Scientia Agricultura Sinica ›› 2016, Vol. 49 ›› Issue (8): 1577-1584.doi: 10.3864/j.issn.0578-1752.2016.08.015

• ANIMAL SCIENCE·VETERINARY SCIENCERE·SOURCE INSECT • Previous Articles     Next Articles

The Interaction of Colonization of Akkermansia muciniphila in Gastrointestinal Tract and Its Host

FENG Ze-meng1, BAO Xian-ying1,2, YIN Yu-long1   

  1. 1Institute of Subtropical Agriculture, Chinese Academy of Sciences, Research Center of Healthy Breeding Livestock & Poultry/Hunan Engineering& Research Center of Animal & Poultry Science, Key Lab Agro-ecology Processing Subtropical Region, Scientific Observational and experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture,   Changsha 410125
    2College of Animal Science and Technology, Hunan Agricultural University, Changsha 410128
  • Received:2014-09-23 Online:2016-04-16 Published:2016-04-16

Abstract: The gastrointestinal tract is a big harbour for various microbes, which have a great influence on the metabolism and development of the host. These intestinal microbiota can be divided into microbiota in inner lumen and in mucus layer, and both have important roles in nutrients delivery and prevention against pathogenic microorganism invasion. Akkermansia muciniphila, a kind of gram-negative bacteria, specially degrades mucin, has a growth preference in animal mucus and has a broad effect on the host. In the gastrointestinal tract, the flora of Akkermansia muciniphila degrade mucin and oligosaccharides, produce short chain fatty acid and propionic acid, respectively, which provide energy to the host and also promote their colonization. At the same time, the degradation of mucin will lead to more mucin secretion, thereby lowering the host protein deposition. The colonization of Akkermansia muciniphila reduce fat deposition, delay the formation of diabetes. Akkermansia muciniphila have no serious pathogenicity, and suitable abundance will promote the development of the host immune system and intestinal health. With the development of more scientific research, the importance of intestinal microbiota will be the hot topic. However, the mechanism of the action of Akkermansia muciniphila to the host is still unclear. The colonized environment, physiological characteristics, host nutrition metabolism disturbance, relation with metabolic diseases, and host immune regulation of Akkermansia muciniphila were summarized in the present paper. Akkermansia muciniphila is a good potential biomarker, and can be applied in nutritional status, metabolic diseases, immunity and even cancer detection, and worth to be further studied.

Key words: mucus, mucin, Akkermansia muciniphila, intestinal microbiota

[1]    Johansson M E, Phillipson M, Petersson J, Velcich A, Holm L, Hansson G C. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proceedings of the National Academy of Sciences U S A, 2008, 105(39):15064-15069.
[2]    Moran A P, Gupta A, Joshi L. Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut, 2011, 60(10):1412-1425.
[3]    Hansson G C. Role of mucus layers in gut infection and inflammation. Current Opinion in Microbiology, 2012, 15(1):57-62.
[4]    Johansson M E, Larsson J M, Hansson G C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proceedings of the National Academy of Sciences U S A, 2011, 108(Suppl. 1):4659-4665.
[5]    Atuma C, Strugala V, Allen A, Holm L. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. American Journal of Physiology, 2001, 280(5):G922-G929.
[6]    Smirnov A, Sklan D, Uni Z. Mucin dynamics in the chick small intestine are altered by starvation. Journal of Nutrition, 2004, 134(4): 736-742.
[7]    Smirnov A, Perez R, Amit-Romach E, Sklan D, Uni Z. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. Journal of Nutrition, 2005, 135(2):187-192.
[8]    Smirnov A, Tako E, Ferket P R, Uni Z. Mucin gene expression and mucin content in the chicken intestinal goblet cells are affected by in ovo feeding of carbohydrates. Poultry Science, 2006, 85(4):669-673.
[9]    Fan X, Liu S, Liu G, Zhao J, Jiao H, Wang X, Song Z, Lin H. Vitamin a deficiency impairs mucin expression and suppresses the mucosal immune function of the respiratory tract in chicks. PLoS One, 2015, 10(9):e0139131.
[10]   Braun H S, Sponder G, Pieper R, Aschenbach J R, Deiner C. GABA selectively increases mucin-1 expression in isolated pig jejunum. Genes and Nutrition, 2015, 10(6):47.
[11]   De Lisle R C. Lubiprostone stimulates small intestinal mucin release. BMC Gastroenterology, 2012, 12:156.
[12]   Kasimanickam R, Kasimanickam V, Kastelic JP. Mucin 1 and cytokines mRNA in endometrium of dairy cows with postpartum uterine disease or repeat breeding. Theriogenology, 2014, 1(7): 952-958.e2.
[13]   Xu J, Gordon J I. Honor thy symbionts. Proceedings of the National Academy of Sciences U S A, 2003, 100:10452-10459.
[14]   Makivuokko H, Lahtinen S J, Wacklin P, Tuovinen E, Tenkanen H, Nikkilä J, Björklund M, Aranko K, Ouwehand A C, Mättö J. Association between the ABO blood group and the human intestinal microbiota composition. BMC Microbiology, 2012, 12:94.
[15]   Wacklin P, Mäkivuokko H, Alakulppi N, Nikkilä J, Tenkanen H, Räbinä J, Partanen J, Aranko K, Mättö J. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS ONE, 2011, 6(5):e20113.
[16]   Barcelo A, Claustre J, Moro F, Chayvialle J A, Cuber J C, Plaisancie P. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut, 2000, 46(2):218-224.
[17]   Smirnova M G, Guo L, Birchall J P, Pearson J P. LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cellular Immunology, 2003, 221(1): 42-49.
[18]   Willemsen L E, Koetsier M A, van Deventer S J, van Tol E A. Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut, 2003, 52(10): 1442-1447.
[19]   Scott K P, Gratz S W, Sheridan P O, Flint H J, Duncan S H. The influence of diet on the gut microbiota. Pharmacological Research, 2013, 69(1):52-60.
[20]   Eckburg P B, Bik E M, Bernstein C N, Purdom E, Dethlefsen L, Sargent M, Gill S R, Nelson K E, Relman D A. Diversity of the human intestinal microbial flora. Science, 2005, 308(5728): 1635-1638.
[21]   Belzer C, de Vos W M. Microbes inside - from diversity to function: the case of Akkermansia. ISME Journal, 2012,6(8): 1449-1458.
[22]   Hildebrand F, Ebersbach T, Nielsen H B, Li X, Sonne S B, Bertalan M, Dimitrov P, Madsen L, Qin J, Wang J, Raes J, Kristiansen K, Licht T R. A comparative analysis of the intestinal metagenomes present in guinea pigs (Cavia porcellus) and humans (Homo sapiens). BMC Genomics, 2012, 13:514.
[23]   van Passel M W, Kant R, Zoetendal E G, Plugge C M, Derrien M, Malfatti S A, Chain P S, Woyke T, Palva A, de Vos W M, Smidt H. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One, 2011, 6(3):e16876.
[24]   Derrien M, Vaughan E E, Plugge C M, de Vos W M. Akkermansia muciniphila gen. nov., sp nov., a human intestinal mucin-degrading bacterium. International Journal of Systematic and Evolutionary Microbiology, 2004, 54:1469-1476.
[25]   Collado M C, Derrien M, Isolauri E, de Vos W M, Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin degrading member of the intestinal microbiota present in infants, adults, and the elderly. Applied and Environmental Microbiology, 2007, 73(23): 7767-7770.
[26]   Derrien M, Collado M C, Ben-Amor K, Salminen S, de Vos W M. The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Applied and Environmental Microbiology, 2008, 74:1646-1648.
[27]   Van den Abbeele P, Grootaert C, Marzorati M, Possemiers S, Verstraete W, Gérard P, Rabot S, Bruneau A, El Aidy S, Derrien M, Zoetendal E, Kleerebezem M, Smidt H, Van de Wiele T. Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. Applied and Environmental Microbiology, 2010, 76(15): 5237-5246.
[28]   Derrien, M.Mucin utilisation and host interactions of the novel intestinal microbe Akkermansia muciniphila[D]. Wageningen: Wageningen University. 2007.
[29]   Georgiades K, Merhej V, Raoult D. The influence of rickettsiologists on post-modern microbiology. Frontiers in Cellular and Infection Microbiology, 2011(1): 8.
[30]   Huang K, Wang M M, Kulinich A, Yao H L, Ma H Y, Martínez J E, Duan X C, Chen H, Cai Z P, Flitsch S L, Liu L, Voglmeir J. Biochemical characterisation of the neuraminidase pool of the human gut symbiont Akkermansia muciniphila. Carbohydrate Research, 2015, 415:60-65.
[31]   Koropatkin N M, Cameron E A, Martens E C. How glycan metabolism shapes the human gut microbiota. Nature Reviews Microbiology, 2012, 10(5):323-335.
[32]   Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende D R, Fernandes G R, Tap J, Bruls T, Batto J M, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S,Torrents D, Ugarte E, Zoetendal E G, Wang J, Guarner F, Pedersen O, de Vos W M, Brunak S, Doré J; MetaHIT Consortium, Antolín M, Artiguenave F, Blottiere H M, Almeida M, Brechot C, Cara C, Chervaux C, Cultrone A, Delorme C, Denariaz G, Dervyn R, Foerstner KU, Friss C, van de Guchte M, Guedon E, Haimet F, Huber W, van Hylckama-Vlieg J, Jamet A, Juste C, Kaci G, Knol J, Lakhdari O, Layec S, Le Roux K, Maguin E, Mérieux A, Melo Minardi R, M'rini C,Muller J, Oozeer R, Parkhill J, Renault P, Rescigno M, Sanchez N, Sunagawa S, Torrejon A, Turner K,Vandemeulebrouck G, Varela E, Winogradsky Y, Zeller G, Weissenbach J, Ehrlich S D, Bork P. Enterotypes of the human gut microbiome. Nature, 2011, 473: 174-180.
[33]   Van den Abbeele P, Gérard P, Rabot S, Bruneau A,  Aidy S E, Derrien M, Kleerebezem M, Zoetendal E G, Smidt H, Verstraete W, Van de Wiele T, Possemiers S. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin- degradation in humanized rats. Environmental Microbiology, 2011, 13(10):2667-2680.
[34]   Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, Wild B, Wanek W, Richter A, Rauch I, Decker T, Loy A, Wagner M. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proceedings of the National Academy of Sciences U S A, 2013, 110(12):4720-4725.
[35]   Axling U, Olsson C, Xu J, Fernandez C, Larsson S, Ström K, Ahrné S, Holm C, Molin G, Berger K. Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6J mice. Nutrition & Metabolism, 2012, 9(1):105.
[36]   Kim B S, Song M Y, Kim H. The anti-obesity effect of Ephedra sinica through modulation of gut microbiota in obese Korean women. Journal of Ethnopharmacology, 2014, 152(3):532-539.
[37]   Everard A, Belzer C, Geurts L, Ouwerkerk J P, Druart C, Bindels L B, Guiot Y, Derrien M, Muccioli G G, Delzenne N M, de Vos W M, Cani P D. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the National Academy of Sciences U S A, 2013, 110(22):9066-9071.
[38]   Karlsson C L, Onnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity (Silver Spring), 2012, 20(11): 2257-2261.
[39]   Santacruz A, Collado M C, García-Valdés L, Segura M T, Martín-Lagos J A, Anjos T, Martí-Romero M, Lopez RM, Florido J, Campoy C, Sanz Y. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. British Journal of Nutrition, 2010, 104(1):83-92.
[40]   Collado MC, Isolauri E, Laitinen K, Salminen S. Effect of mother's weight on infant's microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. American Journal of Clinical Nutrition, 2010, 92(5): 1023-1030.
[41]   Zhang H, DiBaise J K, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell M D, Wing R, Rittmann B E, Krajmalnik-Brown R: Human gut microbiota in obesity and after gastric bypass. Proceedings of the National Academy of Sciences U S A, 2009, 106:2365-2370.
[42]   Teixeira T, Grze?kowiak LM, Salminen S, Laitinen K, Bressan J, Gouveia Peluzio Mdo C. Faecal levels of Bifidobacterium and Clostridium coccoides but not plasma lipopolysaccharide are inversely related to insulin and HOMA index in women. Clinical Nutrition, 2013, 32(6):1017-1022.
[43]   Zhang X, Shen D, Fang Z, Jie Z, Qiu X, Zhang C, Chen Y, Ji L. Human Gut Microbiota Changes Reveal the Progression of Glucose Intolerance. PLoS One, 2013, 8(8):e71108.
[44]   Ellekilde M, Krych L, Hansen C H, Hufeldt M R, Dahl K, Hansen L H, Sørensen S J, Vogensen F K, Nielsen D S, Hansen A K. Characterization of the gut microbiota in leptin deficient obese mice - Correlation to inflammatory and diabetic parameters. Research in Veterinary Science, 2014, 96(2):241-250.
[45]   Tilg H, Moschen A R. Microbiota and diabetes: an evolving relationship. Gut, 2014, 63(9):1513-1521.
[46]   McGuckin M A, Linden S K, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nature Reviews Microbiology, 2011, 9:265-278.
[47]   Bergstrom K S B, Kissoon-Singh V, Gibson D L, Ma C, Montero M, Sham H P, Ryz N, Huang T, Velcich A, Finlay B B, Chadee K, Vallance B A. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. Plos Pathogens, 2010, 6:e1000902.
[48]   Hasnain S Z, Wang H, Ghia JE, Haq N, Deng Y, Velcich A, Grencis R K, Thornton D J, Khan W I. Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology, 2010, 138(5):1763-1771.
[49]   Derrien M, van Passel M W, van de Bovenkamp J H, Schipper R G, de Vos W M, Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes, 2010, 1(4):254-268.
[50]   Ganesh B P, Klopfleisch R, Loh G, Blaut M. Commensal akkermansia muciniphila exacerbates Gut inflammation in salmonella typhimurium- infected gnotobiotic mice. PLoS One, 2013, 8(9): e74963.
[51]   Corazziari E S. Intestinal mucus barrier in normal and inflamed colon. Journal of Pediatric Gastroenterology and Nutrition, 2009, 48: S54-S55.
[52]   Harmsen H J, Wildeboer-Veloo A C, Raangs G C, Wagendorp A A, Klijn N, Bindels J G, Wagendorp A A, Klijn N, Welling G W. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition, 2000, 30(1):61-67.
[53]   Hansen C H, Holm T L, Krych ?, Andresen L, Nielsen D S, Rune I, Hansen A K, Skov S. Gut microbiota regulates NKG2D ligand expression on intestinal epithelial cells. European Journal of Immunology, 2013, 43(2):447-457.
[54]   Kang C S, Ban M, Choi EJ, Moon H G, Jeon J S, Kim D K, Park S K, Jeon S G, Roh T Y, Myung S J, Gho Y S, Kim J G, Kim Y K. Extracellular vesicles derived from Gut microbiota, especially akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS ONE, 2013, 8(10): e76520.
[55]   Swidsinski A, Dörffel Y, Loening-Baucke V, Theissig F, Rückert J C, Ismail M, Rau W A, Gaschler D, Weizenegger M, Kühn S, Schilling J, Dörffel W V. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/ necrophorum. Gut, 2011, 60(1):34-40.
[56]   Campieri M, Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut, 2001, 48(1):132-135.
[57]   Shih D Q, Targan S R. Immunopathogenesis of inflammatory bowel disease. World Journal of Gastroenterology, 2008, 14(3):390-400.
[58]   Candela M, Rampelli S, Turroni S, Severgnini M, Consolandi C, De Bellis G, Masetti R, Ricci G, Pession A, Brigidi P. Unbalance of intestinal microbiota in atopic children. BMC Microbiology, 2012, 12:95.
[59] Sonoyama K, Fujiwara R, Takemura N, Watanabe J, Ito H, Morita T. Response of gut microbiota to fasting and hibernation in Syrian hamsters. Applied and Environmental Microbiology, 2009, 75(20): 6451-6456.
[60]   Sonoyama K, Ogasawara T, Goto H, Yoshida T, Takemura N, Fujiwara R, Watanabe J, Ito H, Morita T, Tokunaga Y, Yanagihara T. Comparison of gut microbiota and allergic reactions in BALB/c mice fed different cultivars of rice. British Journal of Nutrition, 2010, 103(2):218-226.
[61]   Shin N R, Lee J C, Lee H Y, Kim M S, Whon T W, Lee M S, Bae J W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut, 2013, 63:727-735.
[62]   Collado M C, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatric Research, 2012, 72(1):77-85.
[63]   Joyce S A, Gahan C G. The gut microbiota and the metabolic health of the host. Current Opinion in Gastroenterology, 2014, 30(2):120-127.
[64]   Benjdia A, Martens E C, Gordon J I, Berteau O. Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. Journal of Biological Chemistry, 2011, 286(29):25973-25982.
[65]   Turroni F, Bottacini F, Foroni E, Mulder I, Kim J H, Zomer A, Sánchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Fitzgerald G F, Mills D, Margolles A, Kelly D, van Sinderen D, Ventura M. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proceedings of the National Academy of Sciences U S A, 2010, 107(45):19514-19519.
[66]   Huang J Y, Lee S M, Mazmanian S K. The human commensal Bacteroides fragilis binds intestinal mucin. Anaerobe, 2011, 17(4): 137-41.
[67]   Crost E H, Tailford L E, Le Gall G, Fons M, Henrissat B, Juge N. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent. PLoS One, 2013, 8(10): e76341.
[68]   Louis P, Flint H J. Development of a semiquantitative degenerate real-time pcr-based assay for estimation of numbers of butyryl- coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Applied and Environmental Microbiology, 2007, 73: 2009-2012.
[69]   Hippe B, Remely M, Bartosiewicz N, Riedel M, Nichterl C, Schatz L, Pummer S, Haslberger A. Abundance and diversity of GI microbiota ratherthan IgG4 levels correlate with abdominal inconvenience and gut permeability in consumers claiming food intolerances. Endocrine Metabolic & Immune Disorders-Drug Targets, 2014, 14(1): 67-75.
[70]   Png C W, Lindén S K, Gilshenan K S, Zoetendal E G, McSweeney C S, Sly L I, McGuckin M A, Florin T H. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. American Journal of Gastroenterology, 2010, 105(11):2420-2428.
[71]   Brahe L K, Le Chatelier E, Prifti E, Pons N, Kennedy S, Hansen T, Pedersen O, Astrup A, Ehrlich S D, Larsen L H. Specific gut microbiota features and metabolic markers in postmenopausal women with obesity. Nutrition & Diabetes, 2015, 5:e159.
[72]   Wang L, Christophersen C T, Sorich M J, Gerber J P, Angley M T, Conlon M A. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Applied and Environmental Microbiology, 2011, 77(18):6718-6721.
[73]   Miller R S, Hoskins L C. Mucin degradation in human colon ecosystems. Fecal population densities of mucin-degrading bacteria estimated by a “most probable number” method. Gastroenterology, 1981, 81:759-765.
[74]   Weir T L, Manter D K, Sheflin A M, Barnett B A, Heuberger A L, Ryan E P. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One, 2013, 8(8):e70803.
[75]   Zackular J P, Baxter N T, Iverson K D, Sadler W D, Petrosino J F, Chen G Y, Schloss P D. The gut microbiome modulates colon tumorigenesis. MBio, 2013, 4(6):e00692-13.
[76]   Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn R C, Roeselers G. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. MBio, 2014, pii: e01438-14.
[77]   Walsh C J, Guinane C M, O'Toole P W, Cotter P D. Beneficial modulation of the gut microbiota. FEBS Letters, 2014, pii: S0014-5793(14)00254-3.
[78]   Carey H V, Walters W A, Knight R. Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. American Journal of Physiology, 2013, 304(1):R33-R42.
[79]   Costello E K, Gordon J I, Secor S M, Knight R. Postprandial remodeling of the gut microbiota in Burmese pythons. ISME Journal, 2010, 4(11):1375-1385.
[80]   Preidis G A, Ajami N J, Wong M C, Bessard B C, Conner M E, Petrosino J F. Composition and function of the undernourished neonatal mouse intestinal microbiome. Journal of Nutritional Biochemistry, 2015, 26(10):1050-1057.
[81]   Jakobsdottir G, Xu J, Molin G, Ahrn? S, Nyman M. High-fat diet reduces the formation of butyrate, but increases succinate, inflammation, liver fat and cholesterol in rats, while dietary fibre counteracts these effects. PLoS One, 2013, 8(11): e80476.
[82]   Everard A, Lazarevic V, Derrien M, Girard M, Muccioli G G, Neyrinck A M, Possemiers S, Van Holle A, François P, de Vos W M, Delzenne N M, Schrenzel J, Cani P D. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet induced leptin-resistant mice. Diabetes, 2011, 60:2775-2786.
[83]   Chaplin A, Parra P, Serra F, Palou A. Conjugated Linoleic Acid supplementation under a high-fat diet modulates stomach protein expression and intestinal microbiota in adult mice. PLoS One, 2015, 10(4):e0125091.
[84]   Reid D T, Eller L K, Nettleton J E, Reimer R A. Postnatal prebiotic fibre intake mitigates some detrimental metabolic outcomes of early overnutrition in rats. European Journal of Nutrition, 2015. [Epub ahead of print]
[85]   Gómez-Gallego C, Collado M C, Ilo T, Jaakkola U M, Bernal M J, Periago M J, Salminen S, Ros G, Frias R. Infant formula supplemented with polyamines alters the intestinal microbiota in neonatal BALB/ cOlaHsd mice. Journal of Nutritional Biochemistry, 2012, 23(11): 1508-1513.
[86]   Reunanen J, Kainulainen V, Huuskonen L, Ottman N, Belzer C, Huhtinen H, de Vos W M, Satokari R. Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer. Applied and Environmental Microbiology, 2015, 81(11): 3655-3662.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!