Single TNFα trimers mediating NF-κB activation: Stochastic robustness of NF-κB signaling

BMC Bioinformatics

Volumn 8, Issue , 2007, Pages

  Lipniacki, Tomasz ^a   Puszynski, Krzysztof ^c   Paszek, Pawel ^b,d   Brasier, Allan R ^e   Kimmel, Marek ^b,c  

^a INSTITUTE OF FUNDAMENTAL TECHNOLOGICAL RESEARCH   (Poland)

^b Rice University   (United States)

^c SILESIAN UNIVERSITY OF TECHNOLOGY   (Poland)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLIFICATION MECHANISM; CELL SURFACE RECEPTORS; INNATE IMMUNE RESPONSE; MOLECULAR EVENTS; MOLECULAR SPECIES; NUCLEAR TRANSLOCATIONS; REGULATORY NETWORK; STOCHASTIC ROBUSTNESS;

BIOSYNTHESIS; CELL DEATH; GENE EXPRESSION; IMMUNE SYSTEM; LIGANDS; PATHOGENS; STOCHASTIC MODELS; STOCHASTIC SYSTEMS; VIRUSES;

BIOACTIVITY;

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B; I KAPPA B KINASE; LIGAND; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL ACTIVATION; CELL PROLIFERATION; GENE ACTIVATION; GENE AMPLIFICATION; GENE EXPRESSION; GENE TRANSLOCATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MOLECULAR GENETICS; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STOCHASTIC MODEL; ANIMAL; CELL NUCLEUS MEMBRANE; DIMERIZATION; DOSE RESPONSE; DRUG POTENTIATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; NONLINEAR SYSTEM; STATISTICS; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DIMERIZATION; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; LIGANDS; NF-KAPPA B; NONLINEAR DYNAMICS; NUCLEAR ENVELOPE; SIGNAL TRANSDUCTION; STOCHASTIC PROCESSES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 38849139572     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-8-376     Document Type: Article

References (67)

1. Ko MSH Stochastic model for gene induction J Theor Biol 1991, 53:181-194. 10.1016/S0022-5193(05)80421-7
2. Walters MC Fiering S Eidemiller J Magis W Groudine M Martin DIK Enhancers increase the probability but not the level of gene expression Proc Natl Acad Sci USA 1995, 92:7125-7129. 41484 7624382 10.1073/ pnas.92.15.7125
3. Kepler TB Elston TC Stochasticity in transcriptional regulation: origins, consequences, and mathematical representations Biophys J 2001, 81:3116-3136. 1301773 11720979
4. Lipniacki T Paszek P Marciniak-Czochra A Brasier AR Kimmel M Transcriptional stochasticity in gene expression J Theor Biol 2006, 238:348-367. 16039671
5. Paszek P Lipniacki T Brasier AR Tian B Novak DE Kimmel M Stochastic effects of multiple regulators on expression profiles in Eukaryotes J Theor Biol 2005, 233:423-433. 10.1016/j.jtbi.2004.10.023 15652150
6. McAdams HH Arkin A Stochastic mechanisms in gene expression Proc Natl Acad Sci USA 1997, 94:814-819. 19596 9023339 10.1073/pnas.94.3.814
7. Kierzek AM Zaim J Zielenkiewicz P The effect of transcription and translation initiation frequencies on the stochastic fluctuations in prokaryotic gene expression J Biol Chem 2001, 276:8165-8172. 10.1074/ jbc.M006264200 11062240
8. Thattai M Oudenaarden A Intrinsic noise in gene regulatory networks Proc Natl Acad Sci USA 2001, 98:8614-8619. 37484 11438714 10.1073/ pnas.151588598
9. Blake WJ Kaern M Cantor CR Collins JJ Noise in eucaryotic gene expression Nature 2003, 422:633-637. 10.1038/nature01546 12687005
10. Raser JM O'Shea EK Control of stochasticity in eukaryotic gene expression Science 2004, 304:1811-1814. 1410811 15166317 10.1126/ science.1098641
11. Kærn M Elston TC Blake WJ Collins JJ Stochasticity in gene expression from theories to phenotypes Nature Reviews 2005, 6:451-464. 10.1038/nrg1615 15883588
12. Raj A Peskin CS Tranchina D Vargas DY Tyagi S Stochastic mRNA synthesis in mammalian cells PloS Biology 2006, 4:309. 10.1371/journal.pbio.0040309
13. Baylor D How photons start vision Proc Natl Acad Sci USA 1996, 93:560-565. 40091 8570595 10.1073/pnas.93.2.560
14. Davis MM Krogsgaard M Huppa JB Sumen C Purbhoo MA Irvine DJ Wu LC Ehrlich L Dynamics of cell surface molecules during T cell recognition Annu Rev Biochem 2003, 72:717-742. 10.1146/ annurev.biochem.72.121801.161625 14527326
15. Purbhoo MA Irvine DJ Huppa JB Davis MA T cell killing does not require the formation of a stable mature immunological synapse Nature Immunology 2004, 5:524-531. 10.1038/ni1058 15048111
16. Stylianou E O'Neill LAJ Rawlinson L Edbrookell MR Wool P Saklatvala J Interleukin 1 induces NF-κB through its type I but not its type II receptor in lymphocytes J Biol Chem 1992, 267:15636-15641. 1386364
17. Grell M Wajant H Zimmermann G Scheurich P The type 1 receptor (CD120a) is the high-affinity receptor for soluble tumor necrosis factor Proc Natl Acad Sci USA 1998, 95:570-575. 18461 9435233 10.1073/pnas.95.2.570
18. Tian B Brasier AR Identification of a nuclear factor kappa beta-dependent gene network Recent Prog Horm Res 2003, 58:95-130. 10.1210/rp.58.1.95 12795416
19. Hoffmann A Baltimore D Circuitry of nuclear κB factor signaling Immunological Review 2006, 210:171-186. 10.1111/j.0105-2896.2006.00375.x
20. Karin M The beginning of the end: IκB kinase (IKK) and NF-κB activation J Biol Chem 1999, 274:27339-27342. 10.1074/jbc.274.39.27339 10488062
21. Sun S-C Ganchi PA Ballard DW Greene WC NF-κB Controls expression of inhibitor IκBα: Evidence for an inducible autoregulatory pathway Science 1993, 259:1912-1915. 10.1126/science.8096091 8096091
22. Krikos A Laherty CD Dixit VM Transcriptional activation of the tumor necrosis factor alpha-inducible zinc finger protein, A20, is mediated by kappa B elements J Biol Chem 1992, 267:17971-17976. 1381359
23. Lipniacki T Paszek P Brasier AR Luxon B Kimmel M Mathematical model of NF-κB regulatory module J Theor Biol 2004, 228:195-215. 10.1016/ j.jtbi.2004.01.001 15094015
24. Lee EG Boone DL Chai S Libby SL Chien M Lodolce JP Ma A Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice Science 2000, 289:2350-2354. 10.1126/ science.289.5488.2350 11009421
25. Ainbinder E Revach M Wolstein O Moshonov S Diamant N Dikstein R Mechanism of rapid transcriptional induction of tumor necrosis factor alpha-responsive genes by NF-κB Mol Cell Biol 2002, 22:6354-6362. 135646 12192035 10.1128/MCB.22.18.6354-6362.2002
26. Ainbinder E Amir-Zilberstein L Yamaguchi Y Handa H Dikstein R Elongation inhibition by DRB sensitivity-inducing factor is regulated by the A20 promoter via a novel negative element and NF-κB Mol Cell Biol 2004, 24:2444-2454. 355833 14993282 10.1128/MCB.24.6.2444-2454.2004
27. Lipniacki T Kimmel M Deterministic and stochastic models of NFκB pathway Cardiovascular Toxicology, 2007, 7:215–234. 2007, 7:215-34. 17943462 10.1007/s12012-007-9003-x
28. Hoffmann A Levchenko A Scott ML Baltimore D The IκB - NF-κB signaling module: Temporal control and selective gene activation Science 2002, 298:1241-1245. 10.1126/science.1071914 12424381
29. Gerondakis S Grossmann M Nakamura Y Pohl T Grumont R Genetic approaches in mice to understand Rel/NF-κB and IκB function: transgenics and knockouts Oncogene 1999, 18:6888-6895. 10.1038/ sj.onc.1203236 10602464
30. Park SG Lee T Kang HY Park K Cho K-H Jung G The influence of the signal dynamics of activated form of IKK on NF-κB and anti-apoptotic gene expression: A systems biology approach FEBS Letters 2006, 580:822-830. 10.1016/j.febslet.2006.01.004 16413545
31. Nelson G Paraoan L Spiller DG Wilde GJC Browne AM Djali PK Unitt JF Sullivan E Floettmann E White MRH Multi-parameter analysis of the kinetics of NF-κB signaling and transcription in single living cells J Cell Science 2002, 115:1137-1148. 11884514
32. Schooley K Zhu P Dower SK Qwarnström EE Regulation of nuclear translocation of nuclear factor-κB RelA: Evidence for complex dynamics at the single-cell level Biochem J 2003, 369:331-339. 1223076 12350227 10.1042/BJ20020253
33. Nelson DE Ihekwaba AEC Elliot M Johnson JR Gibney CA Foreman BE Nelson G See V Horton CA Spiller DG Edwards SW McDowell HP Unitt JF Sullivan E Grimley R Benson N Broomhead D Kell DB White MRH Oscillations in NF-κB signaling control the dynamics of gene expression Science 2004, 306:704-708. 10.1126/science.1099962 15499023
34. Nelson DE Horton CA See V Johnson JR Nelson G Spiller DG Kell DB White MRH Response to comment on "Oscillations in NF-κB signaling control the dynamics of gene expression" Science 2005, 308:52b. 10.1126/science.1107904
35. Lipniacki T Paszek P Brasier AR Luxon B Kimmel M Stochastic regulation in early immune response Biophys J 2006, 90:725-742. 1367099 16284261 10.1529/biophysj.104.056754
36. Hayot F Jayaprakash C NF-κB oscillations and cell-to-cell variability J Theor Biol 2006, 240:583-591. 10.1016/j.jtbi.2005.10.018 16337239
37. Pogson M Smallwood R Qwarnström E Holcombe M Formal agent-based modelling of intracellular chemical interactions Biosystems 2006, 85:37-45. 10.1016/j.biosystems.2006.02.004 16581178
38. Thattai M van Oudenaarden A Attenuation of Noise in Ultrasensitive Signaling Cascades Biophys J 2002, 82:2943-2950. 1302082 12023217
39. Paulsson J Berg OG Ehrenberg M Stochastic focusing: Fluctuation-enhanced sensitivity of intracellular regulation Proc Natl Acad Sci USA 2000, 97:7148-7153. 16514 10852944 10.1073/pnas.110057697
40. Paulson J Summing up the noise in gene networks Nature 2004, 427:415-418. 10.1038/nature02257 14749823
41. Yang L Ross K Qwarnstrom EE RelA Control of IκB Phosphorylation J Biol Chem 2003, 278:30881-30888. 10.1074/jbc.M212216200 12663663
42. Sauro HM Kholodenko BN Quantitative analysis of signaling networks Progress in Biophysics & Molecular Biology 2004, 86:5-43. 10.1016/ j.pbiomolbio.2004.03.002
43. Hohmann H-P Remy R Piischl B van Loon APGM Tumor necrosis factors-α and β bind to the same two types of tumor necrosis factor receptors and maximally activate the transcription factor NF-κB at low receptor occupancy and within minutes after receptor binding J Biol Chem 1990, 265:15183-15188. 2168404
44. Chan H Aggarwall BB Role of tumor necrosis factor receptors in the activation of nuclear factor κB in human histiocytic lymphoma U-937 cells J Biol Chem 1994, 269:31424-31429. 7989309
45. Cheong R Bergmann A Werner SL Regal J Hoffmann A Levchenko A Transient IκB kinase activity mediates temporal NF-κB dynamics in response to wide rage of tumor necrosis factor-α doses J Biol Chem 2006, 281:2945-2950. 10.1074/jbc.M510085200 16321974
46. Liu P Jamaluddin M Li K Garofalo RP Casola A Brasier AR Retinoic acid-inducible gene I mediates early antiviral response and toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J Virology 2007, 81:1401-11. 10.1038/sj.onc.1209941 17072332
47. O'Donnell SM Holm GH Pierce JM Tian B Watson MJ Chari RS Ballard DW Brasier AR Dermody TS Identification of an NF-κB-dependent gene network in cells infected by mammalian reovirus J Virology 2006, 80(3):1077-1086. 1346919 16414985 10.1128/JVI.80.3.1077-1086.2006
48. Liu P Choudhary S Jamaluddin M Li K Garofalo R Casola A Brasier AR Respiratory syncytial virus activates interferon regulatory factor-3 in airway epithelial cells by upregulating a RIG-I-toll like receptor-3 pathway J Virology 2007, 81:1401-1411. 1797494 17108032 10.1128/ JVI.01740-06
49. Arnold R Konig B Galatti H Werchau H Konig W Cytokine (IL-8, IL-6, TNF-ac) and soluble TNF receptor-I release from human peripheral blood mononuclear cells after respiratory syncytial virus infection Immunology 1995, 85:364-372. 1383908 7558123
50. Werner SL Barken D Hoffmann A Stimulus specificity of gene expression programs determined by temporal control of IKK activity Science 2005, 309:1857-1861. 10.1126/science.1113319 16166517
51. Covert MW Leung TH Gaston JE Baltimore D Achieving stability of Lipopolysaccharide-induced NF-κB activation Science 2005, 309:1854-1857. 10.1126/science.1112304 16166516
52. Tian B Nowak DE Brasier AR A TNF-induced gene expression program under oscillatory NF-κB control BMC Genomics 2005, 6:137-154. 1262712 16191192 10.1186/1471-2164-6-137
53. Sillitoe K Horton C Spiller DG White MRH Single-cell time-lapse imaging of the dynamic control of NF-κB signalling Biochemical Society Transactions 2007, 35(2):263-266. 10.1042/BST0350263 17371255
54. Altan-Bonnet G Germain RN Modeling T cell antigen discrimination based on feedback control of digital ERK responses PLoS Biology 2005, 3:1925-1938. 10.1371/journal.pbio.0030356
55. Ferrell JE Tripping the switch fantastic: How a protein kinase cascade can convert graded inputs into switch-like outputs Trends Biochem Sci 1996, 21:460-466. 10.1016/S0968-0004(96)20026-X 9009826
56. Bagowski CP Besser J Frey CR Ferrell JE The JNK cascade as a biochemical switch in mammalian cells: Ultrasensitive and all-or-none responses Current Biol 2003, 13:315-320. 10.1016/S0960-9822(03)00083-6
57. Vilar JMG Guet CC Leibler S Modeling network dynamics: The lac operon, a case study J Cell Biol 2003, 161:471-476. 10.1083/jcb.200301125 12743100
58. Nho CW O'Dwyer PJ NF-κB activation by the chemopreventive dithiolethione oltipraz is exerted through stimulation of MEKK3 signaling J Biol Chem 2004, 279:26019-26027. 10.1074/jbc.M309022200 15047705
59. Blonska M Shambharkar PB Kobayashi M Zhang D Sakurai H Su B Lin X TAK1 is recruited to the tumor necrosis factor-α (TNF-α) receptor 1 complex in a receptor-interacting protein (RIP)-dependent manner and cooperates with MEKK3 leading to NF-κB activation J Biol Chem 2005, 280:43056-43063. 10.1074/jbc.M507807200 16260783
60. Takaesu G Surabhi RM Park KJ Ninomiya-Tsuji J Matsumoto K Gaynor RB TAK1 is critical for IκB kinase-mediated activation of the NF-κB Pathway J Mol Biol 2003, 326:105-115. 10.1016/S0022-2836(02)01404-3 12547194
61. Shim J-H Xiao C Paschal AE Bailey ST Rao P Hayden MS Lee K-Y Bussey C Steckel M Tanaka N Yamada G Akira S Matsumoto K Ghosh S TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo Genes and Development 2006, 19:2668-2681. 10.1101/gad.1360605
62. Delhase M Hayakawa M Chen Y Karin M Positive and negative regulation of IκB kinase activity through IKKβ subunit phosphorylation Science 1999, 284:309-313. 10.1126/science.284.5412.309 10195894
63. Wertz IE O'Rourke KM Zhou H Eby M Aravind L Seshagiri S Wu P Wiesmann C Baker R Boone DL Ma A Koonin EV Dixit VM De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kB signaling Nature 2004, 430:694-699. 10.1038/nature02794 15258597
64. Zhang SQ Kovalenko A Cantarella G Wallach D Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to Nemo (IKK3) upon receptor stimulation Immunity 2000, 12:301-311. 10.1016/ S1074-7613(00)80183-1 10755617
65. Schomer-Miller B Higashimoto T Lee Y-K Zandi E Regulation of IκB kinase (IKK) complex by IKK-dependent phosphorylation of the T-loop and C terminus of IKK J Biol Chem 2006, 281:15268-15276. 10.1074/ jbc.M513793200 16597623
66. Haseltine EL Rawlings JB Approximate simulation of coupled fast and slow reactions for stochastic chemical kinetics J Chem Phys 2002, 117:6959-6969. 10.1063/1.1505860
67. http://www.ippt.gov.pl/~tlipnia/