Kruppel-like factors and vascular inflammation: Implications for atherosclerosis

Current Atherosclerosis Reports

Volumn 14, Issue 5, 2012, Pages 438-449

  Alaiti, Mohamad Amer ^a   Orasanu, Gabriela ^a   Tugal, Derin ^a   Lu, Yuan ^a   Jain, Mukesh K ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

Atheroprotection; Atherosclerosis; Endothelial cells; Inflammation; Kruppel like factors; Lymphocytes; Macrophages; Transcription factors; Vascular smooth muscle cells

Indexed keywords

CYTOKINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 2; KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 5; KRUPPEL LIKE FACTOR 6; PROTEIN KLF10; PROTEIN KLF13; PROTEIN KLF15; PROTEIN KLF3; RESVERATROL; TRANSCRIPTION FACTOR; TRIFLUOPERAZINE; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTICOAGULATION; ANTIEMETIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CYTOKINE PRODUCTION; DRUG TARGETING; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; LYMPHOCYTE FUNCTION; MACROPHAGE; MONOCYTE; MYOCARDITIS; NONHUMAN; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; SMOOTH MUSCLE FIBER; T LYMPHOCYTE ACTIVATION; VASCULITIS;

ANIMALS; ATHEROSCLEROSIS; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MACROPHAGES; MUSCLE, SMOOTH, VASCULAR;

EID: 84870486843     PISSN: 15233804     EISSN: 15346242     Source Type: Journal    
DOI: 10.1007/s11883-012-0268-6     Document Type: Article

References (108)

1. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, et al. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18-e209.
2. Gresham GA. Atherosclerosis in man: natural history and effects. Proc Nutr Soc. 1972;31(3):303-5.
3. Allam AH, Thompson RC, Wann LS, Miyamoto MI, Nur El-Din AE-H, El-Maksoud GA, et al. Atherosclerosis in ancient Egyptian mummies: the Horus study. JACC Cardiovasc Imaging. 2011;4(4):315-27.
4. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340(2):115-26.
5. Dichtl W. Inflammatory transcription factors in atherosclerosis. Medicinska fakulteten, Lunds universitet; 2000.
6. Arkenbout EK, Dekker RJ, de Vries CJM, Horrevoets AJG, Pannekoek H. Focusing on transcription factor families in atherogenesis: the function of LKLF and TR3. Thromb Haemost. 2003;89(3):522-9.
7. Preiss A, Rosenberg UB, Kienlin A, Seifert E, Jäckle H. Molecular genetics of Krüppel, a gene required for segmentation of the Drosophila embryo. Nature. 1985;313(5997):27-32.
8. Miller IJ, Bieker JJ. A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Krüppel family of nuclear proteins. Mol Cell Biol. 1993;13(5):2776-86.
9. McConnell BB, Yang VW. Mammalian Krüppel-like factors in health and diseases. Physiol Rev. 2010;90(4):1337-81.
10. Wani MA, Means RT, Lingrel JB. Loss of LKLF function results in embryonic lethality in mice. Transgenic Res. 1998;7(4):229-38.
11. Jeyaraj D, Haldar SM, Wan X, McCauley MD, Ripperger JA, Hu K, et al. Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature. 2012;483(7387):96-9.
12. Bieker JJ. Isolation, genomic structure, and expression of human erythroid Krüppel-like factor (EKLF). DNA Cell Biol. 1996;15 (5):347-52.
13. Turner J, Crossley M. Basic Krüppel-like factor functions within a network of interacting haematopoietic transcription factors. Int J Biochem Cell Biol. 1999;31(10):1169-74.
14. Dang DT, Zhao W, Mahatan CS, Geiman DE, Yang VW. Opposing effects of Krüppel-like factor 4 (gut-enriched Krüppel-like factor) and Krüppel-like factor 5 (intestinal-enriched Krüppel-like factor) on the promoter of the Krüppel-like factor 4 gene. Nucleic Acids Res. 2002;30(13):2736-41.
15. Atkins GB, Jain MK. Role of Krüppel-like transcription factors in endothelial biology. Circ Res. 2007;100(12):1686-95.
16. Libby P, Aikawa M, Jain MK. Vascular Endothelium and Atherosclerosis. In: Moncada S, Higgs A, editors. The Vascular Endothelium II [Internet]. Berlin Heidelberg: Springer; 2006. [cited 2012 May 7]. p. 285-306. Available from: http://www.springerlink.com/content/l3l3n38n7261412p/abstract/.
17. Wu W, Xiao H, Laguna-Fernandez A, Villarreal Jr G, Wang K-C, Geary GG, et al. Flow-dependent regulation of Kruppel-like factor 2 is mediated by MicroRNA-92a. Circulation. 2011;124(5):633-41.
18. Chiu J-J, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev. 2011;91(1):327-87.
19. SenBanerjee S, Lin Z, Atkins GB, Greif DM, Rao RM, Kumar A, et al. KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med. 2004;199(10):1305-15.
20. Nayak L, Lin Z, Jain MK. "Go with the flow": how Krüppel-like factor 2 regulates the vasoprotective effects of shear stress. Antioxid Redox Signal. 2011;15(5):1449-61.
21. Lin Z, Natesan V, Shi H, Dong F, Kawanami D, Mahabeleshwar GH, et al. Kruppel-like factor 2 regulates endothelial barrier function. Arterioscler Thromb Vasc Biol. 2010;30(10):1952-9.
22. Kuo CT, Veselits ML, Barton KP, Lu MM, Clendenin C, Leiden JM. The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis. Genes Dev. 1997;11(22):2996-3006.
23. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, et al. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell. 2006;11(6):845-57.
24. Kawanami D, Mahabeleshwar GH, Lin Z, Atkins GB, Hamik A, Haldar SM, et al. Kruppel-like factor 2 inhibits hypoxia-inducible factor 1alpha expression and function in the endothelium. J Biol Chem. 2009;284(31):20522-30.
25. Bhattacharya R, Senbanerjee S, Lin Z, Mir S, Hamik A, Wang P, et al. Inhibition of vascular permeability factor/vascular endothelial growth factor-mediated angiogenesis by the Kruppel-like factor KLF2. J Biol Chem. 2005;280(32):28848-51.
26. Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJG, Zeiher AM, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol. 2012;14(3):249-56.
27. Yet SF, McA'Nulty MM, Folta SC, Yen HW, Yoshizumi M, Hsieh CM, et al. Human EZF, a Krüppel-like zinc finger protein, is expressed in vascular endothelial cells and contains transcriptional activation and repression domains. J Biol Chem. 1998;273 (2):1026-31.
28. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, et al. Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem. 2007;282(18):13769- 79.
29. Ohnesorge N, Viemann D, Schmidt N, Czymai T, Spiering D, Schmolke M, et al. Erk5 activation elicits a vasoprotective endothelial phenotype via induction of Kruppel-like factor 4 (KLF4). J Biol Chem. 2010;285(34):26199-210.
30. Methe H, Balcells M, del Carmen Alegret M, Santacana M, Molins B, Hamik A, et al. Vascular bed origin dictates flow pattern regulation of endothelial adhesion molecule expression. Am J Physiol Heart Circ Physiol. 2007;292(5):H2167-75.
31. Cowan CE, Kohler EE, Dugan TA, Mirza MK, Malik AB, Wary KK. Kruppel-like factor-4 transcriptionally regulates VEcadherin expression and endothelial barrier function. Circ Res. 2010;107(8):959-66.
32. Botella LM, Sánchez-Elsner T, Sanz-Rodriguez F, Kojima S, Shimada J, Guerrero-Esteo M, et al. Transcriptional activation of endoglin and transforming growth factor-beta signaling components by cooperative interaction between Sp1 and KLF6: their potential role in the response to vascular injury. Blood. 2002;100(12):4001-10.
33. Das A, Fernandez-Zapico ME, Cao S, Yao J, Fiorucci S, Hebbel RP, et al. Disruption of an SP2/KLF6 repression complex by SHP is required for farnesoid X receptor-induced endothelial cell migration. J Biol Chem. 2006;281(51):39105-13.
34. Helbing T, Volkmar F, Goebel U, Heinke J, Diehl P, Pahl HL, et al. Krüppel-like factor 15 regulates BMPER in endothelial cells. Cardiovasc Res. 2010;85(3):551-9.
35. Boström K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993;91(4):1800-9.
36. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol. 2006;26(12): 2696-702.
37. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, et al. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci U S A. 2003;100(8): 4754-9.
38. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, Owens GK. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem. 2005;280(10):9719-27.
39. Yoshida T, Kaestner KH, Owens GK. Conditional deletion of Krüppel-like factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ Res. 2008;102(12):1548-57.
40. Gomez D, Owens GK. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovascular research [Internet]. 2012; [cited 2012 May 13]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/22406749.
41. Chamley-Campbell J, Campbell GR, Ross R. The smooth muscle cell in culture. Physiol Rev. 1979;59(1):1-61.
42. Kim S, Ip HS, Lu MM, Clendenin C, Parmacek MS. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol Cell Biol. 1997;17(4):2266-78.
43. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84(3):767-801.
44. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, Owens GK. A G/C element mediates repression of the SM22alpha promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res. 2004;95(10): 981-8.
45. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest. 2006;116(1):36-48.
46. Yoshida T, Gan Q, Owens GK. Kruppel-like factor 4, Elk-1, and histone deacetylases cooperatively suppress smooth muscle cell differentiation markers in response to oxidized phospholipids. Am J Physiol Cell Physiol. 2008;295(5):C1175-82.
47. Cherepanova OA, Pidkovka NA, Sarmento OF, Yoshida T, Gan Q, Adiguzel E, et al. Oxidized phospholipids induce type VIII collagen expression and vascular smooth muscle cell migration. Circ Res. 2009;104(5):609-18.
48. Jiang J, Chan Y-S, Loh Y-H, Cai J, Tong G-Q, Lim C-A, et al. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol. 2008;10(3):353-60.
49. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663-76.
50. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007;448(7151): 318-24.
51. Hagos EG, Ghaleb AM, Dalton WB, Bialkowska AB, Yang VW. Mouse embryonic fibroblasts null for the Krüppel-like factor 4 gene are genetically unstable. Oncogene. 2009;28(9):1197-205.
52. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci U S A. 1973;70(6):1753-6.
53. Schwartz SM, Murry CE. Proliferation and the monoclonal origins of atherosclerotic lesions. Annu Rev Med. 1998;49:437-60.
54. Matturri L, Cazzullo A, Turconi P, Lavezzi AM, Vandone PL, Gabrielli L, et al. Chromosomal alterations in atherosclerotic plaques. Atherosclerosis. 2001;154(3):755-61.
55. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, et al. Krüppel-like factor 4 regulates macrophage polarization. J Clin Invest. 2011;121(7):2736-49.
56. Shen B, Smith Jr RS, Hsu Y-T, Chao L, Chao J. Kruppel-like factor 4 is a novel mediator of Kallistatin in inhibiting endothelial inflammation via increased endothelial nitric-oxide synthase expression. J Biol Chem. 2009;284(51):35471-8.
57. Fang Y, Davies PF. Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arterioscler Thromb Vasc Biol. 2012;32(4):979-87.
58. Hoshino Y, Kurabayashi M, Kanda T, Hasegawa A, Sakamoto H, Okamoto E, et al. Regulated expression of the BTEB2 transcription factor in vascular smooth muscle cells: analysis of developmental and pathological expression profiles shows implications as a predictive factor for restenosis. Circulation. 2000;102(20):2528-34.
59. Ogata T, Kurabayashi M, Hoshino Y, Ishikawa S, Takeyoshi I, Morishita Y, et al. Inducible expression of BTEB2, a member of the zinc-finger family of transcription factors, in cardiac allograft arteriosclerosis. Transplant Proc. 2000;32(7):2032-3.
60. Shindo T, Manabe I, Fukushima Y, Tobe K, Aizawa K, Miyamoto S, et al. Krüppel-like zinc-finger transcription factor KLF5/BTEB2 is a target for angiotensin II signaling and an essential regulator of cardiovascular remodeling. Nat Med. 2002;8(8):856-63.
61. Bafford R, Sui XX, Wang G, Conte M. Angiotensin II and tumor necrosis factor-alpha upregulate survivin and Kruppel-like factor 5 in smooth muscle cells: potential relevance to vein graft hyperplasia. Surgery. 2006;140(2):289-96.
62. Courboulin A, Tremblay VL, Barrier M, Meloche J, Jacob MH, Chapolard M, et al. Krüppel-like Factor 5 contributes to pulmonary artery smooth muscle proliferation and resistance to apoptosis in human pulmonary arterial hypertension. Respir Res. 2011;12:128.
63. Nagai R, Suzuki T, Aizawa K, Miyamoto S, Amaki T, Kawai-Kowase K, et al. Phenotypic modulation of vascular smooth muscle cells: dissection of transcriptional regulatory mechanisms. Ann N Y Acad Sci. 2001;947:56-66. discussion 66-67.
64. Aizawa K, Suzuki T, Kada N, Ishihara A, Kawai-Kowase K, Matsumura T, et al. Regulation of platelet-derived growth factor-A chain by Krüppel-like factor 5: new pathway of cooperative activation with nuclear factor-kappaB. J Biol Chem. 2004;279(1):70-6.
65. Bateman NW, Tan D, Pestell RG, Black JD, Black AR. Intestinal tumor progression is associated with altered function of KLF5. J Biol Chem. 2004;279(13):12093-101.
66. Nandan MO, Chanchevalap S, Dalton WB, Yang VW. Krüppellike factor 5 promotes mitosis by activating the cyclin B1/Cdc2 complex during oncogenic Ras-mediated transformation. FEBS Lett. 2005;579(21):4757-62.
67. Chen C, Benjamin MS, Sun X, Otto KB, Guo P, Dong X-Y, et al. KLF5 promotes cell proliferation and tumorigenesis through gene regulation and the TSU-Pr1 human bladder cancer cell line. Int J Cancer. 2006;118(6):1346-55.
68. Lu Y, Haldar S, Croce K, Wang Y, Sakuma M, Morooka T, et al. Kruppel-like factor 15 regulates smooth muscle response to vascular injury-brief report. Arterioscler Thromb Vasc Biol. 2010;30 (8):1550-2.
69. Haldar SM, Lu Y, Jeyaraj D, Kawanami D, Cui Y, Eapen SJ, et al. Klf15 deficiency is a molecular link between heart failure and aortic aneurysm formation. Sci Transl Med. 2010;2(26):26ra26.
70. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145(3):341-55.
71. Smith JD, Trogan E, Ginsberg M, Grigaux C, Tian J, Miyata M. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc Natl Acad Sci U S A. 1995;92(18):8264-8.
72. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117(1):185-94.
73. Das H, Kumar A, Lin Z, Patino WD, Hwang PM, Feinberg MW, et al. Kruppel-like factor 2 (KLF2) regulates proinflammatory activation of monocytes. Proc Natl Acad Sci U S A. 2006;103 (17):6653-8.
74. Mahabeleshwar GH, Kawanami D, Sharma N, Takami Y, Zhou G, Shi H, et al. The myeloid transcription factor KLF2 regulates the host response to polymicrobial infection and endotoxic shock. Immunity. 2011;34(5):715-28.
75. Atkins GB, Wang Y, Mahabeleshwar GH, Shi H, Gao H, Kawanami D, et al. Hemizygous deficiency of Krüppel-like factor 2 augments experimental atherosclerosis. Circ Res. 2008;103(7):690-3.
76. Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, et al. HIF-1alpha is essential for myeloid cellmediated inflammation. Cell. 2003;112(5):645-57.
77. Bayele HK, Peyssonnaux C, Giatromanolaki A, Arrais-Silva WW, Mohamed HS, Collins H, 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(8):3039-48.
78. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, et al. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J Clin Invest. 2005;115(7):1806-15.
79. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, et al. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature. 2008;453(7196):807-11.
80. Sluimer JC, Gasc J-M, van Wanroij JL, Kisters N, Groeneweg M, Sollewijn Gelpke MD, et al. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol. 2008;51(13):1258-65.
81. Hultén LM, Levin M. The role of hypoxia in atherosclerosis. Curr Opin Lipidol. 2009;20(5):409-14.
82. Parathath S, Mick SL, Feig JE, Joaquin V, Grauer L, Habiel DM, et al. Hypoxia is present in murine atherosclerotic plaques and has multiple adverse effects on macrophage lipid metabolism. Circ Res. 2011;109(10):1141-52.
83. Lingrel JB, Pilcher-Roberts R, Basford JE, Manoharan P, Neumann J, Konaniah ES, et al. Myeloid-Specific Kruppel-Like Factor 2 Inactivation Increases Macrophage and Neutrophil Adhesion and Promotes Atherosclerosis. Circulation research [Internet]. 2012;[cited 2012 May 12]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/22474254.
84. Feinberg MW, Wara AK, Cao Z, Lebedeva MA, Rosenbauer F, Iwasaki H, et al. The Kruppel-like factor KLF4 is a critical regulator of monocyte differentiation. EMBO J. 2007;26 (18):4138-48.
85. Alder JK, Georgantas 3rd RW, Hildreth RL, Kaplan IM, Morisot S, Yu X, et al. Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. J Immunol. 2008;180(8):5645-52.
86. Hoeksema MA, Stöger JL, de Winther MPJ. Molecular pathways regulating macrophage polarization: implications for atherosclerosis. Current atherosclerosis reports [Internet]. 2012;[cited 2012 Mar 20]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/22407286.
87. Luo Q, Ma X, Wahl SM, Bieker JJ, Crossley M, Montaner LJ. Activation and repression of interleukin-12 p40 transcription by erythroid Kruppel-like factor in macrophages. J Biol Chem. 2004;279(18):18451-6.
88. Wara AK, Foo S, Croce K, Sun X, Icli B, Tesmenitsky Y, et al. TGF-β1 signaling and Krüppel-like factor 10 regulate bone marrow-derived proangiogenic cell differentiation, function, and neovascularization. Blood. 2011;118(24):6450-60.
89. Campbell KA, Lipinski MJ, Doran AC, Skaflen MD, Fuster V, McNamara CA. Lymphocytes and the adventitial immune response in atherosclerosis. Circ Res. 2012;110(6):889-900.
90. Buckley AF, Kuo CT, Leiden JM. Transcription factor LKLF is sufficient to program T cell quiescence via a c-Myc-dependent pathway. Nat Immunol. 2001;2(8):698-704.
91. Cyster JG. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol. 2005;23:127-59.
92. Spiegel S, Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol. 2011;11(6):403-15.
93. Zhang X, Srinivasan SV, Lingrel JB. WWP1-dependent ubiquitination and degradation of the lung Krüppel-like factor, KLF2. Biochem Biophys Res Commun. 2004;316(1):139-48.
94. Carlson CM, Endrizzi BT, Wu J, Ding X, Weinreich MA, Walsh ER, et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature. 2006;442(7100):299-302.
95. Sebzda E, Zou Z, Lee JS, Wang T, Kahn ML. Transcription factor KLF2 regulates the migration of naive T cells by restricting chemokine receptor expression patterns. Nat Immunol. 2008;9 (3):292-300.
96. Sen-Banerjee S, Mir S, Lin Z, Hamik A, Atkins GB, Das H, et al. Kruppel-like factor 2 as a novel mediator of statin effects in endothelial cells. Circulation. 2005;112(5):720-6.
97. Bu D, Tarrio M, Grabie N, Zhang Y, Yamazaki H, Stavrakis G, et al. Statin-induced Krüppel-like factor 2 expression in human and mouse T cells reduces inflammatory and pathogenic responses. J Clin Invest. 2010;120(6):1961-70.
98. Kirberg J, Gschwendner C, Dangy J-P, Rückerl F, Frommer F, Bachl J. Proviral integration of an Abelson-murine leukemia virus deregulates BKLF-expression in the hypermutating pre-B cell line 18-81. Mol Immunol. 2005;42(10):1235-42.
99. Akagi K, Suzuki T, Stephens RM, Jenkins NA, Copeland NG. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 2004;32(Database issue):D523-7.
100. Vu TT, Gatto D, Turner V, Funnell APW, Mak KS, Norton LJ, et al. Impaired B cell development in the absence of Krüppel-like factor 3. J Immunol. 2011;187(10):5032-42.
101. Hart GT, Wang X, Hogquist KA, Jameson SC. Krüppel-like factor 2 (KLF2) regulates B-cell reactivity, subset differentiation, and trafficking molecule expression. Proc Natl Acad Sci U S A. 2011;108(2):716-21.
102. An J, Golech S, Klaewsongkram J, Zhang Y, Subedi K, Huston GE, et al. Krüppel-like factor 4 (KLF4) directly regulates proliferation in thymocyte development and IL-17 expression during Th17 differentiation. FASEB J. 2011;25(10):3634-45.
103. Lebson L, Gocke A, Rosenzweig J, Alder J, Civin C, Calabresi PA, et al. Cutting edge: the transcription factor Kruppel-like factor 4 regulates the differentiation of Th17 cells independently of RORγt. J Immunol. 2010;185(12):7161-4.
104. Cao Z, Wara AK, Icli B, Sun X, Packard RRS, Esen F, et al. Kruppel-like factor KLF10 targets transforming growth factorbeta1 to regulate CD4(+)CD25(-) T cells and T regulatory cells. J Biol Chem. 2009;284(37):24914-24.
105. Cao Z, Sun X, Icli B, Wara AK, Feinberg MW. Role of Kruppellike factors in leukocyte development, function, and disease. Blood. 2010;116(22):4404-14.
106. Tuomisto TT, Lumivuori H, Kansanen E, Häkkinen S-K, Turunen MP, van Thienen JV, et al. Simvastatin has an anti-inflammatory effect on macrophages via upregulation of an atheroprotective transcription factor, Kruppel-like factor 2. Cardiovasc Res. 2008;78(1):175-84.
107. Villarreal Jr G, Zhang Y, Larman HB, Gracia-Sancho J, Koo A, García-Cardeña G. Defining the regulation of KLF4 expression and its downstream transcriptional targets in vascular endothelial cells. Biochem Biophys Res Commun. 2010;391(1):984-9.
108. Sangodkar J, Dhawan NS, Melville H, Singh VJ, Yuan E, Rana H, et al. Targeting the FOXO1/KLF6 axis regulates EGFR signaling and treatment response. The Journal of clinical investigation [Internet]. 2012;[cited 2012 Jun 29]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/22653055.