High dietary fat and sucrose result in an extensive and time-dependent deterioration in health of multiple physiological systems in mice

Journal article


Burchfield, James G., Kebede, Melkam A., Meoli, Christopher C., Stockli, Jacqueline, Whitworth, P. T., Wright, Amanda L., Hoffman, Nolan, Minard, Annabel Y., Ma, Xiuquan, Krycer, James R., Nelson, Marin E., Tan, Shi-XIong, Yau, Belinda, Thomas, Kristen C., Wee, Natalie K. P., Khor, Ee-Cheng, Enriquez, Ronaldo F., Vissel, Bryce, Biden, Trevor J., ... Fazakerley, Daniel J.. (2018) High dietary fat and sucrose result in an extensive and time-dependent deterioration in health of multiple physiological systems in mice. Journal of Biological Chemistry. 293(15), pp. 5731 - 5745. https://doi.org/10.1074/jbc.RA117.000808
AuthorsBurchfield, James G., Kebede, Melkam A., Meoli, Christopher C., Stockli, Jacqueline, Whitworth, P. T., Wright, Amanda L., Hoffman, Nolan, Minard, Annabel Y., Ma, Xiuquan, Krycer, James R., Nelson, Marin E., Tan, Shi-XIong, Yau, Belinda, Thomas, Kristen C., Wee, Natalie K. P., Khor, Ee-Cheng, Enriquez, Ronaldo F., Vissel, Bryce, Biden, Trevor J., Baldock, Paul A., Hoehn, Kyle L., Cantley, James, Cooney, Gregory J., James, David E. and Fazakerley, Daniel J.
Abstract

Obesity is associated with metabolic dysfunction, including insulin resistance and hyperinsulinemia, and with disorders such as cardiovascular disease, osteoporosis, and neurodegeneration. Typically, these pathologies are examined in discrete model systems and with limited temporal resolution, and whether these disorders co-occur is therefore unclear. To address this question, here we examined multiple physiological systems in male C57BL/6J mice following prolonged exposure to a high-fat/high-sucrose diet (HFHSD). HFHSD-fed mice rapidly exhibited metabolic alterations, including obesity, hyperleptinemia, physical inactivity, glucose intolerance, peripheral insulin resistance, fasting hyperglycemia, ectopic lipid deposition, and bone deterioration. Prolonged exposure to HFHSD resulted in morbid obesity, ectopic triglyceride deposition in liver and muscle, extensive bone loss, sarcopenia, hyperinsulinemia, and impaired short-term memory. Although many of these defects are typically associated with aging, HFHSD did not alter telomere length in white blood cells, indicating that this diet did not generally promote all aspects of aging. Strikingly, glucose homeostasis was highly dynamic. Glucose intolerance was evident in HFHSD-fed mice after 1 week and was maintained for 24 weeks. Beyond 24 weeks, however, glucose tolerance improved in HFHSD-fed mice, and by 60 weeks, it was indistinguishable from that of chow-fed mice. This improvement coincided with adaptive β-cell hyperplasia and hyperinsulinemia, without changes in insulin sensitivity in muscle or adipose tissue. Assessment of insulin secretion in isolated islets revealed that leptin, which inhibited insulin secretion in the chow-fed mice, potentiated glucose-stimulated insulin secretion in the HFHSD-fed mice after 60 weeks. Overall, the excessive calorie intake was accompanied by deteriorating function of numerous physiological systems.

Keywordsobesity; glucose metabolism; leptin; bone; insulin; secretion; diabetes; beta cell(B-cell); neurodegeneration; Western diet
Year2018
JournalJournal of Biological Chemistry
Journal citation293 (15), pp. 5731 - 5745
PublisherAmerican Society for Biochemistry and Molecular Biology, Inc.
ISSN0021-9258
Digital Object Identifier (DOI)https://doi.org/10.1074/jbc.RA117.000808
Scopus EID2-s2.0-85045401310
Page range5731 - 5745
Research GroupMary MacKillop Institute for Health Research
EditorsL. Gierasch
Permalink -

https://acuresearchbank.acu.edu.au/item/86vvz/high-dietary-fat-and-sucrose-result-in-an-extensive-and-time-dependent-deterioration-in-health-of-multiple-physiological-systems-in-mice

Restricted files

Publisher's version

  • 0
    total views
  • 0
    total downloads
  • 0
    views this month
  • 0
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Phosphoproteomics reveals conserved exercise-stimulated signaling and AMPK regulation of store-operated calcium entry
Nelson, Marin E., Parker, Benjamin L., Burchfield, James G., Hoffman, Nolan J., Needham, Elise J., Cooke, Kristen C., Naim, Timur, Sylow, Lykke, Ling, Naomi X. Y., Francis, Deanne, Norris, Dougall M., Chaudhuri, Rima, Oakhill, Jonathan S., Richter, Erik A., Lynch, Gordon S., Stockli, Jacqueline and James, David E.. (2019) Phosphoproteomics reveals conserved exercise-stimulated signaling and AMPK regulation of store-operated calcium entry. The EMBO Journal. 38(24), pp. 1 - 20. https://doi.org/10.15252/embj.2019102578
High dietary fat and sucrose results in an extensive and time-dependent deterioration in health of multiple physiological systems in mice
Burchfield, James G., Kebede, Melkam A., Meoli, Christopher C., Stockli, Jacqueline, Whitworth, P. Tess, Wright, Amanda L., Hoffman, Nolan John, Minard, Annabel Y., Ma, Xiuquan, Krycer, James R., Nelson, Marin E., Tan, Shi-Xlong, Yau, Belinda, Thomas, Kristen C., Wee, Natalie K.Y., Khor, Ee-Cheng, Enriquez, Ronaldo F., Vissel, Bryce, Biden, Trevor J., ... Fazakerley, Daniel J.. (2018) High dietary fat and sucrose results in an extensive and time-dependent deterioration in health of multiple physiological systems in mice. Journal of Biological Chemistry. 293(15), pp. 5731 - 5745. https://doi.org/10.1074/jbc.RA117.000808
Mitochondrial CoQ deficiency is a common driver of mitochondrial oxidants and insulin resistance
Fazakerley, Daniel J., Chaudhuri, Rima, Yang, Pengyi, Maghzal, Ghassan J., Thomas, Kristen C., Krycer, James R., Humphrey, Sean J., Parker, Benjamin, Fisher-Wellman, Kelsey H., Meoli, Christopher C., Hoffman, Nolan, Diskin, Ciana, Burchfield, James G., Cowley, Mark J., Kaplan, Warren, Modrusan, Zora, Kolumam, Ganesh, Yang, Jean Y. H., Chen, Daniel L., ... James, David E.. (2018) Mitochondrial CoQ deficiency is a common driver of mitochondrial oxidants and insulin resistance. eLife. 7, pp. 1 - 38. https://doi.org/10.7554/eLife.32111
High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans
Leckey, Jill J., Hoffman, Nolan, Parr, Evelyn, Devlin, Brooke, Trewin, Adam J., Stepto, Nigel K., Morton, James P., Burke, Louise and Hawley, John. (2018) High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans. The FASEB Journal. 32(6), pp. 2979 - 2991. https://doi.org/10.1096/fj.201700993R
Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism
Janzen, Natalie, Whitfield, Jamie and Hoffman, Nolan. (2018) Interactive roles for AMPK and glycogen from cellular energy sensing to exercise metabolism. International Journal of Molecular Sciences. 19(11), pp. 1 - 18. https://doi.org/10.3390/ijms19113344
High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans
Leckey, Jill J., Hoffman, Nolan J., Parr, Evelyn B., Devlin, Brooke L., Trewin, Adam J., Stepto, Nigel K., Morton, James P., Burke, Louise M. and Hawley, John A.. (2018) High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans. FASEB Journal. 32(6), pp. 2979 - 2991. https://doi.org/10.1096/fj.201700993R
Metabolomic analysis of insulin resistance across different mouse strains and diets
Stockli, Jacqueline, Fisher-Wellman, Kelsey H., Chaudhuri, Rima, Zeng, Xiao-Yi, Fazakerley, Daniel J., Meoli, Christopher C., Thomas, Kristen C., Hoffman, Nolan, Mangiafico, Salvatore P., Xirouchaki, Chrysovalantou E., Yang, Chieh H., Ilkayeva, Olga, Wong, Kari, Cooney, Gregory J., Andrikopoulos, Sofianos, Muoio, Deborah M. and James, David E.. (2017) Metabolomic analysis of insulin resistance across different mouse strains and diets. Journal of Biological Chemistry. 292(47), pp. 19135 - 19145. https://doi.org/10.1074/jbc.M117.818351
Omics and exercise: global approaches for mapping exercise biological networks
Hoffman, Nolan John. (2017) Omics and exercise: global approaches for mapping exercise biological networks. Cold Spring Harbor Perspectives in Medicine. 7(10), pp. 1 - 17. https://doi.org/10.1101/cshperspect.a029884
Omics and exercise: global approaches for mapping exercise biological networks
Hoffman, Nolan John. (2017) Omics and exercise: global approaches for mapping exercise biological networks. Cold Spring Harbor Perspectives in Medicine. 7(10), pp. 1 - 17. https://doi.org/10.1101/cshperspect.a029884
mTORC2 and AMPK differentially regulate muscle triglyceride content via Perilipin 3
Kleinert, Maximilian, Parker, Benjamin L., Chaudhuri, Rima, Fazakerley, Daniel J., Serup, Annette, Thomas, Kristen C., Krycer, James R., Sylow, Lykke, Fritzen, Andreas M., Hoffman, Nolan John, Jeppesen, Jacob, Schjerling, Peter, Ruegg, Markus A., Kiens, Bente, James, David E. and Richter, Erik A.. (2016) mTORC2 and AMPK differentially regulate muscle triglyceride content via Perilipin 3. Molecular Metabolism. 5(8), pp. 646 - 655. https://doi.org/10.1016/j.molmet.2016.06.007
Glucose-6-phosphate dehydrogenase contributes to the regulation of glucose uptake in skeletal muscle
Lee-Young, Robert S., Hoffman, Nolan John, Murphy, Kate T., Henstridge, Darren C., Samocha-Bonet, Dorit, Siebel, Andrew L., Iliades, Peter, Zivanovic, Borivoj, Hong, Yet H., Colgan, Timothy D., Kraakman, Michael J., Bruce, Clinton R., Gregorevic, Paul, McConell, Glenn K., Lynch, Gordon S., Drummond, Grant R., Kingwell, Bronwyn A., Greenfield, Jerry R. and Febbraio, Mark A.. (2016) Glucose-6-phosphate dehydrogenase contributes to the regulation of glucose uptake in skeletal muscle. Molecular Metabolism. 5(11), pp. 1083 - 1091. https://doi.org/10.1016/j.molmet.2016.09.002
Global phosphoproteomic analysis of human skeletal muscle reveals a network of exercise-regulated kinases and AMPK substrates
Hoffman, Nolan John, Parker, Benjamin L., Chaudhuri, Rima, Fisher-Wellman, Kelsey H., Kleinert, Maximilian, Humphrey, Sean J., Yang, Pengyi, Holliday, Mira, Trefely, Sophie, Fazakerley, Daniel J., Stöckli, Jacqueline, Burchfield, James G., Jensen, Thomas E., Jothi, Raja, Kiens, Bente, Wojtaszewski, Jørgen F. P., Richter, Erik A. and James, David E.. (2015) Global phosphoproteomic analysis of human skeletal muscle reveals a network of exercise-regulated kinases and AMPK substrates. Cell Metabolism. 22(5), pp. 922 - 935. https://doi.org/10.1016/j.cmet.2015.09.001
Dataset from the global phosphoproteomic mapping of early mitotic exit in human cells
Rogers, Samuel, McLoy, Rachel A., Parker, Benjamin L., Chaudhuri, Rima, Gayevskiy, Velimir, Hoffman, Nolan John, Watkins, D. Neil, Daly, Roger J., James, David E. and Burgess, Andrew. (2015) Dataset from the global phosphoproteomic mapping of early mitotic exit in human cells. Data in Brief. 5, pp. 45 - 52. https://doi.org/10.1016/j.dib.2015.08.010
The RabGAP TBC1D1 plays a central role in exercise-regulated glucose metabolism in skeletal muscle
Stockli, Jacqueline, Meoli, Christopher C., Hoffman, Nolan John, Fazakerley, Daniel J., Pant, Himani, Cleasby, Mark E., Ma, Xiuquan, Kleinert, Maximilian, Brandon, Amanda E., Lopez, Jamie A., Cooney, Gregory J. and James, David E.. (2015) The RabGAP TBC1D1 plays a central role in exercise-regulated glucose metabolism in skeletal muscle. Diabetes. 64(6), pp. 1914 - 1922. https://doi.org/10.2337/db13-1489
Global phosphoproteomic mapping of early mitotic exit in human cells identifies novel substrate dephosphorylation motifs
McLoy, Rachael A., Parker, Benjamin L., Rogers, Samuel, Chaudhuri, Rima, Gayevskiy, Velimir, Hoffman, Nolan John, Ali, Naveid, Watkins, D. Neil, Daly, Roger J., James, David E., Lorca, Thierry, Castro, Anna and Burgess, Andrew. (2015) Global phosphoproteomic mapping of early mitotic exit in human cells identifies novel substrate dephosphorylation motifs. Molecular and Cellular Proteomics. 14(8), pp. 2194 - 2212. https://doi.org/10.1074/mcp.M114.046938
PhosphOrtholog: A web-based tool for cross-species mapping of orthologous protein post-translational modifications
Chaudhuri, Rima, Sadrieh, Arash, Hoffman, Nolan J., Parker, Benjamin L., Humphrey, Sean J., Stockli, Jacqueline, Hill, Adam P., James, David E. and Yang, Jean Yee Hwa. (2015) PhosphOrtholog: A web-based tool for cross-species mapping of orthologous protein post-translational modifications. BMC Genomics. 16(617), pp. 1 - 14. https://doi.org/10.1186/s12864-015-1820-x
Structural basis for phosphorylation and lysine acetylation cross-talk in a kinase motif associated with myocardial ischemia and cardioprotection
Parker, Benjamin L., Shepherd, Nicholas E., Trefely, Sophie, Hoffman, Nolan John, White, Melanie Y., Engholm-Keller, Kasper, Hambly, Brett D., Larsen, Martin R., James, David E. and Cordwell, Stuart J.. (2014) Structural basis for phosphorylation and lysine acetylation cross-talk in a kinase motif associated with myocardial ischemia and cardioprotection. Journal of Biological Chemistry. 289(37), pp. 25890 - 25906. https://doi.org/10.1074/jbc.M114.556035
Grb10 deletion enhances muscle cell proliferation, differentiation and GLUT4 plasma membrane translocation
Mokbel, Nancy, Hoffman, Nolan John, Girgis, Christian M., Small, Lewin, Turner, Nigel, Daly, Roger J., Cooney, Gregory J. and Holt, Lowenna J.. (2014) Grb10 deletion enhances muscle cell proliferation, differentiation and GLUT4 plasma membrane translocation. Journal of Cellular Physiology. 229(11), pp. 1753 - 1764. https://doi.org/10.1002/jcp.24628
Structural basis for phosphorylation and lysine acetylation crosstalk in a kinase motif associated with myocardial ischemia and cardioprotection
Parker, Benjamin L., Shepherd, Nicholas E., Trefely, Sophie, Hoffman, Nolan John, White, Melanie Y., Engholm-Keller, Kasper, Hambly, Brett D., Larsen, Martin R., James, David E. and Cordwell, Stuart J.. (2014) Structural basis for phosphorylation and lysine acetylation crosstalk in a kinase motif associated with myocardial ischemia and cardioprotection. Journal of Biological Chemistry. 289(37), pp. 25890 - 25906. https://doi.org/10.1074/jbc.M114.556035
Transient silencing of a type IV P-type ATpase results in decreased GLUT4 translocation and altered signaling of MAPK and PI3K pathways
Hurst, Sarah, Hoffman, Nolan, Elmendorf, Jeffrey and Dhar, Madhu. (2014) Transient silencing of a type IV P-type ATpase results in decreased GLUT4 translocation and altered signaling of MAPK and PI3K pathways. In Obesity Epidemic pp. 1 - 21 CreateSpace Independent Publishing Platform.
Chromium enhances insulin responsiveness via AMPK
Hoffman, Nolan John, Penque, Brent A., Habegger, Kirk M., Sealls, Whitney, Tackett, Lixuan and Elmendorf, Jeffrey S.. (2014) Chromium enhances insulin responsiveness via AMPK. Journal of Nutritional Biochemistry. 25(5), pp. 565 - 572. https://doi.org/10.1016/j.jnutbio.2014.01.007
Ceramide accumulation in L6 skeletal muscle cells due to increased activity of ceramide synthase isoforms has opposing effects on insulin action to those caused by palmitate treatment
Frangioudakis, Georgia, Diakanastasis, Barbara, Liao, Bing-Qing M., Saville, Jennifer T., Hoffman, Nolan John, Mitchell, Todd W. and Schmitz-Peiffer, Carsten. (2013) Ceramide accumulation in L6 skeletal muscle cells due to increased activity of ceramide synthase isoforms has opposing effects on insulin action to those caused by palmitate treatment. Diabetologia. 56(12), pp. 2697 - 2701. https://doi.org/10.1007/s00125-013-3035-5
AMPK enhances insulin-stimulated GLUT4 regulation via lowering membrane cholesterol
Hoffman, Nolan John, Habegger, Kirk M., Ridenour, Colin M., Broznick, Joseph T. and Elmendon, Jeffrey S.. (2012) AMPK enhances insulin-stimulated GLUT4 regulation via lowering membrane cholesterol. Endocrinology. 153(5), pp. 2130 - 2141. https://doi.org/10.1210/en.2011-2099
Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis
Hoffman, Nolan John and Elmendorf, Jeffrey S.. (2011) Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends in Endocrinology and Metabolism. 22(3), pp. 110 - 116. https://doi.org/10.1016/j.tem.2010.12.001