Heterologous expression and delivery of biologically active exendin-4 by lactobacillus paracasei L14

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Zeng, Zhu ^a   Yu, Rui ^a   Zuo, Fanglei ^a   Zhang, Bo ^a   Peng, Deju ^b   Ma, Huiqin ^a   Chen, Shangwu ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Yangling Zhongyang Joint Ranch Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; TRANSCRIPTION FACTOR PDX 1; HOMEODOMAIN PROTEIN; INSULIN; MESSENGER RNA; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; PEPTIDE; RECOMBINANT PROTEIN; TRANSACTIVATOR PROTEIN; VENOM;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL STRAIN; CELL PROLIFERATION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; FEASIBILITY STUDY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; INSULIN SYNTHESIS; LACTOBACILLUS PARACASEI; LIMIT OF QUANTITATION; NONHUMAN; PANCREAS ISLET BETA CELL; PDX1 GENE; RAT; UPREGULATION; ANIMAL; BIOSYNTHESIS; CACO-2 CELL LINE; CELL LINE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PLASMID;

ANIMALS; APOPTOSIS; CACO-2 CELLS; CELL LINE; CELL PROLIFERATION; GENE EXPRESSION REGULATION, BACTERIAL; HOMEODOMAIN PROTEINS; HUMANS; INSULIN; LACTOBACILLUS PARACASEI; PEPTIDES; PLASMIDS; RATS; RECOMBINANT PROTEINS; RNA, MESSENGER; TRANS-ACTIVATORS; UP-REGULATION; VENOMS;

EID: 84992316577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165130     Document Type: Article

References (65)

1. Drucker DJ. Glucagon-like peptides. Diabetes. 1998; 47: 159-169 PMID: 9519708
2. Nauck MA, Wollschlager D, Werner J, Holst JJ, Orskov C, Creutzfeldt W, et al. Effects of subcutaneous glucagon-like peptide 1 (GLP-1 [7-36 amide]) in patients with NIDDM. Diabetologia. 1996; 39: 1546-1553 PMID: 8960841
3. Willms B, Werner J, Holst JJ, Orskov C, Creutzfeldt W, Nauck MA. Gastric emptying, glucose responses and insulin secretion after a liquid test meal: Effects of exogenous glucagon-like peptide-1 (GLP-1)-(7-36) amide in type 2 (noninsulin-dependent) diabetic patients. J Clin Endocrinol Metab. 1996; 81: 327-332 doi: 10.1210/jcem.81.1.8550773 PMID: 8550773
4. Wang Q, Li L, Xu E, Wong V, Rhodes C, Brubaker PL. Glucagon-like peptide-1 regulates proliferation and apoptosis via activation of protein kinase B in pancreatic INS-1 beta cells. Diabetologia. 2004; 47: 478-487 doi: 10.1007/s00125-004-1327-5 PMID: 14762654
5. Verspohl EJ. Novel therapeutics for type 2 diabetes: Incretin hormone mimetics (glucagon-like peptide-1 receptor agonists) and dipeptidyl peptidase-4 inhibitors. Pharmacol Therapeut. 2009; 124: 113-138
6. Zander M, Madsbad S, Madsen JL, Holst JJ. Effect of 6-week course of glucagon-like peptide 1 on glycaemic control, insulin sensitivity, and beta-cell function in type 2 diabetes: a parallel-group study. Lancet. 2002; 359: 824-830 doi: 10.1016/S0140-6736(02)07952-7 PMID: 11897280
7. Sarkar G, Alattar M, Brown RJ, Quon MJ, Harlan DM, Rother KI. Exenatide treatment for 6 months improves insulin sensitivity in adults with type 1 diabetes. Diabetes Care. 2014; 37: 666-670 doi: 10. 2337/dc13-1473 PMID: 24194508
8. Holst JJ, Deacon CF. Inhibition of the activity of dipeptidyl-peptidase IV as a treatment for type 2 diabetes. Diabetes. 1998; 47: 1663-1670 PMID: 9792533
9. Neumiller JJ. Incretin-based therapies. Med Clin North Am. 2015; 99(1): 107-129 doi: 10.1016/j. mcna.2014.08.013 PMID: 25456646
10. Mest HJ, Mentlein R. Dipeptidyl peptidase inhibitors as new drugs for the treatment of type 2 diabetes. Diabetologia. 2005; 48(4): 616-620 doi: 10.1007/s00125-005-1707-5 PMID: 15770466
11. Eng J, Kleinman WA, Singh L, Singh G, Raufman JP. Isolation and characterization of exendin-4, an exendin-3 analogue, from Heloderma suspectum venom. Further evidence for an exendin receptor on dispersed acini from guinea pig pancreas. J Biol Chem. 1992; 267: 7402-7405 PMID: 1313797
12. Edwards CM, Stanley SA, Davis R, Brynes AE, Frost GS, Seal LJ, et al. Exendin-4 reduces fasting and postprandial glucose and decreases energy intake in healthy volunteers. Am J Physiol Endocrinol Metab. 2001; 281: E155-E161 PMID: 11404233
13. Buse JB, Henry RR, Han J, Kim DD, Fineman MS, Baron AD. Effects of exenatide (exendin-4) on glycemic control over 30 weeks in sulfonylurea treated patients with type 2 diabetes. Diabetes Care. 2004; 27: 2628-2635 PMID: 15504997
14. Kendall DM, Riddle MC, Rosenstock J, Zhuang DL, Kim DD, Fineman MS, et al. Effects of exenatide (exendin-4) on glycemic control over 30 weeks in patients with type 2 diabetes mellitus treated with metformin and a sulfonylurea. Diabetes Care. 2005; 28: 1083-1091 PMID: 15855571
15. Xu G, Kaneto H. GLP-1/exendin-4 facilitates β-cell neogenesis in rat and human pancreatic ducts. Diabetes Res Clin Pract. 2006; 73: 107-110 doi: 10.1016/j.diabres.2005.11.007 PMID: 16406191
16. Drucker DJ, Nauck MA. The incretin system: glucagonlike peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. The Lancet. 2006; 368 (9548): 1696-1705
17. Bydureon (exenatide extended-release for injectable suspension) [package insert]. Wilmington, DE: AstraZeneca Pharmaceuticals LP; 2014
18. Shaji J, Patole V. Protein and peptide drug delivery: oral approaches. Indian J Pharm Sci. 2008; 70 (3): 269-277 doi: 10.4103/0250-474X.42967 PMID: 20046732
19. Rekha MA, Sharma CP. Oral delivery of therapeutic protein/peptide for diabetes-Future perspectives. Int J Pharm. 2013; 440: 48-62 doi: 10.1016/j.ijpharm.2012.03.056 PMID: 22503954
20. Bouttefeux O, Beloqui A, PreǍat V. Delivery of peptides via the oral route: diabetes treatment by peptide-loaded nanoparticles. Curr Pharm Design. 2016; 22: 1161-1176
21. Fonte P, Araujo F, Silva C, Pereira C, Reis S, Santos HA, et al. Polymer-based nanoparticles for oral insulin delivery: revisited approaches. Biotechnol Adv. 2015; 33: 1342-1354 doi: 10.1016/j. biotechadv.2015.02.010 PMID: 25728065
22. Gupta V, Hwang BH, Doshi N, Banerjee A, Anselmo AC, Mitragotri S. Delivery of exenatide and insulin using mucoadhesive intestinal devices. Ann Biomed Eng. 2016; 44(6): 1993-2007 doi: 10.1007/s10439-016-1558-x PMID: 26864536
23. SaǍnchez-Navarro M, Garcia J, Giralt E, TeixidoǍ M. Using peptides to increase transport across the intestinal barrier. Adv Drug Deliv Rev. 2016. http://dx.doi.org/10.1016/j.addr.2016.04.031
24. Castro PM, Fonte P, Sousa F, Madureira AR, Sarmento B, Pintado ME. Oral films as breakthrough tools for oral delivery of proteins/peptides. J Control Release. 2015; 211: 63-73 doi: 10.1016/j.jconrel. 2015.05.258 PMID: 25979328
25. Lopes M, Simoes S, Veiga F, Seica R, Ribeiro A. Why most oral insulin formulations do not reach clinical trials. Ther Deliv. 2015; 6: 1-15
26. Wyszynska A, Kobierecka P, Bardowski J, Jagusztyn-Krynicka EK. Lactic acid bacteria 20 years exploring their potential as live vectors for mucosal vaccination. Appl Microbiol Biotechnol. 2015; 99: 2967-2977 doi: 10.1007/s00253-015-6498-0 PMID: 25750046
27. Cano-Garrido O, Seras-Franzoso J, Garcia-FruitoǍs E. Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microb Cell Fact. 2015; 14: 137 doi: 10.1186/s12934-015-0313-6 PMID: 26377321
28. Wang W, Gao ZQ, Zhong YG, Pan L. Lactic acid bacteria as mucosal delivery vehicles: a realistic therapeutic option. Appl Microbiol Biotechnol. 2016; 100: 5691-5701 doi: 10.1007/s00253-016-7557-x PMID: 27154346
29. Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol. 2010; 7: 503-514 doi: 10.1038/nrgastro.2010.117 PMID: 20664519
30. Ouwehand AC, Kirjavainen PV, Gronlund M-M, Isolauri E, Salminen S. Adhesion of probiotic microorganisms to intestinal mucus. Int Dairy J. 1999; 9: 623-630
31. Kaushal G, Trombetta L, Ochs RS, Shao J. Delivery of TEM beta-lactamase by gene-transformed Lactococcus lactis subsp. lactis through cervical cell monolayer. Int J Pharm. 2006; 313(1-2): 29-35 doi: 10.1016/j.ijpharm.2006.01.013 PMID: 16488095
32. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol. 2006; 4 (6): 754-759 doi: 10.1016/j.cgh.2006.03.028 PMID: 16716759
33. Ng DT, Sarkar CA. Nisin-inducible secretion of a biologically active single-chain insulin analog by Lactococcus lactis NZ9000. Biotechnol Bioeng. 2011; 108: 1987-1996 doi: 10.1002/bit.23130 PMID: 21391210
34. Ma Y, Liu J, Hou J, Dong Y, Lu Y, Jin L, et al. Oral administration of recombinant Lactococcus lactis expressing HSP65 and tandemly repeated P277 reduces the incidence of type I diabetes in non-obese diabetic mice. PLOS ONE. 2014; 9: e105701 doi: 10.1371/journal.pone.0105701 PMID: 25157497
35. Agarwal P, Khatri P, Billack B, Low W-K, Shao J. Oral delivery of glucagon like peptide-1 by a recombinant Lactococcus lactis. Pharm. Res. 2014; 31: 3404-3414 doi: 10.1007/s11095-014-1430-3 PMID: 24928365
36. Robert S, Gysemans C, Takiishi T, Korf H, Spagnuolo I, Sebastiani G, et al. Oral delivery of glutamic acid decarboxylase (GAD)-65 and IL10 by Lactococcus lactis reverses diabetes in recent-onset NOD mice. Diabetes. 2014; 63: 2876-2887 doi: 10.2337/db13-1236 PMID: 24677716
37. Wei P, Yang Y, Li T, Ding Q, Sun H. An engineered Bifidobacterium longum secreting a bioactive penetratin-Glucagon-like peptide 1 fusion protein enhances Glucagon-like peptide 1 absorption in the intestine. J Microbiol Biotechn. 2015; doi: 10.4014/jmb.1412.12030 PMID: 25674803
38. Duan FF, Liu JH, March JC. Engineered commensal bacteria reprogram intestinal cells into glucoseresponsive insulin-secreting cells for the treatment of diabetes. Diabetes. 2015; 64: 1794-1803 doi: 10.2337/db14-0635 PMID: 25626737
39. van de Guchte M, van der Vossen JMBM, Kok J, Venema G. Construction of a lactococcal expression vector: expression of hen egg white lysozyme in Lactococcus lactis subsp. lactis. Appl Environ Microbiol. 1989; 55: 224-228 PMID: 2495760
40. Schaégger H. Tricine-sds-page. Nat Protoc. 2006; 1: 16-22 doi: 10.1038/nprot.2006.4 PMID: 17406207
41. Zhang B, Li AD, Zuo FL, Yu R, Zeng Z, Ma HQ, et al. Recombinant Lactococcus lactis NZ9000 secretes a bioactive kisspeptin that inhibits proliferation and migration of human colon carcinoma HT-29 cells. Microb Cell Fact. 2016; 15: 102 doi: 10.1186/s12934-016-0506-7 PMID: 27287327
42. Hohmeier HE, Mulder H, Chen GX, Henkel-Rieger R, Prentki M, Newgard CB. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and-independent glucose-stimulated insulin secretion. Diabetes. 2000; 49: 424-430 PMID: 10868964
43. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008; 3: 1101-1108 PMID: 18546601
44. Hubatsch I, Ragnarsson EGE, Artursson P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat Protoc. 2007; 2: 2111-2119 doi: 10.1038/nprot.2007.303 PMID: 17853866
45. Habener JF, Stoffers DA. A newly discovered role of transcription factors involved in pancreas development and the pathogenesis of diabetes mellitus. Proc Assoc Am Physicians. 1998; 110: 12-21 PMID: 9460079
46. Stoffers DA, Kieffer TJ, Hussain MA, Drucker DJ, Bonner-Weir S, Habener JF, et al. Insulinotropic glucagon-like peptide 1 agonists stimulate expression of homeodomain protein IDX-1 and increase islet size in mouse pancreas. Diabetes. 2000; 49: 741-748 PMID: 10905482
47. Wang X, Zhou J, Doyle ME, Egan JM. Glucagon-like peptide-1 causes pancreatic duodenal homeobox-1 protein translocation from the cytoplasm to the nucleus of pancreatic beta-cells by a cyclic adenosine monophosphate/protein kinase A-dependent mechanism. Endocrinology. 2001; 142: 1820-1827 doi: 10.1210/endo.142.5.8128 PMID: 11316746
48. Thum A, Hupe-Sodmann K, Goke R, Voigt K, Goke B, McGregor GP. Endoproteolysis by isolated membrane peptidases reveal metabolic stability of glucagon-like peptide-1 analogs, exendins-3 and-4. Exp Clin Endocrinol Diabetes. 2002; 110: 113-118 doi: 10.1055/s-2002-29087 PMID: 12012270
49. Belmokhtar CA, Hillion J, SeǍgal-Bendirdjian E. Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene. 2001; 20(26): 3354-3362 doi: 10.1038/sj.onc.1204436 PMID: 11423986
50. Thuret G, Chiquet C, Herrag S, Dumollard JM, Boudard D, Bednarz J, et al. Mechanisms of staurosporine induced apoptosis in a human corneal endothelial cell line. Br J Ophthalmol. 2003; 87(3): 346-352 PMID: 12598452
51. Shao J, Kaushal G. Normal flora: living vehicles for non-invasive protein drug delivery. Int J of Pharm. 2004; 286: 117-124
52. Le Loir Y, Nouaille S, Commissaire J, BreǍtigny L, Gruss A, Langella P. Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis. Appl Environ Microbiol. 2001; 67 (9): 4119-4127 doi: 10.1128/AEM.67.9.4119-4127.2001 PMID: 11526014
53. Schotte L, Steidler L, Vandekerckhove J, Remaut E. Secretion of biologically active murine interleukin-10 by Lactococcus lactis. Enzyme Microb Technol. 2000; 27(10): 761-765 PMID: 11118583
54. Khokhlova EV, Efimov AB, Kafarskaia LI, Shkoporov AN. Heterologous expression of secreted biologically active human interleukin-10 in Bifidobacterium breve. Arch Microbiol. 2010; 192: 769-774 doi: 10.1007/s00203-010-0606-4 PMID: 20631991
55. Wells JM, Mercenier A. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol. 2008; 6(5): 349-362 doi: 10.1038/nrmicro1840 PMID: 18345021
56. Hartstra AV, Bouter KEC, Baéckhed F, Nieuwdorp M. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care. 2015; 38: 159-165 doi: 10.2337/dc14-0769 PMID: 25538312
57. Charman WN, Porter CJ, Mithani S, Dressman JB. Physiochemical and physiological mechanisms for the effects of food on drug absorption: The role of lipids and pH. J Pharm Sci. 1997; 86(3): 269-282 doi: 10.1021/js960085v PMID: 9050793
58. Chepurny OG, Hussain MA, Holz GG. Exendin-4 as a stimulator of rat insulin I gene promoter activity via bZIP/CRE interactions sensitive to serine/threonine protein kinase inhibitor Ro 31-8220. Endocrinology. 2002; 143: 2303-2313 doi: 10.1210/endo.143.6.8870 PMID: 12021195
59. Hirayama K, Rafter J. The role of lactic acid bacteria in colon cancer prevention: mechanistic considerations. Antonie van Leeuwenhoek. 1999; 76: 391-394 PMID: 10532395
60. Nami Y, Abdullah N, Haghshenas B, Radiah D, Rosli R, Khosroushahi AY. Probiotic potential and biotherapeutic effects of newly isolated vaginal Lactobacillus acidophilus 36YL strain on cancer cells. Anaerobe. 2014; 28: 29-36 doi: 10.1016/j.anaerobe.2014.04.012 PMID: 24818631
61. Pinto M, Robine-Leon S, Appay M-D, Kedinger M, Triadou N, Dussaulx E, et al. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell.1983; 47: 323-330
62. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, et al. Selective increases of bifidobacteria in gut microflora improve high-fat diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007; 50: 2374-2383 doi: 10.1007/s00125-007-0791-0 PMID: 17823788
63. Baboota RK, Bishnoi M, Ambalam P, Kondepudi KK, Sarma SM, Boparai RK, et al. Functional food ingredients for the management of obesity and associated co-morbidities-A review. J Funct Foods. 2013; 5: 997-1012
64. Miyoshi M, Ogawa A, Higurashi S, Kadooka Y. Antiobesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in dietinduced obese mice. Eur J Nutr. 2014; 53: 599-606 doi: 10.1007/s00394-013-0568-9 PMID: 23917447
65. Zeng Z, Luo JY, Zuo FL, Zhang Y, Ma HQ, Chen SW. Screening for potential novel probiotic Lactobacillus strains based on high dipeptidyl peptidase IV and a-glucosidase inhibitory activity. J Funct Foods. 2016; 20: 486-495