Generation of food-grade recombinant Lactobacillus casei delivering Myxococcus xanthus prolyl endopeptidase

Applied Microbiology and Biotechnology

Volumn 98, Issue 15, 2014, Pages 6689-6700

  Alvarez Sieiro, Patricia ^a   Martin, Maria Cruz ^a   Redruello, Begoña ^a   Del Rio, Beatriz ^a   Ladero, Victor ^a   Palanski, Brad A ^b,c   Khosla, Chaitan ^b,c   Fernandez, Maria ^a   Alvarez, Miguel A ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b STANFORD UNIVERSITY   (United States)

^c Stanford University   (United States)

Author keywords

Celiac disease; Gluten; Heterologous expression; Lactobacillus casei; Myxococcus xanthus; Prolyl endopeptidase

Indexed keywords

AMINO ACIDS; ENZYME ACTIVITY; PEPTIDES;

CELIAC DISEASE; GLUTEN; HETEROLOGOUS EXPRESSION; LACTOBACILLUS CASEI; MYXOCOCCUS XANTHUS; PROLYL ENDOPEPTIDASE;

STRAIN;

GLUTEN; PROLYL ENDOPEPTIDASE; BACTERIAL PROTEIN; SERINE PROTEINASE;

ARTICLE; BACTERIAL STRAIN; CELLULAR SECRETION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME RELEASE; IN VITRO STUDY; LACTOBACILLUS CASEI; MALE; MOLECULAR CLONING; MYXOCOCCUS XANTHUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; SMALL INTESTINE; CELIAC DISEASE; DRUG DELIVERY SYSTEM; ENZYME THERAPY; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY;

BACTERIAL PROTEINS; CELIAC DISEASE; DRUG DELIVERY SYSTEMS; ENZYME THERAPY; GASTROINTESTINAL TRACT; GENE EXPRESSION; GLUTENS; HUMANS; LACTOBACILLUS CASEI; MYXOCOCCUS XANTHUS; SERINE ENDOPEPTIDASES;

EID: 84904973890     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5730-7     Document Type: Article

References (55)

1. Alvarez MA, Herrero M, Suárez JE (1998) The site-specific recombination system of the Lactobacillus species bacteriophage A2 integrates in gram-positive and gram-negative bacteria. Virology 250(1):185-193. doi:10.1006/viro.1998.9353 (Pubitemid 28471774)
2. Axelsson L (1998) Lactic acid bacteria: Classification and physiology. In: Salminen SVWA (ed) Lactic acid bacteria: Microbiological and functional aspects, 2nd edn. CRC, Boca Raton, pp 1-66
3. Bethune MT, Khosla C (2012) Oral enzyme therapy for celiac sprue. Methods Enzymol 502:241-271
4. Carr FJ, Chill D, Maida N (2002) The lactic acid bacteria: a literature survey. Crit Rev Microbiol 28(4):281-370. doi:10.1080/1040-840291046759 (Pubitemid 36106334)
5. Charteris, Kelly, Morelli, Collins (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84(5):759-768. doi:10.1046/j.1365-2672. 1998.00407.x
6. Clarke G, Cryan JF, Dinan TG, Quigley EM (2012) Review article: probiotics for the treatment of irritable bowel syndrome - focus on lactic acid bacteria. Aliment Pharmacol Ther 35(4):403-413. doi:10.1111/j.1365-2036.2011. 04965.x
7. Comino I, Real A, Vivas S, Síglez MÁ, Caminero A, Nistal E, Casqueiro J, Rodríguez-Herrera A, Cebolla Á, Sousa C (2012) Monitoring of gluten-free diet compliance in celiac patients by assessment of gliadin 33-mer equivalent epitopes in feces. Am J Clin Nutr 95(3): 670-677. doi:10.3945/ajcn.111.026708
8. Conway PL, Gorbach SL, Goldin BR (1987) Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci 70(1):1-12. doi:10.3168/jds.S0022-0302(87)79974-3
9. Corrao G, Corazza GR, Bagnardi V, Brusco G, Ciacci C, Cottone M, Sategna Guidetti C, Usai P, Cesari P, Pelli MA, Loperfido S, Volta U, Calabro A, Certo M (2001)Mortality in patients with coeliac disease and their relatives: a cohort study. Lancet 358(9279):356-361. doi: S0140673601055544
10. Daniel C, Roussel Y, Kleerebezem M, Pot B (2011) Recombinant lactic acid bacteria as mucosal biotherapeutic agents. Trends Biotechnol 29(10):499-508. doi:10.1016/j.tibtech.2011.05.002
11. D'Arienzo R, Maurano F, Luongo D, Mazzarella G, Stefanile R, Troncone R, Auricchio S, Ricca E, David C, Rossi M (2008) Adjuvant effect of Lactobacillus casei in a mouse model of gluten sensitivity. Immunol Lett 119(1-2):78-83 doi:10.1016/j.imlet.200804.006
12. D'Arienzo R, Stefanile R, Maurano F, Mazzarella G, Ricca E, Troncone R, Auricchio S, Rossi M (2011) Immunomodulatory effects of Lactobacillus casei administration in a mouse model of gliadin-sensitive enteropathy. Scand J Immunol 74(4):335-341. doi:10.1111/j.1365-3083.2011.02582.x
13. del Rio B, Dattwyler RJ, Aroso M, Neves V, Meirelles L, Seegers JFML, Gomes-Solecki M (2008) Oral immunization with recombinant Lactobacillus plantarum induces a protective immune response in mice with Lyme disease. Clin Vaccine Immunol 15(9):1429-1435. doi:10.1128/cvi.00169-08
14. del Rio B, Fuente JL, Neves V, Dattwyler R, Seegers JFML, Gomes-Solecki M (2010) Platform technology to deliver prophylactic molecules orally: an example using the class A select agent Yersinia pestis. Vaccine 28(41):6714-6722. doi:10.1016/j.vaccine.2010.07.084
15. Fernández de Palencia P, López P, Corbí AL, Peláez C, Requena T (2008) Probiotic strains: survival under simulated gastrointestinal conditions, in vitro adhesion to Caco-2 cells and effect on cytokine secretion. Eur Food Res Technol 227(5):1475-1484. doi:10.1007/s00217- 008-0870-6
16. Gass J, Ehren J, Strohmeier G, Isaacs I, Khosla C (2005) Fermentation, purification, formulation, and pharmacological evaluation of a prolyl endopeptidase from Myxococcus xanthus: implications for Celiac Sprue therapy. Biotechnol Bioeng 92(6):674-684. doi:10.1002/bit.20643 (Pubitemid 41772463)
17. Green PH, Jabri B (2003) Coeliac disease. Lancet 362(9381):383-391 (Pubitemid 36945070)
18. Gujral N, Freeman HJ, Thomson AB (2012) Celiac disease: prevalence, diagnosis, pathogenesis and treatment. World J Gastroenterol 18(42):6036-6059. doi:10.3748/wjg.v18.i42.6036
19. Hausch F, Shan L, Santiago NA, Gray GM, Khosla C (2002) Intestinal digestive resistance of immunodominant gliadin peptides. Am J Physiol Gastrointest Liver Physiol 283(4):G996-G1003. doi:10.1152/ajpgi.00136.2002 (Pubitemid 35033943)
20. Jankovic I, Ventura M, Meylan V, Rouvet M, Elli M, Zink R (2003) Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. J Bacteriol 185(11):3288-3296. doi:10.1128/jb.185.11. 3288-3296.2003 (Pubitemid 36617740)
21. Janssen GR, Bibb MJ (1993) Derivatives of pUC18 that have BgfII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of Escherichia coli colonies. Gene 124(1):133-134. doi:10.1016/0378-1119(93)90774-W (Pubitemid 23065980)
22. Kabashima T, Fujii M, Meng Y, Ito K, Yoshimoto T (1998) Prolyl endopeptidase from Sphingomonas capsulata: isolation and characterization of the enzyme and nucleotide sequence of the gene. Arch Biochem Biophys 358(1):141-148. doi:10.1006/abbi.1998.0836 (Pubitemid 28471383)
23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
24. Marcotte H, Ferrari S, Cesena C, Hammarström L, Morelli L, Pozzi G, Oggioni MR (2004) The aggregation-promoting factor of Lactobacillus crispatus M247 and its genetic locus. J Appl Microbiol 97(4):749-756. doi:10.1111/j.1365- 2672.2004.02364.x (Pubitemid 39331581)
25. Marietta EV, Murray JA (2012) Animal models to study gluten sensitivity. Semin Immunopathol 34(4):497-511. doi:10.1007/s00281-012-0315-y
26. Marteau P, Minekus M, Havenaar R, Huisin'tVeld JHJ (1997) Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile. J Dairy Sci 80(6):1031-1037. doi:10.3168/jds.S0022-0302(97)76027-2
27. Marti T, Molberg O, Li Q, Gray GM, Khosla C, Sollid LM(2005) Prolyl endopeptidase-mediated destruction of T cell epitopes in whole gluten: chemical and immunological characterization. J Pharmacol Exp Ther 312(1):19-26. doi:10.1124/jpet.104.073312 (Pubitemid 40096448)
28. Martin MC, Alonso JC, Suarez JE, Alvarez MA (2000) Generation of food-grade recombinant lactic acid bacterium strains by site-specific recombination. Appl Environ Microbiol 66(6):2599-2604 (Pubitemid 30353970)
29. Martin MC, Fernandez M, Martin-Alonso JM, Parra F, Boga JA, Alvarez MA (2004) Nisin-controlled expression of Norwalk virus VP60 protein in Lactobacillus casei. FEMS Microbiol Lett 237(2):385-391. doi:10.1016/j.femsle. 2004.07.002 (Pubitemid 39091974)
30. Martin MC, Pant N, Ladero V, Gunaydin G, Andersen KK, Alvarez B, Martinez N, Alvarez MA, Hammarstrom L, Marcotte H (2011) Integrative expression system for delivery of antibody fragments by lactobacilli. Appl Environ Microbiol 77(6):2174-2179. doi:10.1128/AEM.02690-10
31. Mazé A, Boël G, Zúñiga M, Bourand A, Loux V, Yebra MJ, Monedero V, Correia K, Jacques N, Beaufils S, Poncet S, Joyet P, Milohanic E, Casarégola S, Auffray Y, Pérez-Martínez G, Gibrat J-F, Zagorec M, Francke C, Hartke A, Deutscher J (2010) Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J Bacteriol 192(10):2647-2648. doi:10.1128/jb.00076-10
32. Nyanga-Koumou AP, Ouoba LII, Kobawila SC, Louembe D (2012) Response mechanisms of lactic acid bacteria to alkaline environments: a review. Crit Rev Microbiol 38(3):185-190. doi:10.3109/1040841X.2011.640978
33. Parish JH (1986) Genetic manipulation of Streptomyces - a laboratory manual: by D A Hopwood, M J Bibb, K F Chatter; T Kieser CJ Bruton, H M Kieser, D J Lydiate, C P Smith, J M Ward and H Schrempf. pp 356. The John Innes Foundation, Norwich, UK and Cold Spring Harbour Laboratory. 1985. ISBN 0-7084-0336-0. Biochem Educ 14(4):196-196
34. Piper JL, Gray GM, Khosla C (2004) Effect of prolyl endopeptidase on digestive-resistant gliadin peptides in vivo. J Pharmacol Exp Ther 311(1):213-219. doi:10.1124/jpet.104.068429 (Pubitemid 39287800)
35. Pyle GG, Paaso B, Anderson BE, Allen DD, Marti T, Li Q, Siegel M, Khosla C, Gray GM (2005) Effect of pretreatment of food gluten with prolyl endopeptidase on gluten-induced malabsorption in celiac sprue. Clin Gastroenterol Hepatol 3(7):687-694 (Pubitemid 40984730)
36. Qiao SW, Bergseng E, Molberg O, Xia J, Fleckenstein B, Khosla C, Sollid LM (2004) Antigen presentation to celiac lesion-derived T cells of a 33-mer gliadin peptide naturally formed by gastrointestinal digestion. J Immunol 173(3):1757-1762 (Pubitemid 38971607)
37. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
38. Sánchez B, Schmitter JM, Urdaci MC (2009) Identification of novel proteins secreted by Lactobacillus rhamnosus GG grown in de Mann-Rogosa-Sharpe broth. Lett Appl Microbiol 48(5):618-622. doi:10.1111/j.1472-765X.2009.02579.x
39. Savijoki K, Ingmer H, Varmanen P (2006) Proteolytic systems of lactic acid bacteria. Appl Microbiol Biotechnol 71(4):394-406. doi:10.1007/s00253-006- 0427-1 (Pubitemid 44060940)
40. Scheirlinck T, Mahillon J, Joos H, Dhaese P, Michiels F (1989) Integration and expression of alpha-amylase and endoglucanase genes in the Lactobacillus plantarum chromosome. Appl Environ Microbiol 55(9):2130-2137 (Pubitemid 19228844)
41. Schuppan D, Junker Y, Barisani D (2009) Celiac disease: from pathogenesis to novel therapies.Gastroenterology 137(6):1912-1933. doi:10.1053/j.gastro. 2009.09.008
42. Sealey-Voyksner JA, Khosla C, Voyksner RD, Jorgenson JW (2010) Novel aspects of quantitation of immunogenic wheat gluten peptides by liquid chromatography-mass spectrometry/mass spectrometry. J Chromatogr A 1217(25):4167-4183. doi:10.1016/j.chroma.2010.01.067
43. Shan L, Molberg O, Parrot I, Hausch F, Filiz F, Gray GM, Sollid LM, Khosla C (2002) Structural basis for gluten intolerance in celiac sprue. Science 297(5590):2275-2279. doi:10.1126/science.1074129
44. Shan L, Marti T, Sollid LM, Gray GM, Khosla C (2004) Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue. Biochem J 383(Pt 2):311-318. doi:10.1042/BJ20040907 (Pubitemid 39446692)
45. Stoven S, Murray JA, Marietta EV (2013) Latest in vitro and in vivo models of celiac disease. Expert Opin Drug Discov 8(4):445-457. doi:10.1517/17460441.2013.761203
46. Tuohy KM, Probert HM, Smejkal CW, Gibson GR (2003) Using probiotics and prebiotics to improve gut health. Drug Discov Today 8(15):692-700. doi:10.1016/S1359-6446(03)02746-6 (Pubitemid 36970000)
47. Turroni F, Ventura M, Buttó LF, Duranti S, O'Toole PW, Motherway MOC, Sinderen D (2013) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 1-21. doi: 10.1007/s00018-013-1318-0
48. van Overbeek FM, Uil-Dieterman IG, Mol IW, Kohler-Brands L, Heymans HS, Mulder CJ (1997) The daily gluten intake in relatives of patients with coeliac disease compared with that of the general Dutch population. Eur J Gastroenterol Hepatol 9(11):1097-1099 (Pubitemid 27488875)
49. Ventura M, Jankovic I, Walker DC, Pridmore RD, Zink R (2002) Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl Environ Microbiol 68(12):6172-6181. doi:10.1128/aem.68.12.6172-6181.2002 (Pubitemid 36342454)
50. Vieira J, Messing J (1991) New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194
51. Wang J, Zhong Z, Zhang W, Bao Q, Wei A, Meng H, Zhang H (2012) Comparative analysis of the gene expression profile of probiotic Lactobacillus casei Zhang with and without fermented milk as a vehicle during transit in a simulated gastrointestinal tract. Res Microbiol 163(5):357-365. doi:10.1016/j.resmic.2012.04.002
52. Wei M-Q, Rush CM, Norman JM, Hafner LM, Epping RJ, Timms P (1995) An improved method for the transformation of Lactobacillus strains using electroporation. J Microbiol Methods 21(1):97-109. doi:10.1016/0167-7012(94) 00038-9
53. Wells J, Mercenier A (2008) Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol 6(5):349-362. doi:10.1038/nrmicro1040 (Pubitemid 351552656)
54. Yoshimoto T, Walter R, Tsuru D (1980) Proline-specific endopeptidase from Flavobacterium. Purification and properties. J Biol Chem 255(10):4786-4792 (Pubitemid 10049693)
55. Yoshimoto T, Kanatani A, Shimoda T, Inaoka T, Kokubo T, Tsuru D(1991) Prolyl endopeptidase from Flavobacteriummeningosepticum: cloning and sequencing of the enzyme gene. J Biochem 110(6):873-878