First evidence for substrate channeling between proline catabolic enzymes: A validation of domain fusion analysis for predicting protein-protein interactions

Journal of Biological Chemistry

Volumn 290, Issue 4, 2015, Pages 2225-2234

  Sanyal, Nikhilesh ^a   Arentson, Benjamin W ^a   Luo, Min ^c   Tanner, John J ^b,c   Becker, Donald F ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CARBOXYLATION; DISSOCIATION; PROTEINS; REACTION INTERMEDIATES; SUBSTRATES; SURFACE PLASMON RESONANCE;

DISSOCIATION CONSTANT; GRAM-NEGATIVE BACTERIA; MONOFUNCTIONAL ENZYMES; PROLINE DEHYDROGENASE; PROTEIN-PROTEIN INTERACTIONS; SUBSTRATE CHANNELINGS; THERMUS THERMOPHILUS; X RAY CRYSTAL STRUCTURES;

ENZYMES;

PROLINE DEHYDROGENASE; PYRROLINE 5 CARBOXYLATE DEHYDROGENASE; FLAVOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXYGEN; PROLINE; PROTEIN BINDING;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; ENZYME MECHANISM; ENZYME SUBSTRATE; NONHUMAN; PREDICTION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; STEADY STATE; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; THERMUS THERMOPHILUS; WILD TYPE; X RAY ANALYSIS; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MUTATION; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE;

NEGIBACTERIA; THERMUS THERMOPHILUS;

1-PYRROLINE-5-CARBOXYLATE DEHYDROGENASE; CATALYSIS; FLAVOPROTEINS; MODELS, MOLECULAR; MUTATION; NAD; OXYGEN; PROLINE; PROLINE OXIDASE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; SURFACE PLASMON RESONANCE; THERMUS THERMOPHILUS;

EID: 84921445381     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.625483     Document Type: Article

References (58)

1. Phang, J. M., Pandhare, J., and Liu, Y. (2008) The metabolism of proline as microenvironmental stress substrate. J. Nutr. 138, 2008S-2015S
2. Takagi, H. (2008) Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl. Microbiol. Biotechnol. 81, 211-223
3. Krishnan, N., Doster, A. R., Duhamel, G. E., and Becker, D. F. (2008) Characterization of a Helicobacter hepaticus putA mutant strain in host colonization and oxidative stress. Infect. Immun. 76, 3037-3044
4. Curtis, J., Shearer, G., and Kohl, D. H. (2004) Bacteriod proline catabolism affects N2 fixation rate of drought-stressed soybeans. Plant Physiol. 136, 3313-3318
5. Kohl, D. H., Schubert, K. R., Carter, M. B., Hagedorn, C. H., and Shearer, G. (1988) Proline metabolism in N2-fixing root nodules: Energy transfer and regulation of purine synthesis. Proc. Natl. Acad. Sci. U.S.A. 85, 2036-2040
6. Lamour, N., Rivière, L., Coustou, V., Coombs, G. H., Barrett, M. P., and Bringaud, F. (2005) Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. J. Biol. Chem. 280, 11902-11910
7. Tanner, J. J. (2008) Structural biology of proline catabolism. Amino Acids. 35, 719-730
8. Srivastava, D., Schuermann, J. P., White, T. A., Krishnan, N., Sanyal, N., Hura, G. L., Tan, A., Henzl, M. T., Becker, D. F., and Tanner, J. J. (2010) Crystal structure of the bifunctional proline utilization A flavoenzyme from Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S.A. 107, 2878-2883
9. Singh, H., Arentson, B. W., Becker, D. F., and Tanner, J. J. (2014) Structures of the PutA peripheral membrane flavoenzyme reveal a dynamic substrate-channeling tunnel and the quinone-binding site. Proc. Natl. Acad. Sci. U.S.A. 111, 3389-3394
10. Arentson, B. W., Luo, M., Pemberton, T. A., Tanner, J. J., and Becker, D. F. (2014) Kinetic and structural characterization of tunnel-perturbing mutants in Bradyrhizobium japonicum proline utilization A. Biochemistry 53, 5150-5161
11. Moxley, M. A., Sanyal, N., Krishnan, N., Tanner, J. J., and Becker, D. F. (2014) Evidence for hysteretic substrate channeling in the proline dehydrogenase and Delta1-pyrroline-5-carboxylate dehydrogenase coupled reaction of proline utilization A (PutA). J. Biol. Chem. 289, 3639-3651
12. Surber, M. W., and Maloy, S. (1998) The PutA protein of Salmonella typhimurium catalyzes the two steps of proline degradation via a leaky channel. Arch. Biochem. Biophys. 354, 281-287
13. Farrant, R. D., Walker, V., Mills, G. A., Mellor, J. M., and Langley, G. J. (2001) Pyridoxal phosphate de-activation by pyrroline-5-carboxylic acid. Increased risk of vitamin B6 deficiency and seizures in hyperprolinemia type II. J. Biol. Chem. 276, 15107-15116
14. Berney, M., Weimar, M. R., Heikal, A., and Cook, G. M. (2012) Regulation of proline metabolism in mycobacteria and its role in carbon metabolism under hypoxia. Mol. Microbiol. 84, 664-681
15. Bearne, S. L., and Wolfenden, R. (1995) Glutamate γ-semialdehyde as a natural transition state analogue inhibitor of Escherichia coli glucos-amine-6-phosphate synthase. Biochemistry 34, 11515-11520
16. Bearne, S. L., Hekmat, O., and Macdonnell, J. E. (2001) Inhibition of Escherichia coli CTP synthase by glutamate γ-semialdehyde and the role of the allosteric effector GTP in glutamine hydrolysis. Biochem. J. 356, 223-232
17. Thoden, J. B., Huang, X., Raushel, F. M., and Holden, H. M. (1999) The small subunit of carbamoyl phosphate synthetase: snapshots along the reaction pathway. Biochemistry 38, 16158-16166
18. Nishimura, A., Nasuno, R., and Takagi, H. (2012) The proline metabolism intermediate Delta1-pyrroline-5-carboxylate directly inhibits the mitochondrial respiration in budding yeast. FEBS Lett. 586, 2411-2416
19. Nomura, M., and Takagi, H. (2004) Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate. Proc. Natl. Acad. Sci. U.S.A. 101, 12616-12621
20. Maxwell, S. A., and Davis, G. E. (2000) Differential gene expression in p53-mediated apoptosis-resistant vs. apoptosis-sensitive tumor cell lines. Proc. Natl. Acad. Sci. U.S.A. 97, 13009-13014
21. Pang, S., and Curran, S. P. (2014) Adaptive capacity to bacterial diet modulates aging in C. elegans. Cell Metab. 19, 221-231
22. Pang, S., Lynn, D. A., Lo, J. Y., Paek, J., and Curran, S. P. (2014) SKN-1 and Nrf2 couples proline catabolism with lipid metabolism during nutrient deprivation. Nat. Commun. 5, 5048
23. Ekena, K., and Maloy, S. (1990) Regulation of proline utilization in Salmonella typhimurium: how do cells avoid a futile cycle? Mol. Gen. Genet. 220, 492-494
24. Moses, S., Sinner, T., Zaprasis, A., Stöveken, N., Hoffmann, T., Belitsky, B. R., Sonenshein, A. L., and Bremer, E. (2012) Proline utilization by Bacillus subtilis: uptake and catabolism. J. Bacteriol. 194, 745-758
25. Marcotte, E. M., Pellegrini, M., Ng, H. L., Rice, D. W., Yeates, T. O., and Eisenberg, D. (1999) Detecting protein function and protein-protein interactions from genome sequences. Science. 285, 751-753
26. Enright, A. J., Iliopoulos, I., Kyrpides, N. C., and Ouzounis, C. A. (1999) Protein interaction maps for complete genomes based on gene fusion events. Nature 402, 86-90
27. White, T. A., Krishnan, N., Becker, D. F., and Tanner, J. J. (2007) Structure and kinetics of monofunctional proline dehydrogenase from Thermus thermophilus. J. Biol. Chem. 282, 14316-14327
28. Inagaki, E., Ohshima, N., Takahashi, H., Kuroishi, C., Yokoyama, S., and Tahirov, T. H. (2006) Crystal structure of Thermus thermophilus δ1-pyr-roline- 5-carboxylate dehydrogenase. J. Mol. Biol. 362, 490-501
29. Lee, Y. H., Nadaraia, S., Gu, D., Becker, D. F., and Tanner, J. J. (2003) Structure of the proline dehydrogenase domain of the multifunctional PutA flavoprotein. Nat. Struct. Biol. 10, 109-114
30. Luo, M., Arentson, B. W., Srivastava, D., Becker, D. F., and Tanner, J. J. (2012) Crystal structures and kinetics of monofunctional proline dehydrogenase provide insight into substrate recognition and conformational changes associated with flavin reduction and product release. Biochemistry 51, 10099-10108
31. Pemberton, T. A., Srivastava, D., Sanyal, N., Henzl, M. T., Becker, D. F., and Tanner, J. J. (2014) Structural studies of yeast δ(1)-pyrroline-5-carboxylate dehydrogenase (ALDH4A1): active site flexibility and oligomeric state. Biochemistry 53, 1350-1359
32. Williams, I., and Frank, L. (1975) Improved chemical synthesis and enzymatic assay of delta-1-pyrroline-5-carboxylic acid. Anal. Biochem. 64, 85-97
33. Luo, M., Singh, R. K., and Tanner, J. J. (2013) Structural determinants of oligomerization of δ(1)-pyrroline-5-carboxylate dehydrogenase: identification of a hexamerization hot spot. J. Mol. Biol. 425, 3106-3120
34. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85
35. Michaelis, L., and Menten, M. L. (1913) Die Kinetik der Invertinwirkung. Biochim. Z. 49, 333-369
36. Michaelis, L., Menten, M. L., Johnson, K. A., and Goody, R. S. (2011) The original Michaelis constant: translation of the 1913 Michaelis-Menten paper. Biochemistry 50, 8264-8269
37. Meek, T. D., Garvey, E. P., and Santi, D. V. (1985) Purification and characterization of the bifunctional thymidylate synthetase-dihydrofolate reductase from methotrexate-resistant Leishmania tropica. Biochemistry 24, 678-686
38. Geck, M. K., and Kirsch, J. F. (1999) A novel, definitive test for substrate channeling illustrated with the aspartate aminotransferase/malate dehydrogenase system. Biochemistry 38, 8032-8037
39. Mezl, V. A., and Knox, W. E. (1976) Properties and analysis of a stable derivative of pyrroline-5-carboxylic acid for use in metabolic studies. Anal. Biochem. 74, 430-440
40. Baker, P., Carere, J., and Seah, S. Y. (2012) Substrate specificity, substrate channeling, and allostery in BphJ: an acylating aldehyde dehydrogenase associated with the pyruvate aldolase BphI. Biochemistry 51, 4558-4567
41. Zhang, M., White, T. A., Schuermann, J. P., Baban, B. A., Becker, D. F., and Tanner, J. J. (2004) Structures of the Escherichia coli PutA proline dehydrogenase domain in complex with competitive inhibitors. Biochemistry 43, 12539-12548
42. Ostrander, E. L., Larson, J. D., Schuermann, J. P., and Tanner, J. J. (2009) A conserved active site tyrosine residue of proline dehydrogenase helps enforce the preference for proline over hydroxyproline as the substrate. Biochemistry 48, 951-959
43. Huang, X., Holden, H. M., and Raushel, F. M. (2001) Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annu. Rev. Biochem. 70, 149-180
44. Srere, P. A., and Ovadi, J. (1990) Enzyme-enzyme interactions and their metabolic role. FEBS Lett. 268, 360-364
45. Ovadi, J. (1991) Physiological significance of metabolic channelling. J. Theor. Biol. 152, 1-22
46. Ishikawa, M., Tsuchiya, D., Oyama, T., Tsunaka, Y., and Morikawa, K. (2004) Structural basis for channelling mechanism of a fatty acid betaoxidation multienzyme complex. EMBO J. 23, 2745-2754
47. Meyer, F. M., Gerwig, J., Hammer, E., Herzberg, C., Commichau, F. M., Völker, U., and Stülke, J. (2011) Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metab. Eng. 13, 18-27
48. Rudolph, J., and Stubbe, J. (1995) Investigation of the mechanism of phosphoribosylamine transfer from glutamine phosphoribosylpyrophosphate amidotransferase to glycinamide ribonucleotide synthetase. Biochemistry 34, 2241-2250
49. Zhao, H., French, J. B., Fang, Y., and Benkovic, S. J. (2013) The purinosome, a multi-protein complex involved in the de novo biosynthesis of purines in humans. Chem. Commun. 49, 4444-4452
50. Yadid, I., Rudolph, J., Hlouchova, K., and Copley, S. D. (2013) Sequestration of a highly reactive intermediate in an evolving pathway for degradation of pentachlorophenol. Proc. Natl. Acad. Sci. U.S.A. 110, E2182-E2190
51. Perkins, J. R., Diboun, I., Dessailly, B. H., Lees, J. G., and Orengo, C. (2010) Transient protein-protein interactions: structural, functional, and network properties. Structure 18, 1233-1243
52. James, C. L., and Viola, R. E. (2002) Production and characterization of bifunctional enzymes. Substrate channeling in the aspartate pathway. Biochemistry 41, 3726-3731
53. Islam, M. M., Wallin, R., Wynn, R. M., Conway, M., Fujii, H., Mobley, J. A., Chuang, D. T., and Hutson, S. M. (2007) A novel branched-chain amino acid metabolon. Protein-protein interactions in a supramolecular complex. J. Biol. Chem. 282, 11893-11903
54. Monteoliva, M. I., Rizzi, Y. S., Cecchini, N. M., Hajirezaei, M. R., and Alvarez, M. E. (2014) Context of action of proline dehydrogenase (ProDH) in the Hypersensitive Response of Arabidopsis. BMC Plant Biol. 14, 21
55. Miller, G., Honig, A., Stein, H., Suzuki, N., Mittler, R., and Zilberstein, A. (2009) Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J. Biol. Chem. 284, 26482-26492
56. Liu, W., and Phang, J. M. (2012) Proline dehydrogenase (oxidase) in cancer. Biofactors. 38, 398-406
57. Nooren, I. M., and Thornton, J. M. (2003) Structural characterisation and functional significance of transient protein-protein interactions. J. Mol. Biol. 325, 991-1018
58. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797