Quorum sensing peptides selectively penetrate the blood-brain barrier

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Wynendaele, Evelien ^a   Verbeke, Frederick ^a   Stalmans, Sofie ^a   Gevaert, Bert ^a   Janssens, Yorick ^a   Van De Wiele, Christophe ^b   Peremans, Kathelijne ^a   Burvenich, Christian ^a   De Spiegeleer, Bart ^a  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE; QUORUM SENSING PEPTIDE; UNCLASSIFIED DRUG; PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD BRAIN BARRIER; BLOOD LEVEL; BRAIN FUNCTION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PEPTIDE ANALYSIS; PROTEIN TRANSPORT; QUORUM SENSING; TISSUE DISTRIBUTION; ANIMAL; BACTERIUM; BRAIN; FEMALE; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MICROFLORA; PHYSIOLOGY; PLASMA; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BACTERIA; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; FEMALE; HUMANS; MICE; MICE, INBRED ICR; MICROBIOTA; PEPTIDE FRAGMENTS; PLASMA; QUORUM SENSING; TISSUE DISTRIBUTION;

EID: 84951114083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142071     Document Type: Article

References (61)

1. Ryan RP, Dow JM. Diffusible signals and interspecies communication in bacteria. Microbiology 2008; 154: 1845-1858. doi: 10.1099/mic.0.2008/017871-0 PMID: 18599814
2. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet. 2009; 43: 197-222. doi: 10.1146/annurev-genet-102108-134304 PMID: 19686078
3. Costerton JW, Stewart PS, Greenberg EP. Bacterial Biofilms: A common cause of persistent infections. Science 1999; 284: 1318-1322. PMID: 10334980
4. Kumari A, Pasini P, Daunert S. Detection of bacterial quorum sensing N-acyl homoserine lactones in clinical samples. Anal Bioanal Chem. 2008; 391: 1619-1627. doi: 10.1007/s00216-008-2002-3 PMID: 18408921
5. Erickson DL, Endersby R, Kirkham A, Stuber K, Vollman DD, Rabin HR, et al. Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun. 2002; 70: 1783-1790. PMID: 11895939
6. Gitzinger M, Parsons J, Reski R, Fussenegger M. Functional cross-kingdom conservation of mammalian and moss (Physcomitrella patens) transcription, translation and secretion machineries. Plant Biotechnol J. 2009; 7: 73-86. doi: 10.1111/j.1467-7652.2008.00376.x PMID: 19021876
7. Williams P. Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 2007; 153: 3923-3938. PMID: 18048907
8. Kumar S, Kolodkin-Gal I, Engelberg-Kulka H. Novel quorum-sensing peptides mediating interspecies bacterial cell death. mBio 2013. doi: 10.1128/mBio.00314-13 PMID: 23736285
9. Fujiya M, Musch MW, Nakagawa Y, Hu S, Alverdy J, Kohgo Y, et al. The Bacillus subtilis quorum-sensing molecule CSF contributes to intestinal homeostasis via OCTN2, a host cell membrane transporter. Cell Host Microbe 2007; 1: 299-308. PMID: 18005709
10. Wynendaele E, Verbeke F, D'Hondt M, Hendrix A, Van de Wiele C, Burvenich C, et al. Crosstalk between the microbiome and cancer cells by quorum sensing peptides. Peptides 2015; 64: 40-48. doi: 10.1016/j.peptides.2014.12.009 PMID: 25559405
11. De Spiegeleer B, Verbeke F, D'Hondt M, Hendrix A, Van de Wiele C, Burvenich C, et al. The quorum sensing peptides PhrG, CSP and EDF promote angiogenesis and invasion of breast cancer cells in vivo. Plos One 2015. doi: 10.1371/journal.pone.0119471 PMID: 25780927
12. Nassif X, Bourdoulous S, Eugène E, Couraud P-O. How do extracellular pathogens cross the bloodbrain barrier? Trends in Microbiol. 2002; 10: 227-232.
13. Banks WA. Characteristics of compounds that cross the blood-brain barrier. BMC Neurology 2009; 9: S3. doi: 10.1186/1471-2377-9-S1-S3 PMID: 19534732
14. Egleton RD, Davis TP. Development of neuropeptide drugs that cross the blood-brain barrier. NeuroRx 2005; 2: 44-53. PMID: 15717056
15. Stalmans S, Wynendaele E, Bracke N, Knappe D, Hoffmann R, Peremans K, et al. Blood-brain barrier transport of short, proline-rich antimicrobial peptides. Protein Peptide Lett. 2014; 21: 399-406.
16. Kurihara A, Pardridge WM. Imaging brain tumors by targeting peptide radiopharmaceuticals through the blood-brain barrier. Cancer Res. 1999; 59: 6159-6163. PMID: 10626807
17. Deeken JF, Löscher W. The blood-brain barrier and cancer: transporters, treatment, and trojan horses. Clin Cancer Res. 2007; 13: 1663-1674. PMID: 17363519
18. Grenham S, Clarke G, Cryan JF, Dinan TG. Brain-gut-microbiome communication in health and disease. Front Physiol. 2011; 2: 94. doi: 10.3389/fphys.2011.00094 PMID: 22162969
19. Foster JA, McVey Neufeld K-A. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013; 36: 305-312. doi: 10.1016/j.tins.2013.01.005 PMID: 23384445
20. Kang DW, Park JG, Ilhan ZE, Wallstrom G, LaBaer J, Adams JB, Krajmalnik-Brown R. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. Plos One 2013. doi: 10.1371/journal.pone.0068322 PMID: 23844187
21. Sudo N. Role of microbiome in regulating the HPA axis and its relevance to allergy. Chem Immunol Allergy 2012; 98: 163-175. doi: 10.1159/000336510 PMID: 22767063
22. Dinan TG, Stilling RM, Stanton C, Cryan JF. Collective unconscious: how gut microbes shape human behavior. J Psychiatr Res. 2015; 63: 1-9. doi: 10.1016/j.jpsychires.2015.02.021 PMID: 25772005
23. Lyte M. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. Plos Pathog. 2013. doi: 10.1371/journal.ppat.1003726 PMID: 24244158
24. Schmidt C. Mental health: thinking from the gut. Nature 2015; 518: S12-S15. doi: 10.1038/518S13a PMID: 25715275
25. Lyte M, Cryan JF. Microbial endocrinology: the microbiota-gut-brain axis in health and disease. Advances in Experimental Medicine and Biology, Microbial Endocrinology. 1st ed. New York: Springer; 2014.
26. Wynendaele E, Bronselaer A, Nielandt J, D'Hondt M, Stalmans S, Bracke N, et al. Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Res. 2013; 41: D655-D659. doi: 10.1093/nar/gks1137 PMID: 23180797
27. Wynendaele E, Gevaert B, Stalmans S, Verbeke F, De Spiegeleer B. Exploring the chemical space of quorum sensing peptides. Biopolymers 2015. doi: 10.1002/bip.22649 PMID: 25846138
28. Verbeke F, Wynendaele E, Braet S, D'Hondt M, De Spiegeleer B. Quality evaluation of synthetic quorum sensing peptides used in R&D. J Pharm Anal. 2015. doi: 10.1016/j.pha.2014.12.002
29. Baileys GS. The iodogen method for radiolabeling protein. In: Walker JM, editor. The Protein Protocols Handbook. New York City: Humana Press; 1996. pp. 673-674.
30. Wynendaele E, Bracke N, Stalmans S, De Spiegeleer B. Development of peptide and protein based radiopharmaceuticals. Curr Pharm Des. 2014; 20: 2250-2267. PMID: 24025103
31. Baileys GS. The chloramine T method for radiolabeling protein. In: Walker JM, editor. The Protein Protocols Handbook. New York City: Humana Press; 2002. pp. 963-965.
32. Gjedde A. High- and low-affinity transport of D-glucose from blood to brain. J Neurochem. 1981; 36: 1463-1471. PMID: 7264642
33. Pan WH, Banks WA, Fasold MB, Bluth J, Kastin AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 1998; 37: 1553-1561. PMID: 9886678
34. Patlak CS, Blasberg RG, Fenstermacher JD. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab. 1983; 3: 1-7. PMID: 6822610
35. Gjedde A. Calculation of cerebral glucose phosphorylation from brain uptake of glucose analogs in vivo: a re-examination. Brain Res. 1982; 257: 237-274. PMID: 7104768
36. Van Dorpe S, Adriaens A, Polis I, Peremans K, Van Bocxlaer J, De Spiegeleer B. Analytical characterization and comparison of the blood-brain barrier permeability of eight opioid peptides. Peptides 2010; 31: 1390-1399. doi: 10.1016/j.peptides.2010.03.029 PMID: 20347901
37. Wong DF, Gjedde A, Wagner HN Jr. Quantification of neuroreceptors in the living human brain. I. Irreversible binding of ligands. J Cereb Bood Flow Metab 1986; 6; 137-46.
38. Gjedde A, Bauer WR, Wong DF. Neurokinetics: the dynamics of neurobiology in vivo. Springer US 2011. doi: 10.1007/978-1-4419-7409-9
39. Triguero D, Buciak J, Pardridge WM. Capillary depletion method for quantification of blood-brain-barrier transport circulating peptides and plasma-proteins. J Neurochem. 1990; 54: 1882-1888. PMID: 2338547
40. Gutierrez EG, Banks WA, Kastin AJ. Murine tumor-necrosis-factor-alpha is transported from blood to brain in the mouse. J Neuroimmunol. 1993; 47: 169-176. PMID: 8370768
41. Banks WA, Kastin AJ. Quantifying carrier-mediated transport of peptides from brain to the blood. Method Enzymol. 1989; 168: 652-660.
42. Vergote V, Van Dorpe S, Peremans K, Burvenich C, De Spiegeleer B. In vitro metabolic stability of obestatin: kinetics and identification of cleavage products. Peptides 2008; 29: 1740-1748. doi: 10.1016/j.peptides.2008.05.018 PMID: 18602197
43. Knutsen E, Ween O, Havarstein LS. Two separate quorum-sensing systems upregulate transcription of the same ABC transporter in Streptococcus pneumonia. J Bacteriol. 2004; 186: 3078-3085. PMID: 15126469
44. Henriques-Normark B, Normark S. Commensal pathogens, with a focus on Streptococcus pneumonia, and interactions with the human host. Exp Cell Res. 2010; 316: 1408-1414. doi: 10.1016/j.yexcr.2010.03.003 PMID: 20227406
45. Perego M, Brannigan JA. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 2001; 22: 1541-1547. PMID: 11587783
46. Verbeken M, Wynendaele E, Mauchauffee E, Bracke N, Stalmans S, Bojnik E, et al. Blood-brain transfer and antinociception of linear and cyclic N-methyl-guanidine and thiourea-enkephalins. Peptides 2015; 63: 10-21. doi: 10.1016/j.peptides.2014.10.010 PMID: 25451468
47. Kastin AJ, Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes. 2003; 27: 313-318.
48. Stalmans S, Gevaert B, Wynendaele E, Nielandt J, De Tré G, Peremans K, et al. Classification of peptides according to their blood-brain barrier influx. Protein Peptide Lett. 2015. doi: 10.2174/0929866522666150622101223
49. Sternini C, Patierno S, Selmer IS, Kirchgessner A. The opioid system in the gastrointestinal tract. Neurogastroenterol Motil. 2004;Suppl. 3: 3-16.
50. Van Dorpe S, Bronselaer A, Nielandt J, Stalmans S, Wynendaele E, Audenaert K, et al. Brainpeps: the blood-brain barrier peptide database. Brain Struct Funct. 2012; 217: 687-718. doi: 10.1007/s00429-011-0375-0 PMID: 22205159
51. Begley DJ. The Blood-brain Barrier: Principles for targeting peptides and drugs to the central nervous system. J Pharm Pharmacol. 1996; 48: 136-146. PMID: 8935161
52. Hong HA, Khaneja R, Tam NM, Cazzato A, Tan S, Urdaci M, et al. Bacillus subtilis isolated from the human gastrointestinal tract. Res Microbiol. 2009; 160: 134-143. doi: 10.1016/j.resmic.2008.11.002 PMID: 19068230
53. Mitchell J. Streptococcus mitis: walking the line between commensalism and pathogenesis. Mol Oral Microbiol. 2011; 26: 89-98. doi: 10.1111/j.2041-1014.2010.00601.x PMID: 21375700
54. Dürre P, Hollergschwandner C. Initiation of endospore formation in Clostridium acetobutylicum. Anaerobe 2004; 10: 69-74. PMID: 16701502
55. Brüggemann H, Baumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, et al. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. PNAS 2003; 100: 1316-1321. PMID: 12552129
56. Paredes CJ, Alsaker KV, Papoutsakis ET. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol. 2005; 3: 969-978. PMID: 16261177
57. Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen ML, Bolte E, et al. Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis. 2002; 35: S6-S16. PMID: 12173102
58. Bajaj JS, Ridlon JM, Hylemon PB, Thacker LR, Heuman DM, Smith S, et al. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Gastrointest Liver Physiol. 2012; 302: G168-175. doi: 10.1152/ajpgi.00190.2011 PMID: 21940902
59. Luna RA, Foster JA. Gut brain axis: diet microbiota interactions and implications for modulation of anxiety and depression. Curr Opin Biotechnol. 2015; 32: 35-41. doi: 10.1016/j.copbio.2014.10.007 PMID: 25448230
60. Wang Y, Kasper LH. The role of microbiome in central nervous system disorders. Brain Behav Immun. 2014; 38: 1-12. doi: 10.1016/j.bbi.2013.12.015 PMID: 24370461
61. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2011; 25: 397-407. doi: 10.1016/j.bbi.2010.10.023 PMID: 21040780