Worldwide allele frequencies of the human apolipoprotein E gene: Climate, local adaptations, and evolutionary history

American Journal of Physical Anthropology

Volumn 143, Issue 1, 2010, Pages 100-111

  Eisenberg, Dan T A ^a   Kuzawa, Christopher W ^a   Hayes, M Geoffrey ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cholesterol; HGDP CEPH; Metabolism; Population structure; Selection

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL;

ARTICLE; CLIMATE CHANGE; COLD CLIMATE; ENVIRONMENTAL TEMPERATURE; EVOLUTION; GENE FREQUENCY; LATITUDE; LOCAL ADAPTATION; POPULATION STRUCTURE; THERMOGENESIS;

ADAPTATION, BIOLOGICAL; APOLIPOPROTEINS E; BASAL METABOLISM; BIOLOGICAL EVOLUTION; CHOLESTEROL; CLIMATE; DATABASES, GENETIC; GENE FREQUENCY; GENETICS, POPULATION; GEOGRAPHY; HUMANS; REGRESSION ANALYSIS; SELECTION, GENETIC; TEMPERATURE;

EID: 77956130453     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21298     Document Type: Article

References (112)

1. Abeni F, Calamari L, Stefanini L. 2007. Metabolic conditions of lactating Friesian cows during the hot season in the Po valley. I. Blood indicators of heat stress. Int J Biometeorol 52:87-96. (Pubitemid 350172081)
2. Aitbaev KA. 1985. The levels of high density lipoprotein cholesterol and other lipids in the native population of the mountain region of Kirghizia. Vopr Med Khim 31:58-61.
3. Al-Haboubi MH. 1996. Energy expenditure during moderate work at various climates. Int J Ind Ergon 17:379-388.
4. Al-Harthi SS, Karrar O, Almashhadani SA, Saddique AA. 1990. Metabolite and hormonal profiles in heat-stroke patients at mecca pigrimage. J Intern Med 228:343-346. (Pubitemid 20337476)
5. Allen JS, Bruss J, Damasio H. 2005. The aging brain: the cognitive reserve hypothesis and hominid evolution. Am J Hum Biol 17:673-689.
6. Anand LN, Prakash BS. 2008. Comparative profiles of different lipoprotein cholesterol parameters and growth hormone during hot humid and winter season in Murrah Buffaloes. Livest Sci 115:294-300.
7. Askew EW. 2002. Work at high altitude and oxidative stress: antioxidant nutrients. Toxicology 180:107-119.
8. Aucan C, Walley AJ, Hill AVS. 2004. Common apolipoprotein E polymorphisms and risk of clinical malaria in the Gambia. J Med Genet 41:21-24. (Pubitemid 38125683)
9. Austad SN, Finch CE. 2008. Chapter 23: the evolutionary context of human aging and degenerative disease. In: Stearns SC, Koella JC, editors. Evolution in health and disease, 2nd ed. Oxford: Oxford University Press. p 301-311.
10. Bang OY, Kwak YT, Jool IS, Huh K. 2003. Important link between dementia subtype and apolipoprotein E: a meta-analysis. Yonsei Med J 44:401-413.
11. Beall CM. 2007. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104 (Suppl 1):8655-8660.
12. Becher JC, Keeling JW, McIntosh N, Wyatt B, Bell J. 2006. The distribution of apolipoprotein E alleles in Scottish perinatal deaths. J Med Genet 43:414-418.
13. Bellido D, Barragán M, Aguilar M, Colque N. 1993. Perfil lipídico de la población de Viacha. Acta Andina 2:28-29.
14. Bennet AM, Di Angelantonio E, Ye Z, Wensley F, Dahlin A, Ahlbom A, Keavney B, Collins R, Wiman B, de Faire U, Danesh J. 2007. Association of apolipoprotein E genotypes with lipid levels and coronary risk. JAMA 298:1300-1311.
15. Benton D. 1995. Do low-cholesterol levels slow mental processing. Psychosom Med 57:50-53.
16. Borinskaya SA, Kal'ina NR, Sanina ED, Kozhekbaeva ZM, Gupalo EY, Garmash IV, Ogurtsov PP, Parshukova ON, Bojko SG, Veselovsky EM, Vershubskaya GG, Kozlov AI, Rogaev EI, Yankovsky NK. 2007. Polymorphism of the apolipoprotein E gene (APOE) in the populations of Russia and neighboring countries. Russ J Genet 43:1201-1207.
17. Burt TD, Agan BK, Marconi VC, He W, Kulkarni H, Mold JE, Cavrois M, Huang Y, Mahley RW, Dolan MJ, McCune JM, Ahuja SK. 2008. Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE ε4/ε4 genotype accelerates HIV disease progression. Proc Nat Acad Sci 105:8718-8723.
18. Cann HM, de Toma C, Cazes L, Legrand MF, Morel V, Piouffre L, Bodmer J, Bodmer WF, Bonne-Tamir B, Cambon-Thomsen A, Chen Z, Chu JY, Carcassi CY, Contu L, Du RF, Excoffier L, Ferrara GB, Friedlaender JS, Groot H, Gurwitz D, Jenkins T, Herrera RJ, Huang XY, Kidd J, Kidd KK, Langaney A, Lin AA, Mehdi SQ, Parham P, Piazza A, Pistillo MP, Qian YP, Shu QF, Xu JJ, Zhu S, Weber JL, Greely HT, Feldman MW, Thomas G, Dausset J, Cavalli-Sforza LL. 2002. A human genome diversity cell line panel. Science 296:261-262.
19. Cavalli-Sforza LL. 2005. The Human Genome Diversity Project: past, present and future. Nat Rev Genet 6:333-340. (Pubitemid 40469052)
20. Civelek T, Turan MK, Birdane FM, Demirkan I. 2007. Serum lipid concentrations in military patrol dogs trained for controlled aggression. Revue Med Vet 158:7-12.
21. Coello SD, Cabrera De Leon A, Bosa Ojeda F, Perez Mendez LI, Diaz Gonzalez L, Aguirre-Jaime AJ. 2000. High density lipoprotein cholesterol increases with living altitude. Int J Epidemiol 29:65-70.
22. Corbo RM, Scacchi R. 1999. Apolipoprotein E (APOE) allele distribution in the world. Is APOE*4 a 'thrifty' allele? Ann Hum Genet 63:301-310.
23. Corder EH, Robertson K, Lannfelt L, Bogdanovic N, Eggertsen G, Wilkins J, Hall C, Gy. 1998. HIV-infected subjects with the E4 allele for APOE have excess dementia and peripheral neuropathy. Nat Med 4:1182-1184.
24. Cruz-Fuentes CS, Gonzalez-Sobrino BZ, Gomez-Sanchez A, Rueda HM, Chavez-Eakle RA, Sanchez CS. 2005. Distribution of apolipoprotein E alleles in Coras and Huicholes from Nayarit and Nahuas and Mestizos from Veracruz, Mexico. Hum Biol 77:867-872.
25. Cuthbert JA, Lipsky PE. 1987. Provision of cholesterol to lymphocytes by high-density and low-density lipoproteins-requirement for low-density- lipoprotein receptors. J Biol Chem 262:7808-7818.
26. Davis TR. 1964. The influence of climate on nutritional requirements. Am J Public Health Nations Health 54:2051-2067.
27. Dietschy JM, Turley SD. 2001. Cholesterol metabolism in the brain. Curr Opin Lipidol 12:105-112.
28. Dietschy JM, Turley SD. 2004. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45:1375-1397. (Pubitemid 39022664)
29. Dietschy JM, Turley SD, Spady DK. 1993. Role of liver in the maintenance of cholesterol and LDL homeostasis in different animal species, including humans. J Lipid Res 34:1637-1659.
30. Edison RJ, Berg K, Remaley A, Kelley R, Rotimi C, Stevenson RE, Muenke M. 2007. Adverse birth outcome among mothers with low serum cholesterol. Pediatrics 120:723-733.
31. Eisenberg D, Hayes M, Kuzawa C. 2009. Evidence for cholesterol function and local climatic adaptation based on worldwide allele frequency variations of the apoliprotein E (APOE) gene. Am J Hum Biol 21:253.
32. Elias PK, Elias MF, D'Agostino RB, Sullivan LM, Wolf PA. 2005. Serum cholesterol and cognitive performance in the Framingham Heart Study. Psychosom Med 67:24-30.
33. Ewald P. 2008. An evolutionary perspective on the causes of chronic diseases: atherosclerosis as an illustration. In: Trevathan W, Smith EO, McKenna JJ, editors. Evolutionary medicine and health: new perspectives. New York: Oxford University Press. p 350-367.
34. Finch CE. 2007. The biology of human longevity: inflammation, nutrition, and aging in the evolution of life spans , Vol.xiii. Burlington, MA: Academic Press.626p.
35. Finch CE, Stanford CB. 2004. Meat-adaptive genes and the evolution of slower aging in humans. Quart Rev Biol 79:3-50.
36. Fiori G, Facchini F, Pettener D, Rimondi A, Battistini N, Bedogni G. 2000. Relationships between blood pressure, anthropometric characteristics and blood lipids in high- and low-altitude populations from Central Asia. Annals Hum Biol 27: 19-28.
37. Froehle AW, Schoeninger MJ. 2006. Intraspecies variation in BMR does not affect estimates of early hominin total daily energy expenditure. Am J Phys Anthropol 131:552-559.
38. Fullerton SM, Clark AG, Weiss KM, Nickerson DA, Taylor SL, Stengard JH, Salomaa V, Vartiainen E, Perola M, Boerwinkle E, Sing CF. 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.
39. Galli F, Iuliano L. In press. Do statins cause myopathy by lowering vitamin E levels? Med Hypotheses.
40. Gaynor JW, Wernovsky G, Jarvik GP, Bernbaum J, Gerdes M, Zackai E, Nord AS, Clancy RR, Nicolson SC, Spray TL. 2007. Patient characteristics are important determinants of neuro-developmental outcome at one year of age after neonatal and infant cardiac surgery. J Thorac Cardiovasc Surg 133:U1344-U1391.
41. Gerdes LU. 2003. The common polymorphism of apolipoprotein E: geographical aspects and new pathophysiological relations. Clin Chem Lab Med 41:628-631.
42. Gerdes LU, Klausen IC, Sihm I, Faergeman O. 1992. Apolipoprotein- E polymorphism in a Danish population compared to findings in 45 other study populations around the world. Genet Epidemiol 9:155-167.
43. Han X. 2004. The role of apolipoprotein E in lipid metabolism in the central nervous system. Cell Mol Life Sci 61:1896-1906. (Pubitemid 39094797)
44. Harford RR, Reed HL, Morris MT, Sapien IE, Warden R, Dalesandro MM. 1993. Relationship between changes in serum thyrotropin and total and lipoprotein cholesterol with prolonged antarctic residence. Metab Clin Exp 42:1159-1163.
45. Hassi J, Rytkonen M, Kotaniemi J, Rintamaki H. 2005. Impacts of cold climate on human heat balance, performance and health in circumpolar areas. Int J Circumpolar Health 64:459.
46. Henderson VW, Guthrie JR, Dennerstein L. 2003. Serum lipids and memory in a population based cohort of middle age women. J Neurol Neurosurg Psychiatry 74:1530-1535.
47. Hulbert AJ, Else PL. 2004. Basal metabolic rate: history, composition, regulation, and usefulness. Physiol Biochem Zool 77: 869-876.
48. Human Genome Diversity Project. 2007. Stanford University HGDP-CEPH SNP Genotyping Data SUPPLEMENT 1 FLAT FILES. September 20, 2007 ed: Centre d'Etude du Polymorphisme Humain.
49. Itzhaki RF, Dobson CB, Shipley SJ, Wozniak MA. 2004. The role of viruses and of APOE in dementia. Strategies for engineered negligible senescence: why genuine control of aging may be foreseeable. New York: New York Academic Sciences. p 15-18.
50. Jacobs DR, Iribarren C. 2000. Invited commentary: low cholesterol and nonatherosclerotic disease risk: a persistently perplexing question. Am J Epidemiol 151:748-751.
51. Jacobs K. 2008. GLU: BioInformed LLC and the U.S. Department of Health and Human Services.
52. Kanat M, Sipahioglu M, Arinc H, Serin E, Yildiz O, Tunckale A, Celebi H. 2007. Is lipid lowering treatment aiming for very low LDL levels safe in terms of the synthesis of steroid hormones? Med Hypotheses 69:104-112.
53. Kaplan JR, Klein KP, Manuck SB. 1997. Cholesterol meets Darwin: public health and evolutionary implications of the cholesterol- serotonin hypothesis. Evol Anthropol 6:28-37. (Pubitemid 127339320)
54. Keatinge WR, Coleshaw SRK, Easton JC, Cotter F, Mattock MB, Chelliah R. 1986. Increased platelet and red-cell counts, blood-viscosity, and plasma-cholesterol levels during heatstress, and mortality from coronary and cerebral thrombosis. Am J Med 81:795-800.
55. Kesaniemi YA, Ehnholm C, Miettinen TA. 1987. Intestinal cholesterol absorption efficiency in man is related to apoprotein-e phenotype. J Clin Invest 80:578-581.
56. Kesteloot H, Ndam ECN, Kowo M, Njoya O, Cobbaert C, Sasaki S, Seghers V. 1997. Serum lipid levels in a Pygmy and Bantu population sample from Cameroon. Nutr Metab Carbiovasc Dis 7:383-387.
57. Kuzawa CW, Snodgrass JJ, Leonard WR. 2006. Evolutionary medicine and human cholesterol. Am J Hum Biol 18:261-261.
58. Lalovic A, Levy E, Luheshi G, Canetti L, Grenier E, Sequeira A, Turecki G. 2007. Cholesterol content in brains of suicide completers. Int J Neuropsychopharmacol 10:159-166.
59. Leininger-Muller B, Jolivalt C, Bertrand P, Siest G. 1998. Oxidation of human apolipoprotein E and cerebral enzymatic systems. Alzheimers Rep 1:95-99. (Pubitemid 128742487)
60. Leonard WR, Snodgrass JJ, Sorensen MV. 2008. Health consequences of social and ecological adversity among indigenous Siberian populations: biocultural and evolutionary interactions. In: Panter-Brick C, Fuentes A, editors. Health, risk, and adversity. New York: Berghahn Books. p 26-52.
61. Lester D. 2002. Serum cholesterol levels and suicide: a metaanalysis. Suicide Life Threat Behav 32:333-346.
62. Linton M, Farese R Jr, Young S. 1993. Familial hypobetalipoproteinemia. J Lipid Res 34:521.
63. Lopez Herraez D, Bauchet M, Tang K, Theunert C, Pugach I, Li J, Nandineni MR, Gross A, Scholz M, Stoneking M. 2009. Genetic variation and recent positive selection in worldwide human populations: evidence from nearly 1 million SNPs. PLoS One 4:e7888.
64. Lovegrove BG. 2003. The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B-Biochem Syst Environ Physiol 173:87-112.
65. Mahley RW, Rall SC, Ng. 2000. Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1:507-537.
66. Mancilha-Carvalho JJ, Crews DE. 1990. Lipid profiles of Yanomamo indians of Brazil. Prev Med 19:66-75.
67. Martin GM. 1999. APOE alleles and lipophylic pathogens. Neurobiol Aging 20:441-443.
68. Masson LF, McNeill G, Avenell A. 2003. Genetic variation and the lipid response to dietary intervention: a systematic review. Am J Clin Nutr 77:1098-1111.
69. Melton PE, Zlojutro M, Kimminau K, Crawford MH. 2006. Biological aging and Cox hazard analysis of mortality trends in a Mennonite community from south-central Kansas. Am J Hum Biol 18:387-401.
70. Miller K, Rubenstein A, Astrand PO. 1968. Lipid values in Kalahari bushmen. Arch Intern Med 121:414-417.
71. Mohanna S, Baracco R, Seclen S. 2006. Lipid profile, waist circumference, and body mass index in a high altitude population. High Alt Med Biol 7:245-255. (Pubitemid 46157311)
72. Muldoon MF, Marsland A, Flory JD, Rabin BS, Whiteside TL, Manuck SB. 1997. Immune system differences in men with hypo-or hypercholesterolemia. Clin Immunol Immunopathol 84:145-149.
73. Murray D, Schaller M. 2010. Historical prevalence of infectious diseases within 230 geopolitical regions: a tool for investigating origins of culture. J Cross-Cultural Psychol 41:99-108.
74. Nagy B, Rigo J, Fintor L, Karadi I, Toth T. 1998. Apolipoprotein E alleles in women with severe pre-eclampsia. J Clin Pathol 51:324-325.
75. Nickerson DA, Taylor SL, Fullerton SM, Weiss KM, Clark AG, Stengard JH, Salomaa V, Boerwinkle E, Sing CF. 2000. Sequence diversity and large-scale typing of SNPs in the human apolipoprotein E gene. Genome Res 10:1532-1545.
76. Onder G, Volpato S, Liperoti R, D'Arco C, Maraldi C, Fellin R, Bernabei R, Landi F, Invest G. 2006. Total serum cholesterol and recovery from disability among hospitalized older adults. J Gerontol Ser A-Biol Sci Med Sci 61:736-742.
77. Oria RB, Patrick PD, Blackman JA, Lima AAM, Guerrant RL. 2007. Role of apolipoprotein E4 in protecting children against early childhood diarrhea outcomes and implications for later development. Med Hypotheses 68:1099-1107.
78. Oria RB, Patrick PD, Zhang H, Lorntz B, Costa CMD, Brito GAC, Barrett LJ, Lima AAM, Guerrant RL. 2005. APOE4 protects the cognitive development in children with heavy diarrhea burdens in northeast Brazil. Pediatr Res 57:310-316.
79. Patterson N, Price AL, Reich D. 2006. Population structure and Eigen analysis. PLoS Genet 2:e190.
80. Pond WG, Mersmann HJ, Su DR, McGlone JJ, Wheeler MB, Smith EO. 2008. Neonatal dietary cholesterol and alleles of cholesterol 7-α hydroxylase affect piglet cerebrum weight, cholesterol concentration and behavior. J Nutr 138:282-286.
81. Porter CC, Marlowe FW. 2007. How marginal are forager habitats? J Archaeol Sci 34:59-68.
82. Prentice AM, Rayco-Solon P, Moore SE. 2005. Insights from the developing world: thrifty genotypes and thrifty phenotypes. Proc Nutr Soc 64:153-161. (Pubitemid 40813537)
83. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC. 2007. PLINK: a tool set for whole-genome association and population- based linkage analyses. Am J Hum Genet 81:559-575.
84. Putterman L. 2008. Agriculture, diffusion and development: ripple effects of the Neolithic revolution. Economica 75:729-748.
85. Reser JE. 2009. Alzheimer's disease and natural cognitive aging may represent adaptive metabolism reduction programs. Behav Brain Funct 5:13.
86. Rosenberg NA. 2006. Standardized subsets of the HGDP-CEPH human genome diversity cell line panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann Hum Genet 70:841-847.
87. Rosenberg NA, Mahajan S, Ramachandran S, Zhao C, Pritchard JK, Feldman MW. 2005. Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet 1:e70.
88. Schoknecht PA, Ebner S, Pond WG, Zhang SD, McWhinney V, Wong WW, Klein PD, Dudley M, Goddardfinegold J, Mersmann HJ. 1994. Dietary-cholesterol supplementation improves growth and behavioral-response of pigs selected for genetically high and low serum-cholesterol. J Nutr 124:305-314.
89. Sehayek E, Shefer S, Nguyen LB, Ono JG, Merkel M, Breslow JL. 2000. Apolipoprotein E regulates dietary cholesterol absorption and biliary cholesterol excretion: studies in C57BL/6 apolipoprotein E knockout mice. Proc Nat Acad Sci USA 97:3433-3437.
90. Serre D, Montpetit A, Paré G, Engert JC, Yusuf S, Keavney B, Hudson TJ, Anand S. 2008. Correction of population stratification in large multi-ethnic association studies. PLoS ONE 3:e1382.
91. Sing CF, Davignon J. 1985. Role of the apolipoprotein-e polymorphism in determining normal plasma-lipid and lipoprotein variation. Am J Hum Genet 37:268-285. (Pubitemid 15053161)
92. Singh PP, Singh M, Mastana SS. 2006. APOE distribution in world populations with new data from India and the UK. Ann Hum Biol 33:279-308.
93. Smith GD, Song FJ, Sheldon TA. 1993. Cholesterol-lowering and mortality - the importance of considering initial level of risk. Br Med J 306:1367-1373.
94. Smith JD. 2002. Apolipoproteins and aging: emerging mechanisms. Ageing Res Rev 1:345-365.
95. Song YM, Sung JH, Kim JS. 2000. Invited commentary: low cholesterol and nonatherosclerotic disease risk: a persistently perplexing question - response. Am J Epidemiol 151:752-753.
96. Song YQ, Stampfer MJ, Liu SM. 2004. Meta-analysis: apolipoprotein E genotypes and risk for coronary heart disease. Ann Intern Med 141:137-147.
97. Spokas K. 2007. Global Temp Sim Ver. 0.9: United States Department of Agriculture - Agricultural Research Service.
98. Tammi A, Ronnemaa T, Viikari J, Jokinen E, Lapinleimu H, Ehnholm C, Simell O. 2000. Apolipoprotein E4 phenotype increases non-fasting serum triglyceride concentration in infants-the STRIP study. Atherosclerosis 152:135-141.
99. Toracinta ER, Oglesby RJ, Bromwich DH. 2004. Atmospheric response to modified CLIMAP ocean boundary conditions during the last glacial maximum. J Clim 17:504-522.
100. Vamathevan J, Hasan S, Emes R, Amrine-Madsen H, Rajagopalan D, Topp S, Kumar V, Word M, Simmons M, Foord S, et al. 2008. The role of positive selection in determining the molecular cause of species differences in disease. BMC Evol Biol 8:273.
101. Vance JE, Hayashi H, Karten B. 2005. Cholesterol homeostasis in neurons and glial cells. Semin Cell Dev Biol 16:193-212.
102. Vignali M, McKinlay A, LaCount D, Chettier R, Bell R, Sahasrabudhe S, Hughes R, Fields S. 2008. Interaction of an atypical plasmodium falciparum ETRAMP with human apolipoproteins. Malaria J 7:211.
103. von Bergmann K, Lutjohann D, Lindenthal B, Steinmetz A. 2003. Efficiency of intestinal cholesterol absorption in humans is not related to apoE phenotype. J Lipid Res 44:193-197. (Pubitemid 36114785)
104. Wang HY, Zhang FC, Gao JJ, Fan JB, Liu P, Zheng ZJ, Xi H, Sun Y, Gao XC, Huang TZ, Ke J, Guo GR, Feng GY, Breen G, St Clair D, He L. 2000. Apolipoprotein E is a genetic risk factor for fetal iodine deficiency disorder in China. Mol Psych 5:363-368.
105. Woollett LA, Osono Y, Herz J, Dietschy JM. 1995. Apolipoprotein E competitively inhibits receptor-dependent low density lipoprotein uptake by the liver but has no effect on cholesterol absorption or synthesis in the mouse. Proc Nat Acad Sci USA 92:12500-12504.
106. Wozniak MA, Faragher EB, Todd JA, Koram KA, Riley EM, Itzhaki RF. 2003. Does apolipoprotein E polymorphism influence susceptibility to malaria? J Med Genet 40:348-351.
107. Wozniak MA, Itzhaki RF, Faragher EB, James MW, Ryder SD, Irving WL, Trent HCVSG. 2002. Apolipoprotein E-epsilon 4 protects against severe liver disease caused by hepatitis C virus. Hepatology 36:456-463.
108. Wozniak MA, Shipley SJ, Dobson CB, Parker SP, Scott FT, Leedham-Green M, Breuer J, Itzhaki RF. 2007. Does apolipoprotein E determine outcome of infection by varicella zoster virus and by Epstein Barr virus? Eur J Hum Genet 15:672-678.
109. Wright RO, Hu H, Silverman EK, Tsaih SW, Schwartz J, Bellinger D, Palazuelos E, Weiss ST, Hernandez-Avila M. 2003. Apolipoprotein E genotype predicts 24-month Bayley scales infant development score. Pediatr Res 54:819-825.
110. Yamamoto H, Zheng KC, Ariizumi M. 2003. Influence of heat exposure on serum lipid and lipoprotein cholesterol in young male subjects. Ind Health 41:1-7. (Pubitemid 36240964)
111. Zetterberg H, Palmer M, Ricksten A, Poirier J, Palmqvist L, Rymo L, Zafiropoulos A, Arvanitis DA, Spandidos DA, Blennow K. 2002. Influence of the apolipoprotein E epsilon 4 allele on human embryonic development. Neurosci Lett 324:189-192.
112. Zhang J, Muldoon MF, McKeown RE, Cuffe SP. 2005. Association of serum cholesterol and history of school suspension among school-age children and adolescents in the United States. Am J Epidemiol 161:691-699.