Proteomic and protein interaction network analysis of human T lymphocytes during cell-cycle entry

Molecular Systems Biology

Volumn 8, Issue , 2012, Pages

  Orr, Stephen J ^a   Boutz, Daniel R ^b   Wang, Rong ^b,e   Chronis, Constantinos ^a,c,d   Lea, Nicholas C ^a   Thayaparan, Thivyan ^a   Hamilton, Emma ^a   Milewicz, Hanna ^a   Blanc, Eric ^a   Mufti, Ghulam J ^a   Marcotte, Edward M ^b   Thomas, N Shaun B ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research   (United States)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

cell cycle; cell size; mass spectrometry; proteomics; T cells

Indexed keywords

HETEROGENEOUS NUCLEAR RNA; DNA BINDING PROTEIN; EIF6 PROTEIN, HUMAN; INITIATION FACTOR; NUCLEAR MATRIX PROTEIN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; SF3B2 PROTEIN, HUMAN; SF3B4 PROTEIN, HUMAN; XIRP1 PROTEIN, HUMAN;

ARTICLE; BIOGENESIS; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL NUCLEUS MATRIX; CELL PROLIFERATION; HUMAN; HUMAN CELL; LYMPHOCYTE TRANSFORMATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEOMICS; RIBOSOME; RNA SPLICING; T LYMPHOCYTE; UPREGULATION; CELL NUCLEUS; CHROMATIN; CLUSTER ANALYSIS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION;

CELL CYCLE; CELL NUCLEUS; CELL PROLIFERATION; CHROMATIN; CLUSTER ANALYSIS; DNA-BINDING PROTEINS; EUKARYOTIC INITIATION FACTORS; G0 PHASE; G1 PHASE; HUMANS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPS; PROTEOMICS; RNA-BINDING PROTEINS; T-LYMPHOCYTES;

EID: 84863339052     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2012.5     Document Type: Article

References (73)

1. Acuto O, Michel F (2003) CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 3: 939-951 (Pubitemid 37521536)
2. Ahern T, Kay JE (1971) Control of protein synthesis during lymphocyte stimulation. Biochem J 125: 73P-74P
3. Anachkova B, Djeliova V, Russev G (2005) Nuclear matrix support of DNA replication. J Cell Biochem 96: 951-961 (Pubitemid 41688721)
4. Boocock GR, Morrison JA, Popovic M, Richards N, Ellis L, Durie PR, Rommens JM (2003) Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet 33: 97-101 (Pubitemid 36068690)
5. Braisted JC, Kuntumalla S, Vogel C, Marcotte EM, Rodrigues AR,Wang R, Huang ST, Ferlanti ES, Saeed AI, Fleischmann RD, Peterson SN, Pieper R (2008) The APEX Quantitative Proteomics Tool: generating protein quantitation estimates from LC-MS/MS proteomics results. BMC Bioinformatics 9: 529
6. Campos EI, Fillingham J, Li G, Zheng H, Voigt P, Kuo WH, Seepany H, Gao Z, Day LA, Greenblatt JF, Reinberg D (2010) The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol 17: 1343-1351
7. Claeys KG, van der Ven PF, Behin A, Stojkovic T, Eymard B, Dubourg O, Laforet P, Faulkner G, Richard P, Vicart P, Romero NB, Stoltenburg G, Udd B, Fardeau M, Voit T, Fürst DO (2009) Differential involvement of sarcomeric proteins in myofibrillar myopathies: a morphological and immunohistochemical study. Acta Neuropathol 117: 293-307
8. Coldwell MJ, Morley SJ (2006) Specific isoforms of translation initiation factor 4GI show differences in translational activity. Mol Cell Biol 26: 8448-8460 (Pubitemid 44748578)
9. Coller HA (2007) What's taking so long? S-phase entry from quiescence versus proliferation. Nat Rev Mol Cell Biol 8: 667-670 (Pubitemid 47106619)
10. Conlon I, Raff M (2003) Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J Biol 2: 7
11. Darzynkiewicz Z, Crissman H, Traganos F, Steinkamp J (1982) Cell heterogeneity during the cell cycle. J Cell Physiol 113: 465-474 (Pubitemid 13203852)
12. DeGregori J, Kowalik T, Nevins JR (1995) Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/ S-regulatory genes [published erratum appears in Mol Cell Biol 1995; 15(10): 5846-7]. Mol Cell Biol 15: 4215-4224
13. Dessau RB, Pipper CB (2008) ['R'-project for statistical computing]. Ugeskr Laeger 170: 328-330
14. Diehn M, Alizadeh AA, Rando OJ, Liu CL, Stankunas K, Botstein D, Crabtree GR, Brown PO (2002) Genomic expression programs and the integration of the CD28 costimulatory signal in Tcell activation. Proc Natl Acad Sci USA 99: 11796-11801 (Pubitemid 34994478)
15. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E, Wang X, Larsson O, Selvaraj A, Liu Y, Kozma SC, Thomas G, Sonenberg N (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328: 1172-1176
16. Dror Y, Ginzberg H, Dalal I, Cherepanov V, Downey G, Durie P, Roifman CM, Freedman MH (2001) Immune function in patients with Shwachman-Diamond syndrome. Br J Haematol 114: 712-717 (Pubitemid 32953656)
17. Dror Y, Squire J, Durie P, Freedman MH (1998) Malignant myeloid transformation with isochromosome 7q in Shwachman-Diamond syndrome. Leukemia 12: 1591-1595 (Pubitemid 28470444)
18. Fatica A, Tollervey D (2002) Making ribosomes. Curr Opin Cell Biol 14: 313-318 (Pubitemid 34626969)
19. Ferrai C, Naum-Ongania G, Longobardi E, Palazzolo M, Disanza A, Diaz VM, Crippa MP, Scita G, Blasi F (2009) Induction of HoxB transcription by retinoic acid requires actin polymerization. Mol Biol Cell 20: 3543-3551
20. Finch AJ, Hilcenko C, Basse N, Drynan LF, Goyenechea B, Menne TF, Gonzalez Fernandez A, Simpson P, D'Santos CS, Arends MJ, Donadieu J, Bellanné-Chantelot C, Costanzo M, Boone C, McKenzie AN, Freund SM, Warren AJ (2011) Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman- Diamond syndrome. Genes Dev 25: 917-929
21. Gandin V, Miluzio A, Barbieri AM, Beugnet A, Kiyokawa H, Marchisio PC, Biffo S (2008) Eukaryotic initiation factor 6 is rate-limiting in translation, growth and transformation. Nature 455: 684-688
22. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
23. Golas MM, Sander B, Will CL, Luhrmann R, Stark H (2003) Molecular architecture of the multiprotein splicing factor SF3b. Science 300: 980-984 (Pubitemid 36548885)
24. Horsey EW, Jakovljevic J, Miles TD, Harnpicharnchai P,Woolford Jr JL (2004) Role of the yeast Rrp1 protein in the dynamics of pre-ribosome maturation. RNA 10: 813-827 (Pubitemid 38529745)
25. Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L, Coates G, Fairley S, Fitzgerald S, Fernandez-Banet J, Gordon L, Graf S, Haider S, Hammond M, Holland R, Howe K et al (2009) Ensembl 2009. Nucleic Acids Res 37: D690-D697
26. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl 1): S96-104
27. Jain J, Loh C, Rao A (1995) Transcriptional regulation of the IL-2 gene. Curr Opin Immunol 7: 333-342
28. Keller A, Eng J, Zhang N, Li XJ, Aebersold R (2005) A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol 1: 0017
29. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392 (Pubitemid 35215372)
30. Krude T, Musahl C, Laskey RA, Knippers R (1996) Human replication proteins hCdc21, hCdc46 and P1Mcm3 bind chromatin uniformly before S-phase and are displaced locally during DNA replication. J Cell Sci 109 (Part 2): 309-318 (Pubitemid 26057113)
31. Lea NC, Orr SJ, Stoeber K, Williams GH, Lam EW-F, Ibrahim MAA, Mufti GJ, Thomas NSB (2003) Commitment point during G0-4G1 that controls entry into the cell cycle. Mol Cell Biol 23: 2351-2361 (Pubitemid 36351018)
32. Lee DW, Zhang K, Ning ZQ, Raabe EH, Tintner S, Wieland R, Wilkins BJ, Kim JM, Blough RI, Arceci RJ (2000) Proliferation-associated SNF2-like gene (PASG): a SNF2 family member altered in leukemia. Cancer Res 60: 3612-3622 (Pubitemid 30482184)
33. Lee I, Blom M, Wang PI, Shim JE, Marcotte EM (2011a) Prioritizing candidate disease genes by network guilt-by-association of genome-wide association data. 21: 1109-1121
34. Lee I, Blom UM, Wang PI, Shim JE, Marcotte EM (2011b) Prioritizing candidate disease genes by network-based boosting of genomewide association data. Genome Res 21: 1109-1121
35. Liu JO (2005) The yins of T cell activation. Sci STKE 2005: re1
36. Lu P, Vogel C, Wang R, Yao X, Marcotte EM (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 25: 117-124 (Pubitemid 46087910)
37. Menne TF, Goyenechea B, Sanchez-Puig N, Wong CC, Tonkin LM, Ancliff PJ, Brost RL, Costanzo M, Boone C, Warren AJ (2007) The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat Genet 39: 486-495 (Pubitemid 46514776)
38. Miluzio A, Beugnet A, Grosso S, Brina D, Mancino M, Campaner S, Amati B, de Marco A, Biffo S (2011) Impairment of cytoplasmic eIF6 activity restricts lymphomagenesis and tumor progression without affecting normal growth. Cancer Cell 19: 765-775
39. Miron M, Verdu J, Lachance PE, Birnbaum MJ, Lasko PF, Sonenberg N (2001) The translational inhibitor 4E-BP is an effector of PI(3)K/Akt signalling and cell growth in Drosophila. Nat Cell Biol 3: 596-601 (Pubitemid 32536857)
40. Misteli T (2004) Spatial positioning; a new dimension in genome function. Cell 119: 153-156 (Pubitemid 39360898)
41. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, Thomas G (1999) Drosophila S6 kinase: a regulator of cell size. Science 285: 2126-2129 (Pubitemid 29451430)
42. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL (1986) Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 136: 2348-2357 (Pubitemid 16136806)
43. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344 (Part 2): 427-431 (Pubitemid 30011599)
44. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658 (Pubitemid 37082259)
45. Nickerson J (2001) Experimental observations of a nuclear matrix. J Cell Sci 114: 463-474 (Pubitemid 32186105)
46. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, Sonenberg N, Kelly PA, Sotiropoulos A, Pende M (2005) Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 7: 286-294 (Pubitemid 40331130)
47. Olave IA, Reck-Peterson SL, Crabtree GR (2002) Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem 71: 755-781 (Pubitemid 34800234)
48. Orr SJ, Gaymes T, Ladon D, Chronis C, Czepulkowski B, Wang R, Mufti GJ, Marcotte EM, Thomas NS (2010) Reducing MCM levels in human primary T cells during the G(0)-G(1) transition causes genomic instability during the first cell cycle. Oncogene 29: 3803-3814
49. Otten J, van der Ven PF, Vakeel P, Eulitz S, Kirfel G, Brandau O, Boesl M, Schrickel JW, Linhart M, Hayess K, Naya FJ, Milting H, Meyer R, Fürst DO (2010) Complete loss of murine Xin results in a mild cardiac phenotype with altered distribution of intercalated discs. Cardiovasc Res 85: 739-750
50. Pacholsky D, Vakeel P, Himmel M, Lowe T, Stradal T, Rottner K, Furst DO, van der Ven PF (2004) Xin repeats define a novel actinbinding motif. J Cell Sci 117: 5257-5268 (Pubitemid 39562488)
51. Percipalle P, Jonsson A, Nashchekin D, Karlsson C, Bergman T, Guialis A, Daneholt B (2002) Nuclear actin is associated with a specific subset of hnRNP A/B-type proteins. Nucleic Acids Res 30: 1725-1734 (Pubitemid 34679749)
52. Percipalle P, Raju CS, Fukuda N (2009) Actin-associated hnRNP proteins as transacting factors in the control of mRNAtransport and localization. RNA Biol 6: 171-174
53. Ramirez-Valle F, Braunstein S, Zavadil J, Formenti SC, Schneider RJ (2008) eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy. J Cell Biol 181: 293-307 (Pubitemid 351574554)
54. Rosenwald IB, Rhoads DB, Callanan LD, Isselbacher KJ, Schmidt EV (1993) Increased expression of eukaryotic translation initiation factors eIF-4E and eIF-2 alpha in response to growth induction by c-myc. Proc Natl Acad Sci USA 90: 6175-6178 (Pubitemid 23191477)
55. Shahbazian D, Parsyan A, Petroulakis E, Hershey J, Sonenberg N (2010a) eIF4B controls survival and proliferation and is regulated by proto-oncogenic signaling pathways. Cell Cycle 9: 4106-4109
56. Shahbazian D, Parsyan A, Petroulakis E, Hershey J, Sonenberg N (2010a) eIF4B controls survival and proliferation and is regulated by proto-oncogenic signaling pathways. Cell Cycle 9: 4106-4109 Shahbazian D, Parsyan A, Petroulakis E, Topisirovic I, Martineau Y, Gibbs BF, Svitkin Y, Sonenberg N (2010b) Control of cell survival and proliferation by mammalian eukaryotic initiation factor 4B. Mol Cell Biol 30: 1478-1485
57. Simon DN, Zastrow MS, Wilson KL (2010) Direct actin binding to Aand B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus 1: 264-272
58. Thomas NS, Burke LC, Bybee A, Linch DC (1991) The phosphorylation state of the retinoblastoma (RB) protein in G0/G1 is dependent on growth status. Oncogene 6: 317-322 (Pubitemid 21902679)
59. Thomas NS, Pizzey AR, Tiwari S, Williams CD, Yang J (1998) p130, p107, and pRb are differentially regulated in proliferating cells and during cell cycle arrest by alpha-interferon. J Biol Chem 273: 23659-23667 (Pubitemid 28435694)
60. Thomas NSB (2004) Cell cycle regulation. In Textbook of Malignant Haematology, Degos L, Griffin JD, Linch DC, Lowenberg B (eds), pp 33-63. London: Martin Dunitz
61. Valenzuela DM, Chaudhuri A, Maitra U (1982) Eukaryotic ribosomal subunit anti-association activity of calf liver is contained in a single polypeptide chain protein of Mr=25 500 (eukaryotic initiation factor 6). J Biol Chem 257: 7712-7719
62. van der Ven PF, Ehler E, Vakeel P, Eulitz S, Schenk JA, Milting H, Micheel B, Furst DO (2006) Unusual splicing events result in distinct Xin isoforms that associate differentially with filamin c and Mena/VASP. Exp Cell Res 312: 2154-2167 (Pubitemid 43850938)
63. van Leeuwen JE, Samelson LE (1999) T cell antigen-receptor signal transduction. Curr Opin Immunol 11: 242-248 (Pubitemid 29263950)
64. van Oers NS (1999) T cell receptor-mediated signs and signals governing T cell development. Semin Immunol 11: 227-237 (Pubitemid 29401497)
65. Vogel C, Marcotte EM (2008) Calculating absolute and relative protein abundance from mass spectrometry-based protein expression data. Nat Protoc 3: 1444-1451
66. Volta V, Ceci M, Emery B, Bachi A, Petfalski E, Tollervey D, Linder P, Marchisio PC, Piatti S, Biffo S (2005) Sen34p depletion blocks tRNA splicing in vivo and delays rRNA processing. Biochem Biophys Res Commun 337: 89-94 (Pubitemid 41393761)
67. Washburn MP, Wolters D, Yates 3rd JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247 (Pubitemid 32220565)
68. Will CL, Schneider C, Reed R, Luhrmann R (1999) Identification of both shared and distinct proteins in the major and minor spliceosomes. Science 284: 2003-2005 (Pubitemid 29309450)
69. Woods WG, Roloff JS, Lukens JN, Krivit W (1981) The occurrence of leukemia in patients with the Shwachman syndrome. J Pediatr 99: 425-428 (Pubitemid 11029943)
70. Zetterberg A (1996) Cell growth and cell cycle progression in mammalian cells. In Apoptosis and Cell Cycle Control in Cancer,, Thomas NSB (ed) pp 17-36. Oxford, UK: Bios Scientific Publishers Ltd
71. Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, Crabtree GR (1998) Rapid and phosphoinositol-dependent binding of the SWI/ SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95: 625-636 (Pubitemid 28544124)
72. Zheng B, Han M, Bernier M, Wen JK (2009) Nuclear actin and actin-binding proteins in the regulation of transcription and gene expression. FEBS J 276: 2669-2685
73. Zink D, Fischer AH, Nickerson JA (2004) Nuclear structure in cancer cells. Nat Rev 4: 677-687 (Pubitemid 39215066)