High Fat Diet Triggers a Prompt and Transient Increase in Adipose Tissue Granulocyte Colony Stimulating Factor and Circulating Myeloid Cells in Mice
Asian Journal of Immunology,
Page 7-21
Abstract
Scope: The short-term effects of feeding high fat diet (HFD) to mice was investigated with focus on the effect on myelopoesis, circulating neutrophils and the induction of Granulocyte colony stimulating factor (G-CSF).
Methods: Male mice were fed HFD (45%) during a period of 5 weeks with samples taken after 3 days and 1, 3, 4 and 5 weeks. Blood was analyzed for neutrophils and monocytes, for G-CSF and granulocyte-macrophage (GM)-CSF, and for cytokine expression. Visceral adipose tissue (VAT) expression of various genes and production of G-GSF and GM-CSF in cultured VAT was determined.
Results: Three days after commencement of HFD, the number of circulatory neutrophils and monocytes increased but returned to baseline-level at day 8. This transient increase coincided with an increased blood concentration of G-CSF and a transient increase in bone marrow and spleen neutrophils. In supernatant from cultivated visceral adipose tissue isolated from HFD fed mice on day 3 and 8, G-CSF was increased. The expression of Toll-like receptor 4 in adipose tissue was down-regulated from week 4. In vitro, lipopolysaccharide (LPS) was a poor stimulator of G-CSF, while G-CSF or LPS together with G-CSF or GM-CSF induced increased G-CSF production. G-CSF suppressed production of LPS-induced TNFa and increased IL-10 production in dendritic cells suggesting that G-CSF down-regulates LPS-induced inflammation.
Conclusion: HFD induces a transient increase in adipose tissue G-GSF and circulating myeloid cells in mice. We suggest G-CSF induces increased myelopoiesis and simultaneously down-regulates LPS-induced inflammation.
Keywords:
- Adipose tissue
- granulocyte-coloni stimulating factor (G-CSF) production
- high fat diet
- monocytes
- neutrophils
How to Cite
S. Eld, H. M., Madsen, L., Lund, C. H., Metzdorff, S. B., & Frøkiær, H. (2021). High Fat Diet Triggers a Prompt and Transient Increase in Adipose Tissue Granulocyte Colony Stimulating Factor and Circulating Myeloid Cells in Mice. Asian Journal of Immunology, 5(4), 7-21. Retrieved from https://journalaji.com/index.php/AJI/article/view/30164
References
Duan Y, Zeng L, Zheng C, Song B, Li F, Kong, Xu K. Inflammatory Links X Between High Fat Diets and Diseases, Frontiers in Immunology. 2018;9:2649.
Emerson SR, Kurti SP, Harms CA, Haub MD, Melgarejo T, Logan C, Rosenkranz SK, Magnitude and Timing of the Postprandial Inflammatory Response to a High-Fat Meal in Healthy Adults: A Systematic Review, Adv Nutr. 2017;8(2): 213.
Mohammad S, Thiemermann C. Role of Metabolic Endotoxemia in Systemic Inflammation and Potential Interventions, Front Immunol. 2020;11:594150.
Hersoug LG, Møller P, Loft S. Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity, Obesity Reviews. 2016;17(4):297.
Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E. Chylomicrons promote intestinal absorption of lipopolysaccharides, J Lipid Res. 2009; 50(1):90.
Laugerette F, Vors C, Peretti N, Michalski MC. Complex links between dietary lipids, endogenous endotoxins and metabolic inflammation, Biochimie. 2011;93(1):39.
Boettcher S, Gerosa RC, Radpour R, Bauer J, Ampenberger F, Heikenwalder M, Kopf M, Manz MG. Endothelial cells translate pathogen signals into G-CSF-driven emergency granulopoiesis, Blood. 2014;124(9):1393.
Quesenberry P, Morley A, Stohlman F, Rickard K, Howard D, Smith M. Effect of Endotoxin on Granulopoeisis and Colony-Stimulating Factor, The New England Journal of Medicine. 1972;286(5):227.
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. Metabolic endotoxemia initiates obesity and insulin resistance, Diabetes. 2007;56(7):1761.
Ordelheide AM, Gommer N, Bohm A, Hermann C, Thielker I, Machicao F, Fritsche A, Stefan N, Haring HU, Staiger H. Granulocyte colony-stimulating factor (G-CSF): A saturated fatty acid-induced myokine with insulin-desensitizing properties in humans, Mol Metab. 2016; 5(4):305.
Ono-Moore KD, Snodgrass RG, Huang S, Singh S, Freytag TL, Burnett DJ, Bonnel EL, Woodhouse LR, Zunino SJ, Peerson JM, Lee JY, Rutledge JC, Hwang DH. Postprandial Inflammatory Responses and Free Fatty Acids in Plasma of Adults Who Consumed a Moderately High-Fat Breakfast with and without Blueberry Powder in a Randomized Placebo-Controlled Trial, J Nutr. 2016;146(7):1411.
Mo Z, Huang S, Burnett DJ, Rutledge JC, Hwang DH. Endotoxin May Not Be the Major Cause of Postprandial Inflammation in Adults Who Consume a Single High-Fat or Moderately High-Fat Meal, J Nutr. 2020;150(5):1303.
Heydemann A. An Overview of Murine High Fat Diet as a Model for Type 2 Diabetes Mellitus, J Diabetes Res. 2016; 2016:902351.
Nagareddy PR, Kraakman M, Masters SL, Stirzaker RA, Gorman DJ, Grant RW, Dragoljevic D, Hong ES, Abdel-Latif A, Smyth SS, Choi SH, Korner J, Bornfeldt KE, Fisher EA, Dixit VD, Tall AR, Goldberg IJ, Murphy AJ. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity, Cell Metab. 2014; 19(5):821.
Singer K, DelProposto J, Lee Morris D, Zamarron B, Mergian T, Maley N, Cho KW, Geletka L, Subbaiah P, Muir L, Martinez-Santibanez G, Nien-Kai Lumeng C. Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells, Mol Metab. 2014;3(6):664.
Talukdar S, Oh DY, Bandyopadhyay G, Li D, Xu J, McNelis J, Lu M, Li P, Yan Q, Zhu Y, Ofrecio J, Lin M, Brenner MB, Olefsky JM. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase, Nat Med. 2012;18(9):1407.
Elgazar-Carmon V, Rudich A, Hadad N. Levy R. Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding, J Lipid Res. 2008;49(9): 1894.
Fuglsang E, Krych L, Lundsager MT, Nielsen DS, Frokiaer H. Postnatal Administration of Lactobacillus rhamnosus HN001 Ameliorates Perinatal Broad-Spectrum Antibiotic-Induced Reduction in Myelopoiesis and T Cell Activation in Mouse Pups, Mol Nutr Food Res. 2018; 62(22).
Hansen CH, Frokiaer H, Christensen AG, Bergstrom A, Licht TR, Hansen AK, Metzdorff SB. Dietary xylooligosaccharide downregulates IFN-gamma and the low-grade inflammatory cytokine IL-1beta systemically in mice, J Nutr. 2013;143(4): 533.
Yu R, Kim C-S, Kwon B-S, Kawada T. Mesenteric Adipose Tissue-Derived Monocyte Chemoattractant Protein-1 Plays a Crucial Role in Adipose Tissue Macrophage Migration and Activation in Obese Mice, OBESITY. 2006;14(8):1353.
Christensen HR, Frokiaer H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells, J Immunol. 2002;168(1):171.
Gargiulo S, Gramanzini M, Megna R, Greco A, Albanese S, Manfredi C, Brunetti A. Evaluation of growth patterns and body composition in C57Bl/6J mice using dual energy X-ray absorptiometry, Biomed Res Int. 2014;2014:253067.
Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, Cowland JB, Borregaard N. The transcriptional program of terminal granulocytic differentiation, Blood. 2005; 105(4):1785.
Cranford TL, Enos RT, Velazquez KT, McClellan JL, Davis JM, Singh UP, Nagarkatti M, Nagarkatti PS, Robinson CM, Murphy EA. Int J Obes (Lond). 2016;40(5):844.
van den Berg TK, Kraal G. A function for the macrophage F4/80 molecule in tolerance induction, Trends Immunol. 2005;26(10):506.
Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation, Front Immunol, 9: 1298.Front Immunol. 2018;9: 1298.
Liu Y, Lu X, Li X, Du P, Qin G. High-fat diet triggers obesity-related early infiltration of macrophages into adipose tissue and transient reduction of blood monocyte count, Mol Immunol. 2020;117:139.
Semerad CL, Liu F, Gregory AD, Stumpf K, Link DC. G-CSF Is an Essential Regulator of Neutrophil Trafficking from the Bone Marrow to the Blood, Immunity. 2002;17:413.
Tso P, Pitts V, Granger N. Role of Lymph Flow in intestinal chylomicron transport, Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12) 1985, G21.
Lopez-Moreno J, Garcia-Carpintero S, Jimenez-Lucena R, Haro C, Rangel-Zuniga OA, Blanco-Rojo R, Yubero-Serrano EM, Tinahones FJ, Delgado-Lista J, Perez-Martinez P, Roche HM, Lopez-Miranda J, Camargo A. Effect of Dietary Lipids on Endotoxemia Influences Postprandial Inflammatory Response, J Agric Food Chem. 2017;65(35):7756.
Borregaard N. Neutrophils, from marrow to microbes, Immunity. 2010;33(5):657.
Demetri GD, Griffin JD. Granulocyte colony-stimulating factor and its receptor, Blood. 1991;78(11):2791.
Liu F, Wu HY, Wesselschmidt R, Kornaga T, Link DC. Impaired Production and Increased Apoptosis of Neutrophils in Granulocyte Colony-Stimulating Factor Receptor–Deficient Mice, Immunity. 1996;5:491.
Martins A, Han J, Kim SO. The multifaceted effects of granulocyte colony-stimulating factor in immunomodulation and potential roles in intestinal immune homeostasis, IUBMB Life. 2010;62(8):611.
Boneberg E-M, Hartung T. Molecular aspects of anti-inflammatory action of G-CSF', Inflammation Research, Inflammation Research. 2002;51:119.
Nishiki S, Hato F, Kamata N, Sakamoto E, Hasegawa T, Kimura-Eto A, Hino M, Kitagawa S. Selective activation of STAT3 in human monocytes stimulated by G-CSF: implication in inhibition of LPS-induced TNF-a production, Am J Physiol Cell Physiol. 2004;286:C1302.
Görgen I, Hartung T, Leist M, Nierhorster M, Tiegs G, Uhlig S, Weitzel F, Wendel A. Granulocyte colony-stimulating factor treatment protects rodents against ipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha, Immunology. 1992;149:918.
Hartung T, Docke W-D, Gantner F, Krieger G, Sauer A, Stevens P, Volk H-D, Wendel A. Effect of Granulocyte Colony-Stimulating Factor Treatment on Ex Vivo Blood Cytokine Response in Human Volunteers, Blood. 1995;85(9):2482.
Pajkrt D, Manten A, van der Poll T, Tiel-van Buul MMC, Jansen J, Wouter ten Cate J, van Deventer SJH. Modulation of Cytokine Release and Neutrophil Function by Granulocyte Colony-Stimulating Factor During Endotoxemia in Humans, Blood. 1997;90(4):1415.
Rajbhandari P, Thomas BJ, Feng AC, Hong C, Wang J, Vergnes L, Sallam T, Wang B, Sandhu J, Seldin MM, Lusis AJ, Fong LG, Katz M, Lee R, Young SG, Reue K, Smale ST, Tontonoz P. IL-10 Signaling Remodels Adipose Chromatin Architecture to Limit Thermogenesis and Energy Expenditure, Cell. 2018;172(1-2):218.
Emerson SR, Kurti SP, Harms CA, Haub MD, Melgarejo T, Logan C, Rosenkranz SK, Magnitude and Timing of the Postprandial Inflammatory Response to a High-Fat Meal in Healthy Adults: A Systematic Review, Adv Nutr. 2017;8(2): 213.
Mohammad S, Thiemermann C. Role of Metabolic Endotoxemia in Systemic Inflammation and Potential Interventions, Front Immunol. 2020;11:594150.
Hersoug LG, Møller P, Loft S. Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity, Obesity Reviews. 2016;17(4):297.
Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E. Chylomicrons promote intestinal absorption of lipopolysaccharides, J Lipid Res. 2009; 50(1):90.
Laugerette F, Vors C, Peretti N, Michalski MC. Complex links between dietary lipids, endogenous endotoxins and metabolic inflammation, Biochimie. 2011;93(1):39.
Boettcher S, Gerosa RC, Radpour R, Bauer J, Ampenberger F, Heikenwalder M, Kopf M, Manz MG. Endothelial cells translate pathogen signals into G-CSF-driven emergency granulopoiesis, Blood. 2014;124(9):1393.
Quesenberry P, Morley A, Stohlman F, Rickard K, Howard D, Smith M. Effect of Endotoxin on Granulopoeisis and Colony-Stimulating Factor, The New England Journal of Medicine. 1972;286(5):227.
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. Metabolic endotoxemia initiates obesity and insulin resistance, Diabetes. 2007;56(7):1761.
Ordelheide AM, Gommer N, Bohm A, Hermann C, Thielker I, Machicao F, Fritsche A, Stefan N, Haring HU, Staiger H. Granulocyte colony-stimulating factor (G-CSF): A saturated fatty acid-induced myokine with insulin-desensitizing properties in humans, Mol Metab. 2016; 5(4):305.
Ono-Moore KD, Snodgrass RG, Huang S, Singh S, Freytag TL, Burnett DJ, Bonnel EL, Woodhouse LR, Zunino SJ, Peerson JM, Lee JY, Rutledge JC, Hwang DH. Postprandial Inflammatory Responses and Free Fatty Acids in Plasma of Adults Who Consumed a Moderately High-Fat Breakfast with and without Blueberry Powder in a Randomized Placebo-Controlled Trial, J Nutr. 2016;146(7):1411.
Mo Z, Huang S, Burnett DJ, Rutledge JC, Hwang DH. Endotoxin May Not Be the Major Cause of Postprandial Inflammation in Adults Who Consume a Single High-Fat or Moderately High-Fat Meal, J Nutr. 2020;150(5):1303.
Heydemann A. An Overview of Murine High Fat Diet as a Model for Type 2 Diabetes Mellitus, J Diabetes Res. 2016; 2016:902351.
Nagareddy PR, Kraakman M, Masters SL, Stirzaker RA, Gorman DJ, Grant RW, Dragoljevic D, Hong ES, Abdel-Latif A, Smyth SS, Choi SH, Korner J, Bornfeldt KE, Fisher EA, Dixit VD, Tall AR, Goldberg IJ, Murphy AJ. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity, Cell Metab. 2014; 19(5):821.
Singer K, DelProposto J, Lee Morris D, Zamarron B, Mergian T, Maley N, Cho KW, Geletka L, Subbaiah P, Muir L, Martinez-Santibanez G, Nien-Kai Lumeng C. Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells, Mol Metab. 2014;3(6):664.
Talukdar S, Oh DY, Bandyopadhyay G, Li D, Xu J, McNelis J, Lu M, Li P, Yan Q, Zhu Y, Ofrecio J, Lin M, Brenner MB, Olefsky JM. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase, Nat Med. 2012;18(9):1407.
Elgazar-Carmon V, Rudich A, Hadad N. Levy R. Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding, J Lipid Res. 2008;49(9): 1894.
Fuglsang E, Krych L, Lundsager MT, Nielsen DS, Frokiaer H. Postnatal Administration of Lactobacillus rhamnosus HN001 Ameliorates Perinatal Broad-Spectrum Antibiotic-Induced Reduction in Myelopoiesis and T Cell Activation in Mouse Pups, Mol Nutr Food Res. 2018; 62(22).
Hansen CH, Frokiaer H, Christensen AG, Bergstrom A, Licht TR, Hansen AK, Metzdorff SB. Dietary xylooligosaccharide downregulates IFN-gamma and the low-grade inflammatory cytokine IL-1beta systemically in mice, J Nutr. 2013;143(4): 533.
Yu R, Kim C-S, Kwon B-S, Kawada T. Mesenteric Adipose Tissue-Derived Monocyte Chemoattractant Protein-1 Plays a Crucial Role in Adipose Tissue Macrophage Migration and Activation in Obese Mice, OBESITY. 2006;14(8):1353.
Christensen HR, Frokiaer H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells, J Immunol. 2002;168(1):171.
Gargiulo S, Gramanzini M, Megna R, Greco A, Albanese S, Manfredi C, Brunetti A. Evaluation of growth patterns and body composition in C57Bl/6J mice using dual energy X-ray absorptiometry, Biomed Res Int. 2014;2014:253067.
Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, Cowland JB, Borregaard N. The transcriptional program of terminal granulocytic differentiation, Blood. 2005; 105(4):1785.
Cranford TL, Enos RT, Velazquez KT, McClellan JL, Davis JM, Singh UP, Nagarkatti M, Nagarkatti PS, Robinson CM, Murphy EA. Int J Obes (Lond). 2016;40(5):844.
van den Berg TK, Kraal G. A function for the macrophage F4/80 molecule in tolerance induction, Trends Immunol. 2005;26(10):506.
Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation, Front Immunol, 9: 1298.Front Immunol. 2018;9: 1298.
Liu Y, Lu X, Li X, Du P, Qin G. High-fat diet triggers obesity-related early infiltration of macrophages into adipose tissue and transient reduction of blood monocyte count, Mol Immunol. 2020;117:139.
Semerad CL, Liu F, Gregory AD, Stumpf K, Link DC. G-CSF Is an Essential Regulator of Neutrophil Trafficking from the Bone Marrow to the Blood, Immunity. 2002;17:413.
Tso P, Pitts V, Granger N. Role of Lymph Flow in intestinal chylomicron transport, Am. J. Physiol. 249 (Gastrointest. Liver Physiol. 12) 1985, G21.
Lopez-Moreno J, Garcia-Carpintero S, Jimenez-Lucena R, Haro C, Rangel-Zuniga OA, Blanco-Rojo R, Yubero-Serrano EM, Tinahones FJ, Delgado-Lista J, Perez-Martinez P, Roche HM, Lopez-Miranda J, Camargo A. Effect of Dietary Lipids on Endotoxemia Influences Postprandial Inflammatory Response, J Agric Food Chem. 2017;65(35):7756.
Borregaard N. Neutrophils, from marrow to microbes, Immunity. 2010;33(5):657.
Demetri GD, Griffin JD. Granulocyte colony-stimulating factor and its receptor, Blood. 1991;78(11):2791.
Liu F, Wu HY, Wesselschmidt R, Kornaga T, Link DC. Impaired Production and Increased Apoptosis of Neutrophils in Granulocyte Colony-Stimulating Factor Receptor–Deficient Mice, Immunity. 1996;5:491.
Martins A, Han J, Kim SO. The multifaceted effects of granulocyte colony-stimulating factor in immunomodulation and potential roles in intestinal immune homeostasis, IUBMB Life. 2010;62(8):611.
Boneberg E-M, Hartung T. Molecular aspects of anti-inflammatory action of G-CSF', Inflammation Research, Inflammation Research. 2002;51:119.
Nishiki S, Hato F, Kamata N, Sakamoto E, Hasegawa T, Kimura-Eto A, Hino M, Kitagawa S. Selective activation of STAT3 in human monocytes stimulated by G-CSF: implication in inhibition of LPS-induced TNF-a production, Am J Physiol Cell Physiol. 2004;286:C1302.
Görgen I, Hartung T, Leist M, Nierhorster M, Tiegs G, Uhlig S, Weitzel F, Wendel A. Granulocyte colony-stimulating factor treatment protects rodents against ipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha, Immunology. 1992;149:918.
Hartung T, Docke W-D, Gantner F, Krieger G, Sauer A, Stevens P, Volk H-D, Wendel A. Effect of Granulocyte Colony-Stimulating Factor Treatment on Ex Vivo Blood Cytokine Response in Human Volunteers, Blood. 1995;85(9):2482.
Pajkrt D, Manten A, van der Poll T, Tiel-van Buul MMC, Jansen J, Wouter ten Cate J, van Deventer SJH. Modulation of Cytokine Release and Neutrophil Function by Granulocyte Colony-Stimulating Factor During Endotoxemia in Humans, Blood. 1997;90(4):1415.
Rajbhandari P, Thomas BJ, Feng AC, Hong C, Wang J, Vergnes L, Sallam T, Wang B, Sandhu J, Seldin MM, Lusis AJ, Fong LG, Katz M, Lee R, Young SG, Reue K, Smale ST, Tontonoz P. IL-10 Signaling Remodels Adipose Chromatin Architecture to Limit Thermogenesis and Energy Expenditure, Cell. 2018;172(1-2):218.
-
Abstract View: 112 times
PDF Download: 34 times
Download Statistics
Downloads
Download data is not yet available.
