APOE ε4 is associated with higher vitamin D levels in targeted replacement mice and humans

FASEB Journal

Volumn 25, Issue 9, 2011, Pages 3262-3270

  Huebbe, Patricia ^a   Nebel, Almut ^a   Siegert, Sabine ^a   Moehring, Jennifer ^a   Boesch Saadatmandi, Christine ^a   Most, Erika ^b   Pallauf, Josef ^b   Egert, Sarah ^a   Müller, Manfred James ^a   Schreiber, Stefan ^c   Nöthlings, Ute ^a,c   Rimbach, Gerald ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

4 allele; Apolipoprotein E; Evolutionary advantage; Global allele distribution

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BILE ACID; CHOLESTEROL 7ALPHA MONOOXYGENASE; MESSENGER RNA; RNA; VITAMIN D;

ADULT; AGED; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOLIPOPROTEIN E EPSILON4 ALLELE; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BILE ACID BLOOD LEVEL; BLOOD SAMPLING; CALCIUM ABSORPTION; CALCIUM HOMEOSTASIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CLINICAL TRIAL; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; FEMALE; GENE SEQUENCE; GENETIC CODE; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE ABSORPTION; LIVER; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; PRIORITY JOURNAL; RS429358; RS7412; SINGLE BLIND PROCEDURE; SINGLE NUCLEOTIDE POLYMORPHISM; VITAMIN D METABOLISM;

ADULT; AGED; ALLELES; ANIMALS; APOLIPOPROTEIN E4; CALCIUM; FEMALE; GENOTYPE; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; VITAMIN D;

MUS;

EID: 80052658961     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-180935     Document Type: Article

References (46)

1. Mahley, R. W., Weisgraber, K. H., and Huang, Y. (2009) Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS. J. Lipid Res. 50(Suppl.), S183-S188
2. Hanlon, C. S., and Rubinsztein, D. C. (1995) Arginine residues at codons 112 and 158 in the apolipoprotein E gene correspond to the ancestral state in humans. Atherosclerosis 112, 85-90
3. Davignon, J., Bouthillier, D., Nestruck, A. C., and Sing, C. F. (1988) Apolipoprotein E polymorphism and atherosclerosis: insight from a study in octogenarians. Trans. Am. Clin. Climatol. Assoc. 99, 100-110
4. Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., and Pericak-Vance, M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923 (Pubitemid 23275809)
5. Schachter, F., Faure-Delanef, L., Guenot, F., Rouger, H., Froguel, P., Lesueur-Ginot, L., and Cohen, D. (1994) Genetic associations with human longevity at the APOE and ACE loci. Nat. Genet. 6, 29-32 (Pubitemid 24191909)
6. Nebel, A., Croucher, P. J., Stiegeler, R., Nikolaus, S., Krawczak, M., and Schreiber, S. (2005) No association between microsomal triglyceride transfer protein (MTP) haplotype and longevity in humans. Proc. Natl. Acad. Sci. U. S. A. 102, 7906-7909 (Pubitemid 40781036)
7. Payami, H., Zhu, M., Montimurro, J., Keefe, R., McCulloch, C. C., and Moses, L. (2005) One step closer to fixing association studies: evidence for age- and gender-specific allele frequency variations and deviations from Hardy-Weinberg expectations in controls. Hum. Genet. 118, 322-330 (Pubitemid 43091203)
8. Dietrich, M., Hu, Y., Block, G., Olano, E., Packer, L., Morrow, J. D., Hudes, M., Abdukeyum, G., Rimbach, G., and Minihane, A. M. (2005) Associations between apolipoprotein E genotype and circulating F2-isoprostane levels in humans. Lipids 40, 329-334 (Pubitemid 40770942)
9. Jofre-Monseny, L., Loboda, A., Wagner, A. E., Huebbe, P., Boesch-Saadatmandi, C., Jozkowicz, A., Minihane, A. M., Dulak, J., and Rimbach, G. (2007) Effects of apoE genotype on macrophage inflammation and heme oxygenase-1 expression. Biochem. Biophys. Res. Commun. 357, 319-324 (Pubitemid 46574533)
10. Vitek, M. P., Brown, C. M., and Colton, C. A. (2009) APOE genotype-specific differences in the innate immune response. Neurobiol. Aging 30, 1350-1360
11. Fullerton, S. M., Clark, A. G., Weiss, K. M., Nickerson, D. A., Taylor, S. L., Stengard, J. H., Salomaa, V., Vartiainen, E., Perola, M., Boerwinkle, E., and Sing, C. F. (2000) Apolipoprotein E variation at the sequence haplotype level: implications for the origin and maintenance of a major human polymorphism. Am. J. Hum. Genet. 67, 881-900
12. Singh, P. P., Singh, M., and Mastana, S. S. (2006) APOE distribution in world populations with new data from India and the UK. Ann. Hum. Biol. 33, 279-308 (Pubitemid 44232589)
13. Gerdes, L. U. (2003) The common polymorphism of apolipoprotein E: geographical aspects and new pathophysiological relations. Clin. Chem. Lab. Med. 41, 628-631
14. Lucotte, G., Loirat, F., and Hazout, S. (1997) Pattern of gradient of apolipoprotein E allele*4 frequencies in western Europe. Hum. Biol. 69, 253-262 (Pubitemid 27133960)
15. Finch, C. E. (2010) Evolution in Health and Medicine Sackler Colloquium: evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc. Natl. Acad. Sci. U. S. A. 107(Suppl. 1), 1718-1724
16. Finch, C. E., and Stanford, C. B. (2004) Meat-adaptive genes and the evolution of slower aging in humans. Q. Rev. Biol. 79, 3-50 (Pubitemid 38394029)
17. Yuen, A. W., and Jablonski, N. G. (2010) Vitamin D: in the evolution of human skin colour. Med. Hypotheses 74, 39-44
18. Sullivan, P. M., Mezdour, H., Quarfordt, S. H., and Maeda, N. (1998) Type III hyperlipoproteinemia and spontaneous atherosclerosis in mice resulting from gene replacement of mouse Apoe with human Apoe*2. J. Clin. Invest. 102, 130-135 (Pubitemid 28323839)
19. Sullivan, P. M., Mezdour, H., Aratani, Y., Knouff, C., Najib, J., Reddick, R. L., Quarfordt, S. H., and Maeda, N. (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J. Biol. Chem. 272, 17972-17980 (Pubitemid 27306374)
20. Knouff, C., Hinsdale, M. E., Mezdour, H., Altenburg, M. K., Watanabe, M., Quarfordt, S. H., Sullivan, P. M., and Maeda, N. (1999) Apo E structure determines VLDL clearance and atherosclerosis risk in mice. J. Clin. Invest. 103, 1579-1586
21. Walter, A., Rimbach, G., Most, E., and Pallauf, J. (2000) Effect of calcium supplements to a maize-soya diet on the bioavailability of minerals and trace elements and the accumulation of heavy metals in growing rats. J. Vet. Med. A Physiol. Pathol. Clin. Med. 47, 367-377
22. Huang, W., Ma, K., Zhang, J., Qatanani, M., Cuvillier, J., Liu, J., Dong, B., Huang, X., and Moore, D. D. (2006) Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 312, 233-236
23. Gaedicke, S., Zhang, X., Schmelzer, C., Lou, Y., Doering, F., Frank, J., and Rimbach, G. (2008) Vitamin E dependent microRNA regulation in rat liver. FEBS Lett. 582, 3542-3546
24. Egert, S., Bosy-Westphal, A., Seiberl, J., Kurbitz, C., Settler, U., Plachta-Danielzik, S., Wagner, A. E., Frank, J., Schrezenmeir, J., Rimbach, G., Wolffram, S., and Muller, M. J. (2009) Quercetin reduces systolic blood pressure and plasma oxidised low-density lipoprotein concentrations in overweight subjects with a high-cardiovascular disease risk phenotype: a double-blinded, placebo-controlled cross-over study. Br. J. Nutr. 102, 1065-1074
25. Krawczak, M., Nikolaus, S., Von Eberstein, H., Croucher, P. J., El Mokhtari, N. E., and Schreiber, S. (2006) PopGen: population-based recruitment of patients and controls for the analysis of complex genotype-phenotype relationships. Community Genet. 9, 55-61 (Pubitemid 43289519)
26. Zerwekh, J. E. (2008) Blood biomarkers of vitamin D status. Am. J. Clin. Nutr. 87, 1087S-1091S
27. Will, C., Fromm, M., and Muller, D. (2008) Claudin tight junction proteins: novel aspects in paracellular transport. Perit. Dial. Int. 28, 577-584
28. Fujita, H., Chiba, H., Yokozaki, H., Sakai, N., Sugimoto, K., Wada, T., Kojima, T., Yamashita, T., and Sawada, N. (2006) Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J. Histochem. Cytochem. 54, 933-944 (Pubitemid 44106871)
29. Zittermann, A. (2006) Vitamin D and disease prevention with special reference to cardiovascular disease. Prog. Biophys. Mol. Biol. 92, 39-48
30. Zittermann, A., Schleithoff, S. S., and Koerfer, R. (2005) Putting cardiovascular disease and vitamin D insufficiency into perspective. Br. J. Nutr. 94, 483-492 (Pubitemid 41555486)
31. Hofmann, A. F. (1999) Bile acids: the good, the bad, and the ugly. News Physiol. Sci. 14, 24-29
32. Nykjaer, A., Dragun, D., Walther, D., Vorum, H., Jacobsen, C., Herz, J., Melsen, F., Christensen, E. I., and Willnow, T. E. (1999) An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96, 507-515 (Pubitemid 29106838)
33. Daiger, S. P., Schanfield, M. S., and Cavalli-Sforza, L. L. (1975) Group-specific component (Gc) proteins bind vitamin D and 25-hydroxyvitamin D. Proc. Natl. Acad. Sci. U. S. A. 72, 2076-2080
34. Gerdes, L. U., Vestergaard, P., Hermann, A. P., and Mosekilde, L. (2001) Regional and hormone-dependent effects of apolipoprotein E genotype on changes in bone mineral in perimenopausal women. J. Bone Miner. Res. 16, 1906-1916 (Pubitemid 32911499)
35. Holick, M. F. (2011) Vitamin D: evolutionary, physiological and health perspectives. Curr. Drug Targets 12, 4-18
36. Corbo, R. M., and Scacchi, R. (1999) Apolipoprotein E (APOE) allele distribution in the world. Is APOE*4 a 'thrifty' allele? Ann. Hum. Genet. 63, 301-310 (Pubitemid 30021229)
37. Kuhlmann, I., Minihane, A. M., Huebbe, P., Nebel, A., and Rimbach, G. (2010) Apolipoprotein E genotype and hepatitis C, HIV and herpes simplex disease risk: a literature review. Lipids Health Dis. 9, 8
38. Oria, R. B., Patrick, P. D., Oria, M. O., Lorntz, B., Thompson, M. R., Azevedo, O. G., Lobo, R. N., Pinkerton, R. F., Guerrant, R. L., and Lima, A. A. (2010) ApoE polymorphisms and diarrheal outcomes in Brazilian shanty town children. Braz. J. Med. Biol. Res. 43, 249-256
39. Anderson, J. L., May, H. T., Horne, B. D., Bair, T. L., Hall, N. L., Carlquist, J. F., Lappe, D. L., and Muhlestein, J. B. (2010) Relation of vitamin D deficiency to cardiovascular risk factors, disease status, and incident events in a general healthcare population. Am. J. Cardiol. 106, 963-968
40. Geleijnse, J. M. (2011) Vitamin D and the prevention of hypertension and cardiovascular diseases: a review of the current evidence. Am. J. Hypertens. 24, 253-262
41. Holick, M. F. (2011) Vitamin D: evolutionary, physiological and health perspectives. Curr. Drug Targets 12, 4-18
42. Borradale, D., and Kimlin, M. (2009) Vitamin D in health and disease: an insight into traditional functions and new roles for the 'sunshine vitamin.' Nutr. Res. Rev. 22, 118-136
43. Holick, M. F. (2004) Vitamin D: importance in the prevention of cancers, type 1 diabetes, heart disease, and osteoporosis. Am. J. Clin. Nutr. 79, 362-371
44. Ahn, J., Yu, K., Stolzenberg-Solomon, R., Simon, K. C., McCullough, M. L., Gallicchio, L., Jacobs, E. J., Ascherio, A., Helzlsouer, K., Jacobs, K. B., Li, Q., Weinstein, S. J., Purdue, M., Virtamo, J., Horst, R., Wheeler, W., Chanock, S., Hunter, D. J., Hayes, R. B., Kraft, P., and Albanes, D. (2010) Genome-wide association study of circulating vitamin D levels. Hum. Mol. Genet. 19, 2739-2745
45. Engelman, C. D., Meyers, K. J., Ziegler, J. T., Taylor, K. D., Palmer, N. D., Haffner, S. M., Fingerlin, T. E., Wagenknecht, L. E., Rotter, J. I., Bowden, D. W., Langefeld, C. D., and Norris, J. M. (2010) Genome-wide association study of vitamin D concentrations in Hispanic Americans: the IRAS family study. J. Steroid Biochem. Mol. Biol. 122, 186-192
46. Wang, T. J., Zhang, F., Richards, J. B., Kestenbaum, B., Van Meurs, J. B., Berry, D., Kiel, D. P., Streeten, E. A., Ohlsson, C., Koller, D. L., Peltonen, L., Cooper, J. D., O'Reilly, P. F., Houston, D. K., Glazer, N. L., Vandenput, L., Peacock, M., Shi, J., Rivadeneira, F., McCarthy, M. I., Anneli, P., De Boer, I. H., Mangino, M., Kato, B., Smyth, D. J., Booth, S. L., Jacques, P. F., Burke, G. L., Goodarzi, M., Cheung, C. L., Wolf, M., Rice, K., Goltzman, D., Hidiroglou, N., Ladouceur, M., Wareham, N. J., Hocking, L. J., Hart, D., Arden, N. K., Cooper, C., Malik, S., Fraser, W. D., Hartikainen, A. L., Zhai, G., Macdonald, H. M., Forouhi, N. G., Loos, R. J., Reid, D. M., Hakim, A., Dennison, E., Liu, Y., Power, C., Stevens, H. E., Jaana, L., Vasan, R. S., Soranzo, N., Bojunga, J., Psaty, B. M., Lorentzon, M., Foroud, T., Harris, T. B., Hofman, A., Jansson, J. O., Cauley, J. A., Uitterlinden, A. G., Gibson, Q., Jarvelin, M. R., Karasik, D., Siscovick, D. S., Econs, M. J., Kritchevsky, S. B., Florez, J. C., Todd, J. A., Dupuis, J., Hypponen, E., and Spector, T. D. (2010) Common genetic determinants of vitamin D insufficiency: a genome-wide association study. Lancet 376, 180-188