Skip to main content
Top
Published in: European Journal of Nutrition 1/2019

01-02-2019 | Review

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

Authors: Sebastian Torres, Emanuel Fabersani, Antonela Marquez, Paola Gauffin-Cano

Published in: European Journal of Nutrition | Issue 1/2019

Login to get access

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.
Literature
1.
go back to reference 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 4:1–7CrossRef 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 4:1–7CrossRef
2.
go back to reference 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 95–103CrossRef 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 95–103CrossRef
3.
go back to reference 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):792–800CrossRef 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):792–800CrossRef
5.
go back to reference Thiennimitr P, Yasom S, Tunapong W et al (2018) Lactobacillus paracasei HII01, xylooligosaccharides and synbiotics reduced gut disturbance in obese rats. Nutrition 54:40–47CrossRefPubMed Thiennimitr P, Yasom S, Tunapong W et al (2018) Lactobacillus paracasei HII01, xylooligosaccharides and synbiotics reduced gut disturbance in obese rats. Nutrition 54:40–47CrossRefPubMed
6.
go back to reference 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 56:1761–1772CrossRefPubMed 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 56:1761–1772CrossRefPubMed
7.
go back to reference 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):792–800CrossRefPubMed 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):792–800CrossRefPubMed
9.
go back to reference Dahiya DK, Puniya M et al (2017) Gut microbiota modulation and its relationship with obesity using prebiotic fibers and probiotics: a review. Front Microbiol 8:563CrossRefPubMedPubMedCentral Dahiya DK, Puniya M et al (2017) Gut microbiota modulation and its relationship with obesity using prebiotic fibers and probiotics: a review. Front Microbiol 8:563CrossRefPubMedPubMedCentral
10.
11.
go back to reference Rezaee F, Dashty M (2013) Role of adipose tissue in metabolic system disorders adipose tissue is the initiator of metabolic diseases. J Diabetes Metab 13:2 Rezaee F, Dashty M (2013) Role of adipose tissue in metabolic system disorders adipose tissue is the initiator of metabolic diseases. J Diabetes Metab 13:2
13.
go back to reference 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):e12365CrossRefPubMedCentral 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):e12365CrossRefPubMedCentral
14.
go back to reference 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 190:71–81CrossRefPubMedPubMedCentral 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 190:71–81CrossRefPubMedPubMedCentral
15.
go back to reference Schäffler A, Schölmerich J (2010) Innate immunity and adipose tissue biology. Trends Immunol 31:228–235CrossRefPubMed Schäffler A, Schölmerich J (2010) Innate immunity and adipose tissue biology. Trends Immunol 31:228–235CrossRefPubMed
16.
go back to reference Enomoto T, Shibata R, Ohashi K et al (2012) Regulation of adipolin/CTRP12 cleavage by obesity. Biochem Biophys Res Commun 428:155–159CrossRefPubMed Enomoto T, Shibata R, Ohashi K et al (2012) Regulation of adipolin/CTRP12 cleavage by obesity. Biochem Biophys Res Commun 428:155–159CrossRefPubMed
17.
go back to reference 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 8:266CrossRefPubMedPubMedCentral 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 8:266CrossRefPubMedPubMedCentral
18.
go back to reference Zoumpopoulou G, Pot B, Tsakalidou E et al (2017) Dairy probiotics: beyond the role of promoting gut and immune health. Inter Dairy J 67:46–60CrossRef Zoumpopoulou G, Pot B, Tsakalidou E et al (2017) Dairy probiotics: beyond the role of promoting gut and immune health. Inter Dairy J 67:46–60CrossRef
19.
go back to reference 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 112:1796–1808CrossRefPubMedPubMedCentral 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 112:1796–1808CrossRefPubMedPubMedCentral
21.
go back to reference 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 15:930CrossRefPubMedPubMedCentral 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 15:930CrossRefPubMedPubMedCentral
22.
go back to reference 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 42:1140–1150CrossRef 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 42:1140–1150CrossRef
23.
go back to reference Patel H, Patel V (2015) Inflammation and metabolic syndrome: an overview. Curr Res Nutr Food Sci J 3:263–268CrossRef Patel H, Patel V (2015) Inflammation and metabolic syndrome: an overview. Curr Res Nutr Food Sci J 3:263–268CrossRef
24.
go back to reference 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 110:189–193CrossRefPubMed 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 110:189–193CrossRefPubMed
25.
go back to reference 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 105:141–150CrossRefPubMed 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 105:141–150CrossRefPubMed
26.
go back to reference Apostolopoulos V, de Courten M, Stojanovska L (2015) Obesity: an immunological perspective. J Immun Res 2:1–3 Apostolopoulos V, de Courten M, Stojanovska L (2015) Obesity: an immunological perspective. J Immun Res 2:1–3
27.
go back to reference 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):43–57CrossRefPubMed 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):43–57CrossRefPubMed
28.
go back to reference Scarpellini E, Tack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153CrossRefPubMed Scarpellini E, Tack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153CrossRefPubMed
29.
go back to reference 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):1372–1378CrossRef 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):1372–1378CrossRef
30.
go back to reference 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 15:921–929CrossRefPubMedPubMedCentral 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 15:921–929CrossRefPubMedPubMedCentral
31.
go back to reference 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 17:610–617CrossRefPubMedPubMedCentral 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 17:610–617CrossRefPubMedPubMedCentral
32.
go back to reference 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):1019–1030CrossRefPubMedPubMedCentral 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):1019–1030CrossRefPubMedPubMedCentral
33.
go back to reference 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 8:86–95CrossRef 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 8:86–95CrossRef
34.
go back to reference 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):243–247CrossRefPubMedPubMedCentral 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):243–247CrossRefPubMedPubMedCentral
35.
go back to reference 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):3440–3452CrossRefPubMed 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):3440–3452CrossRefPubMed
36.
go back to reference 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):940–945CrossRefPubMedPubMedCentral 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):940–945CrossRefPubMedPubMedCentral
37.
go back to reference Kershaw E, Flier J (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89:2548–2556CrossRefPubMed Kershaw E, Flier J (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89:2548–2556CrossRefPubMed
38.
go back to reference Ruan H, Lodish HF (2003) Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α. Cytokine Growth Factor Rev 14:447–455CrossRefPubMed Ruan H, Lodish HF (2003) Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-α. Cytokine Growth Factor Rev 14:447–455CrossRefPubMed
39.
go back to reference Hotamisligil GS (2003) Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 27(Suppl 3):S53–S55CrossRefPubMed Hotamisligil GS (2003) Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord 27(Suppl 3):S53–S55CrossRefPubMed
40.
go back to reference Donath MY (2014) Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov 13(6):465–476CrossRefPubMed Donath MY (2014) Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov 13(6):465–476CrossRefPubMed
41.
go back to reference 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):R141CrossRef 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):R141CrossRef
42.
go back to reference 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–E150CrossRef 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–E150CrossRef
43.
go back to reference 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):R141CrossRef 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):R141CrossRef
45.
go back to reference 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:e53626CrossRefPubMedPubMedCentral 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:e53626CrossRefPubMedPubMedCentral
46.
go back to reference Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88:1379–1406CrossRefPubMed Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88:1379–1406CrossRefPubMed
47.
go back to reference 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 19:267–280CrossRefPubMed 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 19:267–280CrossRefPubMed
48.
go back to reference 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):844CrossRef 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):844CrossRef
49.
go back to reference 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):26602–26614CrossRefPubMed 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):26602–26614CrossRefPubMed
50.
go back to reference 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 79:86–90CrossRefPubMed 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 79:86–90CrossRefPubMed
51.
go back to reference Singh V, Arora S, Goswami B et al (2009) Metabolic syndrome: a review of emerging markers and management. Diab Metab Synd Clin Res Rev 3:240–254 Singh V, Arora S, Goswami B et al (2009) Metabolic syndrome: a review of emerging markers and management. Diab Metab Synd Clin Res Rev 3:240–254
52.
go back to reference Scarpinelli E, Tjack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153CrossRef Scarpinelli E, Tjack J (2012) Obesity and metabolic syndrome: an inflammatory condition. Dig Dis 30:148–153CrossRef
53.
go back to reference 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–S232 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–S232
54.
go back to reference 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 220:513–519CrossRefPubMed 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 220:513–519CrossRefPubMed
55.
go back to reference Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312CrossRefPubMed Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312CrossRefPubMed
57.
go back to reference Kim J, Kim S, Im J et al (2010) The relationship between visfatin and metabolic syndrome in postmenopausal women. Maturitas 67:67–71CrossRefPubMed Kim J, Kim S, Im J et al (2010) The relationship between visfatin and metabolic syndrome in postmenopausal women. Maturitas 67:67–71CrossRefPubMed
58.
go back to reference 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 62:164–175CrossRefPubMed 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 62:164–175CrossRefPubMed
59.
go back to reference Ohashi K, Shibata R, Murohara T et al (2014) Role of anti-inflammatory adipokines in obesity-related diseases. Trends Endocrinol Metabol 25:348–355CrossRef Ohashi K, Shibata R, Murohara T et al (2014) Role of anti-inflammatory adipokines in obesity-related diseases. Trends Endocrinol Metabol 25:348–355CrossRef
60.
go back to reference 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 156:934–946CrossRefPubMed 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 156:934–946CrossRefPubMed
61.
go back to reference 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)CrossRefPubMed 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)CrossRefPubMed
62.
go back to reference 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):e0122664CrossRefPubMedPubMedCentral 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):e0122664CrossRefPubMedPubMedCentral
63.
go back to reference 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:e0169289CrossRefPubMedPubMedCentral 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:e0169289CrossRefPubMedPubMedCentral
64.
go back to reference 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 51:456–468CrossRefPubMed 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 51:456–468CrossRefPubMed
66.
go back to reference 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):524–543CrossRefPubMed 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):524–543CrossRefPubMed
67.
go back to reference Cintra DE et al (2008) Interleukin-10 is a protective factor against diet-induced insulin resistance in liver. J Hepatol 48:628–637CrossRefPubMed Cintra DE et al (2008) Interleukin-10 is a protective factor against diet-induced insulin resistance in liver. J Hepatol 48:628–637CrossRefPubMed
68.
go back to reference Gao M et al (2013) Hydrodynamic delivery of mIL10 gene protects mice from high-fat diet-induced obesity and glucose intolerance. Mol Ther 21:1852–1861CrossRefPubMedPubMedCentral Gao M et al (2013) Hydrodynamic delivery of mIL10 gene protects mice from high-fat diet-induced obesity and glucose intolerance. Mol Ther 21:1852–1861CrossRefPubMedPubMedCentral
69.
go back to reference 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 54:888–899CrossRefPubMed 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 54:888–899CrossRefPubMed
71.
go back to reference 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)CrossRef 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)CrossRef
72.
go back to reference 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):39CrossRef 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):39CrossRef
73.
go back to reference Ohashi K, Parker J, Ouchi N et al (2010) Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J Biol Chem 285:6153–6160CrossRefPubMed Ohashi K, Parker J, Ouchi N et al (2010) Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J Biol Chem 285:6153–6160CrossRefPubMed
74.
go back to reference Ohashi K, Ouchi N, Matsuzawa Y (2012) Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie 94:2137–2142CrossRefPubMed Ohashi K, Ouchi N, Matsuzawa Y (2012) Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie 94:2137–2142CrossRefPubMed
75.
76.
go back to reference 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 16:73–75CrossRefPubMed 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 16:73–75CrossRefPubMed
77.
go back to reference 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 11:506CrossRefPubMed 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 11:506CrossRefPubMed
79.
go back to reference 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):e41079CrossRefPubMedPubMedCentral 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):e41079CrossRefPubMedPubMedCentral
80.
go back to reference Cani PD, Van Hul M (2015) Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr Opin Biotechnol 32:21–27CrossRefPubMed Cani PD, Van Hul M (2015) Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr Opin Biotechnol 32:21–27CrossRefPubMed
81.
go back to reference 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 152:1671–1678CrossRefPubMed 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 152:1671–1678CrossRefPubMed
82.
go back to reference Brandi G, De Lorenzo S, Candela M et al (2017) Microbiota, NASH, HCC and the potential role of probiotics. Carcinogenesis 38:231–240CrossRefPubMed Brandi G, De Lorenzo S, Candela M et al (2017) Microbiota, NASH, HCC and the potential role of probiotics. Carcinogenesis 38:231–240CrossRefPubMed
83.
go back to reference Cani P, Delzenne N (2011) The gut microbiome as therapeutic target. Pharmacol Therap 130:202–212CrossRef Cani P, Delzenne N (2011) The gut microbiome as therapeutic target. Pharmacol Therap 130:202–212CrossRef
84.
go back to reference Torres-Fuentes C, Schellekens H, Dinan T et al (2017) The microbiota–gut–brain axis in obesity. Lancet Gastroenterol Hepatol 2:747–756CrossRefPubMed Torres-Fuentes C, Schellekens H, Dinan T et al (2017) The microbiota–gut–brain axis in obesity. Lancet Gastroenterol Hepatol 2:747–756CrossRefPubMed
85.
go back to reference Sanz Y, Rastmanesh R, Agostonic C (2013) Understanding the role of gut microbes and probiotics in obesity: How far are we? Pharmacol Res 69:144–155CrossRefPubMed Sanz Y, Rastmanesh R, Agostonic C (2013) Understanding the role of gut microbes and probiotics in obesity: How far are we? Pharmacol Res 69:144–155CrossRefPubMed
86.
go back to reference Guida S, Venema K (2015) Gut microbiota and obesity: involvement of the adipose tissue. J Funct Foods 14:407–423CrossRef Guida S, Venema K (2015) Gut microbiota and obesity: involvement of the adipose tissue. J Funct Foods 14:407–423CrossRef
88.
go back to reference 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 57:306–310CrossRef 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 57:306–310CrossRef
90.
go back to reference 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 28CrossRef 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 28CrossRef
91.
go back to reference 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 5:3611CrossRefPubMed 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 5:3611CrossRefPubMed
92.
go back to reference 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 26CrossRefPubMedPubMedCentral 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 26CrossRefPubMedPubMedCentral
93.
94.
go back to reference 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 25:511–522CrossRef 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 25:511–522CrossRef
95.
go back to reference Priyadarshini M, Wicksteed B, Schiltz G et al (2016) SCFA receptors in pancreatic β cells: novel diabetes targets? Trends Endocrinol Metab 1125:1–12 Priyadarshini M, Wicksteed B, Schiltz G et al (2016) SCFA receptors in pancreatic β cells: novel diabetes targets? Trends Endocrinol Metab 1125:1–12
96.
go back to reference 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 57:256–264CrossRef 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 57:256–264CrossRef
97.
go back to reference Williams KJ, Wu X (2016) Imbalanced insulin action in chronic over nutrition: clinical harm, molecular mechanisms, and a way forward. Atherosclerosis 13:225–282CrossRef Williams KJ, Wu X (2016) Imbalanced insulin action in chronic over nutrition: clinical harm, molecular mechanisms, and a way forward. Atherosclerosis 13:225–282CrossRef
98.
go back to reference Cani PD, Everard A (2016) Talking microbes: when gut bacteria interact with diet and host organs. Mol Nutr Food Res 60:58–66CrossRefPubMed Cani PD, Everard A (2016) Talking microbes: when gut bacteria interact with diet and host organs. Mol Nutr Food Res 60:58–66CrossRefPubMed
99.
go back to reference 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 15:467–479CrossRefPubMedPubMedCentral 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 15:467–479CrossRefPubMedPubMedCentral
100.
go back to reference Dao MC, Clément K (2018) Gut microbiota and obesity: concepts relevant to clinical care. Eur J Internal Med 48:18–24CrossRef Dao MC, Clément K (2018) Gut microbiota and obesity: concepts relevant to clinical care. Eur J Internal Med 48:18–24CrossRef
101.
go back to reference Kelly JR, Clarke G, Cryan JF et al (2016) Brain-gut-microbiota axis: challenges for translation in psychiatry. Ann Epidemiol 26:366–372CrossRefPubMed Kelly JR, Clarke G, Cryan JF et al (2016) Brain-gut-microbiota axis: challenges for translation in psychiatry. Ann Epidemiol 26:366–372CrossRefPubMed
102.
go back to reference Kemgang TS, Kapila S, Shanmugam VP et al (2014) Cross-talk between probiotic lactobacilli and host immune system. J Appl Microbiol 117:303–319CrossRefPubMed Kemgang TS, Kapila S, Shanmugam VP et al (2014) Cross-talk between probiotic lactobacilli and host immune system. J Appl Microbiol 117:303–319CrossRefPubMed
103.
go back to reference 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 135:1752–1756CrossRefPubMed 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 135:1752–1756CrossRefPubMed
104.
go back to reference 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 176:1228–1237CrossRefPubMed 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 176:1228–1237CrossRefPubMed
105.
go back to reference Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S et al (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174CrossRefPubMed Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S et al (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174CrossRefPubMed
108.
go back to reference Devaraj S, Hemarajata P, Versalovic J (2013) The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 59:617–628CrossRefPubMedPubMedCentral Devaraj S, Hemarajata P, Versalovic J (2013) The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 59:617–628CrossRefPubMedPubMedCentral
109.
go back to reference 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 31:1000–1007CrossRefPubMed 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 31:1000–1007CrossRefPubMed
110.
go back to reference 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 1761:736–744CrossRefPubMed 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 1761:736–744CrossRefPubMed
111.
go back to reference 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 49:821–830CrossRefPubMedPubMedCentral 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 49:821–830CrossRefPubMedPubMedCentral
112.
go back to reference 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 99:1013–1017CrossRefPubMed 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 99:1013–1017CrossRefPubMed
113.
go back to reference Takemura N, Okubo T, Sonoyama K (2010) Lactobacillus plantarum strain No. 14 reduces adipocyte size in mice fed high-fat diet. Exp Biol Med 235:849–856CrossRef Takemura N, Okubo T, Sonoyama K (2010) Lactobacillus plantarum strain No. 14 reduces adipocyte size in mice fed high-fat diet. Exp Biol Med 235:849–856CrossRef
114.
go back to reference 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 64:636–643CrossRefPubMed 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 64:636–643CrossRefPubMed
115.
go back to reference 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 10:116CrossRefPubMedPubMedCentral 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 10:116CrossRefPubMedPubMedCentral
116.
go back to reference Karlsson CL, Onnerfält J, Xu J et al (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20:2257–2261CrossRefPubMed Karlsson CL, Onnerfält J, Xu J et al (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20:2257–2261CrossRefPubMed
117.
go back to reference 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 21:2310–2321CrossRef 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 21:2310–2321CrossRef
118.
go back to reference 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 431:258–263CrossRefPubMed 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 431:258–263CrossRefPubMed
121.
go back to reference 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 3:101–107 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 3:101–107
122.
go back to reference 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 59:144–147CrossRefPubMed 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 59:144–147CrossRefPubMed
123.
go back to reference 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 32:93–100CrossRef 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 32:93–100CrossRef
124.
125.
go back to reference 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 9:1–15CrossRefPubMed 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 9:1–15CrossRefPubMed
126.
go back to reference 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 56:240–246CrossRefPubMedPubMedCentral 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 56:240–246CrossRefPubMedPubMedCentral
127.
go back to reference 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 18:1484–1497CrossRef 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 18:1484–1497CrossRef
128.
go back to reference Malaguarnera M, Vacante M, Antic T et al (2012) Bifidobacterium longum with fructo-oligosaccharides in patients with nonalcoholic steatohepatitis. Dig Dis Sci 57:545–553CrossRefPubMed Malaguarnera M, Vacante M, Antic T et al (2012) Bifidobacterium longum with fructo-oligosaccharides in patients with nonalcoholic steatohepatitis. Dig Dis Sci 57:545–553CrossRefPubMed
129.
go back to reference 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 38:38–43PubMedPubMedCentral 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 38:38–43PubMedPubMedCentral
130.
go back to reference 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 32:716–719CrossRefPubMed 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 32:716–719CrossRefPubMed
131.
go back to reference 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 13:190–200CrossRefPubMedPubMedCentral 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 13:190–200CrossRefPubMedPubMedCentral
132.
go back to reference 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 33:417–425CrossRefPubMed 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 33:417–425CrossRefPubMed
133.
go back to reference Drissi F, Raoult D, Merhej V (2016) Metabolic role of lactobacilli in weight modification in humans and animals. Microb Pathog 106:182–194CrossRefPubMed Drissi F, Raoult D, Merhej V (2016) Metabolic role of lactobacilli in weight modification in humans and animals. Microb Pathog 106:182–194CrossRefPubMed
134.
go back to reference 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 24:276–286CrossRef 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 24:276–286CrossRef
135.
go back to reference 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 48:1565–1575CrossRefPubMed 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 48:1565–1575CrossRefPubMed
136.
go back to reference 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 3:168–174CrossRef 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 3:168–174CrossRef
137.
go back to reference 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 236:823–831CrossRef 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 236:823–831CrossRef
138.
go back to reference 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 21:2571–2578CrossRefPubMed 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 21:2571–2578CrossRefPubMed
139.
go back to reference 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 53:599–606CrossRefPubMed 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 53:599–606CrossRefPubMed
140.
go back to reference 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 127:33–45CrossRef 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 127:33–45CrossRef
141.
142.
go back to reference 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:e98401CrossRefPubMedPubMedCentral 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:e98401CrossRefPubMedPubMedCentral
143.
go back to reference 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 30:220–227CrossRef 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 30:220–227CrossRef
144.
go back to reference 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 30:1423–1432CrossRef 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 30:1423–1432CrossRef
145.
go back to reference Bagarolli R, Natália T, Oliveira A et al (2017) Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J Nutr Biochem 50:16–25CrossRefPubMed Bagarolli R, Natália T, Oliveira A et al (2017) Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J Nutr Biochem 50:16–25CrossRefPubMed
147.
go back to reference 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 42:306–311CrossRef 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 42:306–311CrossRef
148.
go back to reference 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 2014:1507–1519CrossRef 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 2014:1507–1519CrossRef
Metadata
Title
Adipose tissue inflammation and metabolic syndrome. The proactive role of probiotics
Authors
Sebastian Torres
Emanuel Fabersani
Antonela Marquez
Paola Gauffin-Cano
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2019
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-018-1790-2

Other articles of this Issue 1/2019

European Journal of Nutrition 1/2019 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.