Polyamines: Emerging players in bacteria-host interactions

International Journal of Medical Microbiology

Volumn 303, Issue 8, 2013, Pages 484-491

  Di Martino, Maria Letizia ^a,b   Campilongo, Rosaria ^a   Casalino, Mariassunta ^b   Micheli, Gioacchino ^c   Colonna, Bianca ^a   Prosseda, Gianni ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c Istituto Di Biologia E Patologia Molecolari Rome   (Italy)

Author keywords

Bacterial evolution; Bacterial pathogens; Bacterial host interactions; Pathogenicity; Polyamines

Indexed keywords

POLYAMINE; SPERMIDINE;

ANTIBIOTIC RESISTANCE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM; BIOFILM; FLEA; FRANCISELLA TULARENSIS; HELICOBACTER PYLORI; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HYPERSENSITIVITY; IMMUNE RESPONSE; MAMMAL; NONHUMAN; POLYAMINE SYNTHESIS; PSEUDOMONAS AERUGINOSA; SALMONELLA TYPHIMURIUM; SHIGELLA; SHORT SURVEY; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS; TYPE III SECRETION SYSTEM; VIBRIO CHOLERAE; YERSINIA PESTIS;

BACTERIAL EVOLUTION; BACTERIAL PATHOGENS; BACTERIAL-HOST INTERACTIONS; PATHOGENICITY; POLYAMINES;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; HOST-PATHOGEN INTERACTIONS; HUMANS; POLYAMINES;

EID: 84887615895     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.06.008     Document Type: Short Survey

References (65)

1. Barbagallo M., Di Martino M.L., Marcocci L., Pietrangeli P., De Carolis E., Casalino M., Colonna B., Prosseda G. A new piece of the Shigella pathogenicity puzzle: spermidine accumulation by silencing of the speG gene. PLoS ONE 2011, 6:e27226.
2. Bliven K.A., Maurelli A.T. Antivirulence genes: insights into pathogen evolution through gene loss. Infect. Immun. 2012, 80:406-4070.
3. Casalino M., Latella M.C., Prosseda G., Ceccarini P., Grimont F., Colonna B. Molecular evolution of the lysine decarboxylase-defective phenotype in Shigella sonnei. Int. J. Med. Microbiol. 2005, 294:503-512.
4. Casalino M., Prosseda G., Barbagallo M., Iacobino A., Ceccarini P., Latella M.C., Nicoletti M., Colonna B. Interference of the CadC regulator in the arginine-dependent acid resistance system of Shigella and enteroinvasive E. coli. Int. J. Med. Microbiol. 2010, 300:289-295.
5. Carlson P.E., Horzempa J., O'Dee D.M., Robinson C.M., Neophytou P., Labrinidis A., Nau G.J. Global transcriptional response to spermine, a component of the intramacrophage environment, reveals regulation of Francisella gene expression through insertion sequence elements. J. Bacteriol. 2009, 191:6855-6864.
6. Chambers H.F., Deleo F.R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009, 7:629-641.
7. Chan Y.Y., Chua K.L. Growth-related changes in intracellular spermidine and its effect on efflux pump expression and quorum sensing in Burkholderia pseudomallei. Microbiology 2010, 156:1144-1154.
8. Chaturvedi R., Cheng Y., Asim M., Bussière F.I., Xu H., Gobert A.P., Hacker A., Casero R.A., Wilson K.T. Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J. Biol. Chem. 2004, 279:40161-40173.
9. Chaturvedi R., Asim M., Hoge S., Lewis N.D., Singh K., Barry D.P., de Sablet T., Piazuelo M.B., Sarvaria A.R., Cheng Y., Closs E.I., Casero R.A., Gobert A.P., Wilson K.T. Polyamines Impair Immunity to Helicobacter pylori by Inhibiting l-Arginine Uptake Required for Nitric Oxide Production. Gastroenterology 2010, 139:1686-1698.
10. Chaturvedi R., Asim M., Romero-Gallo J., Barry D.P., Hoge S., de Sablet T., Delgado A.G., Wroblewski L.E., Piazuelo M.B., Yan F., Israel D.A., Casero R.A., Correa P., Gobert A.P., Polk D.B., Peek R.M., Wilson K.T. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 2011, 141:1696-1708.
11. Day W.A., Fernández R.E., Maurelli A.T. Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect. Immun. 2001, 69:7471-7480.
12. Diep B.A., Gill S.R., Chang R.F., Phan T.H., Chen J.H., Davidson M.G., et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367:731-739.
13. Diep B.A., Stone G.G., Basuino L., Graber C.J., Miller A., des Etages S.A., et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of viruelnce and resistance in the USA300 clone of methicillin-resitant Staphylococcus aureus. J. Infect. Dis. 2008, 197:1523-1530.
14. Driscoll J.A., Brody S.L., Kollef M.H. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 2007, 67:351-368.
15. Durand J.M., Björk G.R. Putrescine or a combination of methionine and arginine restores virulence gene expression in a tRNA modification-deficient mutant of Shigella flexneri: a possible role in adaptation of virulence. Mol. Microbiol. 2003, 47:519-527.
16. Durand J.M., Björk G.R. Metabolic control through ornithine and uracil of epithelial cell invasion by Shigella flexneri. Microbiology 2009, 155:2498-2508.
17. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J.C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 2003, 47:103-118.
18. Falconi M., Prosseda G., Giangrossi M., Beghetto E., Colonna B. Involvement of FIS in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli. Mol. Microbiol. 2001, 42:439-452.
19. Faruque S.M., Biswas K., Udden S.M., Ahmad Q.S., Sack D.A., Nair G.B., Mekalanos J.J. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:6350-6355.
20. Giangrossi M., Prosseda G., Tran C.N., Brandi A., Colonna B., Falconi M. A novel antisense RNA regulates at transcriptional level the virulence gene icsA of Shigella flexneri. Nucleic Acids Res. 2010, 38:3362-3375.
21. Griffiths G.L., Sigel S.P., Payne S.M., Neilands J.B. Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 1984, 259:383-385.
22. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M.L., Lucchini S., et al. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 2008, 10:958-984.
23. Hinnebusch B.J., Perry R.D., Schwan T.G. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 1996, 273:367-370.
24. Hinnebusch B.J., Erickson D.L. Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr. Top. Microbiol. Immunol. 2008, 322:229-248.
25. Ibarra J.A., Steele-Mortimer O. Salmonella - the ultimate insider, Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 2009, 11:1579-1586.
26. Igarashi K., Kashiwagi K. Modulation of cellular function by polyamines. Int. J. Biochem. Cell. Biol. 2010, 42:39-51.
27. Igarashi K., Kashiwagi K. Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol. Biochem. 2010, 48:506-512.
28. Jelsback L., Thomsen L.E., Wallrodt I., Jensen P.R., Olsen J.E. Polyamines are required for virulence in Salmonella enterica serovar Typhimurium. PLoS ONE 2012, 7:e36149.
29. Joshi G.S., Spontak J.S., Klapper D.G., Richardson A.R. ACME encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines. Mol. Microbiol. 2011, 82:9-20.
30. Kadioglu A., Weiser J., Paton J.C., Andrew P.W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 2008, 6:288-301.
31. Karatan E., Duncan T.R., Watnick P.L. NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by non spermidine. J. Bacteriol. 2005, 187:7434-7443.
32. Keseler I.M., Collado-Vides J., Santos-Zavaleta A., Peralta-Gil M., Gama-Castro S., Muniz-Rascado L., Bonavides-Martinez C., Paley S., Krummenacker M., Altman T., Kaipa P., Spaulding A., Pacheco J., Latendresse M., Fulcher C., Sarker M., Shearer A.G., Mackie A., Paulsen I., Gunsalus R.P., Karp P.D. EcoCyc: a comprehensive database of Escherichia coli biology. Nucleic Acids Res. 2011, 39:D583-D590.
33. Kharat A.S., Tomasz A. Drastic reduction in the virulence of Streptococcus pneumoniae expressing type2 capsular polysaccharide but lacking choline residues in the cell wall. Mol. Microbiol. 2006, 60:93-107.
34. Lee J., Sperandio V., Frantz D.E., Longgood J., Camilli A., Phillips M.A., Michael A.J. An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J. Biol. Chem. 2009, 284:9899-9907.
35. Lu C.D., Itoh Y., Nakada Y., Jiang Y. Functional analysis and regulation of the divergent spuABCDEFGH-spuI operons for polyamine uptake and utilization in Pseudomonas aeruginosa PAO1. J. Bacteriol. 2002, 184:3765-3773.
36. Maurelli A.T., Fernandez R.E., Bloch C.A., Rode C.K., Fasano A. Black holes" and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3943-3948.
37. McGinnis M.W., Parker Z.M., Walter N.E., Rutkovsky A.C., Cartaya-Marin C., Karatan E. Spermidine regulates Vibrio cholerae biofilm formation via transport and signaling pathways. FEMS Microbiol. Lett. 2009, 299:166-174.
38. McLendon M.K., Apicella M.A., Allen L.A. Francisella tularensis: taxonomy, genetics, and immunopathogenesis of a potential agent of biowarfare. Annu. Rev. Microbiol. 2006, 60:167-185.
39. Nasrallah G.K., Riveroll A.L., Chong A., Murray L.E., Lewis P.J., Garduño R.A. Legionella pneumophila requires polyamines for optimal intracellular growth. J. Bacteriol. 2011, 193:4346-4360.
40. Parker Z.M., Pendergraft S.S., Sobieraj J., McGinnis M.M., Karatan E. Elevated levels of the norspermidine synthesis enzyme NspC enhance Vibrio cholerae biofilm formation without affecting intracellular nor spermidine concentrations. FEMS Microbiol. Lett. 2012, 329:18-27.
41. Parsot C. Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiol. Lett. 2005, 252:11-18.
42. Patel N.C., Wortham B.W., Lines J.L., Fetherston J.D., Perry R.D., Oliveira M.A. Polyamines are essential for the formation of the plague biofilm. J. Bacteriol. 2006, 188:2355-2363.
43. Polissi A., Pontiggia A., Feger G., Altieri M., Motti H., Ferrari L., Simon D. Large scale identification of virulence genes from Streptococcus pneumoniae. Infect. Immun. 1998, 66:5620-5629.
44. Prosseda G., Falconi M., Nicoletti M., Casalino M., Micheli G., Colonna B. Histone-like protein and Shigella invasivity regulon. Res. Microbiol. 2002, 153:461-468.
45. Prosseda G., Falconi M., Giangrossi M., Gualerzi C.O., Micheli G., Colonna B. The virF promoter in Shigella: more than just a curved DNA stretch. Mol. Microbiol. 2004, 51:523-537.
46. Prosseda G., Latella M.C., Barbagallo M., Nicoletti M., Al Kassas R., Casalino M., Colonna B. The two-faced role of cad genes in the virulence of pathogenic Escherichia coli. Res. Microbiol. 2007, 158:487-493.
47. Prosseda G., Di Martino M.L., Campilongo R., Fioravanti R., Micheli G., Casalino M., Colonna B. Shedding of genes that interfere with the pathogenic lifestyle: the Shigella model. Res. Microbiol. 2012, 163:399-406.
48. Romero P., Wagg J., Green M.L., Kaiser D., Krummenacker M., Karp P.D. Computational prediction of human metabolic pathways from the complete human genome. Genome Biol. 2004, 6:R2.1-R2.17.
49. Russo B.C., Horzempa J., O'Dee D.M., Schmitt D.M., Brown M.J., Carlson P.E., Xavier R.J., Nau G.J. A Francisella tularensis locus required for spermine responsiveness is necessary for virulence. Infect. Immun. 2011, 79:3665-3676.
50. Sansonetti P.J. Shigellosis: an old disease in new clothes?. PLoS Med. 2006, 3:e354.
51. Shah P., Swiatlo E. Immunization with polyamine transport protein PotD protects mice against systemic infection with Streptococcus pneumoniae. Infect. Immun. 2006, 74:5888-5892.
52. Shah P., Swiatlo E. A multifacet role for polyamines in bacterial pathogens. Mol. Microbiol. 2008, 68:4-16.
53. Shah P., Romero D.G., Swiatlo E. Role of polyamine transport in Streptococcus pneumoniae response to physiological stress and murine septicaemia. Microb. Pathog. 2008, 45:167-172.
54. Shah P., Nanduri B., Swiatlo E., Ma Y., Pendarvis K. Polyamine biosynthesis and transport mechanisms are crucial for fitness and pathogenesis of Streptococcus pneumoniae. Microbiology 2011, 157:504-515.
55. Tabor C.W., Tabor H. Polyamines in microorganisms. Microbiol. Rev. 1985, 49:81-99.
56. Thurlow L.R., Josh G.S., Clark J.R., Spontak J.S., Neely C.J., Maile R., Richardson A.R. Functional modularity of the arginine catabolic mobile element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus. Cell Host Microbe 2013, 13:100-107.
57. Tran C.N., Giangrossi M., Prosseda G., Brandi A., Di Martino M.L., Colonna B., Falconi M. A multifactor regulatory circuit involving H-NS, VirF and an antisense RNA modulates transcription of the virulence gene icsA of Shigella flexneri. Nucleic Acids Res. 2011, 39:8122-8134.
58. Ware D., Jiang Y., Lin W., Swiatlo E. Involvement of potD in Streptococcus pneumoniae polyamine transport and pathogenesis. Infect. Immun. 2006, 74:352-361.
59. Wortham B.W., Oliveira M.A., Fetherston J.D., Perry R.D. Polyamines are required for the expression of key Hms proteins important for Yersinia pestis biofilm formation. Environ. Microbiol. 2010, 12:2034-2047.
60. Wu D., Lim S.C., Dong Y., Wu J., Tao F., Zhou L., Zhang L.H., Song H. Structural basis of substrate binding specificity revealed by the crystal structures of polyamine receptors SpuD and SpuE from Pseudomonas aeruginosa. J. Mol. Biol. 2012, 416:697-712.
61. Xu H., Chaturvedi R., Cheng Y., Bussiere F.I., Asim M., Yao M.D., Potosky D., Meltzer S.J., Rhee J.G., Kim S.S., Moss S.F., Hacker A., Wang Y., Casero R.A., Wilson K.T. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res. 2004, 1:8521-8525.
62. Yahr T.L., Wolfang M.C. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 2006, 62:631-640.
63. Yan F., Cao H., Chaturvedi R., Krishna U., Hobbs S.S., Dempsey P.J., Peek R.M., Cover T.L., Washington M.K., Wilson K.T., Polk D.B. Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pylori-induced apoptosis. Gastroenterology 2009, 136:1297-1307.
64. Yoshida M., Kashiwagi K., Shigemasa A., Taniguchi S., Yamamoto K., Makinoshima H., Ishihama A., Igarashi K. A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J. Biol. Chem. 2004, 279:46008-46013.
65. Zhou L., Wang J., Zhang L.H. Modulation of bacterial typeIII secretion system by a spermidine transporter dependent signalling pathway. PLoS ONE 2007, 2:e1291.