Cd14 SNPs regulate the innate immune response

Molecular Immunology

Volumn 51, Issue 2, 2012, Pages 112-127

  Liu, Hong Hsing ^a,e   Hu, Yajing ^a   Zheng, Ming ^a   Suhoski, Megan M ^a   Engleman, Edgar G ^a   Dill, David L ^b   Hudnall, Matt ^a   Wang, Jianmei ^c   Spolski, Rosanne ^d   Leonard, Warren J ^d   Peltz, Gary ^d  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Stanford University   (United States)

^c ROCHE BIOSCIENCE   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e EN CHU KONG HOSPITAL   (Taiwan)

Author keywords

CD14; Genetics; Monocyte

Indexed keywords

BETA INTERFERON; CD14 ANTIGEN; INTERFERON; MESSENGER RNA;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CARTILAGE CELL; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ANTIGENS, CD14; B-LYMPHOCYTES; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE CULTURE TEST, MIXED; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MURINAE;

EID: 84862790677     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.02.112     Document Type: Article

References (84)

1. Akashi-Takamura S., Miyake K. TLR accessory molecules. Curr. Opin. Immunol. 2008, 20:420-425.
2. Alibes A., Yankilevich P., Canada A., Diaz-Uriarte R. IDconverter and IDClight: conversion and annotation of gene and protein IDs. BMC Bioinformatics 2007, 8:9.
3. Baldini M., Lohman I.C., Halonen M., Erickson R.P., Holt P.G., Martinez F.D. A polymorphism* in the 5' flanking region of the CD14 gene is associated with circulating soluble CD14 levels and with total serum immunoglobulin E. Am. J. Respir. Cell Mol. Biol. 1999, 20:976-983.
4. Bazil V., Strominger J.L. Shedding as a mechanism of down-modulation of CD14 on stimulated human monocytes. J. Immunol. 1991, 147:1567-1574.
5. Borzi R.M., Mazzetti I., Macor S., Silvestri T., Bassi A., Cattini L., Facchini A. Flow cytometric analysis of intracellular chemokines in chondrocytes in vivo: constitutive expression and enhancement in osteoarthritis and rheumatoid arthritis. FEBS Lett. 1999, 455:238-242.
6. Brem R.B., Storey J.D., Whittle J., Kruglyak L. Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 2005, 436:701-703.
7. Brem R.B., Yvert G., Clinton R., Kruglyak L. Genetic dissection of transcriptional regulation in budding yeast. Science 2002, 296:752-755.
8. Bsibsi M., Bajramovic J.J., Van Duijvenvoorden E., Persoon C., Ravid R., Van Noort J.M., Vogt M.H. Identification of soluble CD14 as an endogenous agonist for Toll-like receptor 2 on human astrocytes by genome-scale functional screening of glial cell derived proteins. Glia 2007, 55:473-482.
9. Buckland P.R. Allele-specific gene expression differences in humans. Hum. Mol. Genet. 2004, 13(Spec No. 2):R255-R260.
10. Buckland P.R. The importance and identification of regulatory polymorphisms and their mechanisms of action. Biochim. Biophys. Acta 2006, 1762:17-28.
11. Bufler P., Stiegler G., Schuchmann M., Hess S., Kruger C., Stelter F., Eckerskorn C., Schutt C., Engelmann H. Soluble lipopolysaccharide receptor (CD14) is released via two different mechanisms from human monocytes and CD14 transfectants. Eur. J. Immunol. 1995, 25:604-610.
12. Campos E., Shimojo N., Inoue Y., Arima T., Suzuki S., Tomiita M., Matsuura T., Hata A., Suzuki Y., Aoyagi M., Kohno Y. No association of polymorphisms in the 5' region of the CD14 gene and food allergy in a Japanese population. Allergol. Int. 2007, 56:23-27.
13. Caplan A.I. Mesenchymal stem cells. J. Orthop. Res. 1991, 9:641-650.
14. Cauwels A., Frei K., Sansano S., Fearns C., Ulevitch R., Zimmerli W., Landmann R. The origin and function of soluble CD14 in experimental bacterial meningitis. J. Immunol. 1999, 162:4762-4772.
15. Chase J.C., Bosio C.M. The presence of CD14 overcomes evasion of innate immune responses by virulent Franciscella tularensis in human dendritic cells in vitro and pulmonary cells in vivo. Infect. Immun. 2010, 78:154-167.
16. Chau T.L., Gioia R., Gatot J.S., Patrascu F., Carpentier I., Chapelle J.P., O'Neill L., Beyaert R., Piette J., Chariot A. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated?. Trends Biochem. Sci. 2008, 33:171-180.
17. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T., Finberg R.W. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 2003, 77:4588-4596.
18. Corr M., Boyle D.L., Ronacher L.M., Lew B.R., van Baarsen L.G., Tak P.P., Firestein G.S. Interleukin 1 receptor antagonist mediates the beneficial effects of systemic interferon beta in mice: implications for rheumatoid arthritis. Ann. Rheum. Dis. 2011, 70:858-863.
19. de Buhr M.F., Hedrich H.J., Westendorf A.M., Obermeier F., Hofmann C., Zschemisch N.H., Buer J., Bumann D., Goyert S.M., Bleich A. Analysis of Cd14 as a genetic modifier of experimental inflammatory bowel disease (IBD) in mice. Inflamm. Bowel Dis. 2009, 15:1824-1836.
20. Dimas A.S., Deutsch S., Stranger B.E., Montgomery S.B., Borel C., Attar-Cohen H., Ingle C., Beazley C., Gutierrez Arcelus M., Sekowska M., Gagnebin M., Nisbett J., Deloukas P., Dermitzakis E.T., Antonarakis S.E. Common regulatory variation impacts gene expression in a cell type-dependent manner. Science 2009, 325:1246-1250.
21. Franke L., Jansen R.C. eQTL analysis in humans. Methods Mol. Biol. 2009, 573:311-328.
22. Frazer K.A., Eskin E., Kang H.M., Bogue M.A., Hinds D.A., Beilharz E.J., Gupta R.V., Montgomery J., Morenzoni M.M., Nilsen G.B., Pethiyagoda C.L., Stuve L.L., Johnson F.M., Daly M.J., Wade C.M., Cox D.R. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 2007, 448:1050-1053.
23. Fujita M., Kinoshita T. Structural remodeling of GPI anchors during biosynthesis and after attachment to proteins. FEBS Lett. 2010, 584:1670-1677.
24. Gautier L., Moller M., Friis-Hansen L., Knudsen S. Alternative mapping of probes to genes for Affymetrix chips. BMC Bioinformatics 2004, 5:111.
25. Gosset M., Berenbaum F., Thirion S., Jacques C. Primary culture and phenotyping of murine chondrocytes. Nat. Protoc. 2008, 3:1253-1260.
26. Gray N.K., Wickens M. Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 1998, 14:399-458.
27. Guo Y.Y., Liu P., Zhang X., Weller P.M.M., Wang J., Liao G., Zhang Z., Hu J., Allard J., Shafer S., Usuka J., Peltz G. In vitro and in silico pharmacogenetic analysis in mice. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17735-17740.
28. Helms C., Cao L., Krueger J.G., Wijsman E.M., Chamian F., Gordon D., Heffernan M., Daw J.A., Robarge J., Ott J., Kwok P.Y., Menter A., Bowcock A.M. A putative RUNX1 binding site variant between SLC9A3R1 and NAT9 is associated with susceptibility to psoriasis. Nat. Genet. 2003, 35:349-356.
29. Higuchi Y., Hijiya N., Matsuura K., Yasui A., Uchida T., Yamamoto S. Mouse soluble CD14 truncated at amino acid 71 in transgenic mice: preventive effect on endotoxin-mediated toxic shock. Pathobiology 2002, 70:103-114.
30. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 1999, 162:3749-3752.
31. Inoue Y., Shimojo N., Suzuki Y., Campos Alberto E.J., Yamaide A., Suzuki S., Arima T., Matsuura T., Tomiita M., Aoyagi M., Hoshioka A., Honda A., Hata A., Kohno Y. CD14 -550C/T, which is related to the serum level of soluble CD14, is associated with the development of respiratory syncytial virus bronchiolitis in the Japanese population. J. Infect. Dis. 2007, 195:1618-1624.
32. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003, 31:e15.
33. Iwaki D., Nishitani C., Mitsuzawa H., Hyakushima N., Sano H., Kuroki Y. The CD14 region spanning amino acids 57-64 is critical for interaction with the extracellular Toll-like receptor 2 domain. Biochem. Biophys. Res. Commun. 2005, 328:173-176.
34. Jacque B., Stephan K., Smirnova I., Kim B., Gilling D., Poltorak A. Mice expressing high levels of soluble CD14 retain LPS in the circulation and are resistant to LPS-induced lethality. Eur. J. Immunol. 2006, 36:3007-3016.
35. Jansen R.C., Tesson B.M., Fu J., Yang Y., McIntyre L.M. Defining gene and QTL networks. Curr. Opin. Plant Biol. 2009, 12:241-246.
36. Kabesch M., Hasemann K., Schickinger V., Tzotcheva I., Bohnert A., Carr D., Baldini M., Hackstein H., Leupold W., Weiland S.K., Martinez F.D., Mutius E., Bein G. A promoter polymorphism in the CD14 gene is associated with elevated levels of soluble CD14 but not with IgE or atopic diseases. Allergy 2004, 59:520-525.
37. Kimura A., Kishimoto T. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 2010, 40:1830-1835.
38. Kimura A., Naka T., Kishimoto T. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12099-12104.
39. Kirschning C.J., Wesche H., Merrill Ayres T., Rothe M. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 1998, 188:2091-2097.
40. Knight J.C. Regulatory polymorphisms underlying complex disease traits. J. Mol. Med. 2005, 83:97-109.
41. Knight J.C., Udalova I., Hill A.V., Greenwood B.M., Peshu N., Marsh K., Kwiatkowski D. A polymorphism that affects OCT-1 binding to the TNF promoter region is associated with severe malaria. Nat. Genet. 1999, 22:145-150.
42. Kurt-Jones E.A., Popova L., Kwinn L., Haynes L.M., Jones L.P., Tripp R.A., Walsh E.E., Freeman M.W., Golenbock D.T., Anderson L.J., Finberg R.W. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 2000, 1:398-401.
43. Labeta M.O., Durieux J.J., Spagnoli G., Fernandez N., Wijdenes J., Herrmann R. CD14 and tolerance to lipopolysaccharide: biochemical and functional analysis. Immunology 1993, 80:415-423.
44. Lee H.K., Dunzendorfer S., Soldau K., Tobias P.S. Double-stranded RNA-mediated TLR3 activation is enhanced by CD14. Immunity 2006, 24:153-163.
45. LeVan T.D., Bloom J.W., Bailey T.J., Karp C.L., Halonen M., Martinez F.D., Vercelli D. A common single nucleotide polymorphism in the CD14 promoter decreases the affinity of Sp protein binding and enhances transcriptional activity. J. Immunol. 2001, 167:5838-5844.
46. LeVan T.D., Guerra S., Klimecki W., Vasquez M.M., Lohman I.C., Martinez F.D., Halonen M., Wright A.L. The impact of CD14 polymorphisms on the development of soluble CD14 levels during infancy. Genes Immun. 2006, 7:77-80.
47. Levan T.D., Michel O., Dentener M., Thorn J., Vertongen F., Beijer L., Martinez F.D. Association between CD14 polymorphisms and serum soluble CD14 levels: effect of atopy and endotoxin inhalation. J. Allergy Clin. Immunol. 2008, 121:434-440. e1.
48. Li X., Sahbaie P., Zheng M., Ritchie J., Peltz G., Mogil J.S., Clark J.D. Expression genetics identifies spinal mechanisms supporting formalin late phase behaviors. Mol. Pain 2010, 6:11.
49. Liao G., Wang J., Guo J., Allard J., Cheng J., Ng A., Shafer S., Puech A., McPherson J.D., Foernzler D., Peltz G., Usuka J. In Silico genetics: identification of a functional element regulating H2-Ea gene expression. Science 2004, 306:690-695.
50. Liu Y.J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 2005, 23:275-306.
51. Majde J.A. Viral double-stranded RNA, cytokines, and the flu. J. Interferon Cytokine Res. 2000, 20:259-272.
52. Majewski J., Pastinen T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet. 2010, 27:72-79.
53. Mertens J., Bregadze R., Mansur A., Askar E., Bickeboller H., Ramadori G., Mihm S. Functional impact of endotoxin receptor CD14 polymorphisms on transcriptional activity. J. Mol. Med. 2009.
54. Ming J.E., Steinman R.M., Granelli-Piperno A. IL-6 enhances the generation of cytolytic T lymphocytes in the allogeneic mixed leucocyte reaction. Clin. Exp. Immunol. 1992, 89:148-153.
55. Mira E., Lacalle R.A., Buesa J.M., de Buitrago G.G., Jimenez-Baranda S., Gomez-Mouton C., Martinez A.C., Manes S. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J. Cell Sci. 2004, 117:1847-1857.
56. Nakata T., Yasuda M., Fujita M., Kataoka H., Kiura K., Sano H., Shibata K. CD14 directly binds to triacylated lipopeptides and facilitates recognition of the lipopeptides by the receptor complex of Toll-like receptors 2 and 1 without binding to the complex. Cell. Microbiol. 2006, 8:1899-1909.
57. Ozaki K., Ohnishi Y., Iida A., Sekine A., Yamada R., Tsunoda T., Sato H., Hori M., Nakamura Y., Tanaka T. Functional SNPs in the lymphotoxin-alpha gene that are associated with susceptibility to myocardial infarction. Nat. Genet. 2002, 32:650-654.
58. Palmer G., Mezin F., Juge-Aubry C.E., Plater-Zyberk C., Gabay C., Guerne P.A. Interferon beta stimulates interleukin 1 receptor antagonist production in human articular chondrocytes and synovial fibroblasts. Ann. Rheum. Dis. 2004, 63:43-49.
59. Pauligk C., Nain M., Reiling N., Gemsa D., Kaufmann A. CD14 is required for influenza A virus-induced cytokine and chemokine production. Immunobiology 2004, 209:3-10.
60. Poltorak A., He X., Smirnova I., Liu M.Y., Huffel C.V., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
61. Prokunina L., Castillejo-Lopez C., Oberg F., Gunnarsson I., Berg L., Magnusson V., Brookes A.J., Tentler D., Kristjansdottir H., Grondal G., Bolstad A.I., Svenungsson E., Lundberg I., Sturfelt G., Jonssen A., Truedsson L., Lima G., Alcocer-Varela J., Jonsson R., Gyllensten U.B., Harley J.B., Alarcon-Segovia D., Steinsson K., Alarcon-Riquelme M.E. A regulatory polymorphism in PDCD1 is associated with susceptibility to systemic lupus erythematosus in humans. Nat. Genet. 2002, 32:666-669.
62. Ramalingam S., Maxwell S.E., Medof M.E., Chen R., Gerber L.D., Udenfriend S. COOH-terminal processing of nascent polypeptides by the glycosylphosphatidylinositol transamidase in the presence of hydrazine is governed by the same parameters as glycosylphosphatidylinositol addition. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7528-7533.
63. Rathakrishnan C., Tiku M.L. Lucigenin-dependent chemiluminescence in articular chondrocytes. Free Radic. Biol. Med. 1993, 15:143-149.
64. Rey Nores J.E., Bensussan A., Vita N., Stelter F., Arias M.A., Jones M., Lefort S., Borysiewicz L.K., Ferrara P., Labeta M.O. Soluble CD14 acts as a negative regulator of human T cell activation and function. Eur. J. Immunol. 1999, 29:265-276.
65. Saraiva M., O'Garra A. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 2010, 10:170-181.
66. Sato N., Meijer L., Skaltsounis L., Greengard P., Brivanlou A.H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 2004, 10:55-63.
67. Schadt E., Monks S.A., Drake T.A., Lusis A.J., Che N., Colinayo V., Ruff T.G., Milligan S.B., Lamb J.R., Cavet G., Mao M., Stoughton R.B., Friend S.H. Genetics of gene expression surveyed in maize, mouse and man. Nature 2003, 422:297-302.
68. Summers K.L., O'Donnell J.L., Hoy M.S., Peart M., Dekker J., Rothwell A., Hart D.N. Monocyte-macrophage antigen expression on chondrocytes. J. Rheumatol. 1995, 22:1326-1334.
69. Tamura Y., Higuchi Y., Kataoka M., Akizuki S., Matsuura K., Yamamoto S. CD14 transgenic mice expressing membrane and soluble forms: comparisons of levels of cytokines and lethalities in response to lipopolysaccharide between transgenic and non-transgenic mice. Int. Immunol. 1999, 11:333-339.
70. Tesson B.M., Jansen R.C. eQTL analysis in mice and rats. Methods Mol. Biol. 2009, 573:285-309.
71. Tiku M.L., Liu S., Weaver C.W., Teodorescu M., Skosey J.L. Class II histocompatibility antigen-mediated immunologic function of normal articular chondrocytes. J. Immunol. 1985, 135:2923-2928.
72. Tokuhiro S., Yamada R., Chang X., Suzuki A., Kochi Y., Sawada T., Suzuki M., Nagasaki M., Ohtsuki M., Ono M., Furukawa H., Nagashima M., Yoshino S., Mabuchi A., Sekine A., Saito S., Takahashi A., Tsunoda T., Nakamura Y., Yamamoto K. An intronic SNP in a RUNX1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat. Genet. 2003, 35:341-348.
73. van der Velden A.W., Thomas A.A. The role of the 5' untranslated region of an mRNA in translation regulation during development. Int. J. Biochem. Cell Biol. 1999, 31:87-106.
74. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A., Gocayne J.D., Amanatides P., Ballew R.M., Huson D.H., Wortman J.R., Zhang Q., Kodira C.D., Zheng X.H., Chen L., Skupski M., Subramanian G., Thomas P.D., Zhang J., Gabor Miklos G.L., Nelson C., Broder S., Clark A.G., Nadeau J., McKusick V.A., Zinder N., Levine A.J., Roberts R.J., Simon M., Slayman C., Hunkapiller M., Bolanos R., Delcher A., Dew I., Fasulo D., Flanigan M., Florea L., Halpern A., Hannenhalli S., Kravitz S., Levy S., Mobarry C., Reinert K., Remington K., Abu-Threideh J., Beasley E., Biddick K., Bonazzi V., Brandon R., Cargill M., Chandramouliswaran I., Charlab R., Chaturvedi K., Deng Z., Di Francesco V., Dunn P., Eilbeck K., Evangelista C., Gabrielian A.E., Gan W., Ge W., Gong F., Gu Z., Guan P., Heiman T.J., Higgins M.E., Ji R.R., Ke Z., Ketchum K.A., Lai Z., Lei Y., Li Z., Li J., Liang Y., Lin X., Lu F., Merkulov G.V., Milshina N., Moore H.M., Naik A.K., Narayan V.A., Neelam B., Nusskern D., Rusch D.B., Salzberg S., Shao W., Shue B., Sun J., Wang Z., Wang A., Wang X., Wang J., Wei M., Wides R., Xiao C., Yan C., et al. The sequence of the human genome. Science 2001, 291:1304-1351.
75. Visel A., Rubin E.M., Pennacchio L.A. Genomic views of distant-acting enhancers. Nature 2009, 461:199-205.
76. Wang J., Liao G., Chang J., Nguyen A., Guo J., Chou S., Hu S., Bach C., Allard J., Shafer S., Puech A., McPherson J.D., Foernzler D., Peltz G., Usuka J. Haplotypic structure of the mouse genome. Computational Genetics and Genomics: New Tools for Understanding Disease 2005, Humana Press Inc., Totowa, New Jersey, pp. 71-83.
77. Wang J., Peltz G. Haplotype-based computational genetic analysis in mice. Computational Genetics and Genomics: New Tools for Understanding Disease 2005, Humana Press Inc., Totowa, New Jersey, pp. 51-70.
78. Wright S.D., Ramos R.A., Tobias P.S., Ulevitch R.J., Mathison J.C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 1990, 249:1431-1433.
79. Yauch L.E., Mansour M.K., Shoham S., Rottman J.B., Levitz S.M. Involvement of CD14, toll-like receptors 2 and 4, and MyD88 in the host response to the fungal pathogen Cryptococcus neoformans in vivo. Infect. Immun. 2004, 72:5373-5382.
80. Yin G.N., Jeon H., Lee S., Lee H.W., Cho J.Y., Suk K. Role of soluble CD14 in cerebrospinal fluid as a regulator of glial functions. J. Neurosci. Res. 2009, 87:2578-2590.
81. Yvert G., Brem R.B., Whittle J., Akey J.M., Foss E., Smith E.N., Mackelprang R., Kruglyak L. Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat. Genet. 2003, 35:57-64.
82. Zhang L., Pagano J.S. Structure and function of IRF-7. J. Interferon Cytokine Res. 2002, 22:95-101.
83. Zhang X., Liu H.-H., Weller P., Tao W., Wang J., Liao G., Zheng M., Monshouwer M., Peltz G. In silico and in vitro pharmacogenetics: aldehyde oxidase rapidly metabolizes a p38 kinase inhibitor. Pharmacogenomics J. 2011, 11:15-24.
84. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., Levy D.E., Leonard W.J., Littman D.R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 2007, 8:967-974.