Advertisement

European Journal of Nutrition

, Volume 58, Issue 1, pp 27–43 | Cite as

Adipose tissue inflammation and metabolic syndrome. The proactive role of probiotics

  • Sebastian Torres
  • Emanuel Fabersani
  • Antonela Marquez
  • Paola Gauffin-CanoEmail author
Review

Abstract

Purpose

The first part of this review focuses on the role of cells and molecules of adipose tissue involved in metabolic syndrome-induced inflammation and in the maintenance of this pathology. In the second part of the review, the potential role of probiotics-modulating metabolic syndrome-related inflammatory components is summarized and discussed.

Methods

The search for the current scientific literature was carried out using ScienceDirect, PubMed, and Google Scholar search engines. The keywords used were: metabolic syndrome, obesity, insulin resistant, adipose tissue, adipose tissue inflammation, chronic low-grade inflammation, immune cells, adipokines, cytokines, probiotics, and gut microbiota.

Results and Conclusions

Chronic low-grade inflammation that characterized metabolic syndrome can contribute to the development of the metabolic dysfunctions involved in the pathogenesis of its comorbidities. Adipose tissue is a complex organ that performs metabolic and immune functions. During metabolic syndrome, an imbalance in the inflammatory components of adipose tissue (immune cells, cytokines, and adipocytokines), which shift from an anti-inflammatory to a pro-inflammatory profile, can provoke metabolic syndrome linked complications. Further knowledge concerning the immune function of adipose tissue may contribute to finding better alternatives for the treatment or prevention of such disorders. The control of inflammation could result in the management of many of the pathologies related to metabolic syndrome. Due to the strong evidence that gut microbiota composition plays a role modulating the body weight, adipose tissue, and the prevalence of a low-grade inflammatory status, probiotics emerge as valuable tools for the prevention of metabolic syndrome and health recovery.

Keywords

Metabolic syndrome Obesity Chronic low-grade inflammation Adipose tissue Adipokines Probiotics 

Abbreviations

ASP

Acylation stimulating protein

BMI

Body mass index

C3

Complement component 3

CCL4

C–C motif chemokine ligand-4

CNS

Central nervous system

CRP

C-reactive protein

CTRPs

C1qTNF-related proteins

HDL

High-density lipoprotein

IFN

InterFeroN

ICAM-1

Intercellular adhesion molecule 1

IL

InterLeukin

IRS-1

Insulin receptor substrate-1

KLF

Krüppel-like factor proteins

LDL

Low-density lipoprotein

LPS

Lipopolysaccharides

MIP-1

Macrophage inflammatory protein 1

MCP-1

Monocyte chemoattractant protein 1

MIF

Macrophage migration inhibitory factor

NF-κB

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

PAI-1

Plasminogen activator inhibitor-1

PBEF

Pre-B-cell enhancing factor

RANTES

Regulated on activation, normal T cell expressed and secreted

TGF

Tumor growth factor

TLR

Toll-like receptor

TNF

Tumor necrosis factor

VCAM-1

Vascular cell adhesion molecule 1

Notes

Acknowledgements

The present review was supported by the grant PIP215 from CONICET.

Author contributions

All authors contributed to the discussion sessions, held to outline and delimit the content of the manuscript. TS, FE, MA and G-CP performed the literature search and contributed to the writing of the manuscript. All authors contributed to the discussion and interpretation of the literature data and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. 1.
    Dallmeier D, Larson M, Vasan R et al (2012) Metabolic syndrome and inflammatory biomarkers: a community-based cross-sectional study at the Framingham Heart Study. Diabetol Metab Synd 4:1–7Google Scholar
  2. 2.
    Yu R, Kim C, Kang J (2009) Inflammatory components of adipose tissue as target for treatment of metabolic syndrome. In: Yoshikawa T (ed) Food factors for health promotion, forum nutrition, vol 61. Karger, Basel, pp 95–103Google Scholar
  3. 3.
    Rastelli M, Knauf C, Cani PD (2018) Gut Microbes and health: a focus on the mechanisms linking microbes, obesity, and related disorders. Obesity (Silver Spring) 26(5):792–800Google Scholar
  4. 4.
    Fang H, Judd RL (2018) Adiponectin regulation and function. Compr Physiol 8:1031–1063Google Scholar
  5. 5.
    Thiennimitr P, Yasom S, Tunapong W et al (2018) Lactobacillus paracasei HII01, xylooligosaccharides and synbiotics reduced gut disturbance in obese rats. Nutrition 54:40–47Google Scholar
  6. 6.
    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 56:1761–1772Google Scholar
  7. 7.
    Rastelli M, Knauf C, Cani PD (2018) Gut microbes and health: a focus on the mechanisms linking microbes, obesity, and related disorders. Obesity 26(5):792–800Google Scholar
  8. 8.
    He M, Shi B (2017) Gut microbiota as a potential target of metabolic syndrome: the role of probiotics and prebiotics. Cell Bioscience 7:54Google Scholar
  9. 9.
    Dahiya DK, Puniya M et al (2017) Gut microbiota modulation and its relationship with obesity using prebiotic fibers and probiotics: a review. Front Microbiol 8:563Google Scholar
  10. 10.
    Chatzigeorgiou A, Chavakis T (2016) Immune cells and metabolism. Handb Exp Pharmacol 233:221–249Google Scholar
  11. 11.
    Rezaee F, Dashty M (2013) Role of adipose tissue in metabolic system disorders adipose tissue is the initiator of metabolic diseases. J Diabetes Metab 13:2Google Scholar
  12. 12.
    Grant R, Dixit V (2015) Adipose tissue as an immunological organ. Obesity 23:512–518Google Scholar
  13. 13.
    Magnuson AM, Regan DP, Fouts JK, Booth AD, Dow SW, Foster MT (2017) Diet-induced obesity causes visceral, but not subcutaneous, lymph node hyperplasia via increases in specific immune cell populations. Cell Prolif 50(5):e12365Google Scholar
  14. 14.
    Magnuson AM, Fouts JK, Regan DP, Booth AD, Dow SW, Foster MT (2018) Adipose tissue extrinsic factor: obesity-induced inflammation and the role of the visceral lymph node. Physiol Behav 190:71–81Google Scholar
  15. 15.
    Schäffler A, Schölmerich J (2010) Innate immunity and adipose tissue biology. Trends Immunol 31:228–235Google Scholar
  16. 16.
    Enomoto T, Shibata R, Ohashi K et al (2012) Regulation of adipolin/CTRP12 cleavage by obesity. Biochem Biophys Res Commun 428:155–159Google Scholar
  17. 17.
    Fabersani E, Abeijon-Mukdsi MC, Ross R et al (2017) Specific strains of lactic acid bacteria differentially modulate the profile of adipokines in vitro. Front Immunol 8:266Google Scholar
  18. 18.
    Zoumpopoulou G, Pot B, Tsakalidou E et al (2017) Dairy probiotics: beyond the role of promoting gut and immune health. Inter Dairy J 67:46–60Google Scholar
  19. 19.
    Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808Google Scholar
  20. 20.
    Trim W, Turner JE, Thompson D (2018) Parallels in immunometabolic adipose tissue dysfunction with ageing and obesity. Front Immunol 9:169.  https://doi.org/10.3389/fimmu.2018.00169. (eCollection 2018)Google Scholar
  21. 21.
    Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Mathis D (2009) Fat Treg cells: a liaison between the immune and metabolic systems. Nat Med 15:930Google Scholar
  22. 22.
    Miranda K, Yang X, Bam M, Murphy EA. Nagarkatti PS, Nagarkatti M (2018) MicroRNA-30 modulates metabolic inflammation by regulating Notch signaling in adipose tissue macrophages. Int J Obes 42:1140–1150Google Scholar
  23. 23.
    Patel H, Patel V (2015) Inflammation and metabolic syndrome: an overview. Curr Res Nutr Food Sci J 3:263–268Google Scholar
  24. 24.
    Zaibi MS, Kępczyńska MA, Harikumar P, Alomar SY, Trayhurn P (2018) IL-33 stimulates expression of the GPR84 (EX33) fatty acid receptor gene and of cytokine and chemokine genes in human adipocytes. Cytokine 110:189–193Google Scholar
  25. 25.
    Esser N, Legrand-Poels S, Piette J et al (2014) Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 105:141–150Google Scholar
  26. 26.
    Apostolopoulos V, de Courten M, Stojanovska L (2015) Obesity: an immunological perspective. J Immun Res 2:1–3Google Scholar
  27. 27.
    Apostolopoulos V, de Courten MP, Stojanovska L, Blatch GL, Tangalakis K, de Courten B (2016) The complex immunological and inflammatory network of adipose tissue in obesity. Mol Nutr Food Res 60(1):43–57Google Scholar
  28. 28.
    Scarpellini E, Tack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153Google Scholar
  29. 29.
    McDonnell ME, Ganley-Leal LM, Mehta A, Bigornia S, Mott M, Rehman Q et al (2012) B lymphocytes in human subcutaneous adipose crown-like structures. Obesity (Silver Spring) 20(7):1372–1378Google Scholar
  30. 30.
    Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang Y, Zielenski J, Mastronardi F, Maezawa Y, Drucker DJ, Engleman E, Winer D, Dosch HM (2009) Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15:921–929Google Scholar
  31. 31.
    Winer D, Winer S, Shen L et al (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 17:610–617Google Scholar
  32. 32.
    Ying W, Wollam J, Ofrecio JM, Bandyopadhyay G, El Ouarrat D, Lee YS et al (2017) Adipose tissue B2 cells promote insulin resistance through leukotriene LTB4/LTB4R1 signaling. J Clin Invest 127(3):1019–1030Google Scholar
  33. 33.
    Bolus WR, Peterson KR, Hubler MJ, Kennedy AJ, Gruen ML, Hasty AH (2018) Elevating adipose eosinophils in obese mice to physiologically normal levels does not rescue metabolic impairments. Mol Metabol 8:86–95Google Scholar
  34. 34.
    Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Locksley RM (2011) Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332(6026):243–247Google Scholar
  35. 35.
    Ghosh AR, Bhattacharya R, Bhattacharya S, Nargis T, Rahaman O, Duttagupta P et al (2016) Adipose recruitment and activation of Plasmacytoid dendritic cells fuel Metaflammation. Diabetes 65(11):3440–3452Google Scholar
  36. 36.
    Liu J, Divoux A, Sun J, Zhang J, Clement K, Glickman JN et al (2009) Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 15(8):940–945Google Scholar
  37. 37.
    Kershaw E, Flier J (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89:2548–2556Google Scholar
  38. 38.
    Ruan H, Lodish HF (2003) Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α. Cytokine Growth Factor Rev 14:447–455Google Scholar
  39. 39.
    Hotamisligil GS (2003) Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 27(Suppl 3):S53–S55Google Scholar
  40. 40.
    Donath MY (2014) Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov 13(6):465–476Google Scholar
  41. 41.
    Stagakis I, Bertsias G, Karvounaris S et al (2012) Anti-tumor necrosis factor therapy improves insulin resistance, beta cell function and insulin signaling in active rheumatoid arthritis patients with high insulin resistance. Arthritis Res Therapy 14(3):R141Google Scholar
  42. 42.
    Stanley TL, Zanni MV, Johnsen S et al (2011) TNF-α antagonism with etanercept decreases glucose and increases the proportion of high molecular weight adiponectin in obese subjects with features of the metabolic syndrome. J Clin Endocrinol Metabol 96(1):E146–E150Google Scholar
  43. 43.
    Stagakis I, Bertsias G, Karvounaris S, Kavousanaki M, Virla D, Raptopoulou A, Sidiropoulos PI (2012) Anti-tumor necrosis factor therapy improves insulin resistance, beta cell function and insulin signaling in active rheumatoid arthritis patients with high insulin resistance. Arthritis Res Therapy 14(3):R141Google Scholar
  44. 44.
    Bing C (2015) Is interleukin-1β a culprit in macrophage-adipocyte crosstalk in obesity? Adipocyte 4:149–152Google Scholar
  45. 45.
    Nov O, Shapiro H, Ovadia H et al (2013) Interleukin-1β regulates fat-liver crosstalk in obesity by auto-paracrine modulation of adipose tissue inflammation and expandability. PLoS One 8:e53626Google Scholar
  46. 46.
    Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88:1379–1406Google Scholar
  47. 47.
    Timper K, Denson JL, Steculorum SM, Heilinger C, Engstrom-Ruud L, Wunderlich CM et al (2017) IL-6 Improves energy and glucose homeostasis in obesity via enhanced central IL-6 trans-signaling. Cell Rep 19:267–280Google Scholar
  48. 48.
    Cranford TL, Enos RT, Velázquez KT, McClellan JL, Davis JM, Singh UP, Murphy EA (2016) Role of MCP-1 on inflammatory processes and metabolic dysfunction following high-fat feedings in the FVB/N strain. Int J Obes 40(5):844Google Scholar
  49. 49.
    Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T (2006) Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281(36):26602–26614Google Scholar
  50. 50.
    Chedraui P, Pérez-López F, Escobar G et al (2014) Circulating leptin, resistin, adiponectin, visfatin, adipsin and ghrelin levels and insulin resistance in postmenopausal women with and without the metabolic syndrome. Maturitas 79:86–90Google Scholar
  51. 51.
    Singh V, Arora S, Goswami B et al (2009) Metabolic syndrome: a review of emerging markers and management. Diab Metab Synd Clin Res Rev 3:240–254Google Scholar
  52. 52.
    Scarpinelli E, Tjack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153Google Scholar
  53. 53.
    Al Haj Ahmad RM, Al-Domi (2016) Complement 3 serum levels as a pro-inflammatory biomarker for insulin resistance in obesity. Diab Met Syndr 11(1):S229–S232Google Scholar
  54. 54.
    Phillips C, Kesse-Guyot E, Ahluwalia N et al (2012) Dietary fat, abdominal obesity and smoking modulate the relationship between plasma complement component 3 concentrations and metabolic syndrome risk. Atherosclerosis 220:513–519Google Scholar
  55. 55.
    Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312Google Scholar
  56. 56.
    Kumari B, Yadav UCS (2018) Adipokine visfatin’s role in pathogenesis of diabesity and related metabolic derangements. Curr Mol Med.  https://doi.org/10.2174/1566524018666180705114131 Google Scholar
  57. 57.
    Kim J, Kim S, Im J et al (2010) The relationship between visfatin and metabolic syndrome in postmenopausal women. Maturitas 67:67–71Google Scholar
  58. 58.
    Sitticharoon C, Nway N, Chatree S et al (2014) Interactions between adiponectin, visfatin, and omentin in subcutaneous and visceral adipose tissues and serum, and correlations with clinical and peripheral metabolic factors. Peptides 62:164–175Google Scholar
  59. 59.
    Ohashi K, Shibata R, Murohara T et al (2014) Role of anti-inflammatory adipokines in obesity-related diseases. Trends Endocrinol Metabol 25:348–355Google Scholar
  60. 60.
    Matsuda K, Fujishima Y, Maeda N, Mori T, Hirata A, Sekimoto R, Tsushima Y, Masuda S, Yamaoka M, Inoue K, Nishizawa H, Kita S, Ranscht B, Funahashi T, Shimomura I (2015) Positive feedback regulation between adiponectin and T-cadherin impacts adiponectin levels in tissue and plasma of male mice. Endocrinology 156:934–946Google Scholar
  61. 61.
    Kitamoto A, Kitamoto T, Nakamura T, Matsuo T, Nakata Y, Hyogo H, Ochi H, Kamohara S, Miyatake N, Kotani K, Mineo I, Wada J, Ogawa Y, Yoneda M, Nakajima A, Funahashi T, Miyazaki S, Tokunaga K, Masuzaki H, Ueno T, Chayama K, Hamaguchi K, Yamada K, Hanafusa T, Oikawa S, Sakata T, Tanaka K, Matsuzawa Y, Hotta K (2016) CDH13 polymorphisms are associated with adiponectin levels and metabolic syndrome traits independently of visceral fat mass. J Atheroscler Thromb 23(3):309–319.  https://doi.org/10.5551/jat.31567 (Epub 2015 Oct 1)Google Scholar
  62. 62.
    Teng MS, Hsu LA, Wu S, Sun YC, Juan SH5, Ko YL (2015) Association of CDH13 genotypes/haplotypes with circulating adiponectin levels, metabolic syndrome, and related metabolic phenotypes: the role of the suppression effect. PLoS One 10(4):e0122664Google Scholar
  63. 63.
    Cho SA, Joo HJ, Cho JY, Lee SH, Park JH, Hong SJ, Yu CW, Lim DS (2017) Visceral fat area and serum adiponectin level predict the development of metabolic syndrome in a community-based asymptomatic population. PLoS One 12:e0169289Google Scholar
  64. 64.
    He Y, Lu L, Wei X, Jin D, Qian T, Yu A, Sun J, Cui J, Yang Z (2016) The multimerization and secretion of adiponectin are regulated by TNF alpha. Endocrine 51:456–468Google Scholar
  65. 65.
    Mosser DM, Zhang X (2008) Interleukin-10: new perspectives on an old cytokine. Immunol Rev 226(1):205–218Google Scholar
  66. 66.
    Varzaneh FN, Keller B, Unger S, Aghamohammadi A, Warnatz K, Rezaei N (2014) Cytokines in common variable immunodeficiency as signs of immune dysregulation and potential therapeutic targets—a review of the current knowledge. J Clin Immunol 34(5):524–543Google Scholar
  67. 67.
    Cintra DE et al (2008) Interleukin-10 is a protective factor against diet-induced insulin resistance in liver. J Hepatol 48:628–637Google Scholar
  68. 68.
    Gao M et al (2013) Hydrodynamic delivery of mIL10 gene protects mice from high-fat diet-induced obesity and glucose intolerance. Mol Ther 21:1852–1861Google Scholar
  69. 69.
    Kowalski G, Nicholls HT, Risis S et al (2011) Deficiency of haematopoietic-cell-derived IL-10 does not exacerbate high-fat-diet-induced inflammation or insulin resistance in mice. Diabetologia 54:888–899Google Scholar
  70. 70.
    Medeiros NI, Mattos RT, Menezes CA et al (2017) IL-10 and TGF-beta unbalanced levels in neutrophils contribute to increase inflammatory cytokine expression in childhood obesity. Eur J Nutr.  https://doi.org/10.1007/s00394-017-1515-y Google Scholar
  71. 71.
    Rodrigues KF, Pietrani NT, Bosco AA et al (2017) IL-6, TNF-alpha, and IL-10 levels/polymorphisms and their association with type 2 diabetes mellitus and obesity in Brazilian individuals. Archives Endocrinol Metabol 61(5):438–446 (PLoS One 12: e0169289, 2017)Google Scholar
  72. 72.
    Liu Y, Xu D, Yin C, Wang S, Wang M, Xiao Y (2018) IL-10/STAT3 is reduced in childhood obesity with hypertriglyceridemia and is related to triglyceride level in diet-induced obese rats. BMC Endocr Disord 18(1):39Google Scholar
  73. 73.
    Ohashi K, Parker J, Ouchi N et al (2010) Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J Biol Chem 285:6153–6160Google Scholar
  74. 74.
    Ohashi K, Ouchi N, Matsuzawa Y (2012) Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie 94:2137–2142Google Scholar
  75. 75.
    Wong G, Wang J, Hug C et al (2004) A family of Acrp30/adiponectin structural and functional paralogs. Proc Natl Acad Sci USA 101:10302–10307Google Scholar
  76. 76.
    Kumar S, Balagopal P (2018) Vaspin and omentin-1 in obese children with metabolic syndrome: two new kids on the block? Metab Syndr Relat Disord 16:73–75Google Scholar
  77. 77.
    Hill C, Guarner F, Reid G et al (2014) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506Google Scholar
  78. 78.
    Plovier H, Cani PD (2017) Microbial impact on host metabolism: opportunities for novel treatments of nutritional disorders. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.BAD-0002-2016 Google Scholar
  79. 79.
    Gauffin Cano P, Santacruz A, Moya Á et al (2012) Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One 7(7):e41079Google Scholar
  80. 80.
    Cani PD, Van Hul M (2015) Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr Opin Biotechnol 32:21–27Google Scholar
  81. 81.
    Bouter KE, van Raalte DH, Groen AK et al (2017) Role of the gut microbiome in the pathogenesis of obesity and obesity-related metabolic dysfunction. Gastroenterology 152:1671–1678Google Scholar
  82. 82.
    Brandi G, De Lorenzo S, Candela M et al (2017) Microbiota, NASH, HCC and the potential role of probiotics. Carcinogenesis 38:231–240Google Scholar
  83. 83.
    Cani P, Delzenne N (2011) The gut microbiome as therapeutic target. Pharmacol Therap 130:202–212Google Scholar
  84. 84.
    Torres-Fuentes C, Schellekens H, Dinan T et al (2017) The microbiota–gut–brain axis in obesity. Lancet Gastroenterol Hepatol 2:747–756Google Scholar
  85. 85.
    Sanz Y, Rastmanesh R, Agostonic C (2013) Understanding the role of gut microbes and probiotics in obesity: How far are we? Pharmacol Res 69:144–155Google Scholar
  86. 86.
    Guida S, Venema K (2015) Gut microbiota and obesity: involvement of the adipose tissue. J Funct Foods 14:407–423Google Scholar
  87. 87.
    Rouxinol-Dias A, Pinto A, Janeiro C (2016) Probiotics for the control of obesity—its effect on weight change. Porto Biomed J 1:12–24Google Scholar
  88. 88.
    Loman S, van der Kamp JW (2016) Insulin resistance as key factor for linking modulation of gut microbiome to health claims and dietary recommendations to tackle obesity. Trends Food Sci Technol 57:306–310Google Scholar
  89. 89.
    Puddu A, Sanguineti R, Montecucco F et al (2014) Evidence for the gut microbiota short-chain fatty acids as key pathophysiological molecules improving diabetes. Mediators Inflamm 2014:162021.  https://doi.org/10.1155/2014/162021 Google Scholar
  90. 90.
    Lin HV, Frassetto A, Kowalik EJ Jr et al (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 7:e35240 28Google Scholar
  91. 91.
    Frost G, Sleeth ML, Sahuri-Arisoylu M et al (2014) The short chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:3611Google Scholar
  92. 92.
    Tolhurst G, Heffron H, Lam YS et al (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the Gprotein-coupled receptor FFAR2. Diabetes 61:364–371 26Google Scholar
  93. 93.
    Yadav H, Lee JH, Lloyd J et al (2013) Beneficial metabolic effects of a probiotic via butyrate induced GLP-1 secretion. J Biol Chem 288:25088–25097Google Scholar
  94. 94.
    Fernández J, Redondo-Blanco S, Gutiérrez-del-Río I et al (2016) Colon microbiota fermentation of dietary prebiotics towards short-chain fatty acids and their roles as anti-inflammatory and antitumour agents: a review. J Funct Foods 25:511–522Google Scholar
  95. 95.
    Priyadarshini M, Wicksteed B, Schiltz G et al (2016) SCFA receptors in pancreatic β cells: novel diabetes targets? Trends Endocrinol Metab 1125:1–12Google Scholar
  96. 96.
    Neyrinck A, Schüppel V, Lockett T et al (2016) Microbiome and metabolic disorders related to obesity: Which lessons to learn from experimental models? Trends Food Sci Technol 57:256–264Google Scholar
  97. 97.
    Williams KJ, Wu X (2016) Imbalanced insulin action in chronic over nutrition: clinical harm, molecular mechanisms, and a way forward. Atherosclerosis 13:225–282Google Scholar
  98. 98.
    Cani PD, Everard A (2016) Talking microbes: when gut bacteria interact with diet and host organs. Mol Nutr Food Res 60:58–66Google Scholar
  99. 99.
    Borrelli A, Bonelli P, Tuccillo FM et al (2018) Role of gut microbiota and oxidative stress in the progression of non-alcoholic fatty liver disease to hepatocarcinoma: current and innovative therapeutic approaches. Redox Biol 15:467–479Google Scholar
  100. 100.
    Dao MC, Clément K (2018) Gut microbiota and obesity: concepts relevant to clinical care. Eur J Internal Med 48:18–24Google Scholar
  101. 101.
    Kelly JR, Clarke G, Cryan JF et al (2016) Brain-gut-microbiota axis: challenges for translation in psychiatry. Ann Epidemiol 26:366–372Google Scholar
  102. 102.
    Kemgang TS, Kapila S, Shanmugam VP et al (2014) Cross-talk between probiotic lactobacilli and host immune system. J Appl Microbiol 117:303–319Google Scholar
  103. 103.
    Zhang L, Li N, Caicedo R et al (2005) Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 135:1752–1756Google Scholar
  104. 104.
    Tien M-T, Girardin SE, Regnault B et al (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176:1228–1237Google Scholar
  105. 105.
    Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S et al (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174Google Scholar
  106. 106.
    Drakes M, Blanchard T, Czinn S (2004) Bacterial probiotic modulation of dendritic cells. Infect Immun 72:3299–3309Google Scholar
  107. 107.
    Manirarora JN, Parnell SA, Hu YH et al (2011) NOD dendritic cells stimulated with Lactobacilli preferentially produce IL-10 versus IL-12 and decrease diabetes incidence. Clin Dev Immunol 2011:630187.  https://doi.org/10.1155/2011/630187 Google Scholar
  108. 108.
    Devaraj S, Hemarajata P, Versalovic J (2013) The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 59:617–628Google Scholar
  109. 109.
    Novotny Nuñez I, Maldonado C, de Moreno de LeBlanc A et al (2015) Lactobacillus casei CRL 431 administration decreases inflammatory cytokines in a diet-induced obese mouse model. Nutrition 31:1000–1007Google Scholar
  110. 110.
    Lee H, Park J, Seok S et al (2006) Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim Biophys Acta 1761:736–744Google Scholar
  111. 111.
    Ma X, Hua J, Li Z (2008) Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol 49:821–830Google Scholar
  112. 112.
    Sato M, Uzu K, Yoshida T et al (2008) Effects of milk fermented by Lactobacillus gasseri SBT2055 on adipocyte size in rats. Br J Nutr 99:1013–1017Google Scholar
  113. 113.
    Takemura N, Okubo T, Sonoyama K (2010) Lactobacillus plantarum strain No. 14 reduces adipocyte size in mice fed high-fat diet. Exp Biol Med 235:849–856Google Scholar
  114. 114.
    Kadooka Y, Sato M, Imaizumi K et al (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055] in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64:636–643Google Scholar
  115. 115.
    An HM, Park SY, do Lee K et al (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10:116Google Scholar
  116. 116.
    Karlsson CL, Onnerfält J, Xu J et al (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20:2257–2261Google Scholar
  117. 117.
    Gauffin Cano P, Santacruz A, Trejo FM et al (2013) Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet fed mice. Obesity 21:2310–2321Google Scholar
  118. 118.
    Kim SW, Park KY, Kim B et al (2013) Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431:258–263Google Scholar
  119. 119.
    Park DY, Ahn YT, Park SH et al (2013) Supplementation of Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032 in diet-induced obese mice is associated with gut microbial changes and reduction in obesity. PLoS One 8:e59470.  https://doi.org/10.1371/journal.pone.0059470 Google Scholar
  120. 120.
    Ji Y, Park S, Park H et al (2018) Modulation of active gut microbiota by Lactobacillus rhamnosus GG in a diet induced obesity murine model. Front Microbiol 9:710.  https://doi.org/10.3389/fmicb.2018.00710 Google Scholar
  121. 121.
    Holowacz S, Guigne C, Chene G et al (2015) A multispecies Lactobacillus- and Bifidobacterium-containing probiotic mixture attenuates body weight gain and insulin resistance after a short-term challenge with a high-fat diet in C57/BL6J mice. Pharm Nutr 3:101–107Google Scholar
  122. 122.
    Sakai T, Taki T, Nakamoto A et al (2013) Lactobacillus plantarum OLL2712 regulates glucose metabolism in C57BL/6 mice fed a high-fat diet. J Nutr Sci Vitaminol 59:144–147Google Scholar
  123. 123.
    Okubo T, Takemura N, Yoshida A et al (2013) KK/Ta Mice administered Lactobacillus plantarum Strain no. 14 have lower adiposity and higher insulin sensitivity. Biosc Microb Food Health 32:93–100Google Scholar
  124. 124.
    Poutahidis T, Kleinewietfeld M, Smillie C et al (2013) Microbial reprogramming inhibits Western diet-associated obesity. PLoS One 8:e68596Google Scholar
  125. 125.
    Wang J, Tang H, Zhang C et al (2015) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J 9:1–15Google Scholar
  126. 126.
    Park KY, Kim B, Hyun CK (2015) Lactobacillus rhamnosus GG improves glucose tolerance through alleviating ER stress and suppressing macrophage activation in db/db mice. J Clin Biochem Nutr 56:240–246Google Scholar
  127. 127.
    Alard J, Lehrter V, Rhimi M et al (2016) Beneficial metabolic effects of selected probiotics on diet-induced obesity and insulin resistance in mice are associated with improvement of dysbiotic gut microbiota. Environm Microbiol 18:1484–1497Google Scholar
  128. 128.
    Malaguarnera M, Vacante M, Antic T et al (2012) Bifidobacterium longum with fructo-oligosaccharides in patients with nonalcoholic steatohepatitis. Dig Dis Sci 57:545–553Google Scholar
  129. 129.
    Mazloom Z, Yousefinejad A, Dabbaghmanesh MH (2013) Effect of probiotics on lipid profile, glycemic control, insulin action, oxidative stress, and inflammatory markers in patients with type 2 diabetes: a clinical trial. Iran J Med Sci 38:38–43Google Scholar
  130. 130.
    Bernini L, Colado Simão A, Frizon Alfieri D et al (2016) Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: a randomized trial. Nutrition 32:716–719Google Scholar
  131. 131.
    Stenman L, Lehtinen M, Meland N et al (2016) Probiotic with or without fiber controls body fat mass, associated with serum zonulin, in overweight and obese adults—randomized controlled trial. EBioMedicine 13:190–200Google Scholar
  132. 132.
    Zarrati M, Salehi E, Nourijelyani K et al (2014) Effects of probiotic yogurt on fat distribution and gene expression of proinflammatory factors in peripheral blood mononuclear cells in overweight and obese people with or without loss diet. J Am Coll Nutr 33:417–425Google Scholar
  133. 133.
    Drissi F, Raoult D, Merhej V (2016) Metabolic role of lactobacilli in weight modification in humans and animals. Microb Pathog 106:182–194Google Scholar
  134. 134.
    Belguesmia Y, Domenger D, Caron J et al (2016) Novel probiotic evidence of lactobacilli on immunomodulation and regulation of satiety hormones release in intestinal cells. J Function Foods 24:276–286Google Scholar
  135. 135.
    Calcinaro F, Dionisi S, Marinaro M et al (2005) Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 48:1565–1575Google Scholar
  136. 136.
    Zarfeshani A, Khaza’ai H, Mohd Ali R et al (2011) Effect of Lactobacillus casei on the production of pro-inflammatory markers in streptozotocin-induced diabetic rats. Probiotics Antimicro Prot 3:168–174Google Scholar
  137. 137.
    Chen J, Wang R, Li X et al (2011) Bifidobacterium longum supplementation improved high-fat-fed-induced metabolic syndrome and promoted intestinal Reg I gene expression. Exp Biol Med 236:823–831Google Scholar
  138. 138.
    Yoo S, Kim Y, Park D et al (2013) Probiotics L. plantarum and L. curvatus in combination alter hepatic lipid metabolism and suppress diet-induced obesity. Obesity 21:2571–2578Google Scholar
  139. 139.
    Miyoshi M, Ogawa A, Higurashi S et al (2014) Anti-obesity effect of Lactobacillus gasseri SBT2055 accompanied by inhibition of pro-inflammatory gene expression in the visceral adipose tissue in diet-induced obese mice. Eur J Nutr 53:599–606Google Scholar
  140. 140.
    Toral M, Gomez-Guzman M, Jimenez R et al (2014) The probiotic Lactobacillus coryniformis CECT5711 reduces the vascular pro-oxidant and pro-inflammatory status in obese mice. Clin Sci 127:33–45Google Scholar
  141. 141.
    Ritze Y, Bardos G, Claus A et al (2014) Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice. PLoS One 9:e80169Google Scholar
  142. 142.
    Plaza-Diaz J, Gomez-Llorente C, Abadia-Molina F et al (2014) Effects of Lactobacillus paracasei CNCM I-4034, Bifidobacterium breve CNCM I-4035 and Lactobacillus rhamnosus CNCM I-4036 on hepatic steatosis in Zucker rats. PLoS One 9:e98401Google Scholar
  143. 143.
    Zhang X, Wu Y, Wang Y et al (2017) The protective effects of probiotic-fermented soymilk on high-fat diet-induced hyperlipidemia and liver injury. J Funct Foods 30:220–227Google Scholar
  144. 144.
    Novotny Nuñez I, Maldonado C, de Moreno de LeBlanc A et al (2015) Evaluation of immune response, microbiota, and blood markers after probiotic bacteria administration in obese mice induced by a high-fat diet. Nutrition 30:1423–1432Google Scholar
  145. 145.
    Bagarolli R, Natália T, Oliveira A et al (2017) Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J Nutr Biochem 50:16–25Google Scholar
  146. 146.
    Shin J-H, Nam M, Lee H et al (2017) Amelioration of obesity-related characteristics by a probiotic formulation in a high-fat diet-induced obese rat model. Eur J Nutr.  https://doi.org/10.1007/s00394-017-1481-4 Google Scholar
  147. 147.
    Ghanei N, Rezaei N, Amiri G et al (2018) The probiotic supplementation reduced inflammation in polycystic ovary syndrome: a randomized, double-blind, placebo-controlled trial. J Funct Foods 42:306–311Google Scholar
  148. 148.
    Sanchez M, Darimont C, Drapeau V et al (2014) Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Br J Nutr 2014:1507–1519Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Bioprospección y Fisiología Vegetal (INBIOFIV), CONICETTucumánArgentina
  2. 2.Facultad de Ciencias Naturales e IMLUniversidad Nacional de TucumánTucumánArgentina
  3. 3.Facultad de Agronomía y ZootecniaUniversidad Nacional de TucumánTucumánArgentina
  4. 4.Centro de Referencia para Lactobacilos (CERELA), CONICETTucumánArgentina

Personalised recommendations