Bone marrow-specific knock-in of a non-activatable ikkα kinase mutant influences haematopoiesis but not atherosclerosis in Apoe-deficient mice

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Tilstam, Pathricia V ^a   Gijbels, Marion J ^b,c   Habbeddine, Mohamed ^d   Cudejko, Céline ^d   Asare, Yaw ^a   Theelen, Wendy ^a   Zhou, Baixue ^a   Dor̈ing, Yvonne ^e   Drechsler, Maik ^e   Pawig, Lukas ^a   Simsekyilmaz, Sakine ^a   Koenen, Rory R ^b   De Winther, Menno P J ^b,c   Lawrence, Toby ^d   Bernhagen, Jürgen ^a,f   Zernecke, Alma ^g,h,i   Weber, Christian ^b,e,i   Noels, Heidi ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^f UNIVERSITY OF MUNICH   (Germany)

^g UNIVERSITY OF WÜRZBURG   (Germany)

^h TECHNICAL UNIVERSITY OF MUNICH   (Germany)

ⁱ DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; I KAPPA B KINASE ALPHA; INTERLEUKIN 12; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OXIDIZED LOW DENSITY LIPOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B KINASE; LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA ROOT; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; B LYMPHOCYTE; BONE MARROW TRANSPLANTATION; CHIMERA; CONTROLLED STUDY; CYTOKINE RELEASE; EFFECTOR CELL; FOAM CELL; GENE EXPRESSION; HEMATOPOIESIS; MACROPHAGE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; ANIMAL; BONE MARROW; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; DEFICIENCY; FLOW CYTOMETRY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTATION; PATHOLOGY; PROCEDURES; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; B-LYMPHOCYTES; BONE MARROW; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELLS, CULTURED; FLOW CYTOMETRY; HEMATOPOIESIS; I-KAPPA B KINASE; INTERLEUKIN-12; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84896845626     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087452     Document Type: Article

References (63)

1. Hansson GK, Hermansson A (2011) The immune system in atherosclerosis. Nat Immunol 12: 204-212.
2. Weber C, Noels H (2011) Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 17: 1410-1422.
3. de Winther MP, Kanters E, Kraal G, Hofker MH (2005) Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol 25: 904-914. (Pubitemid 40627833)
4. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-kappaB signaling pathways. Nat Immunol 12: 695-708.
5. Pahl HL (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866.
6. Chiba T, Kondo Y, Shinozaki S, Kaneko E, Ishigami A, et al. (2006) A selective NFkappaB inhibitor, DHMEQ, reduced atherosclerosis in ApoE-deficient mice. J Atheroscler Thromb 13: 308-313.
7. Gareus R, Kotsaki E, Xanthoulea S, van der Made I, Gijbels MJ, et al. (2008) Endothelial cell-specific NF-kappaB inhibition protects mice from atherosclerosis. Cell Metab 8: 372-383.
8. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA (2001) Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7: 1291-1297. (Pubitemid 34007932)
9. Greten FR, Arkan MC, Bollrath J, Hsu LC, Goode J, et al. (2007) NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130: 918-931. (Pubitemid 47332565)
10. Fong CH, Bebien M, Didierlaurent A, Nebauer R, Hussell T, et al. (2008) An antiinflammatory role for IKKbeta through the inhibition of "classical" macrophage activation. J Exp Med 205: 1269-1276. (Pubitemid 351831484)
11. Kanters E, Pasparakis M, Gijbels MJ, Vergouwe MN, Partouns-Hendriks I, et al. (2003) Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice. J Clin Invest 112: 1176-1185. (Pubitemid 38056294)
12. Takeda K, Takeuchi O, Tsujimura T, Itami S, Adachi O, et al. (1999) Limb and skin abnormalities in mice lacking IKKalpha. Science 284: 313-316. (Pubitemid 129523448)
13. Li ZW, Chu W, Hu Y, Delhase M, Deerinck T, et al. (1999) The IKK-beta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med 189: 1839-1845. (Pubitemid 29272700)
14. Chariot A (2009) The NF-kappaB-independent functions of IKK subunits in immunity and cancer. Trends Cell Biol 19: 404-413.
15. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, et al. (2001) Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 293: 1495-1499. (Pubitemid 32801552)
16. Perry HM, Bender TP, McNamara CA (2012) B cell subsets in atherosclerosis. Front Immunol 3: 373.
17. Anest V, Hanson JL, Cogswell PC, Steinbrecher KA, Strahl BD, et al. (2003) A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423: 659-663. (Pubitemid 36713228)
18. Yamamoto Y, Verma UN, Prajapati S, Kwak YT, Gaynor RB (2003) Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423: 655-659. (Pubitemid 36713227)
19. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M (2005) IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature 434: 1138-1143. (Pubitemid 40663493)
20. Liu B, Yang Y, Chernishof V, Loo RR, Jang H, et al. (2007) Proinflammatory stimuli induce IKKalpha-mediated phosphorylation of PIAS1 to restrict inflammation and immunity. Cell 129: 903-914. (Pubitemid 46802704)
21. Shembade N, Pujari R, Harhaj NS, Abbott DW, Harhaj EW (2011) The kinase IKKalpha inhibits activation of the transcription factor NF-kappaB by phosphorylating the regulatory molecule TAX1BP1. Nat Immunol 12: 834-843.
22. Cao Y, Bonizzi G, Seagroves TN, Greten FR, Johnson R, et al. (2001) IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107: 763-775. (Pubitemid 34033669)
23. Parini P, Johansson L, Broijersen A, Angelin B, Rudling M (2006) Lipoprotein profiles in plasma and interstitial fluid analyzed with an automated gel-filtration system. Eur J Clin Invest 36: 98-104.
24. Davies J, Gordon S (2005) Isolation and Culture of Murine Macrophages. From: Methods in Molecular Biology; Miller DHa, editor: Humana Press Inc., Totowa, Nj.
25. Marim FM, Silveira TN, Lima DS Jr, Zamboni DS (2010) A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PLoS One 5: e15263.
26. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, et al. (2006) Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 12: 178-180. (Pubitemid 43214743)
27. Sallusto F, Geginat J, Lanzavecchia A (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22: 745-763. (Pubitemid 38680440)
28. Kaisho T, Takeda K, Tsujimura T, Kawai T, Nomura F, et al. (2001) IkappaB kinase alpha is essential for mature B cell development and function. J Exp Med 193: 417-426. (Pubitemid 32524473)
29. Schiemann B, Gommerman JL, Vora K, Cachero TG, Shulga-Morskaya S, et al. (2001) An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111-2114. (Pubitemid 32848063)
30. Balkhi MY, Willette-Brown J, Zhu F, Chen Z, Liu S, et al. (2012) IKKalpha-mediated signaling circuitry regulates early B lymphopoiesis during hematopoiesis. Blood 119: 5467-5477.
31. Mancino A, Habbeddine M, Johnson E, Luron L, Bebien M, et al. (2013) I kappa B kinase alpha (IKKalpha) activity is required for functional maturation of dendritic cells and acquired immunity to infection. Embo J 32: 816-828.
32. Hacker H, Chi L, Rehg JE, Redecke V (2012) NIK prevents the development of hypereosinophilic syndrome-like disease in mice independent of IKKalpha activation. J Immunol 188: 4602-4610.
33. Matsushima A, Kaisho T, Rennert PD, Nakano H, Kurosawa K, et al. (2001) Essential role of nuclear factor (NF)-kappaB-inducing kinase and inhibitor of kappaB (IkappaB) kinase alpha in NF-kappaB activation through lymphotoxin beta receptor, but not through tumor necrosis factor receptor I. J Exp Med 193: 631-636. (Pubitemid 32539559)
34. Fagarasan S, Shinkura R, Kamata T, Nogaki F, Ikuta K, et al. (2000) Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 191: 1477-1486. (Pubitemid 30257345)
35. Xiao G, Harhaj EW, Sun SC (2001) NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 7: 401-409. (Pubitemid 32206507)
36. Hofmann J, Mair F, Greter M, Schmidt-Supprian M, Becher B (2011) NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J Exp Med 208: 1917-1929.
37. Tamura C, Nakazawa M, Kasahara M, Hotta C, Yoshinari M, et al. (2006) Impaired function of dendritic cells in alymphoplasia (aly/aly) mice for expansion of CD25+CD4+ regulatory T cells. Autoimmunity 39: 445-453. (Pubitemid 44575076)
38. Murray SE (2013) Cell-intrinsic role for NF-kappa B-inducing kinase in peripheral maintenance but not thymic development of Foxp3+ regulatory T cells in mice. PLoS One 8: e76216.
39. Kajiura F, Sun S, Nomura T, Izumi K, Ueno T, et al. (2004) NF-kappa B-inducing kinase establishes self-tolerance in a thymic stroma-dependent manner. J Immunol 172: 2067-2075. (Pubitemid 38182352)
40. Tas SW, Vervoordeldonk MJ, Hajji N, Schuitemaker JH, van der Sluijs KF, et al. (2007) Noncanonical NF-kappaB signaling in dendritic cells is required for indoleamine 2,3-dioxygenase (IDO) induction and immune regulation. Blood 110: 1540-1549. (Pubitemid 47443970)
41. Puccetti P, Grohmann U (2007) IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 7: 817-823. (Pubitemid 47480306)
42. Chen W, Liang X, Peterson AJ, Munn DH, Blazar BR (2008) The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 181: 5396-5404.
43. Pallotta MT, Orabona C, Volpi C, Vacca C, Belladonna ML, et al. (2011) Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol 12: 870-878.
44. Proietto AI, van Dommelen S, Zhou P, Rizzitelli A, D'Amico A, et al. (2008) Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci U S A 105: 19869-19874.
45. Klingenberg R, Gerdes N, Badeau RM, Gistera A, Strodthoff D, et al. (2013) Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 123: 1323-1334.
46. Major AS, Fazio S, Linton MF (2002) B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler Thromb Vasc Biol 22: 1892-1898. (Pubitemid 35315778)
47. Sasaki Y, Casola S, Kutok JL, Rajewsky K, Schmidt-Supprian M (2004) TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J Immunol 173: 2245-2252. (Pubitemid 39063079)
48. Kyaw T, Tay C, Hosseini H, Kanellakis P, Gadowski T, et al. (2012) Depletion of B2 but not B1a B cells in BAFF receptor-deficient ApoE mice attenuates atherosclerosis by potently ameliorating arterial inflammation. PLoS One 7: e29371.
49. Sage AP, Tsiantoulas D, Baker L, Harrison J, Masters L, et al. (2012) BAFF receptor deficiency reduces the development of atherosclerosis in mice-brief report. Arterioscler Thromb Vasc Biol 32: 1573-1576.
50. Ammirati E, Cianflone D, Vecchio V, Banfi M, Vermi AC, et al. (2012) Effector Memory T cells Are Associated With Atherosclerosis in Humans and Animal Models. J Am Heart Assoc 1: 27-41.
51. Lutgens E, Lievens D, Beckers L, Wijnands E, Soehnlein O, et al. (2010) Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile. J Exp Med 207: 391-404.
52. Tabas I (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 10: 36-46.
53. Baitsch D, Bock HH, Engel T, Telgmann R, Muller-Tidow C, et al. (2011) Apolipoprotein E induces antiinflammatory phenotype in macrophages. Arterioscler Thromb Vasc Biol 31: 1160-1168.
54. Brand K, Page S, Rogler G, Bartsch A, Brandl R, et al. (1996) Activated transcription factor nuclear factor-kappa B is present in the atherosclerotic lesion. J Clin Invest 97: 1715-1722. (Pubitemid 26105480)
55. Wilson SH, Best PJ, Edwards WD, Holmes DR Jr, Carlson PJ, et al. (2002) Nuclear factor-kappaB immunoreactivity is present in human coronary plaque and enhanced in patients with unstable angina pectoris. Atherosclerosis 160: 147-153. (Pubitemid 34082720)
56. Monaco C, Andreakos E, Kiriakidis S, Mauri C, Bicknell C, et al. (2004) Canonical pathway of nuclear factor kappa B activation selectively regulates proinflammatory and prothrombotic responses in human atherosclerosis. Proc Natl Acad Sci U S A 101: 5634-5639. (Pubitemid 38481208)
57. Kanters E, Gijbels MJ, van der Made I, Vergouwe MN, Heeringa P, et al. (2004) Hematopoietic NF-kappaB1 deficiency results in small atherosclerotic lesions with an inflammatory phenotype. Blood 103: 934-940. (Pubitemid 38129553)
58. Li T, Morgan MJ, Choksi S, Zhang Y, Kim YS, et al. (2010) MicroRNAs modulate the noncanonical transcription factor NF-kappaB pathway by regulating expression of the kinase IKKalpha during macrophage differentiation. Nat Immunol 11: 799-805.
59. Smook ML, Heeringa P, Damoiseaux JG, Daemen MJ, de Winther MP, et al. (2005) Leukocyte CD40L deficiency affects the CD25(+) CD4 T cell population but does not affect atherosclerosis. Atherosclerosis 183: 275-282. (Pubitemid 41579278)
60. Bavendiek U, Zirlik A, LaClair S, MacFarlane L, Libby P, et al. (2005) Atherogenesis in mice does not require CD40 ligand from bone marrow-derived cells. Arterioscler Thromb Vasc Biol 25: 1244-1249. (Pubitemid 40776616)
61. Stachon P, Missiou A, Walter C, Varo N, Colberg C, et al. (2010) Tumor necrosis factor receptor associated factor 6 is not required for atherogenesis in mice and does not associate with atherosclerosis in humans. PLoS One 5: e11589.
62. Wouters K, Cudejko C, Gijbels MJ, Fuentes L, Bantubungi K, et al. (2012) Bone marrow p16INK4a-deficiency does not modulate obesity, glucose homeostasis or atherosclerosis development. PLoS One 7: e32440.
63. Cudejko C, Wouters K, Fuentes L, Hannou SA, Paquet C, et al. (2011) p16INK4a deficiency promotes IL-4-induced polarization and inhibits proinflammatory signaling in macrophages. Blood 118: 2556-2566.