and L.G. Raisz The role of prostaglandins in the regulation of bone metabolism Clin. Orthop. Relat. Res. 313 1995 36 46
105. K.A. Blackwell, L.G. Raisz, and C.C. Pilbeam Prostaglandins in bone: bad cop, good cop? Trends Endocrinol. Metab. 21 2010 294 301
106. C.C. Pilbeam, L.G. Raisz, O. Voznesensky, C.B. Alander, B.N. Delman, and H. Kawaguchi Autoregulation of inducible prostaglandin G/H synthase in osteoblastic cells by prostaglandins J. Bone Miner. Res. 10 1995 406 414
107. S. Dekel, G. Lenthall, and M.J. Francis Release of prostaglandins from bone and muscle after tibial fracture. An experimental study in rabbits J. Bone Joint Surg. Br. 63 1981 185 189
108. J. Keller Effects of indomethacin and local prostaglandin E2 on fracture healing in rabbits Dan. Med. Bull. 43 1996 317 329
109. B.A. Watkins, Y. Li, and M.F. Seifert Lipids as modulators of bone remodelling Curr. Opin. Clin. Nutr. Metab. Care 4 2001 105 110
110. L.F. Bonewald, and M.L. Johnson Osteocytes, mechanosensing and Wnt signaling Bone 42 2008 606 615
111. X.H. Liu, A. Kirschenbaum, S. Yao, and A.C. Levine Interactive effect of interleukin-6 and prostaglandin E2 on osteoclastogenesis via the OPG/RANKL/RANK system Ann. N. Y. Acad. Sci. 1068 2006 225 233
112. K. Yoshida, H. Oida, T. Kobayashi, T. Maruyama, M. Tanaka, T. Katayama, and et al. Stimulation of bone formation and prevention of bone loss by prostaglandin E EP4 receptor activation Proc. Natl. Acad. Sci. USA 99 2002 4580 4585
113. T.L. McCarthy, M. Centrella, L.G. Raisz, and E. Canalis Prostaglandin E2 stimulates insulin-like growth factor I synthesis in osteoblast-enriched cultures from fetal rat bone Endocrinology 128 1991 2895 2900
114. M. Li, D.D. Thompson, and V.M. Paralkar Prostaglandin E(2) receptors in bone formation Int. Orthop. 31 2007 767 772
115. M. Zhang, H.C. Ho, T.J. Sheu, M.D. Breyer, L.M. Flick, J.H. Jonason, and et al. EP1(-/-) mice have enhanced osteoblast differentiation and accelerated fracture repair J. Bone Miner. Res. 26 2011 792 802
116. S. Graham, Z. Gamie, I. Polyzois, A.A. Narvani, K. Tzafetta, E. Tsiridis, and et al. Prostaglandin EP2 and EP4 receptor agonists in bone formation and bone healing: in vivo and in vitro evidence Expert Opin. Investig. Drugs 18 2009 746 766
117. A. Elbrecht, Y. Chen, C.A. Cullinan, N. Hayes, M. Leibowitz, D.E. Moller, and et al. Molecular cloning, expression and characterization of human peroxisome proliferator activated receptors gamma 1 and gamma 2 Biochem. Biophys. Res. Commun. 224 1996 431 437
118. K.R. Shockley, O.P. Lazarenko, P.J. Czernik, C.J. Rosen, G.A. Churchill, and B. Lecka-Czernik PPARgamma2 nuclear receptor controls multiple regulatory pathways of osteoblast differentiation from marrow mesenchymal stem cells J. Cell. Biochem. 106 2009 232 246
119. S.A. Kliewer, S.S. Sundseth, S.A. Jones, P.J. Brown, G.B. Wisely, C.S. Koble, and et al. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma Proc. Natl. Acad. Sci. USA 94 1997 4318 4323
120. M.A. Gallant, R. Samadfam, J.A. Hackett, J. Antoniou, J.L. Parent, and A.J. de Brum-Fernandes Production of prostaglandin D(2) by human osteoblasts and modulation of osteoprotegerin, RANKL, and cellular migration by DP and CRTH2 receptors J. Bone Miner. Res. 20 2005 672 681
121. C. Haberl, L. Hultner, A. Flugel, M. Falk, S. Geuenich, W. Wilmanns, and et al. Release of prostaglandin D2 by murine mast cells: importance of metabolite formation for antiproliferative activity Mediators Inflamm. 7 1998 79 84
122. T. Shibata, M. Kondo, T. Osawa, N. Shibata, M. Kobayashi, and K. Uchida 15-deoxy-delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes J. Biol. Chem. 277 2002 10459 10466
123. M. Kawai, K.M. Sousa, O.A. MacDougald, and C.J. Rosen The many facets of PPARgamma: novel insights for the skeleton Am. J. Physiol. Endocrinol. Metab. 299 2010 E3 E9
124. Gijsen H. Sadie-Van, F.S. Hough, and W.F. Ferris Determinants of bone marrow adiposity: the modulation of peroxisome proliferator-activated receptor-gamma2 activity as a central mechanism Bone 56 2013 255 265
125. Y. Wan, L.W. Chong, and R.M. Evans PPAR-gamma regulates osteoclastogenesis in mice Nat. Med. 13 2007 1496 1503
126. J.J. Patel, O.R. Butters, and T.R. Arnett PPAR agonists stimulate adipogenesis at the expense of osteoblast differentiation while inhibiting osteoclast formation and activity Cell Biochem. Funct. 32 2014 368 377
127. T. Sanbe, T. Tomofuji, D. Ekuni, T. Azuma, N. Tamaki, and T. Yamamoto Oral administration of vitamin C prevents alveolar bone resorption induced by high dietary cholesterol in rats J. Periodontol. 78 2007 2165 2170
128. L. You, Z.Y. Sheng, C.L. Tang, L. Chen, L. Pan, and J.Y. Chen High cholesterol diet increases osteoporosis risk via inhibiting bone formation in rats Acta Pharmacol. Sin. 32 2011 1498 1504
129. E.R. Nelson, C.D. DuSell, X. Wang, M.K. Howe, G. Evans, R.D. Michalek, and et al. The oxysterol, 27-hydroxycholesterol, links cholesterol metabolism to bone homeostasis through its actions on the estrogen and liver X receptors Endocrinology 152 2011 4691 4705
130. D.J. McNamara Dietary cholesterol and the optimal diet for reducing risk of atherosclerosis Can. J. Cardiol. 11 Suppl G 1995 123G 126G
131. L.H. Cui, M.H. Shin, E.K. Chung, Y.H. Lee, S.S. Kweon, K.S. Park, and et al. Association between bone mineral densities and serum lipid profiles of pre- and post-menopausal rural women in South Korea Osteoporos. Int. 16 2005 1975 1981
132. L.B. Tanko, Y.Z. Bagger, S.B. Nielsen, and C. Christiansen Does serum cholesterol contribute to vertebral bone loss in postmenopausal women? Bone 32 2003 8 14
133. T. Majima, A. Shimatsu, Y. Komatsu, N. Satoh, A. Fukao, K. Ninomiya, and et al. Increased bone turnover in patients with hypercholesterolemia Endocr. J. 55 2008 143 151
134. J. Makovey, J.S. Chen, C. Hayward, F.M. Williams, and P.N. Sambrook Association between serum cholesterol and bone mineral density Bone 44 2009 208 213
135. E.J. Samelson, L.A. Cupples, M.T. Hannan, P.W. Wilson, S.A. Williams, V. Vaccarino, and et al. Long-term effects of serum cholesterol on bone mineral density in women and men: the Framingham Osteoporosis Study Bone 34 2004 557 561
136. D.H. Solomon, J. Avorn, C.F. Canning, and P.S. Wang Lipid levels and bone mineral density Am. J. Med. 118 2005 1414
137. E. Luegmayr, H. Glantschnig, G.A. Wesolowski, M.A. Gentile, J.E. Fisher, G.A. Rodan, and et al. Osteoclast formation, survival and morphology are highly dependent on exogenous cholesterol/lipoproteins Cell Death Differ. 11 Suppl 1 2004 S108 S118
138. J.D. Bergstrom, R.G. Bostedor, P.J. Masarachia, A.A. Reszka, and G. Rodan Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase Arch. Biochem. Biophys. 373 2000 231 241
139. T. Maeda, A. Matsunuma, T. Kawane, and N. Horiuchi Simvastatin promotes osteoblast differentiation and mineralization in MC3T3-E1 cells Biochem. Biophys. Res. Commun. 280 2001 874 877
140. G. Mundy, R. Garrett, S. Harris, J. Chan, D. Chen, G. Rossini, and et al. Stimulation of bone formation in vitro and in rodents by statins Science 286 1999 1946 1949
141. S. Chuengsamarn, S. Rattanamongkoulgul, S. Suwanwalaikorn, S. Wattanasirichaigoon, and L. Kaufman Effects of statins vs. non-statin lipid-lowering therapy on bone formation and bone mineral density biomarkers in patients with hyperlipidemia Bone 46 2010 1011 1015
142. H. Kaji, J. Naito, Y. Inoue, H. Sowa, T. Sugimoto, and K. Chihara Statin suppresses apoptosis in osteoblastic cells: role of transforming growth factor-beta-Smad3 pathway Horm. Metab. Res. 40 2008 746 751
143. W.A. Grasser, A.P. Baumann, S.F. Petras, H.J. Harwood Jr., R. Devalaraja, R. Renkiewicz, and et al. Regulation of osteoclast differentiation by statins J. Musculoskelet. Neuronal Interact. 3 2003 53 62
144. F. Ruan, Q. Zheng, and J. Wang Mechanisms of bone anabolism regulated by statins Biosci. Rep. 32 2012 511 519
145. F.P. Coxon, K. Thompson, A.J. Roelofs, F.H. Ebetino, and M.J. Rogers Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells Bone 42 2008 848 860
146. J.E. Dunford, K. Thompson, F.P. Coxon, S.P. Luckman, F.M. Hahn, C.D. Poulter, and et al. Structure-activity relationships for inhibition of farnesyl diphosphate synthase in vitro and inhibition of bone resorption in vivo by nitrogen-containing bisphosphonates J. Pharmacol. Exp. Therap. 296 2001 235 242
147. M.J. Rogers, J.C. Crockett, F.P. Coxon, and J. Monkkonen Biochemical and molecular mechanisms of action of bisphosphonates Bone 49 2010 34 41
148. R. Karuna, A.G. Holleboom, M.M. Motazacker, J.A. Kuivenhoven, R. Frikke-Schmidt, A. Tybjaerg-Hansen, and et al. Plasma levels of 27-hydroxycholesterol in humans and mice with monogenic disturbances of high density lipoprotein metabolism Atherosclerosis 214 2011 448 455
149. S. Zhou, M.S. LeBoff, and J. Glowacki Vitamin D metabolism and action in human bone marrow stromal cells Endocrinology 151 2010 14 22
150. L.M. Helvering, R. Liu, N.H. Kulkarni, T. Wei, P. Chen, S. Huang, and et al. Expression profiling of rat femur revealed suppression of bone formation genes by treatment with alendronate and estrogen but not raloxifene Mol. Pharmacol. 68 2005 1225 1238
151. D.W. Russell Oxysterol biosynthetic enzymes Biochim. Biophys. Acta 1529 2000 126 135
152. M. Umetani, and P.W. Shaul 27-Hydroxycholesterol: the first identified endogenous SERM Trends Endocrinol. Metab. 22 2011 130 135
153. B.J. Deroo, and K.S. Korach Estrogen receptors and human disease J. Clin. Invest. 116 2006 561 570
154. C.D. DuSell, E.R. Nelson, X. Wang, J. Abdo, U.I. Modder, M. Umetani, and et al. The endogenous selective estrogen receptor modulator 27-hydroxycholesterol is a negative regulator of bone homeostasis Endocrinology 151 2010 3675 3685
155. B.C. Jeong, Y.S. Lee, Y.Y. Park, I.H. Bae, D.K. Kim, S.H. Koo, and et al. The orphan nuclear receptor estrogen receptor-related receptor gamma negatively regulates BMP2-induced osteoblast differentiation and bone formation J. Biol. Chem. 284 2009 14211 14218
156. E.R. Nelson, S.E. Wardell, and D.P. McDonnell The molecular mechanisms underlying the pharmacological actions of estrogens, SERMs and oxysterols: implications for the treatment and prevention of osteoporosis Bone 53 2013 42 50
157. H.C. Anderson, R. Garimella, and S.E. Tague The role of matrix vesicles in growth plate development and biomineralization Front. Biosci. 10 2005 822 837
158. E.E. Golub Biomineralization and matrix vesicles in biology and pathology Semin. Immunopathol. 33 2011 409 417
159. N.S. Peress, H.C. Anderson, and S.W. Sajdera The lipids of matrix vesicles from bovine fetal epiphyseal cartilage Calcif. Tissue Res. 14 1974 275 281
160. R.E. Wuthier Lipid composition of isolated epiphyseal cartilage cells, membranes and matrix vesicles Biochim. Biophys. Acta 409 1975 128 143
161. C. Thouverey, A. Strzelecka-Kiliszek, M. Balcerzak, R. Buchet, and S. Pikula Matrix vesicles originate from apical membrane microvilli of mineralizing osteoblast-like Saos-2 cells J. Cell. Biochem. 106 2009 127 138
162. T. Kirsch, H.D. Nah, D.R. Demuth, G. Harrison, E.E. Golub, S.L. Adams, and et al. Annexin V-mediated calcium flux across membranes is dependent on the lipid composition: implications for cartilage mineralization Biochemistry 36 1997 3359 3367
163. R.E. Wuthier, and S.T. Gore Partition of inorganic ions and phospholipids in isolated cell, membrane and matrix vesicle fractions: evidence for Ca-Pi-acidic phospholipid complexes Calcif. Tissue Res. 24 1977 163 171
164. L.N. Wu, B.R. Genge, D.G. Dunkelberger, R.Z. LeGeros, B. Concannon, and R.E. Wuthier Physicochemical characterization of the nucleational core of matrix vesicles J. Biol. Chem. 272 1997 4404 4411
165. B.R. Genge, L.N. Wu, and R.E. Wuthier Mineralization of annexin-5-containing lipid-calcium-phosphate complexes: modulation by varying lipid composition and incubation with cartilage collagens J. Biol. Chem. 283 2008 9737 9748
166. J.L. Meyer Can biological calcification occur in the presence of pyrophosphate? Arch. Biochem. Biophys. 231 1984 1 8
167. H. Orimo The mechanism of mineralization and the role of alkaline phosphatase in health and disease J. Nihon Med. Sch. 77 2010 4 12
168. B. Houston, A.J. Stewart, and C. Farquharson PHOSPHO1-A novel phosphatase specifically expressed at sites of mineralisation in bone and cartilage Bone 34 2004 629 637
169. A.J. Stewart, S.J. Roberts, E. Seawright, M.G. Davey, R.H. Fleming, and C. Farquharson The presence of PHOSPHO1 in matrix vesicles and its developmental expression prior to skeletal mineralization Bone 39 2006 1000 1007
170. S. Roberts, S. Narisawa, D. Harmey, J.L. Millan, and C. Farquharson Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization J. Bone Miner. Res. 22 2007 617 627
171. S.J. Roberts, A.J. Stewart, P.J. Sadler, and C. Farquharson Human PHOSPHO1 exhibits high specific phosphoethanolamine and phosphocholine phosphatase activities Biochem. J. 382 2004 59 65
172. C. Huesa, M.C. Yadav, M.A. Finnila, S.R. Goodyear, S.P. Robins, K.E. Tanner, and et al. PHOSPHO1 is essential for mechanically competent mineralization and the avoidance of spontaneous fractures Bone 48 2011 1066 1074
173. M.C. Yadav, A.M. Simao, S. Narisawa, C. Huesa, M.D. McKee, C. Farquharson, and et al. Loss of skeletal mineralization by the simultaneous ablation of PHOSPHO1 and alkaline phosphatase function: a unified model of the mechanisms of initiation of skeletal calcification J. Bone Miner. Res. 26 2011 286 297
174. Z. Li, G. Wu, R.B. Sher, Z. Khavandgar, M. Hermansson, G.A. Cox, and et al. Choline kinase beta is required for normal endochondral bone formation Biochim. Biophys. Acta 1840 2014 2112 2122
175. L.N. Wu, B.R. Genge, M.W. Kang, A.L. Arsenault, and R.E. Wuthier Changes in phospholipid extractability and composition accompany mineralization of chicken growth plate cartilage matrix vesicles J. Biol. Chem. 277 2002 5126 5133
176. I. Aubin, C.P. Adams, S. Opsahl, D. Septier, C.E. Bishop, N. Auge, and et al. A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse Nat. Genet. 37 2005 803 805
177. M. Goldberg, S. Opsahl, I. Aubin, D. Septier, C. Chaussain-Miller, A. Boskey, and et al. Sphingomyelin degradation is a key factor in dentin and bone mineralization: lessons from the fro/fro mouse. The chemistry and histochemistry of dentin lipids J. Dent. Res. 87 2008 9 13
178. Z. Khavandgar, C. Poirier, C.J. Clarke, J. Li, N. Wang, M.D. McKee, and et al. A cell-autonomous requirement for neutral sphingomyelinase 2 in bone mineralization J. Cell Biol. 194 2011 277 289
179. Z. Khavandgar, S. Alebrahim, H. Eimar, F. Tamimi, M.D. McKee, and M. Murshed Local regulation of tooth mineralization by sphingomyelin phosphodiesterase 3 J. Dent. Res. 92 2013 358 364
180. M.V. Airola, and Y.A. Hannun Sphingolipid metabolism and neutral sphingomyelinases Handb. Exp. Pharmacol. 215 2013 57 76
181. Z. Khavandgar, and M. Murshed Sphingolipid metabolism and its role in the skeletal tissues Cell. Mol. Life Sci. 72 2015 959 969
182. M. Ishii, and J. Kikuta Sphingosine-1-phosphate signaling controlling osteoclasts and bone homeostasis Biochim. Biophys. Acta 1831 2013 223 227
183. P.A. Hill, and A. Tumber Ceramide-induced cell death/survival in murine osteoblasts J. Endocrinol. 206 2010 225 233
184. H. Takeda, K. Ozaki, H. Yasuda, M. Ishida, S. Kitano, and S. Hanazawa Sphingomyelinase and ceramide inhibit formation of F-actin ring in and bone resorption by rabbit mature osteoclasts FEBS Lett. 422 1998 255 258
185. J. Ryu, H.J. Kim, E.J. Chang, H. Huang, Y. Banno, and H.H. Kim Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling EMBO J. 25 2006 5840 5851
186. L. Pederson, M. Ruan, J.J. Westendorf, S. Khosla, and M.J. Oursler Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate Proc. Natl. Acad. Sci. USA 105 2008 20764 20769
187. J. Keller, P. Catala-Lehnen, A.K. Huebner, A. Jeschke, T. Heckt, A. Lueth, and et al. Calcitonin controls bone formation by inhibiting the release of sphingosine 1-phosphate from osteoclasts Nat. Commun. 5 2014 5215
188. A. Grey, X. Xu, B. Hill, M. Watson, K. Callon, I.R. Reid, and et al. Osteoblastic cells express phospholipid receptors and phosphatases and proliferate in response to sphingosine-1-phosphate Calcif. Tissue Int. 74 2004 542 550
189. M. Ishii, J.G. Egen, F. Klauschen, M. Meier-Schellersheim, Y. Saeki, J. Vacher, and et al. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis Nature 458 2009 524 528
190. S.H. Lee, S.Y. Lee, Y.S. Lee, B.J. Kim, K.H. Lim, E.H. Cho, and et al. Higher circulating sphingosine 1-phosphate levels are associated with lower bone mineral density and higher bone resorption marker in humans J. Clin. Endocrinol. Metab. 97 2012 E1421 E1428
191. B.J. Kim, J.M. Koh, S.Y. Lee, Y.S. Lee, S.H. Lee, K.H. Lim, and et al. Plasma sphingosine 1-phosphate levels and the risk of vertebral fracture in postmenopausal women J. Clin. Endocrinol. Metab. 97 2012 3807 3814
192. S.H. Ahn, J.M. Koh, E.J. Gong, S. Byun, S.Y. Lee, B.J. Kim, and et al. Association of bone marrow sphingosine 1-phosphate levels with osteoporotic hip fractures J. Bone Metab. 20 2013 61 65
193. P. Quint, M. Ruan, L. Pederson, M. Kassem, J.J. Westendorf, S. Khosla, and et al. Sphingosine 1-phosphate (S1P) receptors 1 and 2 coordinately induce mesenchymal cell migration through S1P activation of complementary kinase pathways J. Biol. Chem. 288 2013 5398 5406
194. Y. Takuwa Subtype-specific differential regulation of Rho family G proteins and cell migration by the Edg family sphingosine-1-phosphate receptors Biochim. Biophys. Acta 1582 2002 112 120
195. M. Ishii, J. Kikuta, Y. Shimazu, M. Meier-Schellersheim, and R.N. Germain Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo J. Exp. Med. 207 2010 2793 2798
196. N. Panupinthu, J.T. Rogers, L. Zhao, L.P. Solano-Flores, F. Possmayer, S.M. Sims, and et al. P2X7 receptors on osteoblasts couple to production of lysophosphatidic acid: a signaling axis promoting osteogenesis J. Cell Biol. 181 2008 859 871
197. J. Blackburn, and J.P. Mansell The emerging role of lysophosphatidic acid (LPA) in skeletal biology Bone 50 2012 756 762
198. S.M. Sims, N. Panupinthu, D.M. Lapierre, A. Pereverzev, and S.J. Dixon Lysophosphatidic acid: a potential mediator of osteoblast-osteoclast signaling in bone Biochim. Biophys. Acta 1831 2013 109 116
199. L.M. Masiello, J.S. Fotos, D.S. Galileo, and N.J. Karin Lysophosphatidic acid induces chemotaxis in MC3T3-E1 osteoblastic cells Bone 39 2006 72 82
200. D.M. Lapierre, N. Tanabe, A. Pereverzev, M. Spencer, R.P. Shugg, S.J. Dixon, and et al. Lysophosphatidic acid signals through multiple receptors in osteoclasts to elevate cytosolic calcium concentration, evoke retraction, and promote cell survival J. Biol. Chem. 285 2010 25792 25801
201. R. Dziak, B.M. Yang, B.W. Leung, S. Li, N. Marzec, J. Margarone, and et al. Effects of sphingosine-1-phosphate and lysophosphatidic acid on human osteoblastic cells Prostaglandins Leukot. Essent. Fatty Acids 68 2003 239 249
202. Y.B. Liu, Y. Kharode, P.V. Bodine, P.J. Yaworsky, J.A. Robinson, and J. Billiard LPA induces osteoblast differentiation through interplay of two receptors: LPA1 and LPA4 J. Cell. Biochem. 109 2010 794 800
203. I. Gennero, S. Laurencin-Dalicieux, F. Conte-Auriol, F. Briand-Mesange, D. Laurencin, J. Rue, and et al. Absence of the lysophosphatidic acid receptor LPA1 results in abnormal bone development and decreased bone mass Bone 49 2011 395 403
204. M. David, I. Machuca-Gayet, J. Kikuta, P. Ottewell, F. Mima, R. Leblanc, and et al. Lysophosphatidic acid receptor type 1 (LPA1) plays a functional role in osteoclast differentiation and bone resorption activity J. Biol. Chem. 289 2014 6551 6564
205. J.P. Salles, S. Laurencin-Dalicieux, F. Conte-Auriol, F. Briand-Mesange, and I. Gennero Bone defects in LPA receptor genetically modified mice Biochim. Biophys. Acta 1831 2013 93 98
206. E.K. Farrell, and D.J. Merkler Biosynthesis, degradation and pharmacological importance of the fatty acid amides Drug Discov. Today 13 2008 558 568
207. J. Tam, V. Trembovler, V. Di Marzo, S. Petrosino, G. Leo, A. Alexandrovich, and et al. The cannabinoid CB1 receptor regulates bone formation by modulating adrenergic signaling FASEB J. 22 2008 285 294
208. F. Rossi, D. Siniscalco, L. Luongo, L. De Petrocellis, G. Bellini, S. Petrosino, and et al. The endovanilloid/endocannabinoid system in human osteoclasts: possible involvement in bone formation and resorption Bone 44 2009 476 484
209. I. Bab, O. Ofek, J. Tam, J. Rehnelt, and A. Zimmer Endocannabinoids and the regulation of bone metabolism J. Neuroendocrinol. 20 Suppl 1 2008 69 74
210. S. Jiang, M. Alberich-Jorda, R. Zagozdzon, K. Parmar, Y. Fu, P. Mauch, and et al. Cannabinoid receptor 2 and its agonists mediate hematopoiesis and hematopoietic stem and progenitor cell mobilization Blood 117 2011 827 838
211. L.S. Whyte, L. Ford, S.A. Ridge, G.A. Cameron, M.J. Rogers, and R.A. Ross Cannabinoids and bone: endocannabinoids modulate human osteoclast function in vitro Br. J. Pharmacol. 165 2012 2584 2597
212. K.A. Willoughby, S.F. Moore, B.R. Martin, and E.F. Ellis The biodisposition and metabolism of anandamide in mice J. Pharmacol. Exp. Therap. 282 1997 243 247
213. I. Bab, and A. Zimmer Cannabinoid receptors and the regulation of bone mass Br. J. Pharmacol. 153 2008 182 188
214. A.I. Idris, and S.H. Ralston Role of cannabinoids in the regulation of bone remodeling Front. Endocrinol. (Lausanne) 3 2012 136
215. A.I. Idris, R.J. Van't Hof, I.R. Greig, S.A. Ridge, D. Baker, R.A. Ross, and et al. Regulation of bone mass, bone loss and osteoclast activity by cannabinoid receptors Nat. Med. 11 2005 774 779
216. A.I. Idris, A. Sophocleous, E. Landao-Bassonga, M. Canals, G. Milligan, D. Baker, and et al. Cannabinoid receptor type 1 protects against age-related osteoporosis by regulating osteoblast and adipocyte differentiation in marrow stromal cells Cell Metab. 10 2009 139 147
217. A. Gowran, K. McKayed, and V.A. Campbell The cannabinoid receptor type 1 is essential for mesenchymal stem cell survival and differentiation: implications for bone health Stem Cells Int. 2013 2013 796715
218. J. Tam, O. Ofek, E. Fride, C. Ledent, Y. Gabet, R. Muller, and et al. Involvement of neuronal cannabinoid receptor CB1 in regulation of bone mass and bone remodeling Mol. Pharmacol. 70 2006 786 792
219. S. Takeda, F. Elefteriou, R. Levasseur, X. Liu, L. Zhao, K.L. Parker, and et al. Leptin regulates bone formation via the sympathetic nervous system Cell 111 2002 305 317
220. O. Ofek, M. Karsak, N. Leclerc, M. Fogel, B. Frenkel, K. Wright, and et al. Peripheral cannabinoid receptor, CB2, regulates bone mass Proc. Natl. Acad. Sci. USA 103 2006 696 701
221. A. Sophocleous, E. Landao-Bassonga, R.J. Van't Hof, A.I. Idris, and S.H. Ralston The type 2 cannabinoid receptor regulates bone mass and ovariectomy-induced bone loss by affecting osteoblast differentiation and bone formation Endocrinology 152 2011 2141 2149
222. A.I. Idris, A. Sophocleous, E. Landao-Bassonga, R.J. Van't Hof, and S.H. Ralston Regulation of bone mass, osteoclast function, and ovariectomy-induced bone loss by the type 2 cannabinoid receptor Endocrinology 149 2008 5619 5626
223. D.C. Geng, Y.Z. Xu, H.L. Yang, G.M. Zhu, X.B. Wang, and X.S. Zhu Cannabinoid receptor-2 selective antagonist negatively regulates receptor activator of nuclear factor kappa B ligand mediated osteoclastogenesis Chin. Med. J. (Engl.) 124 2011 586 590
224. S.A. Ridge, L. Ford, G.A. Cameron, R.A. Ross, and M.J. Rogers Endocannabinoids are produced by bone cells and stimulate bone resorption in vitro Bone 40 2007 S120
225. M. Karsak, M. Cohen-Solal, J. Freudenberg, A. Ostertag, C. Morieux, U. Kornak, and et al. Cannabinoid receptor type 2 gene is associated with human osteoporosis Hum. Mol. Genet. 14 2005 3389 3396
226. Y. Yamada, F. Ando, and H. Shimokata Association of candidate gene polymorphisms with bone mineral density in community-dwelling Japanese women and men Int. J. Mol. Med. 19 2007 791 801
227. J.H. Woo, H. Kim, J.H. Kim, and J.G. Kim Cannabinoid receptor gene polymorphisms and bone mineral density in Korean postmenopausal women Menopause 22 2015 512 519
228. L.S. Whyte, E. Ryberg, N.A. Sims, S.A. Ridge, K. Mackie, P.J. Greasley, and et al. The putative cannabinoid receptor GPR55 affects osteoclast function in vitro and bone mass in vivo Proc. Natl. Acad. Sci. USA 106 2009 16511 16516
229. O. Ofek, M. Attar-Namdar, V. Kram, M. Dvir-Ginzberg, R. Mechoulam, A. Zimmer, and et al. CB2 cannabinoid receptor targets mitogenic Gi protein-cyclin D1 axis in osteoblasts J. Bone Miner. Res. 26 2011 308 316
230. R. Smoum, A. Bar, B. Tan, G. Milman, M. Attar-Namdar, O. Ofek, and et al. Oleoyl serine, an endogenous N-acyl amide, modulates bone remodeling and mass Proc. Natl. Acad. Sci. USA 107 2010 17710 17715
231. A.P. Davenport, S.P. Alexander, J.L. Sharman, A.J. Pawson, H.E. Benson, A.E. Monaghan, and et al. International union of basic and clinical pharmacology. LXXXVIII. G protein-coupled receptor list: recommendations for new pairings with cognate ligands Pharmacol. Rev. 65 2013 967 986
232. D.S. Im Intercellular lipid mediators and GPCR drug discovery Biomol. Therap. (Seoul) 21 2013 411 422
233. J. Chun, T. Hla, K.R. Lynch, S. Spiegel, and W.H. Moolenaar International union of basic and clinical pharmacology. LXXVIII. Lysophospholipid receptor nomenclature Pharmacol. Rev. 62 2010 579 587