Grb10 deletion enhances muscle cell proliferation, differentiation and GLUT4 plasma membrane translocation

Journal article


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
AuthorsMokbel, Nancy, Hoffman, Nolan John, Girgis, Christian M., Small, Lewin, Turner, Nigel, Daly, Roger J., Cooney, Gregory J. and Holt, Lowenna J.
Abstract

Grb10 is an intracellular adaptor protein which binds directly to several growth factor receptors, including those for insulin and insulin-like growth factor receptor-1 (IGF-1), and negatively regulates their actions. Grb10-ablated (Grb10-/-) mice exhibit improved whole body glucose homeostasis and an increase in muscle mass associated specifically with an increase in myofiber number. This suggests that Grb10 may act as a negative regulator of myogenesis. In this study, we investigated in vitro, the molecular mechanisms underlying the increase in muscle mass and the improved glucose metabolism. Primary muscle cells isolated from Grb10-/- mice exhibited increased rates of proliferation and differentiation compared to primary cells isolated from wild-type mice. The improved proliferation capacity was associated with an enhanced phosphorylation of Akt and ERK in the basal state and changes in the expression of key cell cycle progression markers involved in regulating transition of cells from the G1 to S phase (e.g., retinoblastoma (Rb) and p21). The absence of Grb10 also promoted a faster transition to a myogenin positive, differentiated state. Glucose uptake was higher in Grb10-/- primary myotubes in the basal state and was associated with enhanced insulin signaling and an increase in GLUT4 translocation to the plasma membrane. These data demonstrate an important role for Grb10 as a link between muscle growth and metabolism with therapeutic implications for diseases, such as muscle wasting and type 2 diabetes.

Year2014
JournalJournal of Cellular Physiology
Journal citation229 (11), pp. 1753 - 1764
PublisherJohn Wiley & Sons Inc.
ISSN0021-9541
Digital Object Identifier (DOI)https://doi.org/10.1002/jcp.24628
Scopus EID2-s2.0-84904878276
Page range1753 - 1764
Research GroupMary MacKillop Institute for Health Research
Place of publicationUnited States
Permalink -

https://acuresearchbank.acu.edu.au/item/8q536/grb10-deletion-enhances-muscle-cell-proliferation-differentiation-and-glut4-plasma-membrane-translocation

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 and sucrose result 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. 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
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
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