The Myeloid Transcription Factor KLF2 Regulates the Host Response to Polymicrobial Infection and Endotoxic Shock

Immunity

Volumn 34, Issue 5, 2011, Pages 715-728

  Mahabeleshwar, Ganapati H ^a   Kawanami, Daiji ^a   Sharma, Nikunj ^a   Takami, Yoichi ^a   Zhou, Guangjin ^a   Shi, Hong ^a   Nayak, Lalitha ^a   Jeyaraj, Darwin ^a   Grealy, Robert ^b   White, Mary ^b   McManus, Ross ^b   Ryan, Thomas ^b   Leahy, Patrick ^c   Lin, Zhiyong ^a   Haldar, Saptarsi M ^a   Atkins, G Brandon ^a   Wong, Hector R ^d   Lingrel, Jerry B ^d   Jain, Mukesh K ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KRUPPEL LIKE FACTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BONE MARROW CELL; CELL ACTIVATION; CONTROLLED STUDY; IMMUNE RESPONSE; INNATE IMMUNITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEPTIC SHOCK;

ANIMALS; BACTERIAL INFECTIONS; CELL LINE; FEMALE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNITY, INNATE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, TRANSGENIC; MYELOID CELLS; NF-KAPPA B; SHOCK, SEPTIC;

EID: 79956305398     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.04.014     Document Type: Article

References (45)

1. Ahmad N., Lingrel J.B. Kruppel-like factor 2 transcriptional regulation involves heterogeneous nuclear ribonucleoproteins and acetyltransferases. Biochemistry 2005, 44:6276-6285.
2. Aird W.C. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 2003, 101:3765-3777.
3. Anderson K.P., Kern C.B., Crable S.C., Lingrel J.B. Isolation of a gene encoding a functional zinc finger protein homologous to erythroid Krüppel-like factor: Identification of a new multigene family. Mol. Cell. Biol. 1995, 15:5957-5965.
4. Atkins G.B., Jain M.K. Role of Krüppel-like transcription factors in endothelial biology. Circ. Res. 2007, 100:1686-1695.
5. Atkins G.B., Wang Y., Mahabeleshwar G.H., Shi H., Gao H., Kawanami D., Natesan V., Lin Z., Simon D.I., Jain M.K. Hemizygous deficiency of Krüppel-like factor 2 augments experimental atherosclerosis. Circ. Res. 2008, 103:690-693.
6. Barish G.D., Atkins A.R., Downes M., Olson P., Chong L.W., Nelson M., Zou Y., Hwang H., Kang H., Curtiss L., et al. PPARdelta regulates multiple proinflammatory pathways to suppress atherosclerosis. Proc. Natl. Acad. Sci. USA 2008, 105:4271-4276.
7. Bayele H.K., Peyssonnaux C., Giatromanolaki A., Arrais-Silva W.W., Mohamed H.S., Collins H., Giorgio S., Koukourakis M., Johnson R.S., Blackwell J.M., et al. HIF-1 regulates heritable variation and allele expression phenotypes of the macrophage immune response gene SLC11A1 from a Z-DNA forming microsatellite. Blood 2007, 110:3039-3048.
8. Bista P., Mele D.A., Baez D.V., Huber B.T. Lymphocyte quiescence factor Dpp2 is transcriptionally activated by KLF2 and TOB1. Mol. Immunol. 2008, 45:3618-3623.
9. Blouin C.C., Pagé E.L., Soucy G.M., Richard D.E. Hypoxic gene activation by lipopolysaccharide in macrophages: Implication of hypoxia-inducible factor 1alpha. Blood 2004, 103:1124-1130.
10. Buckley A.F., Kuo C.T., Leiden J.M. Transcription factor LKLF is sufficient to program T cell quiescence via a c-Myc-dependent pathway. Nat. Immunol. 2001, 2:698-704.
11. Buras J.A., Holzmann B., Sitkovsky M. Animal models of sepsis: Setting the stage. Nat. Rev. Drug Discov. 2005, 4:854-865.
12. Cao Z., Sun X., Icli B., Wara A.K., Feinberg M.W. Role of Kruppel-like factors in leukocyte development, function, and disease. Blood 2010, 116:4404-4414.
13. Cramer T., Yamanishi Y., Clausen B.E., Förster I., Pawlinski R., Mackman N., Haase V.H., Jaenisch R., Corr M., Nizet V., et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 2003, 112:645-657.
14. Culver C., Sundqvist A., Mudie S., Melvin A., Xirodimas D., Rocha S. Mechanism of hypoxia-induced NF-kappaB. Mol. Cell. Biol. 2010, 30:4901-4921.
15. Das H., Kumar A., Lin Z., Patino W.D., Hwang P.M., Feinberg M.W., Majumder P.K., Jain M.K. Kruppel-like factor 2 (KLF2) regulates proinflammatory activation of monocytes. Proc. Natl. Acad. Sci. USA 2006, 103:6653-6658.
16. Dekker R.J., Boon R.A., Rondaij M.G., Kragt A., Volger O.L., Elderkamp Y.W., Meijers J.C., Voorberg J., Pannekoek H., Horrevoets A.J. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 2006, 107:4354-4363.
17. Gill S.E., Huizar I., Bench E.M., Sussman S.W., Wang Y., Khokha R., Parks W.C. Tissue inhibitor of metalloproteinases 3 regulates resolution of inflammation following acute lung injury. Am. J. Pathol. 2010, 176:64-73.
18. Gordon S., Martinez F.O. Alternative activation of macrophages: Mechanism and functions. Immunity 2010, 32:593-604.
19. Kawanami D., Mahabeleshwar G.H., Lin Z., Atkins G.B., Hamik A., Haldar S.M., Maemura K., Lamanna J.C., Jain M.K. Kruppel-like factor 2 inhibits hypoxia-inducible factor 1alpha expression and function in the endothelium. J. Biol. Chem. 2009, 284:20522-20530.
20. Kellam P., Weiss R.A. Infectogenomics: Insights from the host genome into infectious diseases. Cell 2006, 124:695-697.
21. Kolls J.K., McCray P.B., Chan Y.R. Cytokine-mediated regulation of antimicrobial proteins. Nat. Rev. Immunol. 2008, 8:829-835.
22. Kong D., Park E.J., Stephen A.G., Calvani M., Cardellina J.H., Monks A., Fisher R.J., Shoemaker R.H., Melillo G. Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res. 2005, 65:9047-9055.
23. Krauss S., Brand M.D., Buttgereit F. Signaling takes a breath-New quantitative perspectives on bioenergetics and signal transduction. Immunity 2001, 15:497-502.
24. Kumar A., Lin Z., SenBanerjee S., Jain M.K. Tumor necrosis factor alpha-mediated reduction of KLF2 is due to inhibition of MEF2 by NF-kappaB and histone deacetylases. Mol. Cell. Biol. 2005, 25:5893-5903.
25. Liappis A.P., Kan V.L., Rochester C.G., Simon G.L. The effect of statins on mortality in patients with bacteremia. Clin. Infect. Dis. 2001, 33:1352-1357.
26. Lin Z., Kumar A., SenBanerjee S., Staniszewski K., Parmar K., Vaughan D.E., Gimbrone M.A., Balasubramanian V., García-Cardeña G., Jain M.K. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ. Res. 2005, 96:e48-e57.
27. Lin Z., Hamik A., Jain R., Kumar A., Jain M.K. Kruppel-like factor 2 inhibits protease activated receptor-1 expression and thrombin-mediated endothelial activation. Arterioscler. Thromb. Vasc. Biol. 2006, 26:1185-1189.
28. Lin Z., Natesan V., Shi H., Dong F., Kawanami D., Mahabeleshwar G.H., Atkins G.B., Nayak L., Cui Y., Finigan J.H., Jain M.K. Kruppel-like factor 2 regulates endothelial barrier function. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1952-1959.
29. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: An immunologic functional perspective. Annu. Rev. Immunol. 2009, 27:451-483.
30. Munford R.S. Severe sepsis and septic shock: The role of gram-negative bacteremia. Annu. Rev. Pathol. 2006, 1:467-496.
31. Nair M.G., Du Y., Perrigoue J.G., Zaph C., Taylor J.J., Goldschmidt M., Swain G.P., Yancopoulos G.D., Valenzuela D.M., Murphy A., et al. Alternatively activated macrophage-derived RELM-alpha is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 2009, 206:937-952.
32. Nizet V., Johnson R.S. Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 2009, 9:609-617.
33. Peyssonnaux C., Datta V., Cramer T., Doedens A., Theodorakis E.A., Gallo R.L., Hurtado-Ziola N., Nizet V., Johnson R.S. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 2005, 115:1806-1815.
34. Peyssonnaux C., Cejudo-Martin P., Doedens A., Zinkernagel A.S., Johnson R.S., Nizet V. Cutting edge: Essential role of hypoxia inducible factor-1alpha in development of lipopolysaccharide-induced sepsis. J. Immunol. 2007, 178:7516-7519.
35. Rittirsch D., Huber-Lang M.S., Flierl M.A., Ward P.A. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 2009, 4:31-36.
36. Rius J., Guma M., Schachtrup C., Akassoglou K., Zinkernagel A.S., Nizet V., Johnson R.S., Haddad G.G., Karin M. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 2008, 453:807-811.
37. Russell J.A. Management of sepsis. N. Engl. J. Med. 2006, 355:1699-1713.
38. Schouten M., Wiersinga W.J., Levi M., van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J. Leukoc. Biol. 2008, 83:536-545.
39. SenBanerjee S., Lin Z., Atkins G.B., Greif D.M., Rao R.M., Kumar A., Feinberg M.W., Chen Z., Simon D.I., Luscinskas F.W., et al. KLF2 is a novel transcriptional regulator of endothelial proinflammatory activation. J. Exp. Med. 2004, 199:1305-1315.
40. Serbina N.V., Pamer E.G. Coordinating innate immune cells to optimize microbial killing. Immunity 2008, 29:672-674.
41. Serbina N.V., Jia T., Hohl T.M., Pamer E.G. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 2008, 26:421-452.
42. Walmsley S.R., Print C., Farahi N., Peyssonnaux C., Johnson R.S., Cramer T., Sobolewski A., Condliffe A.M., Cowburn A.S., Johnson N., Chilvers E.R. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 2005, 201:105-115.
43. Wang Z., Gerstein M., Snyder M. RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10:57-63.
44. Weinreich M.A., Takada K., Skon C., Reiner S.L., Jameson S.C., Hogquist K.A. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 2009, 31:122-130.
45. Wong H.R., Cvijanovich N., Lin R., Allen G.L., Thomas N.J., Willson D.F., Freishtat R.J., Anas N., Meyer K., Checchia P.A., et al. Identification of pediatric septic shock subclasses based on genome-wide expression profiling. BMC Med. 2009, 7:34.