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Journal of Physiology and Biochemistry

, Volume 71, Issue 3, pp 509–525 | Cite as

Gut microbiota: a key player in health and disease. A review focused on obesity

  • M. J. Villanueva-Millán
  • P. Pérez-Matute
  • J. A. Oteo
Original Paper

Abstract

Gut microbiota, its evolutive dynamics and influence on host through its protective, trophic and metabolic actions, has a key role in health and opens unique opportunities for the identification of new markers of the physiopathological state of each individual. Alterations in gut microbiota composition have been associated with plenty disorders. Of interest, the vast number of studies demonstrates the role of microbiota in obesity, a serious public health problem that has reached epidemic proportions in many developed and middle-income countries. The economic and health costs of this condition and its comorbidities such as fatty liver, insulin resistance/diabetes, or cardiovascular events are considerable. Therefore, every strategy designed to reduce obesity would imply important savings. Targeting microbiota, in order to restore/modulate the microbiota composition with antibiotics, probiotics, prebiotics, or even fecal transplants, is considered as a promising strategy for the development of new solutions for the treatment of obesity. However, there is still lot to do in this field in order to identify the exact composition of microbiota in “health” and the specific mechanisms that regulate the host-microbiotal crosstalk. In addition, it is important to note that changes not only in the gut microbiota profile (abundance) but also in its metabolism and functions need to be taken into account in the context of contribution in the physiopathology of obesity and related disorders.

Keywords

Gut microbiota Gastrointestinal physiology Obesity Metabolic disorders 

Abbreviations

2-AG

2-Arachidonoylglycerol

ACC

Acetyl-CoA carboxylase

AMP

Adenosine monophosphate

AMPK

Adenosine monophosphate-activated protein kinase

AOX

Alternative oxidase

AP-1

Activator protein 1

BMI

Body mass index

CB1R/CB2R

Cannabinoid receptor 1/2

Ccl2

Chemokine (C-C motif) ligand 2

CD14

CD14 molecule

Cd36

CD36 molecule (thrombospondin receptor)

Cd68

CD68 molecule

CFU

Colony-forming unit

ChREBP

Carbohydrate response element-binding protein

Cpt1

Carnitine palmitoyltransferase 1

eCB

Endocannabinoid system

FAAH

Fatty acid amide hydrolase

Ffar2

Free fatty acid receptor 2

FIAF

Fasting-induced adipocyte factor

FMT

Fecal transplantation

Gαi/Gαo/Gαq

Guanine nucleotide-binding protein (G protein), alpha subunit i/o/q

GLP-1/2

Glucagon-like peptide 1/2

GPRs

G-protein-coupled receptors

HDL

High-density lipoprotein

HFD

High-fat diet

HMP

Human Microbiome Project

IL-18

Interleukin 18

IL-1β

Interleukin 1β

LPL

Lipoprotein lipase

LPS

Lipopolysaccharide

MD2

Myeloid differentiation protein-2

MetaHIT

Metagenomics of the Human Intestinal Tract

MyD88

Myeloid differentiation primary response gene 88

NAFLD

Nonalcoholic fatty liver disease

NF-κB

Nuclear factor kappa-light-chain-enhancer of activated B cells

NLRs

Nuclear oligodimerization receptors

NOD1/2

Nucleotide-binding oligomerization domain-containing protein 1/2

PGC-1

Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha

Ppara

Peroxisome proliferator-activated receptor alpha

PYY

Peptide YY

SCFA

Short chain fatty acids

SREBP-1

Sterol response element-binding protein type-1

TG

Triglyceride

Th17 cell

T helper 17 cell

TLRs

Toll-like receptors

TMAO

Trimethylamine N-oxide

Tregs

Regulatory T cells

WHO

World Health Organization

ZO-1

Zonula occludens protein-1

Notes

Acknowledgments

This study was supported by Ref-Bio (POLYFrEsNOL project) and by Fundación Rioja Salud, Spain. MJ Villanueva-Millán was supported by a predoctoral grant from Consejería de Industria, Innovación y Empleo (La Rioja Government).

References

  1. 1.
    Abdallah Ismail N, Ragab SH, Abd Elbaky A, Shoeib AR, Alhosary Y, Fekry D (2011) Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci 7:501–507PubMedCentralCrossRefPubMedGoogle Scholar
  2. 2.
    Ali AA, Velasquez MT, Hansen CT, Mohamed AI, Bhathena SJ (2005) Modulation of carbohydrate metabolism and peptide hormones by soybean isoflavones and probiotics in obesity and diabetes. J Nutr Biochem 16:693–699CrossRefPubMedGoogle Scholar
  3. 3.
    An HM, Park SY, Lee Do K, Kim JR, Cha MK, Lee SW, Lim HT, Kim KJ, Ha NJ (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10:116PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Anderson JL, Edney RJ, Whelan K (2012) Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 36:503–516CrossRefPubMedGoogle Scholar
  5. 5.
    Angelakis E, Merhej V, Raoult D (2013) Related actions of probiotics and antibiotics on gut microbiota and weight modification. Lancet Infect Dis 13:889–899CrossRefPubMedGoogle Scholar
  6. 6.
    Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, 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 EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Dore J, Antolin M, Artiguenave F, Blottiere HM, 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, Merieux 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 SD, Bork P (2011) Enterotypes of the human gut microbiome. Nature 473:174–180PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Cmaj 185:385–394PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718–15723PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920CrossRefPubMedGoogle Scholar
  10. 10.
    Backhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A 104:979–984PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Bailey MT (2011) Influence of stressor-induced nervous system activation on the intestinal microbiota and the importance for immunomodulation. Adv Exp Med Biol 817:255–276CrossRefGoogle Scholar
  12. 12.
    Bellahcene M, O'Dowd JF, Wargent ET, Zaibi MS, Hislop DC, Ngala RA, Smith DM, Cawthorne MA, Stocker CJ, Arch JR (2013) Male mice that lack the G-protein-coupled receptor GPR41 have low energy expenditure and increased body fat content. Br J Nutr 109:1755–1764CrossRefPubMedGoogle Scholar
  13. 13.
    Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, Vael C, Goossens H, Desager KN, Vankerckhoven V (2013) Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog 5:10PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Bindels LB, Dewulf EM, Delzenne NM (2013) GPR43/FFA2: physiopathological relevance and therapeutic prospects. Trends Pharmacol Sci 34:226–232CrossRefPubMedGoogle Scholar
  15. 15.
    Brenchley JM, Douek DC (2012) Microbial translocation across the GI tract. Annu Rev Immunol 30:149–173PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Burcelin R, Serino M, Chabo C, Garidou L, Pomie C, Courtney M, Amar J, Bouloumie A (2013) Metagenome and metabolism: the tissue microbiota hypothesis. Diabetes Obes Metab 15(Suppl 3):61–70CrossRefPubMedGoogle Scholar
  17. 17.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772CrossRefPubMedGoogle Scholar
  18. 18.
    Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470–1481CrossRefPubMedGoogle Scholar
  19. 19.
    Cani PD, Delzenne NM (2012) Involvement of the gut microbiota in the development of low grade inflammation associated with obesity: focus on this neglected partner. Acta Gastroenterol Belg 73:267–269Google Scholar
  20. 20.
    Cani PD, Hoste S, Guiot Y, Delzenne NM (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98:32–37CrossRefPubMedGoogle Scholar
  21. 21.
    Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50:2374–2383CrossRefPubMedGoogle Scholar
  22. 22.
    Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091–1103PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Cederroth CR, Vinciguerra M, Gjinovci A, Kuhne F, Klein M, Cederroth M, Caille D, Suter M, Neumann D, James RW, Doerge DR, Wallimann T, Meda P, Foti M, Rohner-Jeanrenaud F, Vassalli JD, Nef S (2008) Dietary phytoestrogens activate AMP-activated protein kinase with improvement in lipid and glucose metabolism. Diabetes 57:1176–1185CrossRefPubMedGoogle Scholar
  24. 24.
    Chen Z, Guo L, Zhang Y, Walzem RL, Pendergast JS, Printz RL, Morris LC, Matafonova E, Stien X, Kang L, Coulon D, McGuinness OP, Niswender KD, Davies SS (2014) Incorporation of therapeutically modified bacteria into gut microbiota inhibits obesity. J Clin Invest 124:3391–3406PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE (2010) Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 299:G440–G448CrossRefGoogle Scholar
  26. 26.
    DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA (2008) Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 3:e3056PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, Flint HJ (2008) Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 32:1720–1724CrossRefGoogle Scholar
  28. 28.
    Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, Moulton L, Glawe A, Wang Y, Leone V, Antonopoulos DA, Smith D, Chang EB, Ciancio MJ (2014) Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One 9:e92193PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Everard A, Geurts L, Caesar R, Van Hul M, Matamoros S, Duparc T, Denis RG, Cochez P, Pierard F, Castel J, Bindels LB, Plovier H, Robine S, Muccioli GG, Renauld JC, Dumoutier L, Delzenne NM, Luquet S, Backhed F, Cani PD (2014) Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nat Commun 5:5648PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, Possemiers S, Van Holle A, Francois P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60:2775–2786PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM (2014) Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes 4:e121PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Finucane MM, Sharpton TJ, Laurent TJ, Pollard KS (2014) A taxonomic signature of obesity in the microbiome? Getting to the guts of the matter. PLoS One 9:e84689PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Foolad N, Armstrong AW (2014) Prebiotics and probiotics: the prevention and reduction in severity of atopic dermatitis in children. Benef Microbes 5:151–160CrossRefPubMedGoogle Scholar
  34. 34.
    Fujimura KE, Slusher NA, Cabana MD, Lynch SV (2010) Role of the gut microbiota in defining human health. Expert Rev Anti Infect Ther 8:435–454PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Dore J, Henegar C, Rizkalla S, Clement K (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59:3049–3057PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ (2011) Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34:794–806CrossRefPubMedGoogle Scholar
  37. 37.
    Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Gordon JI, Hooper LV, McNevin MS, Wong M, Bry L (1997) Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am J Physiol 273:G565–G570PubMedGoogle Scholar
  39. 39.
    Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361:512–519CrossRefPubMedGoogle Scholar
  40. 40.
    Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Van Immerseel F (2010) From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr Res Rev 23:366–384CrossRefPubMedGoogle Scholar
  41. 41.
    Harris K, Kassis A, Major G, Chou CJ (2012) Is the gut microbiota a new factor contributing to obesity and its metabolic disorders? J Obes 2012:879151PubMedCentralPubMedGoogle Scholar
  42. 42.
    Hoskin-Parr L, Teyhan A, Blocker A, Henderson AJ (2013) Antibiotic exposure in the first two years of life and development of asthma and other allergic diseases by 7.5 yr: a dose-dependent relationship. Pediatr Allergy Immunol 24:762–771PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Hossain P, Kawar B, El Nahas M (2007) Obesity and diabetes in the developing world—a growing challenge. N Engl J Med 356:213–215CrossRefPubMedGoogle Scholar
  44. 44.
    http://www.who.int/mediacentre/factsheets/fs311/en/ (WHO: obesity and overweight. World Health Organization. Archived from the original on December 18, 2008. Retrieved November 29, 2014)
  45. 45.
    Ianiro G, Bibbo S, Gasbarrini A, Cammarota G (2014) Therapeutic modulation of gut microbiota: current clinical applications and future perspectives. Curr Drug Targets 15:762–770CrossRefPubMedGoogle Scholar
  46. 46.
    Inoue D, Tsujimoto G, Kimura I (2014) Regulation of energy homeostasis by GPR41. Front Endocrinol (Lausanne) 5:81Google Scholar
  47. 47.
    Jorth P, Turner KH, Gumus P, Nizam N, Buduneli N, Whiteley M (2014) Metatranscriptomics of the human oral microbiome during health and disease. MBio 5:e01012–e01014PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Kamada N, Chen GY, Inohara N, Nunez G (2013) Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 14:685–690PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Kamada N, Nunez G (2013) Role of the gut microbiota in the development and function of lymphoid cells. J Immunol 190:1389–1395PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Kim DH, Jung EA, Sohng IS, Han JA, Kim TH, Han MJ (1998) Intestinal bacterial metabolism of flavonoids and its relation to some biological activities. Arch Pharm Res 21:17–23CrossRefPubMedGoogle Scholar
  51. 51.
    Lee CY, Abizaid A (2014) The gut-brain-axis as a target to treat stress-induced obesity. Front Endocrinol (Lausanne) 5:117Google Scholar
  52. 52.
    Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070–11075PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023CrossRefPubMedGoogle Scholar
  54. 54.
    Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM (2013) Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med 5:178ra141CrossRefGoogle Scholar
  55. 55.
    Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Lyte M (2013) Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog 9:e1003726PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S–1045SPubMedGoogle Scholar
  58. 58.
    Manach C, Donovan JL (2004) Pharmacokinetics and metabolism of dietary flavonoids in humans. Free Radic Res 38:771–785CrossRefPubMedGoogle Scholar
  59. 59.
    Martinez JA, Parra MD, Santos JL, Moreno-Aliaga MJ, Marti A, Martinez-Gonzalez MA (2008) Genotype-dependent response to energy-restricted diets in obese subjects: towards personalized nutrition. Asia Pac J Clin Nutr 17(Suppl 1):119–122PubMedGoogle Scholar
  60. 60.
    Martinez I, Wallace G, Zhang C, Legge R, Benson AK, Carr TP, Moriyama EN, Walter J (2009) Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol 75:4175–4184PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Matsumoto M, Kibe R, Ooga T, Aiba Y, Sawaki E, Koga Y, Benno Y (2013) Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front Syst Neurosci 7:9PubMedCentralCrossRefPubMedGoogle Scholar
  62. 62.
    Mesonero JE, Latorre E, Mendoza C, Matheus N, Alcalde AI (2012) Papel del sistema serotoninérgico en la fisiopatología intestinal. Gaceta de Ciencias Veterinarias 15:72–79Google Scholar
  63. 63.
    Morgan XC, Segata N, Huttenhower C (2013) Biodiversity and functional genomics in the human microbiome. Trends Genet 29:51–58PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Munyaka PM, Khafipour E, Ghia JE (2014) External influence of early childhood establishment of gut microbiota and subsequent health implications. Front Pediatr 2:109PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Nadal I, Santacruz A, Marcos A, Warnberg J, Garagorri JM, Moreno LA, Martin-Matillas M, Campoy C, Marti A, Moleres A, Delgado M, Veiga OL, Garcia-Fuentes M, Redondo CG, Sanz Y (2009) Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes (Lond) 33:758–767CrossRefGoogle Scholar
  66. 66.
    Naito E, Yoshida Y, Makino K, Kounoshi Y, Kunihiro S, Takahashi R, Matsuzaki T, Miyazaki K, Ishikawa F (2011) Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol 110:650–657CrossRefPubMedGoogle Scholar
  67. 67.
    Ottman N, Smidt H, de Vos WM, Belzer C (2012) The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2:104PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Panda S, El khader I, Casellas F, Lopez Vivancos J, Garcia Cors M, Santiago A, Cuenca S, Guarner F, Manichanh C (2014) Short-term effect of antibiotics on human gut microbiota. PLoS One 9:e95476PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Paolella G, Mandato C, Pierri L, Poeta M, Di Stasi M, Vajro P (2014) Gut-liver axis and probiotics: their role in non-alcoholic fatty liver disease. World J Gastroenterol 20:15518–15531PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Pathak R, Enuh HA, Patel A (2013) Treatment of relapsing Clostridium difficile infection using fecal microbiota transplantation. Clin Exp Gastroenterol 2014:1–6Google Scholar
  71. 71.
    Poggi M, Bastelica D, Gual P, Iglesias MA, Gremeaux T, Knauf C, Peiretti F, Verdier M, Juhan-Vague I, Tanti JF, Burcelin R, Alessi MC (2007) C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50:1267–1276CrossRefPubMedGoogle Scholar
  72. 72.
    Puigserver P, Spiegelman BM (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 24:78–90CrossRefPubMedGoogle Scholar
  73. 73.
    Purchiaroni F, Tortora A, Gabrielli M, Bertucci F, Gigante G, Ianiro G, Ojetti V, Scarpellini E, Gasbarrini A (2013) The role of intestinal microbiota and the immune system. Eur Rev Med Pharmacol Sci 17:323–333PubMedGoogle Scholar
  74. 74.
    Quigley EM (2013) Gut bacteria in health and disease. Gastroenterol Hepatol (N Y) 9:560–569Google Scholar
  75. 75.
    Raoult D, Henrissat B (2014) Are stool samples suitable for studying the link between gut microbiota and obesity? Eur J Epidemiol 29:307–309CrossRefPubMedGoogle Scholar
  76. 76.
    Rautava S, Luoto R, Salminen S, Isolauri E (2012) Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol 9:565–576CrossRefPubMedGoogle Scholar
  77. 77.
    Robles-Alonso V, Guarner F (2013) Progress in the knowledge of the intestinal human microbiota. Nutr Hosp 28:553–557PubMedGoogle Scholar
  78. 78.
    Salazar N, Arboleya S, Valdes L, Stanton C, Ross P, Ruiz L, Gueimonde M, de Los Reyes-Gavilan CG (2014) The human intestinal microbiome at extreme ages of life. Dietary intervention as a way to counteract alterations. Front Genet 5:406PubMedCentralCrossRefPubMedGoogle Scholar
  79. 79.
    Santacruz A, Marcos A, Warnberg J, Marti A, Martin-Matillas M, Campoy C, Moreno LA, Veiga O, Redondo-Figuero C, Garagorri JM, Azcona C, Delgado M, Garcia-Fuentes M, Collado MC, Sanz Y (2009) Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 17:1906–1915CrossRefGoogle Scholar
  80. 80.
    Scalbert A, Williamson G (2000) Dietary intake and bioavailability of polyphenols. J Nutr 130:2073S–2085SPubMedGoogle Scholar
  81. 81.
    Setchell KD, Lawson AM, Borriello SP, Harkness R, Gordon H, Morgan DM, Kirk DN, Adlercreatz H, Anderson LC, Axelson M (1981) Lignan formation in man—microbial involvement and possible roles in relation to cancer. Lancet 2:4–7CrossRefPubMedGoogle Scholar
  82. 82.
    Shen J, Obin MS, Zhao L (2013) The gut microbiota, obesity and insulin resistance. Mol Aspects Med 34:39–58CrossRefPubMedGoogle Scholar
  83. 83.
    Shu Z, Ma J, Tuerhong D, Yang C, Upur H (2013) How intestinal bacteria can promote HIV replication. AIDS Rev 15:32–37PubMedGoogle Scholar
  84. 84.
    Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573CrossRefPubMedGoogle Scholar
  85. 85.
    Smits LP, Bouter KE, de Vos WM, Borody TJ, Nieuwdorp M (2013) Therapeutic potential of fecal microbiota transplantation. Gastroenterology 145:946–953CrossRefPubMedGoogle Scholar
  86. 86.
    Sridharan GV, Choi K, Klemashevich C, Wu C, Prabakaran D, Pan LB, Steinmeyer S, Mueller C, Yousofshahi M, Alaniz RC, Lee K, Jayaraman A (2014) Prediction and quantification of bioactive microbiota metabolites in the mouse gut. Nat Commun 5:5492CrossRefPubMedGoogle Scholar
  87. 87.
    Tsukumo DM, Carvalho BM, Carvalho-Filho MA, Saad MJ (2009) Translational research into gut microbiota: new horizons in obesity treatment. Arq Bras Endocrinol Metabol 53:139–144CrossRefPubMedGoogle Scholar
  88. 88.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031CrossRefPubMedGoogle Scholar
  89. 89.
    Udayappan SD, Hartstra AV, Dallinga-Thie GM, Nieuwdorp M (2014) Intestinal microbiota and faecal transplantation as treatment modality for insulin resistance and type 2 diabetes mellitus. Clin Exp Immunol 177:24–29PubMedCentralCrossRefPubMedGoogle Scholar
  90. 90.
    Ursell LK, Clemente JC, Rideout JR, Gevers D, Caporaso JG, Knight R (2012) The interpersonal and intrapersonal diversity of human-associated microbiota in key body sites. J Allergy Clin Immunol 129:1204–1208PubMedCentralCrossRefPubMedGoogle Scholar
  91. 91.
    Verdam FJ, Fuentes S, de Jonge C, Zoetendal EG, Erbil R, Greve JW, Buurman WA, de Vos WM, Rensen SS (2013) Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring) 21:E607–E615CrossRefGoogle Scholar
  92. 92.
    Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, Sitaraman SV, Knight R, Ley RE, Gewirtz AT (2010) Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328:228–231CrossRefPubMedGoogle Scholar
  93. 93.
    Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(913–916):e917Google Scholar
  94. 94.
    Wang B, Mao YK, Diorio C, Pasyk M, Wu RY, Bienenstock J, Kunze WA (2010) Luminal administration ex vivo of a live Lactobacillus species moderates mouse jejunal motility within minutes. Faseb J 24:4078–4088CrossRefPubMedGoogle Scholar
  95. 95.
    Wilson ID, Nicholson JK (2009) The role of gut microbiota in drug response. Curr Pharm Des 15:1519–1523CrossRefPubMedGoogle Scholar
  96. 96.
    Zaibi MS, Stocker CJ, O'Dowd J, Davies A, Bellahcene M, Cawthorne MA, Brown AJ, Smith DM, Arch JR (2010) Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett 584:2381–2386CrossRefPubMedGoogle Scholar
  97. 97.
    Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 106:2365–2370PubMedCentralCrossRefPubMedGoogle Scholar
  98. 98.
    Zhao J, Murray S, Lipuma JJ (2014) Modeling the impact of antibiotic exposure on human microbiota. Sci Rep 4:4345PubMedCentralPubMedGoogle Scholar

Copyright information

© University of Navarra 2015

Authors and Affiliations

  • M. J. Villanueva-Millán
    • 1
  • P. Pérez-Matute
    • 1
  • J. A. Oteo
    • 1
    • 2
  1. 1.HIV and Associated Metabolic Alterations Unit, Infectious Diseases DepartmentCenter for Biomedical Research of La Rioja (CIBIR)LogroñoSpain
  2. 2.Infectious Diseases DepartmentHospital San PedroLogroñoSpain

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