APOε4 is associated with enhanced in vivo innate immune responses in human subjects

Journal of Allergy and Clinical Immunology

Volumn 134, Issue 1, 2014, Pages

  Gale, Stephen C ^a,e   Gao, Li ^b   Mikacenic, Carmen ^c   Coyle, Susette M ^a   Rafaels, Nicholas ^b   Murray Dudenkov, Tanda ^b   Madenspacher, Jennifer H ^a   Draper, David W ^a   Ge, William ^a   Aloor, Jim J ^a   Azzam, Kathleen M ^a   Lai, Lihua ^a   Blackshear, Perry J ^d   Calvano, Steven E ^a   Barnes, Kathleen C ^b   Lowry, Stephen F ^a   Corbett, Siobhan ^a   Wurfel, Mark M ^c   Fessler, Michael B ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e EAST TEXAS MEDICAL CENTER   (United States)

Author keywords

Apolipoprotein; LPS; Toll like receptor

Indexed keywords

APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LIGAND; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA; IL6 PROTEIN, HUMAN; TLR2 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TLR5 PROTEIN, HUMAN;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD CLOTTING DISORDER; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE SEVERITY; EUROPEAN AMERICAN; EX VIVO STUDY; FEMALE; GENOTYPE; HUMAN; HUMAN CELL; HYPERTHERMIA; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; LIPID RAFT; LIVER INJURY; LUNG EDEMA; LYMPHOCYTE; MACROPHAGE; MAJOR CLINICAL STUDY; MONOCYTE; MOUSE; NONHUMAN; ORGAN INJURY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SEPSIS; SIGNAL TRANSDUCTION; ADULT; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; PATHOLOGY; TRANSGENIC MOUSE;

ADULT; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; CELLS, CULTURED; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-6; LIGANDS; LIPOPOLYSACCHARIDES; MICE; MICE, TRANSGENIC; MONOCYTES; SEPSIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84903743112     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.01.032     Document Type: Article

References (53)

1. M. Van Oosten, P.C. Rensen, E.S. Van Amersfoort, M. Van Eck, A.M. Van Dam, and J.J. Breve et al. Apolipoprotein E protects against bacterial lipopolysaccharide-induced lethality. A new therapeutic approach to treat gram-negative sepsis J Biol Chem 276 2001 8820 8824
2. S.E. Roselaar, and A. Daugherty Apolipoprotein E-deficient mice have impaired innate immune responses to Listeria monocytogenes in vivo J Lipid Res 39 1998 1740 1743
3. N. de Bont, M.G. Netea, P.N. Demacker, B.J. Kullberg, J.W. van der Meer, and A.F. Stalenhoef Apolipoprotein E-deficient mice have an impaired immune response to Klebsiella pneumoniae Eur J Clin Invest 30 2000 818 822
4. D. Baitsch, H.H. Bock, T. Engel, R. Telgmann, C. Muller-Tidow, and G. Varga et al. Apolipoprotein E induces antiinflammatory phenotype in macrophages Arterioscler Thromb Vasc Biol 31 2011 1160 1168
5. P.C. Rensen, M. Oosten, E. Bilt, M. Eck, J. Kuiper, and T.J. Berkel Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats In vivo J Clin Invest 99 1997 2438 2445
6. R.W. Mahley, and S.C. Rall Jr. Apolipoprotein E: far more than a lipid transport protein Annu Rev Genomics Hum Genet 1 2000 507 537
7. L.M. Dong, C. Wilson, M.R. Wardell, T. Simmons, R.W. Mahley, and K.H. Weisgraber et al. Human apolipoprotein E. Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms J Biol Chem 269 1994 22358 22365
8. D.M. Hatters, C.A. Peters-Libeu, and K.H. Weisgraber Apolipoprotein E structure: insights into function Trends Biochem Sci 31 2006 445 454
9. L. Jofre-Monseny, A. Loboda, A.E. Wagner, P. Huebbe, C. Boesch-Saadatmandi, and A. Jozkowicz et al. Effects of apoE genotype on macrophage inflammation and heme oxygenase-1 expression Biochem Biophys Res Commun 357 2007 319 324
10. H. Wang, D.J. Christensen, M.P. Vitek, P.M. Sullivan, and D.T. Laskowitz APOE genotype affects outcome in a murine model of sepsis: implications for a new treatment strategy Anaesth Intensive Care 37 2009 38 45
11. P.C. Chulada, E. Vainorius, S. Garantziotis, L.H. Burch, P.J. Blackshear, and D.C. Zeldin The Environmental Polymorphism Registry: a unique resource that facilitates translational research of environmental disease Environ Health Perspect 119 2011 1523 1527
12. M.M. Wurfel, A.C. Gordon, T.D. Holden, F. Radella, J. Strout, and O. Kajikawa et al. Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis Am J Respir Crit Care Med 178 2008 710 720
13. S.F. Lowry Human endotoxemia: a model for mechanistic insight and therapeutic targeting Shock 24 Suppl 1 2005 94 100
14. L. Gao, A. Grant, I. Halder, R. Brower, J. Sevransky, and J.P. Maloney et al. Novel polymorphisms in the myosin light chain kinase gene confer risk for acute lung injury Am J Respir Cell Mol Biol 34 2006 487 495
15. J.L. Vincent Organ dysfunction scores in critical illness J Organ Dysfunction 1 2005 18 23
16. O. Takeuchi, S. Sato, T. Horiuchi, K. Hoshino, K. Takeda, and Z. Dong et al. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins J Immunol 169 2002 10 14
17. T. Kawai, O. Takeuchi, T. Fujita, J. Inoue, P.F. Muhlradt, and S. Sato et al. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes J Immunol 167 2001 5887 5894
18. M.B. Fessler, and J.S. Parks Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling J Immunol 187 2011 1529 1535
19. A.J. Murphy, M. Akhtari, S. Tolani, T. Pagler, N. Bijl, and C.L. Kuo et al. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice J Clin Invest 121 2011 4138 4149
20. E.U. Okoro, Y. Zhao, Z. Guo, L. Zhou, X. Lin, and H. Yang Apolipoprotein E4 is deficient in inducing macrophage ABCA1 expression and stimulating the Sp1 signaling pathway PLoS One 7 2012 e44430
21. L. Janot, T. Secher, D. Torres, I. Maillet, J. Pfeilschifter, and V.F. Quesniaux et al. CD14 works with toll-like receptor 2 to contribute to recognition and control of Listeria monocytogenes infection J Infect Dis 198 2008 115 124
22. J.C. Chow, D.W. Young, D.T. Golenbock, W.J. Christ, and F. Gusovsky Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction J Biol Chem 274 1999 10689 10692
23. C.L. Baumann, I.M. Aspalter, O. Sharif, A. Pichlmair, S. Bluml, and F. Grebien et al. CD14 is a coreceptor of Toll-like receptors 7 and 9 J Exp Med 207 2010 2689 2701
24. S.J. van Deventer, H.R. Buller, J.W. ten Cate, A. Sturk, and W. Pauw Endotoxaemia: an early predictor of septicaemia in febrile patients Lancet 1 1988 605 609
25. W.A. Knaus, E.A. Draper, D.P. Wagner, and J.E. Zimmerman APACHE II: a severity of disease classification system Crit Care Med 13 1985 818 829
26. I. Kuhlmann, A.M. Minihane, P. Huebbe, A. Nebel, and G. Rimbach Apolipoprotein E genotype and hepatitis C, HIV and herpes simplex disease risk: a literature review Lipids Health Dis 9 2010 8
27. H.P. Grocott, M.F. Newman, H. El-Moalem, D. Bainbridge, A. Butler, and D.T. Laskowitz Apolipoprotein E genotype differentially influences the proinflammatory and anti-inflammatory response to cardiopulmonary bypass J Thorac Cardiovasc Surg 122 2001 622 623
28. N. Semeraro, C.T. Ammollo, F. Semeraro, and M. Colucci Sepsis, thrombosis and organ dysfunction Thromb Res 129 2012 290 295
29. D. Cox, S.W. Kerrigan, and S.P. Watson Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation J Thromb Haemost 9 2011 1097 1107
30. Y. Huo, A. Schober, S.B. Forlow, D.F. Smith, M.C. Hyman, and S. Jung et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E Nat Med 9 2003 61 67
31. T. Marcourakis, V.S. Bahia, E.M. Kawamoto, C.D. Munhoz, R. Gorjao, and R. Artes et al. Apolipoprotein E genotype is related to nitric oxide production in platelets Cell Biochem Funct 26 2008 852 858
32. D.R. Riddell, A. Graham, and J.S. Owen Apolipoprotein E inhibits platelet aggregation through the L-arginine:nitric oxide pathway. Implications for vascular disease J Biol Chem 272 1997 89 95
33. A. Dong, J. Caicedo, S.G. Han, P. Mueller, S. Saha, and S.S. Smyth et al. Enhanced platelet reactivity and thrombosis in Apoe-/- mice exposed to cigarette smoke is attenuated by P2Y12 antagonism Thromb Res 126 2010 e312 e317
34. Y. Ma, M.Z. Ashraf, and E.A. Podrez Scavenger receptor BI modulates platelet reactivity and thrombosis in dyslipidemia Blood 116 2010 1932 1941
35. V.S. Dole, J. Matuskova, E. Vasile, A. Yesilaltay, W. Bergmeier, and M. Bernimoulin et al. Thrombocytopenia and platelet abnormalities in high-density lipoprotein receptor-deficient mice Arterioscler Thromb Vasc Biol 28 2008 1111 1116
36. M.H. Chang, A. Yesupriya, R.M. Ned, P.W. Mueller, and N.F. Dowling Genetic variants associated with fasting blood lipids in the U.S. population: Third National Health and Nutrition Examination Survey BMC Med Genet 11 2010 62
37. R.C. Deo, D. Reich, A. Tandon, E. Akylbekova, N. Patterson, and A. Waliszewska et al. Genetic differences between the determinants of lipid profile phenotypes in African and European Americans: the Jackson Heart Study PLoS Genet 5 2009 e1000342
38. D.C. Ewbank Differences in the association between apolipoprotein E genotype and mortality across populations J Gerontol A Biol Sci Med Sci 62 2007 899 907
39. Z. Ozturk, B. Enkhmaa, N.S. Shachter, L. Berglund, and E. Anuurad Integrated role of two apoliprotein E polymorphisms on apolipoprotein B levels and coronary artery disease in a biethnic population Metab Syndr Relat Disord 8 2010 531 538
40. M.X. Tang, Y. Stern, K. Marder, K. Bell, B. Gurland, and R. Lantigua et al. The APOE-epsilon4 allele and the risk of Alzheimer disease among African Americans, whites, and Hispanics JAMA 279 1998 751 755
41. R. Qayyum, B.M. Snively, E. Ziv, M.A. Nalls, Y. Liu, and W. Tang et al. A meta-analysis and genome-wide association study of platelet count and mean platelet volume in African Americans PLoS Genet 8 2012 e1002491
42. J.B. Segal, and A.R. Moliterno Platelet counts differ by sex, ethnicity, and age in the United States Ann Epidemiol 16 2006 123 130
43. L.C. Edelstein, L.M. Simon, R.T. Montoya, M. Holinstat, E.S. Chen, and A. Bergeron et al. Racial differences in human platelet PAR4 reactivity reflect expression of PCTP and miR-376c Nat Med 19 2013 1609 1616
44. A.J. Murphy, N. Bijl, L. Yvan-Charvet, C.B. Welch, N. Bhagwat, and A. Reheman et al. Cholesterol efflux in megakaryocyte progenitors suppresses platelet production and thrombocytosis Nat Med 19 2013 586 594
45. J.H. Madenspacher, K.M. Azzam, W. Gong, K.M. Gowdy, M.P. Vitek, and D.T. Laskowitz et al. Apolipoproteins and apolipoprotein mimetic peptides modulate phagocyte trafficking through chemotactic activity J Biol Chem 287 2012 43730 43740
46. K. Singh, R. Chaturvedi, D.P. Barry, L.A. Coburn, M. Asim, and N.D. Lewis et al. The apolipoprotein E-mimetic peptide COG112 inhibits NF-kappaB signaling, proinflammatory cytokine expression, and disease activity in murine models of colitis J Biol Chem 286 2011 3839 3850
47. G.M. Buga, M. Navab, S. Imaizumi, S.T. Reddy, B. Yekta, and G. Hough et al. L-4F alters hyperlipidemic (but not healthy) mouse plasma to reduce platelet aggregation Arterioscler Thromb Vasc Biol 30 2010 283 289
48. G.R. Bernard, A. Artigas, K.L. Brigham, J. Carlet, K. Falke, and L. Hudson et al. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination Am J Respir Crit Care Med 149 1994 818 824
49. American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis Crit Care Med 20 1992 864 874
50. W.A. Knaus, E.A. Draper, D.P. Wagner, and J.E. Zimmerman APACHE II: a severity of disease classification system Crit Care Med 13 1985 818 829
51. J.L. Vincent Organ dysfunction scores in critical illness J Organ Dysfunction 1 2005 18 23
52. J.K. Pritchard, M. Stephens, and P. Donnelly Inference of population structure using multilocus genotype data Genetics 155 2000 945 959
53. B.A. Merrick, S. Dhungana, J.G. Williams, J.J. Aloor, S. Peddada, and K.B. Tomer et al. Proteomic profiling of S-acylated macrophage proteins identifies a role for palmitoylation in mitochondrial targeting of phospholipid scramblase 3 Mol Cell Proteomics 10 2011 M110.006007