PLAU inferred from a correlation network is critical for suppressor function of regulatory T cells

Molecular Systems Biology

Volumn 8, Issue , 2012, Pages

  He, Feng ^a,b   Chen, Hairong ^a   Probst Kepper, Michael ^c   Geffers, Robert ^d   Eifes, Serge ^b   Del Sol, Antonio ^b   Schughart, Klaus ^a   Zeng, An Ping ^d,e   Balling, Rudi ^b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^c KLINIKUM BRAUNSCHWEIG   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^e HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

high time resolution time series; human CD4 regulatory T cell; infer key genes from undirected gene networks; Plau knockout mice; Treg development and suppressor function

Indexed keywords

TRANSCRIPTOME; UROKINASE; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; HERMES ANTIGEN; L SELECTIN; MITOGEN ACTIVATED PROTEIN KINASE; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; DOWN REGULATION; ENZYMOLOGY; GENE SILENCING; GENETICS; METABOLISM; MOUSE MUTANT; SIGNAL TRANSDUCTION; TIME;

MURINAE; MUS;

ANIMALS; ANTIGENS, CD44; CYTOKINES; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FORKHEAD TRANSCRIPTION FACTORS; GENE KNOCKDOWN TECHNIQUES; HUMANS; L-SELECTIN; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TRANSCRIPTOME; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84870790944     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2012.56     Document Type: Article

References (79)

1. Aizawa S, Nakano H, Ishida T, Horie R, Nagai M, Ito K, Yagita H, Okumura K, Inoue J, Watanabe T (1997) Tumor necrosis factor receptor-associated factor (TRAF) 5 and TRAF2 are involved in CD30-mediated NFkappaB activation. J Biol Chem 272: 2042-2045 (Pubitemid 27058475)
2. Ambroise J, Bearzatto B, Robert A, Govaerts B, Macq B, Gala JL (2011) Impact of the spotted microarray preprocessing method on foldchange
3. Amit I, Citri A, Shay T, Lu Y, KatzM, Zhang F, Tarcic G, Siwak D, Lahad J, Jacob-Hirsch J, Amariglio N, Vaisman N, Segal E, Rechavi G, Alon U, Mills G, Domany E, Yarden Y (2007) A module of negative feedback regulators defines growth factor signaling. Nat Genet 39: 503-515
4. Anastassiou D (2007) Computational analysis of the synergy among multiple interacting genes. Mol Syst Biol 3: 83
5. Bacchetta R, Gambineri E, Roncarolo MG (2007) Role of regulatory Tcells and FOXP3 in human diseases. J Allergy Clin Immunol 120: 227-235quiz 236-227 (Pubitemid 47102400)
6. Bar-Joseph Z, Gitter A, Simon I (2012) Studying and modeling dynamic biological processes using time-series gene expression data. Nat Rev Genet 13: 552-564
7. Basso K, Margolin AA, Stolovitzky G, Klein U, Dalla-Favera R, Califano A (2005) Reverse engineering of regulatory networks in human B cells. Nat Genet 37: 382-390
8. Belkaid Y (2007) Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 7: 875-888 (Pubitemid 350006238)
9. Bruder D, Probst-Kepper M, Westendorf AM, Geffers R, Beissert S, Loser K, von Boehmer H, Buer J, HansenW(2004) Neuropilin-1: a surface marker of regulatory T cells. Eur J Immunol 34: 623-630 (Pubitemid 39255909)
10. Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R, De Vos R, van den Oord JJ, Collen D, Mulligan RC (1994) Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368: 419-424 (Pubitemid 24115347)
11. Chatila TA (2005) Role of regulatory Tcells in human diseases. J Allergy Clin Immunol 116: 949-959quiz 960
12. Cohen SD, Israel E, Spiess-Meier B,Wainberg MA (1981) Plasminogen activator is an apparent lymphocyte mitogen. J Immunol 126: 1415-1420 (Pubitemid 11149237)
13. Connolly BM, Choi EY, Gardsvoll H, Bey AL, Currie BM, Chavakis T, Liu S, Molinolo A, Ploug M, Leppla SH, Bugge TH (2010) Selective abrogation of the uPA-uPAR interaction in vivo reveals a novel role in suppression of fibrin-associated inflammation. Blood 116: 1593-1603
14. Crellin NK, Garcia RV, Levings MK (2007) Flow cytometry-based methods for studying signaling in human CD4CD25FOXP3p T regulatory cells. J Immunol Methods 324: 92-104 (Pubitemid 47001432)
15. Dakic A, Shao QX, D'Amico A, O'Keeffe M, Chen WF, Shortman K, Wu L (2004) Development of the dendritic cell system during mouse ontogeny. J Immunol 172: 1018-1027 (Pubitemid 38113761)
16. de la Fuente A, Bing N, Hoeschele I, Mendes P (2004) Discovery of meaningful associations in genomic data using partial correlation coefficients. Bioinformatics 20: 3565-3574 (Pubitemid 40136792)
17. Della Gatta G, Palomero T, Perez-Garcia A, Ambesi-Impiombato A, Bansal M, Carpenter ZW, De Keersmaecker K, Sole X, Xu L, Paietta E, Racevskis J, Wiernik PH, Rowe JM, Meijerink JP, Califano A, Ferrando AA (2012) Reverse engineering of TLX oncogenic transcriptional networks identifies RUNX1 as tumor suppressor in T-ALL. Nat Med 18: 436-440
18. FeuererM, Hill JA, Kretschmer K, von Boehmer H, Mathis D, Benoist C (2010) Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc Natl Acad Sci USA 107: 5919-5924
19. Finckh U, van Hadeln K, Muller-Thomsen T, Alberici A, Binetti G, Hock C, Nitsch RM, Stoppe G, Reiss J, Gal A (2003) Association of late-onset Alzheimer disease with a genotype of PLAU, the gene encoding urokinase-type plasminogen activator on chromosome 10q22.2. Neurogenetics 4: 213-217 (Pubitemid 37122223)
20. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4CD25 regulatory Tcells. Nat Immunol 4: 330-336 (Pubitemid 36432314)
21. FuW, Ergun A, Lu T, Hill JA, Haxhinasto S, Fassett MS, Gazit R, Adoro S, Glimcher L, Chan S, Kastner P, Rossi D, Collins JJ, Mathis D, Benoist C (2012) A multiply redundant genetic switch 'locks in' the transcriptional signature of regulatory T cells. Nat Immunol 13: 972-980
22. Garin MI, Chu CC, Golshayan D, Cernuda-Morollon E,Wait R, Lechler RI (2007) Galectin-1: a key effector of regulation mediated by CD4CD25 T cells. Blood 109: 2058-2065 (Pubitemid 46348206)
23. Germain RN (2008) Special regulatory T-cell review: A rose by any other name: from suppressor T cells to Tregs, approbation to unbridled enthusiasm. Immunology 123: 20-27 (Pubitemid 350256015)
24. Gyetko MR, Libre EA, Fuller JA, Chen GH, Toews G (1999) Urokinase is required for T lymphocyte proliferation and activation in vitro. J Lab Clin Med 133: 274-288 (Pubitemid 29112090)
25. He F, Balling R (2012) The role of regulatory T cells in neurodegenerative diseases. Wiley Interdiscip Rev Syst Biol Med DOI doi:10.1002/wsbm.1187
26. He F, Balling R, Zeng AP (2009) Reverse engineering and verification of gene networks: principles, assumptions, and limitations of present methods and future perspectives. J Biotechnol 144: 190-203
27. He F, Zeng AP (2006) In search of functional association from timeseries microarray data based on the change trend and level of gene expression. BMC Bioinformatics 7: 69
28. Hill JA, Feuerer M, Tash K, Haxhinasto S, Perez J, Melamed R, Mathis D, Benoist C (2007) Foxp3 transcription-factor-dependent and - independent regulation of the regulatory T cell transcriptional signature. Immunity 27: 786-800 (Pubitemid 350110546)
29. Honma K, Kimura D, Tominaga N, Miyakoda M, Matsuyama T, Yui K (2008) Interferon regulatory factor 4 differentially regulates the production of Th2 cytokines in naive versus effector/memory CD4 T cells. Proc Natl Acad Sci USA 105: 15890-15895
30. Huttenhower C, Hibbs M, Myers C, Troyanskaya OG (2006) A scalable method for integration and functional analysis of multiple microarray datasets. Bioinformatics 22: 2890-2897 (Pubitemid 44811560)
31. Huynh-Thu VA, Irrthum A, Wehenkel L, Geurts P (2010) Inferring regulatory networks from expression data using tree-based methods. PLoS ONE 5: pii: e12776.
32. Josefowicz SZ, Rudensky A (2009) Control of regulatory Tcell lineage commitment and maintenance. Immunity 30: 616-625
33. Knutson KL, Disis ML, Salazar LG (2007) CD4 regulatory T cells in human cancer pathogenesis. Cancer Immunol Immunother 56: 271-285 (Pubitemid 46035899)
34. Kubach J, Lutter P, Bopp T, Stoll S, Becker C, Huter E, Richter C, Weingarten P, Warger T, Knop J, Mullner S, Wijdenes J, Schild H, Schmitt E, Jonuleit H (2007) Human CD4CD25 regulatory T cells: proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function. Blood 110: 1550-1558 (Pubitemid 47443971)
35. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559
36. Le Beau MM, Espinosa 3rd R, Neuman WL, Stock W, Roulston D, Larson RA, Keinanen M, Westbrook CA (1993) Cytogenetic and molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases. Proc Natl Acad Sci USA 90: 5484-5488 (Pubitemid 23176185)
37. Lee I, Date SV, Adai AT, Marcotte EM (2004) A probabilistic functional network of yeast genes. Science 306: 1555-1558 (Pubitemid 39564951)
38. Lee I, Li Z, Marcotte EM (2007) An improved, bias-reduced probabilistic functional gene network of Baker's Yeast, Saccharomyces cerevisiae. PLoS ONE 2: e988
39. Li H, Dai M, Zhuang Y (2004) A T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 21: 551-560 (Pubitemid 39370510)
40. Liu G, Burns S, Huang G, Boyd K, Proia RL, Flavell RA, Chi H (2009) The receptor S1P1 overrides regulatory T cell-mediated immune suppression through Akt-mTOR. Nat Immunol 10: 769-777
41. Lu LJ, Xia Y, Paccanaro A, Yu H, GersteinM(2005) Assessing the limits of genomic data integration for predicting protein networks. Genome Res 15: 945-953 (Pubitemid 40994214)
42. Margolin AA, Wang K, Califano A, Nemenman I (2010) Multivariate dependence and genetic networks inference. IET Syst Biol 4: 428-440
43. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD, Levine SS, Fraenkel E, von Boehmer H, Young RA (2007) Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445: 931-935
44. McClintick JN, Edenberg HJ (2006) Effects of filtering by Present call on analysis of microarray experiments. BMC Bioinformatics 7: 49
45. Mondino A, Blasi F (2004) uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol 25: 450-455 (Pubitemid 38951087)
46. Murawski MR, Litherland SA, Clare-Salzler MJ, Davoodi-Semiromi A (2006) Upregulation of Foxp3 expression in mouse and human Treg is IL-2/STAT5 dependent: implications for the NOD STAT5B mutation in diabetes pathogenesis. Ann NY Acad Sci 1079: 198-204 (Pubitemid 44968724)
47. Niedbala W, Wei X, Liew FY (2002) IL-15 induces type 1 and type 2 CD4 and CD8 T cells proliferation but is unable to drive cytokine production in the absence of TCR activation or IL-12/ IL-4 stimulation in vitro. Eur J Immunol 32: 341-347 (Pubitemid 34173325)
48. Nikitin A, Egorov S, Daraselia N, Mazo I (2003) Pathway studio - the analysis and navigation of molecular networks. Bioinformatics 19: 2155-2157 (Pubitemid 37408171)
49. Ochs HD, Ziegler SF, Torgerson TR (2005) FOXP3 acts as a rheostat of the immune response. Immunol Rev 203: 156-164 (Pubitemid 40179700)
50. Ono M, Yaguchi H, Ohkura N, Kitabayashi I, Nagamura Y, Nomura T, Miyachi Y, Tsukada T, Sakaguchi S (2007) Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446: 685-689 (Pubitemid 46606883)
51. Pan F, Yu H, Dang EV, Barbi J, Pan X, Grosso JF, Jinasena D, Sharma SM, McCadden EM, Getnet D, Drake CG, Liu JO, Ostrowski MC, PardollDM (2009) Eos mediates Foxp3-dependent gene silencing in CD4 regulatory T cells. Science 325: 1142-1146
52. Pfoertner S, Jeron A, Probst-Kepper M, Guzman CA, Hansen W, Westendorf AM, Toepfer T, Schrader AJ, Franzke A, Buer J, Geffers R (2006) Signatures of human regulatory Tcells: an encounter with old friends and new players. Genome Biol 7: R54
53. Probst-Kepper M, Balling R, Buer J (2010) FOXP3: required but not sufficient. the role of GARP (LRRC32) as a safeguard of the regulatory phenotype. Curr Mol Med 10: 533-539
54. Probst-Kepper M, Geffers R, Kroger A, Viegas N, Erck C, Hecht HJ, Lunsdorf H, Roubin R, Moharregh-Khiabani D, Wagner K, Ocklenburg F, Jeron A, Garritsen H, Arstila TP, Kekalainen E, Balling R, Hauser H, Buer J, Weiss S (2009) GARP: a key receptor controlling FOXP3 in human regulatory T cells. J Cell Mol Med 13: 3343-3357
55. Qian J, Dolled-Filhart M, Lin J, Yu H, Gerstein M (2001) Beyond synexpression relationships: local clustering of time-shifted and inverted gene expression profiles identifies new, biologically relevant interactions. J Mol Biol 314: 1053-1066 (Pubitemid 34073069)
56. Quo CF, Kaddi C, Phan JH, Zollanvari A, Xu M,Wang MD, Alterovitz G (2012) Reverse engineering biomolecular systems using -omic data: challenges, progress and opportunities. Brief Bioinformatics 13: 430-445
57. Ruan J, Dean AK, Zhang W (2010) A general co-expression networkbased approach to gene expression analysis: comparison and applications. BMC Syst Biol 4: 8
58. Sakaguchi S (2004) Naturally arising CD4 regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22: 531-562 (Pubitemid 38680433)
59. Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25CD4 regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6: 345-352 (Pubitemid 41716771)
60. Sakaguchi S, Miyara M, Costantino CM, Hafler DA (2010) FOXP3 regulatory Tcells in the human immune system. Nat Rev Immunol 10: 490-500
61. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T (2006) Foxp3 CD25 CD4 natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212: 8-27 (Pubitemid 44116697)
62. Schafer J, Strimmer K (2005) An empirical Bayes approach to inferring large-scale gene association networks. Bioinformatics 21: 754-764 (Pubitemid 40439411)
63. Shalev I, Liu H, Koscik C, Bartczak A, Javadi M, Wong KM, Maknojia A, HeW, Liu MF, Diao J, Winter E, Manuel J, McCarthy D, Cattral M, Gommerman J, Clark DA, Phillips MJ, Gorczynski RR, Zhang L, Downey G et al (2008) Targeted deletion of fgl2 leads to impaired regulatory T cell activity and development of autoimmune glomerulonephritis. J Immunol 180: 249-260
64. Shevach EM (2009) Mechanisms of foxp3 Tregulatory cell-mediated suppression. Immunity 30: 636-645
65. Stelniec-Klotz I, Legewie S, Tchernitsa O, Witzel F, Klinger B, Sers C, Herzel H, Bluthgen N, Schafer R (2012) Reverse engineering a hierarchical regulatory network downstream of oncogenic KRAS. Mol Syst Biol 8: 601
66. Stockis J, Fink W, Francois V, Connerotte T, de Smet C, Knoops L, van der Bruggen P, Boon T, Coulie PG, Lucas S (2009) Comparison of stable human Treg and Th clones by transcriptional profiling. Eur J Immunol 39: 869-882
67. Subramanian S, Shahaf G, Ozeri E, Miller LM, Vandenbark AA, Lewis EC, Offner H (2011) Sustained expression of circulating human alpha-1 antitrypsin reduces inflammation, increases CD4FoxP3 Treg cell population and prevents signs of experimental autoimmune encephalomyelitis in mice. Metab Brain Dis 26: 107-113
68. Toh H, Horimoto K (2002) Inference of a genetic network by a combined approach of cluster analysis and graphical Gaussian modeling. Bioinformatics 18: 287-297 (Pubitemid 34183106)
69. Tran DQ, Andersson J, Hardwick D, Bebris L, Illei GG, Shevach EM (2009) Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3 regulatory T cells allows for their purification from expansion cultures. Blood 113: 5125-5133
70. Ulisse S, Baldini E, Sorrenti S, D'Armiento M (2009) The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets 9: 32-71
71. Walhout AJ (2011) What does biologically meaningful mean? A perspective on gene regulatory network validation. Genome Biol 12: 109
72. Wang R, Kozhaya L, Mercer F, Khaitan A, Fujii H, Unutmaz D (2009) Expression of GARP selectively identifies activated human FOXP3 regulatory Tcells. Proc Natl Acad Sci USA 106: 13439-13444
73. Wing K, Sakaguchi S (2010) Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 11: 7-13
74. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A (2006) FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126: 375-387 (Pubitemid 44092960)
75. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, Martin-Orozco N, Kang HS, Ma L, Panopoulos AD, Craig S, Watowich SS, Jetten AM, Tian Q, Dong C (2008) CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 181: 8391-8401
76. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15
77. Yu B, Chen Y,Wu Q, Li P, Shao Y, Zhang J, Zhong Q, Peng X, Yang H, Hu X, Chen B, Guan M, Wan J, Zhang W (2011) The association between single-nucleotide polymorphisms of NCF2 and systemic lupus erythematosus in Chinese mainland population. Clin Rheumatol 30: 521-527
78. Zheng Y, Chaudhry A, Kas A, deRoos P, Kim JM, Chu TT, Corcoran L, Treuting P, Klein U, Rudensky AY (2009) Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 458: 351-356
79. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY (2007) Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445: 936-940 Ziegler SF (2006) FOXP3: of mice and men. Annu Rev Immunol 24: 209-226