Host-pathogen interaction profiling using self-assembling human protein arrays

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1920-1936

  Yu, Xiaobo ^a   Decker, Kimberly B ^b   Barker, Kristi ^a   Neunuebel, M Ramona ^b   Saul, Justin ^a   Graves, Morgan ^a   Westcott, Nathan ^c   Hang, Howard ^c   Labaer, Joshua ^a   Qiu, Ji ^a   Machner, Matthias P ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

AMPylation; interactome; LidA; nucleic acid programmable protein array (NAPPA); Rab1; SidM

Indexed keywords

ADENOSINE PHOSPHATE; BINDING PROTEIN; PROTEIN LIDA; PROTEIN SIDM; RAB PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; COMPLEMENTARY DNA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PRIMER DNA; PROTEIN; SIDM PROTEIN, LEGIONELLA PNEUMOPHILA;

ADENYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL VACUOLE; CLICK CHEMISTRY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VITRO STUDY; IN VIVO STUDY; LEGIONELLA PNEUMOPHILA; NONHUMAN; NUCLEIC ACID PROGRAMMABLE PROTEIN ARRAY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY; PLASMID; PROCEDURES; SPECIES DIFFERENCE;

LEGIONELLA PNEUMOPHILA;

BACTERIAL PROTEINS; DNA PRIMERS; DNA, COMPLEMENTARY; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEGIONELLA PNEUMOPHILA; MICROSCOPY, FLUORESCENCE; PLASMIDS; PROTEIN ARRAY ANALYSIS; PROTEINS; RAB GTP-BINDING PROTEINS; SPECIES SPECIFICITY;

EID: 84926512827     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5013015     Document Type: Article

References (64)

1. Ensminger, A. W.; Isberg, R. R. Legionella pneumophila Dot/Icm translocated substrates: A sum of parts Curr. Opin. Microbiol. 2009, 12 (1) 67-73
2. Hubber, A.; Roy, C. R. Modulation of host cell function by Legionella pneumophila type IV effectors Ann. Rev. Cell Dev. Biol. 2010, 26, 261-83
3. Vogel, J. P.; Isberg, R. R. Cell biology of Legionella pneumophila Curr. Opin. Microbiol. 1999, 2 (1) 30-4
4. Sherwood, R. K.; Roy, C. R. A rab-centric perspective of bacterial pathogen-occupied vacuoles Cell Host Microbe 2013, 14 (3) 256-68
5. Machner, M. P.; Chen, Y. Catch and release: Rab1 exploitation by Legionella pneumophila Cell. Logist. 2011, 1 (4) 133-138
6. Neunuebel, M. R.; Machner, M. P. The taming of a Rab GTPase by Legionella pneumophila Small GTPases 2012, 3 (1) 28-33
7. Machner, M. P.; Isberg, R. R. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila Dev. Cell 2006, 11 (1) 47-56
8. Murata, T.; Delprato, A.; Ingmundson, A.; Toomre, D. K.; Lambright, D. G.; Roy, C. R. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor Nat. Cell Biol. 2006, 8 (9) 971-7
9. Muller, M. P.; Peters, H.; Blumer, J.; Blankenfeldt, W.; Goody, R. S.; Itzen, A. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b Science 2010, 329 (5994) 946-9
10. Choy, A.; Dancourt, J.; Mugo, B.; OConnor, T. J.; Isberg, R. R.; Melia, T. J.; Roy, C. R. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation Science 2012, 338 (6110) 1072-6
11. Gaspar, A. H.; Machner, M. P. VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion Proc. Natl. Acad. Sci. U.S.A. 2014, 111 (12) 4560-5
12. Lomma, M.; Dervins-Ravault, D.; Rolando, M.; Nora, T.; Newton, H. J.; Sansom, F. M.; Sahr, T.; Gomez-Valero, L.; Jules, M.; Hartland, E. L.; Buchrieser, C. The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication Cell. Microbiol. 2010, 12 (9) 1272-91
13. Losick, V. P.; Haenssler, E.; Moy, M. Y.; Isberg, R. R. LnaB: A Legionella pneumophila activator of NF-kappaB Cell. Microbiol. 2010, 12 (8) 1083-97
14. Mukherjee, S.; Liu, X.; Arasaki, K.; McDonough, J.; Galan, J. E.; Roy, C. R. Modulation of Rab GTPase function by a protein phosphocholine transferase Nature 2011, 477 (7362) 103-6
15. Belyi, Y.; Tartakovskaya, D.; Tais, A.; Fitzke, E.; Tzivelekidis, T.; Jank, T.; Rospert, S.; Aktories, K. Elongation factor 1A is the target of growth inhibition in yeast caused by Legionella pneumophila glucosyltransferase Lgt1 J. Biol. Chem. 2012, 287 (31) 26029-37
16. Woolery, A. R.; Yu, X.; LaBaer, J.; Orth, K. AMPylation of Rho GTPases subverts multiple host signaling processes J. Biol. Chem. 2014, 289 (47) 32977-88
17. Ramachandran, N.; Hainsworth, E.; Bhullar, B.; Eisenstein, S.; Rosen, B.; Lau, A. Y.; Walter, J. C.; LaBaer, J. Self-assembling protein microarrays Science 2004, 305 (5680) 86-90
18. Carlson, E. D.; Gan, R.; Hodgman, C. E.; Jewett, M. C. Cell-free protein synthesis: applications come of age Biotechnol. Adv. 2012, 30 (5) 1185-94
19. Los, G. V.; Encell, L. P.; McDougall, M. G.; Hartzell, D. D.; Karassina, N.; Zimprich, C.; Wood, M. G.; Learish, R.; Ohana, R. F.; Urh, M.; Simpson, D.; Mendez, J.; Zimmerman, K.; Otto, P.; Vidugiris, G.; Zhu, J.; Darzins, A.; Klaubert, D. H.; Bulleit, R. F.; Wood, K. V. HaloTag: A novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 2008, 3 (6) 373-82
20. Yu, B.; Xiao, B.; Throop, A.; Song, L.; Moral, L.; Park, J.; Seiler, C. Y.; Fiacco, M.; Steel, J.; Hunter, P.; Saul, J.; Wang, J.; Qiu, J.; Pipas, J.; LaBaer, J. Exploration of panviral proteome: High-throughput cloning and functional implications in virus-host interactions Theranostics 2014, 4 (8) 808-822
21. Yu, X.; Woolery, A. R.; Luong, P.; Hao, Y. H.; Grammel, M.; Westcott, N.; Park, J.; Wang, J.; Bian, X.; Demirkan, G.; Hang, H. C.; Orth, K.; LaBaer, J. Click chemistry-based detection of global pathogen-host AMPylation on self-assembled human protein microarrays Mol. Cell. Proteomics 2014, 13 (11) 3164-76
22. Gabay, J. E.; Horwitz, M. A. Isolation and characterization of the cytoplasmic and outer membranes of the Legionnaires disease bacterium (Legionella pneumophila) J. Exp. Med. 1985, 161 (2) 409-22
23. Feeley, J. C.; Gibson, R. J.; Gorman, G. W.; Langford, N. C.; Rasheed, J. K.; Mackel, D. C.; Baine, W. B. Charcoal-yeast extract agar: Primary isolation medium for Legionella pneumophila J. Clin. Microbiol. 1979, 10 (4) 437-41
24. Berger, K. H.; Isberg, R. R. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila Mol. Microbiol. 1993, 7 (1) 7-19
25. Berger, K. H.; Isberg, R. R. Intracellular survival by Legionella MethodsCell Biol. 1994, 45, 247-59
26. Hutchison, C. A., III; Phillips, S.; Edgell, M. H.; Gillam, S.; Jahnke, P.; Smith, M. Mutagenesis at a specific position in a DNA sequence J. Biol. Chem. 1978, 253 (18) 6551-60
27. Berger, K. H.; Merriam, J. J.; Isberg, R. R. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene Mol. Microbiol. 1994, 14 (4) 809-22
28. Wang, J.; Barker, K.; Steel, J.; Park, J.; Saul, J.; Festa, F.; Wallstrom, G.; Yu, X.; Bian, X.; Anderson, K. S.; Figueroa, J. D.; LaBaer, J.; Qiu, J. A versatile protein microarray platform enabling antibody profiling against denatured proteins Proteomics Clin Appl. 2013, 7 (5-6) 378-83
29. Yu, X.; Wallstrom, G.; Magee, D. M.; Qiu, J.; Mendoza, D. E.; Wang, J.; Bian, X.; Graves, M.; LaBaer, J. Quantifying antibody binding on protein microarrays using microarray nonlinear calibration BioTechniques 2013, 54 (5) 257-64
30. Gibson, D. S.; Qiu, J.; Mendoza, E. A.; Barker, K.; Rooney, M. E.; LaBaer, J. Circulating and synovial antibody profiling of juvenile arthritis patients by nucleic acid programmable protein arrays Arthritis Res. Ther. 2012, 14 (2) R77
31. Neunuebel, M. R.; Chen, Y.; Gaspar, A. H.; Backlund, P. S., Jr.; Yergey, A.; Machner, M. P. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila Science 2011, 333 (6041) 453-6
32. Ramachandran, N.; Raphael, J. V.; Hainsworth, E.; Demirkan, G.; Fuentes, M. G.; Rolfs, A.; Hu, Y.; LaBaer, J. Next-generation high-density self-assembling functional protein arrays Nat. Methods 2008, 5 (6) 535-8
33. Montor, W. R.; Huang, J.; Hu, Y.; Hainsworth, E.; Lynch, S.; Kronish, J. W.; Ordonez, C. L.; Logvinenko, T.; Lory, S.; LaBaer, J. Genome-wide study of Pseudomonas aeruginosa outer membrane protein immunogenicity using self-assembling protein microarrays Infect. Immun. 2009, 77 (11) 4877-86
34. Joiner, K. A.; Fuhrman, S. A.; Miettinen, H. M.; Kasper, L. H.; Mellman, I. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts Science 1990, 249 (4969) 641-6
35. Abramoff, M. D.; Magalhaes, P. J.; Ram, S. J. Image processing with ImageJ Biophotonics Int. 2004, 11 (7) 36-42
36. Schoebel, S.; Cichy, A. L.; Goody, R. S.; Itzen, A. Protein LidA from Legionella is a Rab GTPase supereffector Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (44) 17945-50
37. Suh, H. Y.; Lee, D. W.; Lee, K. H.; Ku, B.; Choi, S. J.; Woo, J. S.; Kim, Y. G.; Oh, B. H. Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA EMBO J. 2010, 29 (2) 496-504
38. Cheng, W.; Yin, K.; Lu, D.; Li, B.; Zhu, D.; Chen, Y.; Zhang, H.; Xu, S.; Chai, J.; Gu, L. Structural insights into a unique Legionella pneumophila effector LidA recognizing both GDP and GTP bound Rab1 in their active state PLoS Pathog. 2012, 8 (3) e1002528
39. Yarbrough, M. L.; Li, Y.; Kinch, L. N.; Grishin, N. V.; Ball, H. L.; Orth, K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling Science 2009, 323 (5911) 269-72
40. Worby, C. A.; Mattoo, S.; Kruger, R. P.; Corbeil, L. B.; Koller, A.; Mendez, J. C.; Zekarias, B.; Lazar, C.; Dixon, J. E. The fic domain: regulation of cell signaling by adenylylation Mol. Cell 2009, 34 (1) 93-103
41. Xu, Y.; Carr, P. D.; Vasudevan, S. G.; Ollis, D. L. Structure of the adenylylation domain of E. coli glutamine synthetase adenylyl transferase: Evidence for gene duplication and evolution of a new active site J. Mol. Biol. 2010, 396 (3) 773-84
42. Kinch, L. N.; Yarbrough, M. L.; Orth, K.; Grishin, N. V. Fido, a novel AMPylation domain common to fic, doc, and AvrB PLoS One 2009, 4 (6) e5818
43. Yang, X.; Boehm, J. S.; Salehi-Ashtiani, K.; Hao, T.; Shen, Y.; Lubonja, R.; Thomas, S. R.; Alkan, O.; Bhimdi, T.; Green, T. M.; Johannessen, C. M.; Silver, S. J.; Nguyen, C.; Murray, R. R.; Hieronymus, H.; Balcha, D.; Fan, C.; Lin, C.; Ghamsari, L.; Vidal, M.; Hahn, W. C.; Hill, D. E.; Root, D. E. A public genome-scale lentiviral expression library of human ORFs Nat. Methods 2011, 8 (8) 659-61
44. Grammel, M.; Luong, P.; Orth, K.; Hang, H. C. A chemical reporter for protein AMPylation J. Am. Chem. Soc. 2011, 133 (43) 17103-5
45. Broncel, M.; Serwa, R. A.; Tate, E. W. A new chemical handle for protein AMPylation at the host-pathogen interface ChemBioChem 2012, 13 (2) 183-5
46. Ingmundson, A.; Delprato, A.; Lambright, D. G.; Roy, C. R. Legionella pneumophila proteins that regulate Rab1 membrane cycling Nature 2007, 450 (7168) 365-9
47. Kagan, J. C.; Stein, M. P.; Pypaert, M.; Roy, C. R. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle J. Exp. Med. 2004, 199 (9) 1201-11
48. Isberg, R. R.; OConnor, T. J.; Heidtman, M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells Nat. Rev. Microbiol. 2009, 7 (1) 13-24
49. Urwyler, S.; Nyfeler, Y.; Ragaz, C.; Lee, H.; Mueller, L. N.; Aebersold, R.; Hilbi, H. Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases Traffic 2009, 10 (1) 76-87
50. Wasmeier, C.; Romao, M.; Plowright, L.; Bennett, D. C.; Raposo, G.; Seabra, M. C. Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes J. Cell Biol. 2006, 175 (2) 271-81
51. Colicelli, J. Human RAS superfamily proteins and related GTPases Sci. STKE 2004, 2004 (250) RE13
52. Degtyar, E.; Zusman, T.; Ehrlich, M.; Segal, G. A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria Cell. Microbiol. 2009, 11 (8) 1219-35
53. Li, T.; Lu, Q.; Wang, G.; Xu, H.; Huang, H.; Cai, T.; Kan, B.; Ge, J.; Shao, F. SET-domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription EMBO Rep. 2013, 14 (8) 733-40
54. Derre, I.; Isberg, R. R. LidA, a translocated substrate of the Legionella pneumophila type IV secretion system, interferes with the early secretory pathway Infect. immun. 2005, 73 (7) 4370-80
55. English, A. R.; Voeltz, G. K. Rab10 GTPase regulates ER dynamics and morphology Nat. Cell Biol. 2013, 15 (2) 169-78
56. Ostrowski, M.; Carmo, N. B.; Krumeich, S.; Fanget, I.; Raposo, G.; Savina, A.; Moita, C. F.; Schauer, K.; Hume, A. N.; Freitas, R. P.; Goud, B.; Benaroch, P.; Hacohen, N.; Fukuda, M.; Desnos, C.; Seabra, M. C.; Darchen, F.; Amigorena, S.; Moita, L. F.; Thery, C. Rab27a and Rab27b control different steps of the exosome secretion pathway Nat. Cell Biol. 2010, 12 (1) 19-30; sup pp 1-13
57. Furuse, M.; Hirase, T.; Itoh, M.; Nagafuchi, A.; Yonemura, S.; Tsukita, S. Occludin: A novel integral membrane protein localizing at tight junctions J. Cell Biol. 1993, 123 (6 Pt. 2) 1777-88
58. Wu, Z.; Nybom, P.; Magnusson, K. E. Distinct effects of Vibrio cholerae haemagglutinin/protease on the structure and localization of the tight junction-associated proteins occludin and ZO-1 Cell. Microbiol. 2000, 2 (1) 11-7
59. Simonovic, I.; Rosenberg, J.; Koutsouris, A.; Hecht, G. Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions Cell. Microbiol. 2000, 2 (4) 305-15
60. Kubori, T.; Hyakutake, A.; Nagai, H. Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions Mol. Microbiol. 2008, 67 (6) 1307-19
61. Lu, W.; Du, J.; Stahl, M.; Tzivelekidis, T.; Belyi, Y.; Gerhardt, S.; Aktories, K.; Einsle, O. Structural basis of the action of glucosyltransferase Lgt1 from Legionella pneumophila J. Mol. Biol. 2010, 396 (2) 321-31
62. Ribet, D.; Cossart, P. Pathogen-mediated posttranslational modifications: A re-emerging field Cell 2010, 143 (5) 694-702
63. Salomon, D.; Orth, K. What pathogens have taught us about posttranslational modifications Cell Host Microbe 2013, 14 (3) 269-79
64. Saul, J.; Petritis, B.; Sau, S.; Rauf, F.; Gaskin, M.; Ober-Reynolds, B.; Mineyev, I.; Magee, M.; Chaput, J.; Qiu, J.; LaBaer, J. Development of a full-length human protein production pipeline Protein Sci. 2014, 23 (8) 1123-35