publication . Article . 2015

Fish Oil-Derived Long-Chain n-3 Polyunsaturated Fatty Acids Reduce Expression of M1-Associated Macrophage Markers in an ex vivo Adipose Tissue Culture Model, in Part through Adiponectin.

Anna A. De Boer; Jennifer M. Monk; Jennifer M. Monk; Danyelle M. Liddle; Krista A. Power; David W.L. Ma; Lindsay E. Robinson;
Open Access English
  • Published: 13 Oct 2015 Journal: Frontiers in Nutrition, volume 2 (eissn: 2296-861X, Copyright policy)
  • Publisher: Frontiers Media S.A.
Abstract
Adipose tissue (AT) macrophages (ATM) play a key role in obesity-associated pathologies, and their phenotype can be influenced by the local tissue microenvironment. Interestingly, long-chain n-3 polyunsaturated fatty acids (LC n-3 PUFA) and the LC n-3 PUFA-upregulated adipokine, adiponectin (Ad), may mitigate excessive ATM inflammatory M1-polarization responses. However, to what extent LC n-3 PUFA and Ad work in concert to affect macrophage phenotype has not been examined. Thus, we used an established ex vivo AT organ culture model using visceral AT from mice fed a control (CON; 10% w/w safflower oil) n-6 PUFA-rich diet or an isocaloric fish oil (FO; 3% w/w menh...
Subjects
free text keywords: Nutrition, Original Research, obesity, adipose tissue, M1 macrophage, n-3 polyunsaturated fatty acids, adiponectin, lipopolysaccharide, Nutrition. Foods and food supply, TX341-641, Adipokine, Inflammation, medicine.symptom, medicine, Internal medicine, medicine.medical_specialty, Tumor necrosis factor alpha, Macrophage polarization, Endocrinology, Polyunsaturated fatty acid, chemistry.chemical_classification, chemistry, Biology, Ex vivo
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
63 references, page 1 of 5

1 Winer S Chan Y Paltser G Truong D Tsui H Bahrami J Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med (2009) 15:921–9.10.1038/nm.2001 19633657 [OpenAIRE] [PubMed] [DOI]

2 Nishimura S Manabe I Nagasaki M Eto K Yamashita H Ohsugi M CD8 effector T c ells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med (2009) 15:914–20.10.1038/nm.1964 19633658 [OpenAIRE] [PubMed] [DOI]

3 Kosteli A Sugaru E Haemmerle G Martin JF Lei J Zechner R Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest (2010) 120:3466.10.1172/JCI42845 20877011 [OpenAIRE] [PubMed] [DOI]

4 Xu X Grijalva A Skowronski A van Eijk M Serlie MJ Ferrante AW. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab (2013) 18:816–30.10.1016/j.cmet.2013.11.001 24315368 [OpenAIRE] [PubMed] [DOI]

5 Dey A Allen J Hankey-Giblin PA. Ontogeny and polarization of macrophages in inflammation: blood monocytes versus tissue macrophages. Front Immunol (2014) 5:683.10.3389/fimmu.2014.00683 25657646 [OpenAIRE] [PubMed] [DOI]

6 Wentworth JM Naselli G Brown WA Doyle L Phipson B Smyth GK Pro-inflammatory CD11c CD206 adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes (2010) 59:1648–56.10.2337/db09-0287 20357360 [OpenAIRE] [PubMed] [DOI]

7 Lumeng CN Bodzin JL Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest (2007) 117:175.10.1172/JCI29881 17200717 [OpenAIRE] [PubMed] [DOI]

8 Fujisaka S Usui I Bukhari A Ikutani M Oya T Kanatani Y Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes (2009) 58:2574–82.10.2337/db08-1475 19690061 [OpenAIRE] [PubMed] [DOI]

9 Morris DL Cho KW DelProposto JL Oatmen KE Geletka LM Martinez-Santiban ez G Adipose tissue macrophages function as antigen-presenting cells and regulate adipose tissue CD4 T cells in mice. Diabetes (2013) 62:2762–72.10.2337/db12-1404 23493569 [OpenAIRE] [PubMed] [DOI]

10 Suganami T Nishida J Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes role of free fatty acids and tumor necrosis factor α. Arterioscler Thromb Vasc Biol (2005) 25:2062–8.10.1161/01.ATV.0000183883.72263.13 16123319 [OpenAIRE] [PubMed] [DOI]

11 Cani PD Amar J Iglesias MA Poggi M Knauf C Bastelica D Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes (2007) 56:1761–72.10.2337/db06-1491 17456850 [OpenAIRE] [PubMed] [DOI]

12 West MA Heagy W Endotoxin tolerance: a review. Crit Care Med (2002) 30:S64–73.10.1097/00003246-200201001-00009 [OpenAIRE] [DOI]

13 Folco EJ Rocha VZ López-Ilasaca M Libby P. Adiponectin inhibits pro-inflammatory signaling in human macrophages independent of interleukin-10. J Biol Chem (2009) 284:25569–75.10.1074/jbc.M109.019786 19617629 [OpenAIRE] [PubMed] [DOI]

14 Ohashi K Parker JL Ouchi N Higuchi A Vita JA Gokce N Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J Biol Chem (2010) 285:6153–60.10.1074/jbc.M109.088708 20028977 [OpenAIRE] [PubMed] [DOI]

15 Mandal P Pratt BT Barnes M McMullen MR Nagy LE. Molecular mechanism for adiponectin-dependent M2 macrophage polarization link between the metabolic and innate immune activity of full-length adiponectin. J Biol Chem (2011) 286:13460–9.10.1074/jbc.M110.204644 21357416 [OpenAIRE] [PubMed] [DOI]

63 references, page 1 of 5
Abstract
Adipose tissue (AT) macrophages (ATM) play a key role in obesity-associated pathologies, and their phenotype can be influenced by the local tissue microenvironment. Interestingly, long-chain n-3 polyunsaturated fatty acids (LC n-3 PUFA) and the LC n-3 PUFA-upregulated adipokine, adiponectin (Ad), may mitigate excessive ATM inflammatory M1-polarization responses. However, to what extent LC n-3 PUFA and Ad work in concert to affect macrophage phenotype has not been examined. Thus, we used an established ex vivo AT organ culture model using visceral AT from mice fed a control (CON; 10% w/w safflower oil) n-6 PUFA-rich diet or an isocaloric fish oil (FO; 3% w/w menh...
Subjects
free text keywords: Nutrition, Original Research, obesity, adipose tissue, M1 macrophage, n-3 polyunsaturated fatty acids, adiponectin, lipopolysaccharide, Nutrition. Foods and food supply, TX341-641, Adipokine, Inflammation, medicine.symptom, medicine, Internal medicine, medicine.medical_specialty, Tumor necrosis factor alpha, Macrophage polarization, Endocrinology, Polyunsaturated fatty acid, chemistry.chemical_classification, chemistry, Biology, Ex vivo
Funded by
NSERC
Project
  • Funder: Natural Sciences and Engineering Research Council of Canada (NSERC)
63 references, page 1 of 5

1 Winer S Chan Y Paltser G Truong D Tsui H Bahrami J Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med (2009) 15:921–9.10.1038/nm.2001 19633657 [OpenAIRE] [PubMed] [DOI]

2 Nishimura S Manabe I Nagasaki M Eto K Yamashita H Ohsugi M CD8 effector T c ells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med (2009) 15:914–20.10.1038/nm.1964 19633658 [OpenAIRE] [PubMed] [DOI]

3 Kosteli A Sugaru E Haemmerle G Martin JF Lei J Zechner R Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Invest (2010) 120:3466.10.1172/JCI42845 20877011 [OpenAIRE] [PubMed] [DOI]

4 Xu X Grijalva A Skowronski A van Eijk M Serlie MJ Ferrante AW. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab (2013) 18:816–30.10.1016/j.cmet.2013.11.001 24315368 [OpenAIRE] [PubMed] [DOI]

5 Dey A Allen J Hankey-Giblin PA. Ontogeny and polarization of macrophages in inflammation: blood monocytes versus tissue macrophages. Front Immunol (2014) 5:683.10.3389/fimmu.2014.00683 25657646 [OpenAIRE] [PubMed] [DOI]

6 Wentworth JM Naselli G Brown WA Doyle L Phipson B Smyth GK Pro-inflammatory CD11c CD206 adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes (2010) 59:1648–56.10.2337/db09-0287 20357360 [OpenAIRE] [PubMed] [DOI]

7 Lumeng CN Bodzin JL Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest (2007) 117:175.10.1172/JCI29881 17200717 [OpenAIRE] [PubMed] [DOI]

8 Fujisaka S Usui I Bukhari A Ikutani M Oya T Kanatani Y Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes (2009) 58:2574–82.10.2337/db08-1475 19690061 [OpenAIRE] [PubMed] [DOI]

9 Morris DL Cho KW DelProposto JL Oatmen KE Geletka LM Martinez-Santiban ez G Adipose tissue macrophages function as antigen-presenting cells and regulate adipose tissue CD4 T cells in mice. Diabetes (2013) 62:2762–72.10.2337/db12-1404 23493569 [OpenAIRE] [PubMed] [DOI]

10 Suganami T Nishida J Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes role of free fatty acids and tumor necrosis factor α. Arterioscler Thromb Vasc Biol (2005) 25:2062–8.10.1161/01.ATV.0000183883.72263.13 16123319 [OpenAIRE] [PubMed] [DOI]

11 Cani PD Amar J Iglesias MA Poggi M Knauf C Bastelica D Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes (2007) 56:1761–72.10.2337/db06-1491 17456850 [OpenAIRE] [PubMed] [DOI]

12 West MA Heagy W Endotoxin tolerance: a review. Crit Care Med (2002) 30:S64–73.10.1097/00003246-200201001-00009 [OpenAIRE] [DOI]

13 Folco EJ Rocha VZ López-Ilasaca M Libby P. Adiponectin inhibits pro-inflammatory signaling in human macrophages independent of interleukin-10. J Biol Chem (2009) 284:25569–75.10.1074/jbc.M109.019786 19617629 [OpenAIRE] [PubMed] [DOI]

14 Ohashi K Parker JL Ouchi N Higuchi A Vita JA Gokce N Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J Biol Chem (2010) 285:6153–60.10.1074/jbc.M109.088708 20028977 [OpenAIRE] [PubMed] [DOI]

15 Mandal P Pratt BT Barnes M McMullen MR Nagy LE. Molecular mechanism for adiponectin-dependent M2 macrophage polarization link between the metabolic and innate immune activity of full-length adiponectin. J Biol Chem (2011) 286:13460–9.10.1074/jbc.M110.204644 21357416 [OpenAIRE] [PubMed] [DOI]

63 references, page 1 of 5
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