Ten years of subproteome investigations in lactic acid bacteria: A key for food starter and probiotic typing

Journal of Proteomics

Volumn 127, Issue , 2015, Pages 332-339

  Mangiapane, E ^a   Mazzoli, R ^a   Pessione, A ^a   Svensson, B ^b   Riedel, K ^c   Pessione, E ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

2DE; Adhesion; Biogenic amines; Food bacteria; Moonlighting proteins; Subproteomes

Indexed keywords

BIOGENIC AMINE; CRYOPROTECTIVE AGENT; EXTRACELLULAR PROTEOME; NUTRACEUTICAL; PROBIOTIC AGENT; PROTEOME; SELENIUM; SUBPROTEOME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LACTIC ACID;

BACTERIAL STRAIN; DIET SUPPLEMENTATION; ECOLOGICAL NICHE; FOOD; FREEZE DRYING; GEL ELECTROPHORESIS; LACTIC ACID BACTERIUM; METABOLISM; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEOMICS; REVIEW; RISK; SURVIVAL; TWO DIMENSIONAL FLUORESCENCE DIFFERENCE GEL ELECTROPHORESIS; BACTERIUM; HUMAN; MICROBIAL VIABILITY; PROCEDURES;

BACTERIA; BACTERIAL PROTEINS; FREEZE DRYING; HUMANS; LACTIC ACID; MICROBIAL VIABILITY; PROTEOME; PROTEOMICS;

EID: 84944153504     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.04.028     Document Type: Review

References (98)

1. Perin L.M., Miranda R.O., Todorov S.D., Franco B.D., Nero L.A. Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterocci isolated from goat milk. Int J Food Microbiol 2014, 185:121-126.
2. Schindler B.K., Bruns S., Lach G. Biogenic amines - a possible source for nicotine in mushrooms? A discussion of published literature data. Food Chem 2015, 171:379-381.
3. Fernandez de Palencia P., Fernandez M., Mohedano M.L., Ladero V., Quevedo C., Alvarez M.A., et al. Role of tyramine synthesis by food-borne Enterococcus durans in adaptation to the gastrointestinal tract environment. Appl Environ Microbiol 2011, 77:699-702.
4. Meisel H. Overview on milk protein-derived peptides. Int Dairy J 1998, 8:363-373.
5. Pigeon R.M., Cuesta E.P., Gililliand S.E. Binding of free bile acids by cells of yogurt starter culture bacteria. J Dairy Sci 2002, 85:2705-2710.
6. Pessi T., Sütas Y., Hurme M., Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 2000, 30:1804-1808.
7. Karimi K., Inman M.D., Bienenstock J., Forsythe P. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med 2009, 179:186-193.
8. Cho Y.R., Chang J.Y., Chang H.C. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol 2007, 17:104-109.
9. Mazzoli R. Neuro-active compounds produced by probiotics. Interactive Probiotics 2014, 148-176. CRC press, Boca Raton. E. Pessione (Ed.).
10. Lamberti C., Genovese F., Coisson J.D., Lo Bianco G., Cocolin L.S., Pessione E. Anti-S. aureus and anti-L. monocytogenes molecules produced by cheese-isolated lab. Czech J Food Sci 2014, 32:54-60.
11. Raman M., Ambalam P., Kondepudi K.K., Pithva S., Kothari C., Patel A.T., et al. Potential of probiotics, prebiotics and synbiotics for management of colorectal cancer. Gut Microbes 2013, 4(3):181-192.
12. Lamberti C., Mangiapane E., Pessione A., Mazzoli R., Giunta C., Pessione E. Proteomic characterization of a selenium-metabolizing probiotic Lactobacillus reuteri Lb2 BM for nutraceutical applications. Proteomics 2011, 11:2212-2221.
13. Mangiapane E., Lamberti C., Pessione A., Galano E., Amoresano A., Pessione E. Selenium effects on the metabolism of a Se-metabolizing Lactobacillus reuteri: analysis of envelope-enriched and extracellular proteomes. Mol Biosyst 2014, 10(6):1272-1280.
14. Wall R., Cryan J.F., Ross R.P., Fitzgerald G.F., Dinan T.G., Stanton C. Bacterial neuroactive compounds produced by psychobiotics. Adv Exp Med Biol 2014, 817:221-239.
15. Song S., Bae D.W., Lim K., Griffiths M.W., Oh S. Cold stress improves the ability of Lactobacillus plantarum L67 to survive to freezing. Int J Food Microbiol 2014, 191C:135-143.
16. Velly H., Bouix M., Passot S., Penicaud C., Beinsteiner H., Ghorbal S., et al. Cyclopropanation of unsaturated fatty acids and membrane rigidification improve the freeze-drying resistance of Lactococcus lactis subsp. lactis TOMSC161. Appl Microbiol Biotechnol 2015, 99:907-918.
17. Cecconi D., Milli A., Rinalducci S., Zolla L., Zapparoli G. Proteomic analysis of Oenococcus oeni freeze-dried cultures in order to assess the importance of cell acclimatation to conduct malo-lactic fermentation in wine. Electrophoresis 2009, 30:2988-2995.
18. Pessione A., Lamberti C., Pessione E. Proteomics as a tool to study biogenic amine production. Mol Biosyst 2010, 6(8):1419-1430.
19. O'Connel Motherway M., Zomer A., Leahy S.C., Reunanen J., Bottacini F., Claesson M.J., et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. PNAS 2011, 108(27):11217-11222.
20. Sanchez B., Ruiz L., Suarez A., de los Reyes-Gavilan C.G., Margolles A. Human cecum content modulates production of extracellular proteins by food and probiotic bacteria. FEMS Microbiol Lett 2011, 324:189-194.
21. O'Flaherty S. Probiotic-mediated modulation of host gene expression. Interactive Probiotics 2014, 81-98. CRC press, Boca Raton. E. Pessione (Ed.).
22. Al Naseri A., Bowman J.P., Wilson R., Nilsson R.E., Britz M.L. Impact of lactose starvation on the physiology of Lactobacillus casei GCRL163 in the presence or absence of Tween 80. J Proteome Res 2013, 12:5313-5322.
23. Heunis T., Deane S., Smit S., Dicks L.M. Proteomic profiling of the acid stress response in Lactobacillus plantarum 423. J Proteome Res 2014, 13:4028-4039.
24. Pessione E., Mazzoli R., Giuffrida M.G., Lamberti C., Garcia-Moruno E., Barello C., et al. A proteomic approach to studying biogenic amine producing lactic acid bacteria. Proteomics 2005, 5(3):687-698.
25. Mazzoli R., Fattori P., Lamberti C., Giuffrida M.G., Zapponi M., Giunta C., et al. High isoelectric point sub-proteomes analysis of Acinetobacter radioresistens S13 reveals envelope stress responses induced by aromatic compounds. Mol Biosyst 2011, 7(3):598-607.
26. Le Marechal C., Peton V., Plé C., Vroland C., Jardin J., Briard-Bion V., et al. Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties. J Proteomics 2015, 113:447-461.
27. Costantini A., Pietroniro R., Doria F., Pessione E., Garcia-Moruno E. Putrescine production from different amino acid precursors by lactic acid bacteria from wine and cider. Int J Food Microbiol 2013, 165:11-17.
28. Moreno-Arribas M.V., Polo M.C., Jorganes F., Muñoz R. Screening of biogenic amine production by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol 2003, 84(1):117-123.
29. Millichap J.G., Yee M.M. The diet factor in pediatric and adolescent migraine. Pediatr Neurol 2003, 28:9-15.
30. Konings W.N. Microbial transport: adaptation to natural environments. Antonie Van Leeuwenhoek 2006, 90(4):325-342.
31. Pessione E., Pessione A., Lamberti C., Coisson J.D., Riedel K., Mazzoli R., et al. First evidence of a membrane-bound, tyramine and β-phenylethylamine producing, tyrosine decarboxylase in Enterococcus faecalis: a two-dimensional electrophoresis proteomic study. Proteomics 2009, 9(10):2695-2710.
32. Lamberti C., Purrotti M., Mazzoli R., Fattori P., Barello C., Coisson J.D., et al. ADI pathway and histidine decarboxylation are reciprocally regulated in Lactobacillus hilgardii ISE 5211: proteomic evidence. Amino Acids 2011, 41(2):517-527.
33. Mazzoli R., Pessione E., Dufour M., Laroute V., Giuffrida M.G., Giunta C., et al. Glutamate-induced metabolic changes in Lactococcus lactis NCDO 2118 during GABA production: combined transcriptomic and proteomic analysis. Amino Acids 2010, 39(3):727-737.
34. Recsei P.A., Snell E.E. Pyruvoyl-dependent histidine decarboxylases. Mechanism of cleavage of the proenzyme from Lactobacillus buchneri. J Biol Chem 1985, 260(5):2804-2806.
35. Rodriguez-Caso C., Rodriguez-Agudo D., Moya-Garcia A.A., Fajardo I., Medina M.A., Subramaniam V., et al. Local changes in the catalytic site of mammalian histidine decarboxylase can affect its global conformation and stability. Eur J Biochem 2003, 270(21):4376-4387.
36. Bourdineaud J.P. Both arginine and fructose stimulate pH-independent resistance in the wine bacteria Oenococcus oeni. Int J Food Microbiol 2006, 107(3):274-280.
37. Zuobi-Hasona K., Crowley P.J., Hasona A., Bleiweis A.S., Brady L.J. Solubilization of cellular membrane proteins from Streptococcus mutans for two-dimensional electrophoresis. Electrophoresis 2005, 26:1200-1205.
38. Deshusses J.M.P., Burgess J.A., Scherl A., Wenger Y., Walter N., Converset V., et al. Exploitation of specific properties of trifluoroethanol for extraction and separation of membrane proteins. Proteomics 2003, 3(8):1418-1424.
39. Clarke G., Cryan J.F., Dinan T.G., Quigley E.M. Review article: probiotics for the treatment of irritable bowel sytndrome-focus on lactic acid bacteria. Aliment Pharmacol Ther 2012, 35:403-413.
40. Logan A.C., Katzman M. Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses 2005, 64(3):533-538.
41. Bravo J.A., Forsythe P., Chew M.V., Escaravage E., Savignac H.M., Dinan T.G., et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 2011, 108(38):16050-16055.
42. Ma X., Mao Y.K., Wang B., Huizinga J.D., Bienenstock J., Kunze W. Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am J Physiol Gastrointest Liver Physiol 2009, 296:G868-G875.
43. Kim N.Y., Ji G.E. Characterization of the production of biogenic amines and gamma-aminobutyric acid in the soybean pastes fermented by Aspergillus orizae and Lactobacillus brevis. J Microbiol Biotechnol 2014, 10.4014/jmb.1409.09081.
44. Nielsen J.C., Prahl C., Lonvaud-Funel A. Malolactic fermentation in wine by direct inoculation with freeze-dried Leuconostoc oenos cultures. Am J Enol Vitic 1996, 47:42-48.
45. Saadatzadeh A., Fazeli M.R., Jamalifar H., Dinarvand R. Probiotic properties of lyophilized cell free extract of Lactobacillus casei. Jundishapur J Nat Pharm Prod 2013, 8(3):131-137.
46. Benkerroum N., Daoudi A., Hamraoui T., Ghalfi H., Duroy M., Evrart P., et al. Lyophilized preparations of bacteriocinogenic Lactobacillus curvatus and Lactococcus lactis ssp. lactis as potential protective adjuncts to control Listeria monocytogenes in dry-fermented sausages. J Appl Microbiol 2005, 98:56-63.
47. Moiset G., Lopez C.A., Bartelds R., Syga L., Rijpkema E., Cukkemane A., et al. Disaccharides impact the lateral organization of lipid membranes. J Am Chem Soc 2014, 136:16167-16175.
48. Tymczyszyn E.E., Gomez-Zavaglia A., Disalvo E.A. Effects of sugars and growth media on the dehydration of Lactobacillus delbrueckii ssp. bulgaricus. J Appl Microbiol 2007, 102:845-851.
49. Jofré A., Aymerich T., Garriga M. Impact of different cryoprotectants on the survival of freeze-dried Lactobacillus rhamnosus and Lactobacillus casei/paracasei during long term storage. Benefic Microbes 2014, 6:1-6.
50. Genovese F., Coisson J.D., Majumder A., Pessione A., Svensson B., Jacobsen S., et al. An exoproteome approach to monitor safety of a cheese-isolated Lactococcus lactis. Food Res Int 2013, 54(1):1072-1079.
51. Sanchez B., Gonzales-Tejedo C., Ruas-Madiedo P., Urdaci M., Margolles A. L. plantarum extracellular chitin-binding protein and its role in the interaction between CaCo2 cells and mucin. Appl Environ Microbiol 2011, 77:1123-1126.
52. Centeno J.A., Menendez S., Hermida M., Rodriguez-Otero J.L. Effects of the addition of Enterococcus faecalis in Cebreiro cheese manufacture. Int J Food Microbiol 1999, 48(2):97-111.
53. Giraffa G. Functionality of enterococci in dairy products. Int J Food Microbiol 2003, 88:215-222.
54. Franz C.M.A.P., Stiles M.E., Schleifer K.H., Holzapfel W.H. Enterococci in foods, a conundrum for food safety. Int J Food Microbiol 2003, 88:105-122.
55. Balla E., Dicks J.M.T., Du Toit M., van der Merwe M.J., Holzapfel W.H. Characterization and cloning of the genes encoding enterocin 1071a and enterocin 1071b, two antimicrobial peptides produced by Enterococcus faecalis BFE1071. Appl Environ Microbiol 2000, 66:1298-1304.
56. Franz C.M.A.P., Worobo R.W., Quadri L.E.N., Schillinger U., Holzapfel W.H., Vederas J.C., et al. Atypical genetic locus associated with constitutive production of enterocin B by Enterococcus faecium BFE 900. Appl Environ Microbiol 1999, 65(5):2170-2178.
57. Ramos S., Igrejas G., Rodrigues J., Capelo-Martinez J.L., Poeta P. Genetic characterization of antibiotic resistance and virulence factors in vanA-containing enterococci from cattle, sheep and pigs subsequent to the discontinuation of the use of avoparcin. Vet J 2012, 193(1):301-303.
58. Miller W.R., Munita J.M., Arias C.A. Mechanisms of antibiotic resistance in enterococci. Expert Rev Anti Infect Ther 2014, 12(10):1221-1236.
59. Shankar N., Baghdayan A.S., Gilmore M.S. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 2002, 417:746-750.
60. Semedo T., Santos M.A., Lopes M.F.S., Marques J.J.F., Crespo M.T.B., Tenreiro R. Virulence factors in food, clinical and reference enterococci: a common trait in the genus?. Syst Appl Microbiol 2003, 26:13-22.
61. Péréz-Martin F., Seseña S., Izquierdo P.M., Palop M.L. Are Enterococcus populations present during malolactic fermentation of red wine safe?. Food Microbiol 2014, 42:95-101.
62. Pessione A., Lamberti C., Cocolin L., Campolongo S., Grunau A., Giubergia S., et al. Different protein expression profiles in cheese and clinical isolates of Enterococcus faecalis revealed by proteomic analysis. Proteomics 2012, 12(3):431-447.
63. Anonymous Guidelines for the evaluation of probiotics in food. Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food 2002, 11. FAO, London, Ontario.
64. Pessione E. Lactic acid bacteria contribution to gut complexity: lights and shadows. Front Cell Infect Microbiol 2012, 2:86.
65. Sauer J., Richter K.K., Pool-Zobel B.L. Physiological concentration of butyrate favorably modulate genes of oxidative and metabolic stress in primary human colon cells. J Nutr Biochem 2007, 18:736-745.
66. Pellizzaro C., Coradini D., Daidone M.G. Modulation of angiogenesis-related proteins synthesis by sodium butyrate in colon cancer cell line HT29. Carcinogenesis 2002, 23:735-740.
67. Minucci S., Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006, 6:38-51.
68. Wahle K.W., Heys S.D., Rotondo D. Conjugated linoleic acids: are they beneficial or detrimental to health?. Prog Lipid Res 2004, 43:553-587.
69. Lupton J.R. Microbial degradation products influence colon cancer risk: the butyrate controversy. J Nutr 2004, 134:479-482.
70. Deutsch S.-M., Gwenael J. New probiotics. Dairy propionibacteria and the modulation of gut microbiota and physiology. Interactive Probiotics 2014, 122-147. CRC press, Boca Raton. E. Pessione (Ed.).
71. Smith I.M., Christensen J.E., Arneborg N., Jespersen L. Yeast modulation of human dendritic cell cytokine secretion: an in vitro study. PLoS One 2014, 9(5):e96595.
72. Pontier-Bres R., Munro P., Boyer L., Anty R., Imbert V., Terciolo C., et al. Saccharomyces boulardii modifies Salmonella Typhimurium traffic and host immune responses along the intestinal tract. PLoS One 2014, 9(8):e103069.
73. Collins J.K., Thornton G., Sullivan O.G. Selection of probiotic strains for human applications. Int Dairy J 1998, 8:487-490.
74. Even S., Bouchard D., Le Loir Y. Lactic acid bacteria to modulate virulence expression in pathogenic bacteria. Interactive Probiotics 2014, 52-80. CRC press, Boca Raton. E. Pessione (Ed.).
75. Desvaux M., Dumas E., Chafsey I., Hébraud M. Protein cell surface display in gram-positive bacteria: from single protein to macromolecular protein structure. FEMS Microbiol Lett 2006, 256:1-15.
76. Sanchez B., Champomier-Verges M.C., Anglade P., Baraige F., de los Reyes-Gavilan C.G., Margolles A., et al. A preliminary analysis of Bifidobacterium longum exported proteins by two-dimensional electrophoresis. J Mol Microbiol Biotechnol 2008, 14:74-79.
77. Antikainen J., Kuparinen V., Lahteenmaaki K., Kohronen T.K. pH-Dependent association of enolase and glyceraldheyde 3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J Bacteriol 2007, 189:4539-4543.
78. Jeffery C.J. Moonlighting proteins: complications and implications for proteomic research. Drug Discov Today TARGETS 2004, 3:71-78.
79. Candela M., Bergmann S., Vici M., Vitali B., Turroni S., Eikmanns B.J., et al. Binding of human plasminogen to Bifidobacterium. J Bacteriol 2007, 189(16):5929-5936.
80. Granato D., Bergonzelli G.E., Pridmore R.D., Marvin L., Rouvet M., Corthesy-Theulaz I. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucin. Infect Immun 2004, 72:2160-2169.
81. Gilad O., Svensson B., Viborg A.H., Stuer-Lauridsen B., Jacobsen S. The extracellular proteome of Bifidobacterium animalis subsp. lactis BB-12 reveals proteins with putative roles in probiotic effects. Proteomics 2011, 12(12):2503-2514.
82. Alam S.I., Bansod S., Kumar R.B., Sengupta N., Singh L. Differential proteomic analysis of Clostridium perfringens ATCC13124; identification of dominant, surface and structure associated proteins. BMC Microbiol 2009, 9:162.
83. Mangiapane E., Lamberti C., Pessione A., Ceruti P., Galano E., Novelli F., et al. Integrating proteomics and physiological tests to understand adhesion mechanism of the probiotic Lactobacillus reuteri Lb2 BM DSM 16341. Jiomics 2013, 3:145-156.
84. Pessione A, Lo Bianco G, Mangiapane E, Cirrincione S, Pessione E. Characterization of potentially probiotic lactic acid bacteria isolated from olives: evaluation of short chain fatty acids production and analysis of the extracellular proteome. Food Res Int 201;67:247-254.
85. Yan S., Wu G. Signal peptide of cellulase. Appl Microbiol Biotechnol 2014, 98:5329-5362.
86. Granato D., Bergonzelli G.E., Pridmore R.D., Marvin L., Rouvet M., Corthesy-Theulaz I. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucin. Infect Immun 2004, 72:2160-2169.
87. Sanchez B., Urdaci M.C., Margolles A. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology 2010, 156:3232-3242.
88. Lee K., Lee H.G., Choi Y.J. Proteomic analysis of the effects of bile salts on the intestinal and probiotic bacterium Lactobacillus reuteri. J Biotechnol 2008, 137:14-19.
89. Lee K., Pi K. Effect of transient acid stress on the proteome of intestinal probiotic Lactobacillus reuteri. Biochemistry 2010, 75:460-465.
90. Axelsson L.T., Chung T.C., Dobrogosz W.J., Lindgren S.E. Production of a broad spectrum antimicrobial substance by Lactobacillus reuteri. Microb Ecol Health Dis 1989, 2:131-136.
91. Kabuchi T., Saito T., Kawai Y., Uemura J., Itoh T. Production, purification and characterization of reutericin 6, a bacteriocin with lytic activity produced by Lactobacillus reuteri LA6. Int J Food Microbiol 1997, 34:145-156.
92. Holtzel A., Ganzle M.G., Nicholson G.J., Hammes W.P., Jung G. The first low molecular weight antibiotic from lactic acid bacteria: reutericyclin, a new tetrameric acid. Angew Chem Int Ed 2000, 39:2766-2768.
93. Vielfort K., Sjolinder H., Roos S., Jonsson H., Aro H. Adherence of clinically isolated lactobacilli to human cervical cells in competition with Neisseria gonorrhoeae. Microbes Infect 2008, 10:1325-1334.
94. Li J., Wang W., Xu S.X., Margarvey N.A., McCormick J.K. Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. PNAS 2011, 108:3360-3365.
95. Hernandez-Mendoza A., Gonzalez-Cordova A.F., Vallejo-Cordoba B., Garcia H.S. Effect of oral supplementation of Lactobacillus reuteri in reduction of intestinal absorption of aflatoxin B(1) in rats. J Basic Microbiol 2011, 51:263-268.
96. Gromer S., Eubel J.K., Lee B.L., Jacob J. Human selenoproteins at a glance. Cell Mol Life Sci 2005, 62:2414-2437.
97. Galano E., Mangiapane E., Bianga J., Palmese A., Pessione E., Szpunar J., et al. Privileged incorporation of selenium as selenocysteine in Lactobacillus reuteri proteins demonstrated by selenium-specific imaging and proteomics. Mol Cell Proteomics 2013, 12(8):2196-2204.
98. Mangiapane E., Pessione A., Pessione E. Selenium and selenoproteins: an overview on different biological systems. Curr Protein Pept Sci 2014, 15(6):598-607.