A novel putrescine exporter SapBCDF of Escherichia coli

Journal of Biological Chemistry

Volumn 291, Issue 51, 2016, Pages 26343-26351

  Sugiyama, Yuta ^a   Nakamura, Atsuo ^b   Matsumoto, Mitsuharu ^b   Kanbe, Ayaka ^c   Sakanaka, Mikiyasu ^a   Higashi, Kyohei ^d   Igarashi, Kazuei ^d   Katayama, Takane ^a,e   Suzuki, Hideyuki ^c   Kurihara, Shin ^a  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^b Nishitama gun   (Japan)

^c KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

^d CHIBA UNIVERSITY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; AMINO ACIDS; GENES; ISOTOPES; PEPTIDES; POLYPEPTIDES; SALMONELLA;

ANTIMICROBIAL PEPTIDE; CULTURE SUPERNATANT; HAEMOPHILUS INFLUENZAE; INTESTINAL BACTERIA; NATURAL FUNCTIONS; NEUTRAL CONDITIONS; RECENT RESEARCHES; SALMONELLA ENTERICA;

ESCHERICHIA COLI;

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; PUTRESCINE; ABC TRANSPORTER; ANTIMICROBIAL CATIONIC PEPTIDE; ANTIPORTER; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; POTE PROTEIN, E COLI; SAPD PROTEIN, E COLI;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; GENE INACTIVATION; HAEMOPHILUS INFLUENZAE; ISOTOPE LABELING; LIMIT OF QUANTITATION; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SAPBCDF GENE; ACTIVE TRANSPORT; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

ANTIMICROBIAL CATIONIC PEPTIDES; ANTIPORTERS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; PUTRESCINE;

EID: 85006314357     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.762450     Document Type: Article

References (46)

1. Tabor, C. W., and Tabor, H. (1985) Polyamines in microorganisms. Microbiol. Rev. 49, 81-99
2. Wortham, B. W., Patel, C. N., and Oliveira, M. A. (2007) Polyamines in bacteria: pleiotropic effects yet specific mechanisms. Adv. Exp. Med. Biol. 603, 106-115
3. Pegg, A. E. (2009) Mammalian polyamine metabolism and function. IUBMB Life 61, 880-894
4. Tiburcio, A. F., Altabella, T., Bitrián, M., and Alcázar, R. (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 1-18
5. Babbar, N., and Gerner, E. W. (2011) Targeting polyamines and inflammation for cancer prevention. Recent Results Cancer Res. 188, 49-64
6. Igarashi, K., and Kashiwagi, K. (2000) Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 271, 559-564
7. Matsumoto, M., Kibe, R., Ooga, T., Aiba, Y., Kurihara, S., Sawaki, E., Koga, Y., and Benno, Y. (2012) Impact of intestinal microbiota on intestinal luminal metabolome. Sci. Rep. 2, 233
8. Goodwin, A. C., Destefano Shields, C. E., Wu, S., Huso, D. L., Wu, X., Murray-Stewart, T. R., Hacker-Prietz, A., Rabizadeh, S., Woster, P. M., Sears, C. L., and Casero, R. A., Jr. (2011) Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 15354-15359
9. Thompson, P. A., Wertheim, B. C., Zell, J. A., Chen, W. P., McLaren, C. E., LaFleur, B. J., Meyskens, F. L., and Gerner, E. W. (2010) Levels of rectal mucosal polyamines and prostaglandin E2 predict ability of DFMO and sulindac to prevent colorectal adenoma. Gastroenterology 139, 797-805
10. Dubin, K., Callahan, M. K., Ren, B., Khanin, R., Viale, A., Ling, L., No, D., Gobourne, A., Littmann, E., Huttenhower, C., Pamer, E. G., and Wolchok, J. D. (2016) Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat. Commun. 7, 10391
11. Matsumoto, M., Kurihara, S., Kibe, R., Ashida, H., and Benno, Y. (2011) Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLoS ONE 6, e23652
12. Kibe, R., Kurihara, S., Sakai, Y., Suzuki, H., Ooga, T., Sawaki, E., Muramatsu, K., Nakamura, A., Yamashita, A., Kitada, Y., Kakeyama, M., Benno, Y., and Matsumoto, M. (2014) Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice. Sci. Rep. 4, 4548
13. Soda, K., Dobashi, Y., Kano, Y., Tsujinaka, S., and Konishi, F. (2009) Polyamine- rich food decreases age-associated pathology and mortality in aged mice. Exp. Gerontol. 44, 727-732
14. Pistocchi, R., Kashiwagi, K., Miyamoto, S., Nukui, E., Sadakata, Y., Kobayashi, H., and Igarashi, K. (1993) Characteristics of the operon for a putrescine transport system that maps at 19 minutes on the Escherichia coli chromosome. J. Biol. Chem. 268, 146-152
15. Furuchi, T., Kashiwagi, K., Kobayashi, H., and Igarashi, K. (1991) Characteristics of the gene for a spermidine and putrescine transport system that maps at 15 min on the Escherichia coli chromosome. J. Biol. Chem. 266, 20928-20933
16. Kurihara, S., Tsuboi, Y., Oda, S., Kim, H. G., Kumagai, H., and Suzuki, H. (2009) The putrescine importer PuuP of Escherichia coli K-12. J. Bacteriol. 191, 2776-2782
17. Kurihara, S., Sakai, Y., Suzuki, H., Muth, A., Phanstiel, O., 4th, and Rather, P. N. (2013) Putrescine importer PlaP contributes to swarming motility and urothelial cell invasion in Proteus mirabilis. J. Biol. Chem. 288, 15668-15676
18. Kashiwagi, K., Miyamoto, S., Suzuki, F., Kobayashi, H., and Igarashi, K. (1992) Excretion of putrescine by the putrescine-ornithine antiporter encoded by the potE gene of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 89, 4529-4533
19. Kashiwagi, K., Shibuya, S., Tomitori, H., Kuraishi, A., and Igarashi, K. (1997) Excretion and uptake of putrescine by the PotE protein in Escherichia coli. J. Biol. Chem. 272, 6318-6323
20. Kashiwagi, K., Suzuki, T., Suzuki, F., Furuchi, T., Kobayashi, H., and Igarashi, K. (1991) Coexistence of the genes for putrescine transport protein and ornithine decarboxylase at 16 min on Escherichia coli chromosome. J. Biol. Chem. 266, 20922-20927
21. Schiller, D., Kruse, D., Kneifel, H., Krämer, R., and Burkovski, A. (2000) Polyamine transport and role of potE in response to osmotic stress in Escherichia coli. J. Bacteriol. 182, 6247-6249
22. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 0008
23. Parra-Lopez, C., Baer, M. T., and Groisman, E. A. (1993) Molecular genetic analysis of a locus required for resistance to antimicrobial peptides in Salmonella typhimurium. EMBO J. 12, 4053-4062
24. Mason, K. M., Munson, R. S., Jr, and Bakaletz, L. O. (2005) A mutation in the sap operon attenuates survival of nontypeable Haemophilus influenzae in a chinchilla model of otitis media. Infect. Immun. 73, 599-608
25. Higashi, K., Ishigure, H., Demizu, R., Uemura, T., Nishino, K., Yamaguchi, A., Kashiwagi, K., and Igarashi, K. (2008) Identification of a spermidine excretion protein complex (MdtJI) in Escherichia coli. J. Bacteriol. 190, 872-878
26. Woolridge, D. P., Vazquez-Laslop, N., Markham, P. N., Chevalier, M. S., Gerner, E. W., and Neyfakh, A. A. (1997) Efflux of the natural polyamine spermidine facilitated by the Bacillus subtilis multidrug transporter Blt. J. Biol. Chem. 272, 8864-8866
27. Leuzzi, A., Di Martino, M. L., Campilongo, R., Falconi, M., Barbagallo, M., Marcocci, L., Pietrangeli, P., Casalino, M., Grossi, M., Micheli, G., Colonna, B., and Prosseda, G. (2015) Multifactor regulation of the MdtJI polyamine transporter in Shigella. PLoS ONE 10, e0136744
28. Sasahara, A., Nanatani, K., Enomoto, M., Kuwahara, S., and Abe, K. (2011) Substrate specificity of the aspartate:alanine antiporter (AspT) of Tetragenococcus halophilus in reconstituted liposomes. J. Biol. Chem. 286, 29044-29052
29. Pathania, A., and Sardesai, A. A. (2015) Distinct paths for basic amino acid export in Escherichia coli: YbjE (LysO) mediates export of L-lysine. J. Bacteriol. 197, 2036-2047
30. Shelton, C. L., Raffel, F. K., Beatty, W. L., Johnson, S. M., and Mason, K. M. (2011) Sap transporter mediated import and subsequent degradation of antimicrobial peptides in Haemophilus. PLoS Pathog. 7, e1002360
31. Harms, C., Domoto, Y., Celik, C., Rahe, E., Stumpe, S., Schmid, R., Nakamura, T., and Bakker, E. P. (2001) Identification of the ABC protein SapD as the subunit that confers ATP dependence to the K+-uptake systems Trk(H) and Trk(G) from Escherichia coli K-12. Microbiology 147, 2991-3003
32. Mason, K. M., Bruggeman, M. E., Munson, R. S., and Bakaletz, L. O. (2006) The non-typeable Haemophilus influenzae Sap transporter provides a mechanism of antimicrobial peptide resistance and SapD-dependent potassium acquisition. Mol. Microbiol. 62, 1357-1372
33. Liu, K., Fu, H., Bei, Q., and Luan, S. (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124, 1315-1326
34. Lopatin, A. N., Makhina, E. N., and Nichols, C. G. (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372, 366-369
35. Vandenberg, C. A. (2008) Integrins step up the pace of cell migration through polyamines and potassium channels. Proc. Natl. Acad. Sci. U.S.A. 105, 7109-7110
36. Kurihara, S., Oda, S., Kato, K., Kim, H. G., Koyanagi, T., Kumagai, H., and Suzuki, H. (2005) A novel putrescine utilization pathway involves γ-glutamylated intermediates of Escherichia coli K-12. J. Biol. Chem. 280, 4602-4608
37. Kurihara, S., Oda, S., Kumagai, H., and Suzuki, H. (2006) γ-Glutamyl-γ- aminobutyrate hydrolase in the putrescine utilization pathway of Escherichia coli K-12. FEMS Microbiol. Lett. 256, 318-323
38. Kurihara, S., Oda, S., Tsuboi, Y., Kim, H. G., Oshida, M., Kumagai, H., and Suzuki, H. (2008) γ-Glutamylputrescine synthetase in the putrescine utilization pathway of Escherichia coli K-12. J. Biol. Chem. 283, 19981-19990
39. Kurihara, S., Kato, K., Asada, K., Kumagai, H., and Suzuki, H. (2010) A putrescine-inducible pathway comprising PuuE-YneI in which γ-ami-nobutyrate is degraded into succinate in Escherichia coli K-12. J. Bacteriol. 192, 4582-4591
40. Nemoto, N., Kurihara, S., Kitahara, Y., Asada, K., Kato, K., and Suzuki, H. (2012) Mechanism for regulation of the putrescine utilization pathway by the transcription factor PuuR in Escherichia coli K-12. J. Bacteriol. 194, 3437-3447
41. Miller, J. H. (1972) A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Bacteria, pp. 263-274 and 437, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
42. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
43. Harwig, S. S., Ganz, T., and Lehrer, R. I. (1994) Neutrophil defensins: purification, characterization, and antimicrobial testing. Methods Enzymol. 236, 160-172
44. Sakanaka, M., Sugiyama, Y., Kitakata, A., Katayama, T., and Kurihara, S. (2016) Carboxyspermidine decarboxylase of the prominent intestinal microbiota species Bacteroides thetaiotaomicron is required for spermidine biosynthesis and contributes to normal growth. Amino Acids 48, 2443-2451
45. Chen, G. G., Turecki, G., and Mamer, O. A. (2009) A quantitative GC-MS method for three major polyamines in postmortem brain cortex. J. Mass Spectrom. 44, 1203-1210
46. Grenier, F., Matteau, D., Baby, V., and Rodrigue, S. (2014) Complete genome sequence of Escherichia coli BW25113. Genome Announc. 2, e01038