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The Potential Role of the Dipeptidyl Peptidase-4-Like Activity From the Gut Microbiota on the Host Health

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Olivares Sevilla, Marta [UCL] Schüppel, Valentina Hassan, Ahmed M. Beaumont, Martin [UCL] Neyrinck, Audrey M. [UCL] Bindels, Laure B. [UCL] Delzenne, Nathalie M. [UCL]

The Dipeptidyl peptidase-4 (DPP-4) activity influences metabolic, behavioral and intestinal disorders through the cleavage of key hormones and peptides. Some studies describe the existence of human DPP-4 homologs in commensal bacteria, for instance in Prevotella or Lactobacillus. However, the role of the gut microbiota as a source of DPP-4-like activity has never been investigated. Through the comparison of the DPP-4 activity in the cecal content of germ-free mice (GFM) and gnotobiotic mice colonized with the gut microbiota of a healthy subject, we bring the proof of concept that a significant DPP-4-like activity occurs in the microbiota. By analyzing the existing literature, we propose that DPP-4-like activity encoded by the intestinal microbiome could constitute a novel mechanism to modulate protein digestion as well as host metabolism and behavior.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2018
Language Anglais
Journal information "Frontiers in Microbiology" - Vol. 9, p. 1900 [1-10] (2018)
Peer reviewed yes
Publisher Frontiers Research Foundation ((Switzerland) Basel)
e-issn 1664-302X
Publication status Publié
Affiliation UCL - SSS/LDRI - Louvain Drug Research Institute
Keywords Microbiology (medical) ; Microbiology ; DPP-4 activity ; PepX activity ; Gut microbiota ; Microbiome ; Metabolism ; Behavior
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  1. Ahmed Radwan H., Huri Hasniza Zaman, Muniandy Sekaran, Al-Hamodi Zaid, Al-absi Boshra, Alsalahi Abdulsamad, Razif Muhammad FM, Altered circulating concentrations of active glucagon-like peptide (GLP-1) and dipeptidyl peptidase 4 (DPP4) in obese subjects and their association with insulin resistance, 10.1016/j.clinbiochem.2017.03.008
  2. Anastasiou R., Papadelli M., Georgalaki M.D., Kalantzopoulos G., Tsakalidou E., Cloning and sequencing of the gene encoding X-prolyl-dipeptidyl aminopeptidase (PepX) fromStreptococcus thermophilusstrain ACA-DC 4, 10.1046/j.1365-2672.2002.01659.x
  3. Anderberg Rozita H, Richard Jennifer E, Hansson Caroline, Nissbrandt Hans, Bergquist Filip, Skibicka Karolina P., GLP-1 is both anxiogenic and antidepressant; divergent effects of acute and chronic GLP-1 on emotionality, 10.1016/j.psyneuen.2015.11.021
  4. Bansal T., Alaniz R. C., Wood T. K., Jayaraman A., The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation, 10.1073/pnas.0906112107
  5. Blachier F., Mariotti F., Huneau J. F., Tomé D., Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences, 10.1007/s00726-006-0477-9
  6. Breton Jonathan, Tennoune Naouel, Lucas Nicolas, Francois Marie, Legrand Romain, Jacquemot Justine, Goichon Alexis, Guérin Charlène, Peltier Johann, Pestel-Caron Martine, Chan Philippe, Vaudry David, do Rego Jean-Claude, Liénard Fabienne, Pénicaud Luc, Fioramonti Xavier, Ebenezer Ivor S., Hökfelt Tomas, Déchelotte Pierre, Fetissov Sergueï O., Gut Commensal E. coli Proteins Activate Host Satiety Pathways following Nutrient-Induced Bacterial Growth, 10.1016/j.cmet.2015.10.017
  7. Caminero Alberto, Galipeau Heather J., McCarville Justin L., Johnston Chad W., Bernier Steve P., Russell Amy K., Jury Jennifer, Herran Alexandra R., Casqueiro Javier, Tye-Din Jason A., Surette Michael G., Magarvey Nathan A., Schuppan Detlef, Verdu Elena F., Duodenal Bacteria From Patients With Celiac Disease and Healthy Subjects Distinctly Affect Gluten Breakdown and Immunogenicity, 10.1053/j.gastro.2016.06.041
  8. Cani Patrice D., Gut microbiota — at the intersection of everything?, 10.1038/nrgastro.2017.54
  9. Cani Patrice D., Neyrinck Audrey M., Maton Nicole, Delzenne Nathalie M., Oligofructose Promotes Satiety in Rats Fed a High-Fat Diet: Involvement of Glucagon-Like Peptide-1, 10.1038/oby.2005.117
  10. Canneva Fabio, Golub Yulia, Distler Joerg, Dobner Julia, Meyer Sandra, von Hörsten Stephan, DPP4-deficient congenic rats display blunted stress, improved fear extinction and increased central NPY, 10.1016/j.psyneuen.2015.01.007
  11. Conarello S. L., Li Z., Ronan J., Roy R. S., Zhu L., Jiang G., Liu F., Woods J., Zycband E., Moller D. E., Thornberry N. A., Zhang B. B., Mice lacking dipeptidyl peptidase IV are protected against obesity and insulin resistance, 10.1073/pnas.0631828100
  12. Cooper K. G., Woods J. P., Secreted Dipeptidyl Peptidase IV Activity in the Dimorphic Fungal Pathogen Histoplasma capsulatum, 10.1128/iai.01345-08
  13. Cordero Oscar J., Salgado Francisco J., Nogueira Montserrat, On the origin of serum CD26 and its altered concentration in cancer patients, 10.1007/s00262-009-0728-1
  14. Cox Helen M., Peptide YY: A neuroendocrine neighbor of note, 10.1016/j.peptides.2006.07.023
  15. Cuenco Joyceline, Minnion James, Tan Tricia, Scott Rebecca, Germain Natacha, Ling Yiin, Chen Rong, Ghatei Mohammad, Bloom Stephen, Degradation Paradigm of the Gut Hormone, Pancreatic Polypeptide, by Hepatic and Renal Peptidases, 10.1210/en.2016-1827
  16. De Angelis M., Cassone A., Rizzello C. G., Gagliardi F., Minervini F., Calasso M., Di Cagno R., Francavilla R., Gobbetti M., Mechanism of Degradation of Immunogenic Gluten Epitopes from Triticum turgidum L. var. durum by Sourdough Lactobacilli and Fungal Proteases, 10.1128/aem.01630-09
  17. Delzenne Nathalie M., Bindels Laure B., Gut microbiota in 2017: Contribution of gut microbiota–host cooperation to drug efficacy, 10.1038/nrgastro.2017.170
  18. Delzenne Nathalie M., Cani Patrice D., Everard Amandine, Neyrinck Audrey M., Bindels Laure B., Gut microorganisms as promising targets for the management of type 2 diabetes, 10.1007/s00125-015-3712-7
  19. Delzenne Nathalie M., Neyrinck Audrey M., Bäckhed Fredrik, Cani Patrice D., Targeting gut microbiota in obesity: effects of prebiotics and probiotics, 10.1038/nrendo.2011.126
  20. Detel Dijana, Per??i?? Mladen, Varljen Jadranka, Serum and Intestinal Dipeptidyl Peptidase IV (DPP IV/CD26) Activity in Children With Celiac Disease : , 10.1097/mpg.0b013e318054b085
  21. Detel Dijana, Pugel Ester Pernjak, Pucar Lara Baticic, Buljevic Suncica, Varljen Jadranka, Development and resolution of colitis in mice with target deletion of dipeptidyl peptidase IV : Colitis in CD26-deficient mice, 10.1113/expphysiol.2011.061143
  22. Do Thi Thu Huong, Hindlet Patrick, Waligora-Dupriet Anne-Judith, Kapel Nathalie, Neveux Nathalie, Mignon Virginie, Deloménie Claudine, Farinotti Robert, Fève Bruno, Buyse Marion, Disturbed intestinal nitrogen homeostasis in a mouse model of high-fat diet-induced obesity and glucose intolerance, 10.1152/ajpendo.00437.2013
  23. ELYACOUBI M, VAUGEOIS J, MARGUET D, SAUZE N, GUIEU R, COSTENTIN J, FENOUILLET E, Behavioral characterization of CD26 deficient mice in animal tests of anxiety and antidepressant-like activity, 10.1016/j.bbr.2006.04.003
  24. Elgün Serenay, Keskinege Aytaç, Kumbasar Hakan, Dipeptidyl peptidase IV and adenosine deaminase activity, 10.1016/s0306-4530(99)00039-6
  25. Everard Amandine, Cani Patrice D., Gut microbiota and GLP-1, 10.1007/s11154-014-9288-6
  26. Fteita Dareen, Könönen Eija, Gürsoy Mervi, Söderling Eva, Gürsoy Ulvi Kahraman, Does estradiol have an impact on the dipeptidyl peptidase IV enzyme activity of the Prevotella intermedia group bacteria?, 10.1016/j.anaerobe.2015.09.002
  27. Fteita Dareen, Musrati Ahmed Ali, Könönen Eija, Ma Xiaochu, Gürsoy Mervi, Peurla Markus, Söderling Eva, Sintim Herman O., Gürsoy Ulvi Kahraman, Dipeptidyl peptidase IV and quorum sensing signaling in biofilm-related virulence of Prevotella aurantiaca, 10.1016/j.anaerobe.2017.08.009
  28. Gatti M., De Dea Lindner J., Gardini F., Mucchetti G., Bevacqua D., Fornasari M.E., Neviani E., A Model to Assess Lactic Acid Bacteria Aminopeptidase Activities in Parmigiano Reggiano Cheese During Ripening, 10.3168/jds.2008-1069
  29. Geier Mark S., Tenikoff Danik, Yazbeck Roger, McCaughan Geoffrey W., Abbott Catherine A., Howarth Gordon S., Development and resolution of experimental colitis in mice with targeted deletion of dipeptidyl peptidase IV, 10.1002/jcp.20333
  30. Glaser Philippe, Rusniok Christophe, Buchrieser Carmen, Chevalier Fabien, Frangeul Lionel, Msadek Tarek, Zouine Mohamed, Couvé Elisabeth, Lalioui Lila, Poyart Claire, Trieu-Cuot Patrick, Kunst Frank, Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease : Genome sequence of Streptococcus agalactiae, 10.1046/j.1365-2958.2002.03126.x
  31. Goldstein J. M., Banbula A., Kordula T., Mayo J. A., Travis J., Novel Extracellular x-Prolyl Dipeptidyl-Peptidase (DPP) from Streptococcus gordonii FSS2: an Emerging Subfamily of Viridans Streptococcal x-Prolyl DPPs, 10.1128/iai.69.9.5494-5501.2001
  32. Gorrell M. D., Gysbers V., McCaughan G. W., CD26: A Multifunctional Integral Membrane and Secreted Protein of Activated Lymphocytes, 10.1046/j.1365-3083.2001.00984.x
  33. GUIEU R, FENOUILLET E, DEVAUX C, FAJLOUN Z, CARREGA L, SABATIER J, SAUZE N, MARGUET D, CD26 modulates nociception in mice via its dipeptidyl-peptidase IV activity, 10.1016/j.bbr.2005.08.003
  34. Hassan Ahmed M., Jain Piyush, Mayerhofer Raphaela, Fröhlich Esther E., Farzi Aitak, Reichmann Florian, Herzog Herbert, Holzer Peter, Visceral hyperalgesia caused by peptide YY deletion and Y2 receptor antagonism, 10.1038/srep40968
  35. HELLSTRÖM P. M., HEIN J., BYTZER P., BJÖRNSSÖN E., KRISTENSEN J., SCHAMBYE H., Clinical trial: the glucagon-like peptide-1 analogue ROSE-010 for management of acute pain in patients with irritable bowel syndrome: a randomized, placebo-controlled, double-blind study, 10.1111/j.1365-2036.2008.03870.x
  36. M. Hildebrandt, M. Rose, J. Rüter,, Dipeptidyl Peptidase IV (DP IV, CD26) in Patients with Inflammatory Bowel Disease, 10.1080/003655201750422675
  37. Holzer Peter, Reichmann Florian, Farzi Aitak, Neuropeptide Y, peptide YY and pancreatic polypeptide in the gut–brain axis, 10.1016/j.npep.2012.08.005
  38. Hopsu-Havu V�in� K., Glenner George G., A new dipeptide naphthylamidase hydrolyzing glycyl-prolyl-?-naphthylamide, 10.1007/bf00577838
  39. Isacson Ruben, Nielsen Elisabet, Dannaeus Karin, Bertilsson Göran, Patrone Cesare, Zachrisson Olof, Wikström Lilian, The glucagon-like peptide 1 receptor agonist exendin-4 improves reference memory performance and decreases immobility in the forced swim test, 10.1016/j.ejphar.2010.10.008
  40. Kamble Mayur, Gupta Rachna, Rehan Harmeet S., Gupta Lalit K., Neurobehavioral effects of liraglutide and sitagliptin in experimental models, 10.1016/j.ejphar.2016.02.003
  41. Karagiannis T., Paschos P., Paletas K., Matthews D. R., Tsapas A., Dipeptidyl peptidase-4 inhibitors for treatment of type 2 diabetes mellitus in the clinical setting: systematic review and meta-analysis, 10.1136/bmj.e1369
  42. Klemann C., Wagner L., Stephan M., von Hörsten S., Cut to the chase: a review of CD26/dipeptidyl peptidase-4's (DPP4) entanglement in the immune system : CD26/DPP4 in the immune system, 10.1111/cei.12781
  43. Kozakova Hana, Kolinska Jirina, Lojda Zdenek, Rehakova Zuzana, Sinkora Jiri, Zakostelecka Marie, Splichal Igor, Tlaskalova-Hogenova Helena, Effect of bacterial monoassociation on brush-border enzyme activities in ex-germ-free piglets: comparison of commensal and pathogenic Escherichia coli strains, 10.1016/j.micinf.2006.07.008
  44. Kozáková H., Řeháková Z., Kolínská J., Bifidobacterium bifidum monoassociation of gnotobiotic mice: Effect on enterocyte brush-border enzymes, 10.1007/bf02818005
  45. Kozáková, Physiol. Res., 47, 253 (1998)
  46. Laparra J.M., Sanz Y., Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion, 10.1002/jcb.22459
  47. Lin Yin, Krogh-Andersen Kasper, Pelletier Julien, Marcotte Harold, Östenson Claes-Göran, Hammarström Lennart, Oral Delivery of Pentameric Glucagon-Like Peptide-1 by Recombinant Lactobacillus in Diabetic Rats, 10.1371/journal.pone.0162733
  48. Ma MingJie, Hasegawa Yu, Koibuchi Nobutaka, Toyama Kensuke, Uekawa Ken, Nakagawa Takashi, Lin Bowen, Kim-Mitsuyama Shokei, DPP-4 inhibition with linagliptin ameliorates cognitive impairment and brain atrophy induced by transient cerebral ischemia in type 2 diabetic mice, 10.1186/s12933-015-0218-z
  49. Magdy Yosra M., El-Kharashi Omnyah A., Nabih Enas S., Shaker Safaa M., Abd-Elaziz Lobna F., Aboul-Fotouh Sawsan, Potential involvement of JNK1 repression in the hepatic effect of sitagliptin and metformin in rats subjected to high fat diet and chronic mild distress, 10.1016/j.biopha.2016.10.098
  50. Marguet D., Baggio L., Kobayashi T., Bernard A.-M., Pierres M., Nielsen P. F., Ribel U., Watanabe T., Drucker D. J., Wagtmann N., Enhanced insulin secretion and improved glucose tolerance in mice lacking CD26, 10.1073/pnas.120069197
  51. Mascolo Annamaria, Rafaniello Concetta, Sportiello Liberata, Sessa Maurizio, Cimmaruta Daniela, Rossi Francesco, Capuano Annalisa, Dipeptidyl Peptidase (DPP)-4 Inhibitor-Induced Arthritis/Arthralgia: A Review of Clinical Cases, 10.1007/s40264-016-0399-8
  52. Matos, Appl. Environ. Microbiol., 64, 4591 (1998)
  53. Mimura Shunya, Ando Takafumi, Ishiguro Kazuhiro, Maeda Osamu, Watanabe Osamu, Ujihara Masaki, Hirayama Yutaka, Morise Kazuhiro, Maeda Keiko, Matsushita Masanobu, Funasaka Kohei, Nakamura Masanao, Miyahara Ryoji, Ozaki Nobuaki, Goto Hidemi, Dipeptidyl peptidase-4 inhibitor anagliptin facilitates restoration of dextran sulfate sodium-induced colitis, 10.3109/00365521.2013.832366
  54. Moran G.W., O'Neill C., Padfield P., McLaughlin J.T., Dipeptidyl peptidase-4 expression is reduced in Crohn's disease, 10.1016/j.regpep.2012.04.006
  55. Moulton C.D., Pickup J.C., Amiel S.A., Winkley K., Ismail K., Investigating incretin-based therapies as a novel treatment for depression in type 2 diabetes: Findings from the South London Diabetes (SOUL-D) Study, 10.1016/j.pcd.2015.06.003
  56. Mulvihill Erin E., Varin Elodie M., Gladanac Bojana, Campbell Jonathan E., Ussher John R., Baggio Laurie L., Yusta Bernardo, Ayala Jennifer, Burmeister Melissa A., Matthews Dianne, Bang K.W. Annie, Ayala Julio E., Drucker Daniel J., Cellular Sites and Mechanisms Linking Reduction of Dipeptidyl Peptidase-4 Activity to Control of Incretin Hormone Action and Glucose Homeostasis, 10.1016/j.cmet.2016.10.007
  57. Naveilhan Philippe, Hassani Hessameh, Lucas Guilherme, Blakeman Karin Hygge, Hao Jing-Xia, Xu Xiao-Jun, Wiesenfeld-Hallin Zsuzsanna, Thorén Peter, Ernfors Patrik, Reduced antinociception and plasma extravasation in mice lacking a neuropeptide Y receptor, 10.1038/35054063
  58. Nozu Tsukasa, Miyagishi Saori, Kumei Shima, Nozu Rintaro, Takakusaki Kaoru, Okumura Toshikatsu, Glucagon-like peptide-1 analog, liraglutide, improves visceral sensation and gut permeability in rats : Liraglutide improves visceral sensation, 10.1111/jgh.13808
  59. Olivares Marta, Neyrinck Audrey M., Pötgens Sarah A., Beaumont Martin, Salazar Nuria, Cani Patrice D., Bindels Laure B., Delzenne Nathalie M., The DPP-4 inhibitor vildagliptin impacts the gut microbiota and prevents disruption of intestinal homeostasis induced by a Western diet in mice, 10.1007/s00125-018-4647-6
  60. Pedersen Helle Krogh, Gudmundsdottir Valborg, Nielsen Henrik Bjørn, Hyotylainen Tuulia, Nielsen Trine, Jensen Benjamin A. H., Forslund Kristoffer, Hildebrand Falk, Prifti Edi, Falony Gwen, Le Chatelier Emmanuelle, Levenez Florence, Doré Joel, Mattila Ismo, Plichta Damian R., Pöhö Päivi, Hellgren Lars I., Arumugam Manimozhiyan, Sunagawa Shinichi, Vieira-Silva Sara, Jørgensen Torben, Holm Jacob Bak, Trošt Kajetan, Consortium MetaHIT, Kristiansen Karsten, Brix Susanne, Raes Jeroen, Wang Jun, Hansen Torben, Bork Peer, Brunak Søren, Oresic Matej, Ehrlich S. Dusko, Pedersen Oluf, Human gut microbes impact host serum metabolome and insulin sensitivity, 10.1038/nature18646
  61. Rawlings Neil D., Barrett Alan J., Finn Robert, Twenty years of theMEROPSdatabase of proteolytic enzymes, their substrates and inhibitors, 10.1093/nar/gkv1118
  62. Redrobe J, The Neuropeptide Y (NPY) Y1 Receptor Subtype Mediates NPY-induced Antidepressant-like Activity in the Mouse Forced Swimming Test, 10.1016/s0893-133x(01)00403-1
  63. Rigolet Pascal, Xi Xu Guang, Rety Stephane, Chich Jean-François, The structural comparison of the bacterial PepX and human DPP-IV reveals sites for the design of inhibitors of PepX activity : Sites for the design of inhibitors of PepX activity, 10.1111/j.1742-4658.2005.04631.x
  64. Rosmaninho-Salgado Joana, Marques Ana Patricia, Estrada Marta, Santana Magda, Cortez Vera, Grouzmann Eric, Cavadas Cláudia, Dipeptidyl-peptidase-IV by cleaving neuropeptide Y induces lipid accumulation and PPAR-γ expression, 10.1016/j.peptides.2012.06.014
  65. Salaga Maciej, Mokrowiecka Anna, Zielinska Marta, Malecka-Panas Ewa, Kordek Radzislaw, Kamysz Elzbieta, Fichna Jakub, New Peptide Inhibitor of Dipeptidyl Peptidase IV, EMDB-1 Extends the Half-Life of GLP-2 and Attenuates Colitis in Mice after Topical Administration, 10.1124/jpet.117.242586
  66. Sanz Y., Toldra F., Purification and Characterization of an X-Prolyl-Dipeptidyl Peptidase from Lactobacillus sakei, 10.1128/aem.67.4.1815-1820.2001
  67. Seino Yutaka, Fukushima Mitsuo, Yabe Daisuke, GIP and GLP-1, the two incretin hormones: Similarities and differences : Similarities and differences of GIP and GLP-1, 10.1111/j.2040-1124.2010.00022.x
  68. Shan Lu, Qiao Shuo-Wang, Arentz-Hansen Helene, Molberg Øyvind, Gray Gary M., Sollid Ludvig M., Khosla Chaitan, Identification and Analysis of Multivalent Proteolytically Resistant Peptides from Gluten:  Implications for Celiac Sprue, 10.1021/pr050173t
  69. Shannon R. P., DPP-4 Inhibition and Neuroprotection: Do Mechanisms Matter?, 10.2337/db12-1794
  70. Shibata Y., Miwa Y., Hirai K., Fujimura S., Purification and partial characterization of a dipeptidyl peptidase from Prevotella intermedia, 10.1034/j.1399-302x.2003.00057.x
  71. Sommer Felix, Bäckhed Fredrik, The gut microbiota — masters of host development and physiology, 10.1038/nrmicro2974
  72. Stengel Andreas, Goebel-Stengel Miriam, Teuffel Pauline, Hofmann Tobias, Buße Petra, Kobelt Peter, Rose Matthias, Klapp Burghard F., Obese patients have higher circulating protein levels of dipeptidyl peptidase IV, 10.1016/j.peptides.2014.09.006
  73. Sterkel Alana K., Lorenzini Jenna L., Fites J. Scott, Subramanian Vignesh Kavitha, Sullivan Thomas D., Wuthrich Marcel, Brandhorst Tristan, Hernandez-Santos Nydiaris, Deepe George S., Klein Bruce S., Fungal Mimicry of a Mammalian Aminopeptidase Disables Innate Immunity and Promotes Pathogenicity, 10.1016/j.chom.2016.02.001
  74. Stressler Timo, Eisele Thomas, Schlayer Michael, Lutz-Wahl Sabine, Fischer Lutz, Characterization of the Recombinant Exopeptidases PepX and PepN from Lactobacillus helveticus ATCC 12046 Important for Food Protein Hydrolysis, 10.1371/journal.pone.0070055
  75. Üstün-Aytekin Özlem, Arısoy Sevda, Aytekin Ali Özhan, Yıldız Ece, Statistical optimization of cell disruption techniques for releasing intracellular X-prolyl dipeptidyl aminopeptidase from Lactococcus lactis spp. lactis, 10.1016/j.ultsonch.2015.09.010
  76. Varmanen P., Savijoki K., Avall S., Palva A., Tynkkynen S., X-Prolyl Dipeptidyl Aminopeptidase Gene (pepX) Is Part of the glnRA Operon in Lactobacillus rhamnosus, 10.1128/jb.182.1.146-154.2000
  77. Walker N. D., Cloning and functional expression of dipeptidyl peptidase IV from the ruminal bacterium Prevotella albensis M384T, 10.1099/mic.0.26119-0
  78. Wallace R.John, McKain Nest, Broderick Glen A, Rode Lyle M, Walker Nicola D, Newbold C.James, Kopecny Jan, Peptidases of the Rumen Bacterium,Prevotella ruminicola, 10.1006/anae.1996.0065
  79. Wang Zhong, Zeng Ximin, Mo Yiming, Smith Katie, Guo Yuming, Lin Jun, Identification and Characterization of a Bile Salt Hydrolase from Lactobacillus salivarius for Development of Novel Alternatives to Antibiotic Growth Promoters, 10.1128/aem.02519-12
  80. Zhong Jixin, Gong Quan, Goud Aditya, Srinivasamaharaj Srividya, Rajagopalan Sanjay, Recent Advances in Dipeptidyl-Peptidase-4 Inhibition Therapy: Lessons from the Bench and Clinical Trials, 10.1155/2015/606031
Bibliographic reference Olivares Sevilla, Marta ; Schüppel, Valentina ; Hassan, Ahmed M. ; Beaumont, Martin ; Neyrinck, Audrey M. ; et. al. The Potential Role of the Dipeptidyl Peptidase-4-Like Activity From the Gut Microbiota on the Host Health. In: Frontiers in Microbiology, Vol. 9, p. 1900 [1-10] (2018)
Permanent URL http://hdl.handle.net/2078.1/201984