The role of Apolipoprotein E in bone metabolism

Bone

Volumn 50, Issue 2, 2012, Pages 518-524

  Niemeier, Andreas ^a   Schinke, Thorsten ^a   Heeren, Joerg ^a   Amling, Michael ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Adipocyte; Apolipoprotein E; Lipoprotein receptor; Osteoblast; Vitamin K

Indexed keywords

APOLIPOPROTEIN E; ISOPROTEIN; PHYTOMENADIONE; VITAMIN K GROUP;

ALZHEIMER DISEASE; APOLIPOPROTEIN E GENE; ARTICLE; ATHEROSCLEROSIS; BONE DENSITY; BONE METABOLISM; COMORBIDITY; DISEASE ASSOCIATION; ETHNICITY; GENE FUNCTION; GENETIC ASSOCIATION; HIP FRACTURE; HUMAN; HYPERLIPOPROTEINEMIA TYPE 2; MUTATOR GENE; NONHUMAN; OSTEOLYSIS; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; VERTEBRA FRACTURE; VITAMIN INTAKE;

ANIMALS; APOLIPOPROTEINS E; BONE AND BONES; BONE DENSITY; FRACTURES, BONE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; PROTEIN ISOFORMS;

EID: 84855902689     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.07.015     Document Type: Article

References (71)

1. Li Y., Seifert M.F., Ney D.M., Grahn M., Grant A.L., Allen K.G., et al. Dietary conjugated linoleic acids alter serum IGF-I and IGF binding protein concentrations and reduce bone formation in rats fed (n-6) or (n-3) fatty acids. J Bone Miner Res 1999, 14:1153-1162.
2. Reinwald S., Li Y., Moriguchi T., Salem N., Watkins B.A. Repletion with (n-3) fatty acids reverses bone structural deficits in (n-3)-deficient rats. J Nutr 2004, 134:388-394.
3. Maurin A.C., Chavassieux P.M., Meunier P.J. Expression of PPARgamma and beta/delta in human primary osteoblastic cells: influence of polyunsaturated fatty acids. Calcif Tissue Int 2005, 76:385-392.
4. Vermelin L., Baroukh B., Llorens A., Saffar J.L. Effects of essential fatty acid deficiency on periodontal tissue adaptation to spontaneous tooth migration. Calcif Tissue Int 2005, 77:30-36.
5. Coetzee M., Haag M., Kruger M.C. Effects of arachidonic acid and docosahexaenoic acid on differentiation and mineralization of MC3T3-E1 osteoblast-like cells. Cell Biochem Funct 2009, 27:3-11.
6. Kruger M.C., Coetzee M., Haag M., Weiler H. Long-chain polyunsaturated fatty acids: selected mechanisms of action on bone. Prog Lipid Res 2010, 49:438-449.
7. Braam L.A., Knapen M.H., Geusens P., Brouns F., Hamulyak K., Gerichhausen M.J., et al. Vitamin K1 supplementation retards bone loss in postmenopausal women between 50 and 60years of age. Calcif Tissue Int 2003, 73:21-26.
8. Knapen M.H., Schurgers L.J., Vermeer C. Vitamin K2 supplementation improves hip bone geometry and bone strength indices in postmenopausal women. Osteoporos Int 2007, 18:963-972.
9. Bolton-Smith C., McMurdo M.E., Paterson C.R., Mole P.A., Harvey J.M., Fenton S.T., et al. Two-year randomized controlled trial of vitamin K1 (phylloquinone) and vitamin D3 plus calcium on the bone health of older women. J Bone Miner Res 2007, 22:509-519.
10. Macdonald H.M., McGuigan F.E., Lanham-New S.A., Fraser W.D., Ralston S.H., Reid D.M. Vitamin K1 intake is associated with higher bone mineral density and reduced bone resorption in early postmenopausal Scottish women: no evidence of gene-nutrient interaction with apolipoprotein E polymorphisms. Am J Clin Nutr 2008, 87:1513-1520.
11. Binkley N., Harke J., Krueger D., Engelke J., Vallarta-Ast N., Gemar D., et al. Vitamin K treatment reduces undercarboxylated osteocalcin but does not alter bone turnover, density, or geometry in healthy postmenopausal North American women. J Bone Miner Res 2009, 24:983-991.
12. Gundberg C.M. Vitamin K and bone: past, present, and future. J Bone Miner Res 2009, 24:980-982.
13. Yamaguchi M., Weitzmann M.N. Vitamin K2 stimulates osteoblastogenesis and suppresses osteoclastogenesis by suppressing NF-kappaB activation. Int J Mol Med 2011, 27:3-14.
14. Heeren J., Beisiegel U., Grewal T. Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis. Arterioscler Thromb Vasc Biol 2006, 26:442-448.
15. Williams K.J. Molecular processes that handle - and mishandle - dietary lipids. J Clin Invest 2008, 118:3247-3259.
16. Zhang S.H., Reddick R.L., Piedrahita J.A., Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992, 258:468-471.
17. Plump A.S., Smith J.D., Hayek T., Aalto-Setala K., Walsh A., Verstuyft J.G., et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992, 71:343-353.
18. Kolovou G., Anagnostopoulou K., Mikhailidis D.P., Cokkinos D.V. Apolipoprotein E knockout models. Curr Pharm Des 2008, 14:338-351.
19. Mahley R.W. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240:622-630.
20. Schneider W.J., Kovanen P.T., Brown M.S., Goldstein J.L., Utermann G., Weber W., et al. Familial dysbetalipoproteinemia. Abnormal binding of mutant apoprotein E to low density lipoprotein receptors of human fibroblasts and membranes from liver and adrenal of rats, rabbits, and cows. J Clin Invest 1981, 68:1075-1085.
21. Mahley R.W., Huang Y. Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr Opin Lipidol 1999, 10:207-217.
22. Huang Y. Mechanisms linking apolipoprotein E isoforms with cardiovascular and neurological diseases. Curr Opin Lipidol 2010, 21:337-345.
23. Shiraki M., Shiraki Y., Aoki C., Hosoi T., Inoue S., Kaneki M., et al. Association of bone mineral density with apolipoprotein E phenotype. J Bone Miner Res 1997, 12:1438-1445.
24. Sanada M., Nakagawa H., Kodama I., Sakasita T., Ohama K. Apolipoprotein E phenotype associations with plasma lipoproteins and bone mass in postmenopausal women. Climacteric 1998, 1:188-195.
25. Kohlmeier M., Saupe J., Schaefer K., Asmus G. Bone fracture history and prospective bone fracture risk of hemodialysis patients are related to apolipoprotein E genotype. Calcif Tissue Int 1998, 62:278-281.
26. Johnston J.M., Cauley J.A., Ganguli M. APOE 4 and hip fracture risk in a community-based study of older adults. J Am Geriatr Soc 1999, 47:1342-1345.
27. Cauley J.A., Zmuda J.M., Yaffe K., Kuller L.H., Ferrell R.E., Wisniewski S.R., et al. Apolipoprotein E polymorphism: a new genetic marker of hip fracture risk-the study of osteoporotic fractures. J Bone Miner Res 1999, 14:1175-1181.
28. Salamone L.M., Cauley J.A., Zmuda J., Pasagian-Macaulay A., Epstein R.S., Ferrell R.E., et al. Apolipoprotein E gene polymorphism and bone loss: estrogen status modifies the influence of apolipoprotein E on bone loss. J Bone Miner Res 2000, 15:308-314.
29. Zajickova K., Zofkova I., Hill M., Horinek A., Novakova A. Apolipoprotein E 4 allele is associated with low bone density in postmenopausal women. J Endocrinol Invest 2003, 26:312-315.
30. Booth S.L., Tucker K.L., Chen H., Hannan M.T., Gagnon D.R., Cupples L.A., et al. Dietary vitamin K intakes are associated with hip fracture but not with bone mineral density in elderly men and women. Am J Clin Nutr 2000, 71:1201-1208.
31. Heikkinen A.M., Kroger H., Niskanen L., Komulainen M.H., Ryynanen M., Parviainen M.T., et al. Does apolipoprotein E genotype relate to BMD and bone markers in postmenopausal women?. Maturitas 2000, 34:33-41.
32. von Muhlen D.G., Barrett-Connor E., Schneider D.L., Morin P.A., Parry P. Osteoporosis and apolipoprotein E genotype in older adults: the Rancho Bernardo study. Osteoporos Int 2001, 12:332-335.
33. Stulc T., Ceska R., Horinek A., Stepan J. Bone mineral density in patients with apolipoprotein E type 2/2 and 4/4 genotype. Physiol Res 2000, 49:435-439.
34. Gerdes L.U., Vestergaard P., Hermann A.P., Mosekilde L. Regional and hormone-dependent effects of apolipoprotein E genotype on changes in bone mineral in perimenopausal women. J Bone Miner Res 2001, 16:1906-1916.
35. Pluijm S.M., Dik M.G., Jonker C., Deeg D.J., van Kamp G.J., Lips P. Effects of gender and age on the association of apolipoprotein E epsilon4 with bone mineral density, bone turnover and the risk of fractures in older people. Osteoporos Int 2002, 13:701-709.
36. Dick I.M., Devine A., Marangou A., Dhaliwal S.S., Laws S., Martins R.N., et al. Apolipoprotein E4 is associated with reduced calcaneal quantitative ultrasound measurements and bone mineral density in elderly women. Bone 2002, 31:497-502.
37. Lui L.Y., Stone K., Cauley J.A., Hillier T., Yaffe K. Bone loss predicts subsequent cognitive decline in older women: the study of osteoporotic fractures. J Am Geriatr Soc 2003, 51:38-43.
38. Sennels H.P., Sand J.C., Madsen B., Lauritzen J.B., Fenger M., Jorgensen H.L. Association between polymorphisms of apolipoprotein E, bone mineral density of the lower forearm, quantitative ultrasound of the calcaneus and osteoporotic fractures in postmenopausal women with hip or lower forearm fracture. Scand J Clin Lab Invest 2003, 63:247-258.
39. Efstathiadou Z., Koukoulis G., Stakias N., Challa A., Tsatsoulis A. Apolipoprotein E polymorphism is not associated with spinal bone mineral density in peri- and postmenopausal Greek women. Maturitas 2004, 48:259-264.
40. Schoofs M.W., van der Klift M., Hofman A., van Duijn C.M., Stricker B.H., Pols H.A., et al. ApoE gene polymorphisms, BMD, and fracture risk in elderly men and women: the Rotterdam study. J Bone Miner Res 2004, 19:1490-1496.
41. Wong S.Y., Lau E.M., Li M., Chung T., Sham A., Woo J. The prevalence of Apo E4 genotype and its relationship to bone mineral density in Hong Kong Chinese. J Bone Miner Metab 2005, 23:261-265.
42. Lee S.I., Lee S.Y., Yoo W.H. Association of apolipoprotein E polymorphism with bone mineral density in postmenopausal women with rheumatoid arthritis. Rheumatology (Oxford) 2005, 44:1067-1068.
43. Bagger Y.Z., Rasmussen H.B., Alexandersen P., Werge T., Christiansen C., Tanko L.B. Links between cardiovascular disease and osteoporosis in postmenopausal women: serum lipids or atherosclerosis per se?. Osteoporos Int 2007, 18:505-512.
44. Tolonen S., Mikkila V., Laaksonen M., Sievanen H., Mononen N., Hernesniemi J., et al. Association of apolipoprotein E promoter polymorphisms with bone structural traits is modified by dietary saturated fat intake - the cardiovascular risk in Young Finns study. Bone 2011 May 1, 48(5):1058-1065.
45. Peter I., Crosier M.D., Yoshida M., Booth S.L., Cupples L.A., Dawson-Hughes B., et al. Associations of APOE gene polymorphisms with bone mineral density and fracture risk: a meta-analysis. Osteoporos Int 2011 Apr, 22(4):1199-1209.
46. Kannel W.B., Feinleib M., McNamara P.M., Garrison R.J., Castelli W.P. An investigation of coronary heart disease in families. The Framingham offspring study. Am J Epidemiol 1979, 110:281-290.
47. Booth S.L., Dallal G., Shea M.K., Gundberg C., Peterson J.W., Dawson-Hughes B. Effect of vitamin K supplementation on bone loss in elderly men and women. J Clin Endocrinol Metab 2008, 93:1217-1223.
48. Bullido M.J., Artiga M.J., Recuero M., Sastre I., Garcia M.A., Aldudo J., et al. A polymorphism in the regulatory region of APOE associated with risk for Alzheimer's dementia. Nat Genet 1998, 18:69-71.
49. Long J.R., Liu P.Y., Liu Y.J., Lu Y., Shen H., Zhao L.J., et al. APOE haplotypes influence bone mineral density in Caucasian males but not females. Calcif Tissue Int 2004, 75:299-304.
50. Singh M., Singh P., Singh S., Juneja P.K., Kaur T. A susceptible haplotype within APOE gene influences BMD and intensifies the osteoporosis risk in postmenopausal women of Northwest India. Maturitas 2010, 67:239-244.
51. Tong T.Y., Yong R.Y., Goh V.H., Liang S., Chong A.P., Mok H.P., et al. Association between an intronic apolipoprotein E polymorphism and bone mineral density in Singaporean Chinese females. Bone 2010, 47:503-510.
52. Bachner D., Schroder D., Betat N., Ahrens M., Gross G. Apolipoprotein E (ApoE), a Bmp-2 (bone morphogenetic protein) upregulated gene in mesenchymal progenitors (C3H10T1/2), is highly expressed in murine embryonic development. Biofactors 1999, 9:11-17.
53. Schilling A.F., Schinke T., Munch C., Gebauer M., Niemeier A., Priemel M., et al. Increased bone formation in mice lacking apolipoprotein E. J Bone Miner Res 2005, 20:274-282.
54. Niemeier A., Kassem M., Toedter K., Wendt D., Ruether W., Beisiegel U., et al. Expression of LRP1 by human osteoblasts: a mechanism for the delivery of lipoproteins and vitamin K1 to bone. J Bone Miner Res 2005, 20:283-293.
55. Niemeier A., Niedzielska D., Secer R., Schilling A., Merkel M., Enrich C., et al. Uptake of postprandial lipoproteins into bone in vivo: impact on osteoblast function. Bone 2008, 43:230-237.
56. Lamon-Fava S., Sadowski J.A., Davidson K.W., O'Brien M.E., McNamara J.R., Schaefer E.J. Plasma lipoproteins as carriers of phylloquinone (vitamin K1) in humans. Am J Clin Nutr 1998, 67:1226-1231.
57. Price P.A. Vitamin K-dependent formation of bone Gla protein (osteocalcin) and its function. Vitam Horm 1985, 42:65-108.
58. Price P.A., Nishimoto S.K. Radioimmunoassay for the vitamin K-dependent protein of bone and its discovery in plasma. Proc Natl Acad Sci U S A 1980, 77:2234-2238.
59. Bugel S. Vitamin K and bone health in adult humans. Vitam Horm 2008, 78:393-416.
60. Ducy P., Desbois C., Boyce B., Pinero G., Story B., Dunstan C., et al. Increased bone formation in osteocalcin-deficient mice. Nature 1996, 382:448-452.
61. Caruso A., Motolese M., Iacovelli L., Caraci F., Copani A., Nicoletti F., et al. Inhibition of the canonical Wnt signaling pathway by apolipoprotein E4 in PC12 cells. J Neurochem 2006, 98:364-371.
62. Magoori K., Kang M.J., Ito M.R., Kakuuchi H., Ioka R.X., Kamataki A., et al. Severe hypercholesterolemia, impaired fat tolerance, and advanced atherosclerosis in mice lacking both low density lipoprotein receptor-related protein 5 and apolipoprotein E. J Biol Chem 2003, 278:11331-11336.
63. De Ferrari G.V., Papassotiropoulos A., Biechele T., Wavrant De-Vrieze F., Avila M.E., Major M.B., et al. Common genetic variation within the low-density lipoprotein receptor-related protein 6 and late-onset Alzheimer's disease. Proc Natl Acad Sci U S A 2007, 104:9434-9439.
64. Ross S.E., Hemati N., Longo K.A., Bennett C.N., Lucas P.C., Erickson R.L., et al. Inhibition of adipogenesis by Wnt signaling. Science 2000, 289:950-953.
65. Bennett C.N., Ross S.E., Longo K.A., Bajnok L., Hemati N., Johnson K.W., et al. Regulation of Wnt signaling during adipogenesis. J Biol Chem 2002, 277:30998-31004.
66. Bartelt A., Beil F.T., Schinke T., Roeser K., Ruether W., Heeren J., et al. Apolipoprotein E-dependent inverse regulation of vertebral bone and adipose tissue mass in C57Bl/6 mice: modulation by diet-induced obesity. Bone 2010, 47:736-745.
67. Lee N.K., Sowa H., Hinoi E., Ferron M., Ahn J.D., Confavreux C., et al. Endocrine regulation of energy metabolism by the skeleton. Cell 2007, 130:456-469.
68. Ferron M., Hinoi E., Karsenty G., Ducy P. Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci U S A 2008, 105:5266-5270.
69. Hirasawa H., Tanaka S., Sakai A., Tsutsui M., Shimokawa H., Miyata H., et al. ApoE gene deficiency enhances the reduction of bone formation induced by a high-fat diet through the stimulation of p53-mediated apoptosis in osteoblastic cells. J Bone Miner Res 2007, 22:1020-1030.
70. Getz G.S., Reardon C.A. Diet and murine atherosclerosis. Arterioscler Thromb Vasc Biol 2006, 26:242-249.
71. Nikolov I.G., Joki N., Nguyen-Khoa T., Ivanovski O., Phan O., Lacour B., et al. Chronic kidney disease bone and mineral disorder (CKD-MBD) in apolipoprotein E-deficient mice with chronic renal failure. Bone 2010, 47:156-163.