Autophagy induced during apoptosis degrades mitochondria and inhibits type I interferon secretion

Journal article


Lindqvist, Lisa M., Frank, Daniel, McArthur, Kate, Dite, Toby A., Lazarou, Michael, Oakhill, Jon, Kile, Benjamin T. and Vaux, David L.. (2018). Autophagy induced during apoptosis degrades mitochondria and inhibits type I interferon secretion. Cell Death and Differentiation. 25(4), pp. 782 - 794. https://doi.org/10.1038/s41418-017-0017-z
AuthorsLindqvist, Lisa M., Frank, Daniel, McArthur, Kate, Dite, Toby A., Lazarou, Michael, Oakhill, Jon, Kile, Benjamin T. and Vaux, David L.
Abstract

Cells undergoing Bax/Bak-mediated apoptosis exhibit signs of autophagy, but how it is activated and its significance is unknown. By directly activating Bax/Bak with BH3-only proteins or BH3 mimetic compounds, we demonstrate that mitochondrial damage correlated with a rapid increase in intracellular [AMP]/[ATP], phosphorylation of 5′ AMP-activated protein kinase (AMPK), and activation of unc-51 like autophagy activating kinase 1 (ULK1). Consequently, autophagic flux was triggered early in the apoptotic pathway, as activation of the apoptosome and caspases were not necessary for its induction. Bax/Bak-triggered autophagy resulted in the clearance of damaged mitochondria in an ATG5/7-dependent manner that did not require Parkin. Importantly, Bax/Bak-mediated autophagy inhibited the secretion of the pro-inflammatory cytokine interferon-β (IFN-β) produced in response to mitochondrial damage, but not another cytokine interleukin-6 (IL-6). These findings show that Bax/Bak stimulated autophagy is essential for ensuring immunological silence during apoptosis.

Year2018
JournalCell Death and Differentiation
Journal citation25 (4), pp. 782 - 794
PublisherNature Publishing Group
ISSN1350-9047
Digital Object Identifier (DOI)https://doi.org/10.1038/s41418-017-0017-z
Scopus EID2-s2.0-85037705823
Page range782 - 794
Research GroupMary MacKillop Institute for Health Research
Publisher's version
File Access Level
Controlled
Place of publicationUnited Kingdom
EditorsG. Melino
Permalink -

https://acuresearchbank.acu.edu.au/item/89wq8/autophagy-induced-during-apoptosis-degrades-mitochondria-and-inhibits-type-i-interferon-secretion

Restricted files

Publisher's version

  • 83
    total views
  • 0
    total downloads
  • 1
    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

AMPK protects endothelial cells against HSV-1 replication via inhibition of mTORC1 and ACC1
Doshi, Heena, Spengler, Katrin, Godbole, Amod, Gee, Yi Sing, Baell, Jonathan B., Oakhill, Jonathan, Henke, Andreas and Heller, Regine. (2023). AMPK protects endothelial cells against HSV-1 replication via inhibition of mTORC1 and ACC1. Microbiology Spectrum. 11(5), pp. 1-22. https://doi.org/10.1128/spectrum.00417-23
SGC-CAMKK2-1 : A chemical probe for CAMKK2
Wells, Carrow, Liang, Yi, Pulliam, Thomas L., Lin, Chenchu, Awad, Dominik, Eduful, Benjamin, O’Byrne, Sean, Hossain, Mohammad Anwar, Catta-Preta, Carolina Moura Costa, Ramos, Priscila Zonzini, Gileadi, Opher, Gileadi, Carina, Couñago, Rafael M., Stork, Brittany, Langendorf, Christopher G., Nay, Kevin, Oakhill, Jonathan S., Mukherjee, Debarati, Racioppi, Luigi, ... Drewry, David H.. (2023). SGC-CAMKK2-1 : A chemical probe for CAMKK2. Cells. 12(2), p. Article 287. https://doi.org/10.3390/cells12020287
Elevated basal AMP-activated protein kinase activity sensitizes colorectal cancer cells to growth inhibition by metformin
Morrison, Kaitlin R., Wang, Tingting, Chan, Kuan Yoow, Trotter, Eleanor W., Gillespie, Ari, Michael, Michael Z., Oakhill, Jonathan S., Hagan, Iain M. and Petersen, Janni. (2023). Elevated basal AMP-activated protein kinase activity sensitizes colorectal cancer cells to growth inhibition by metformin. Open Biology. 13(4), p. Article 230021. https://doi.org/10.1098/rsob.230021
Neuropeptide Y1 receptor antagonism protects β-cells and improves glycemic control in type 2 diabetes
Yang, Chieh-Hsin, Ann-Onda, Danise, Lin, Xushu, Fynch, Stacey, Nadarajah, Shaktypreya, Pappas, Evan G., Liu, Xin, Scott, John W., Oakhill, Jonathan S., Galic, Sandra, Shi, Yanchuan, Moreno-Asso, Alba, Smith, Cassandra, Loudovaris, Thomas, Levinger, Itamar, Eizirik, Decio L., Laybutt, D. Ross, Herzog, Herbert, Thomas, Helen E. and Loh, Kim. (2022). Neuropeptide Y1 receptor antagonism protects β-cells and improves glycemic control in type 2 diabetes. Molecular Metabolism. 55(1), p. Article 101413. https://doi.org/10.1016/j.molmet.2021.101413
An AMPKa2-specific phospho-switch controls lysosomal targeting for activation
Morrison, Kaitlin R., Smiles, William J., Ling, Naomi X. Y., Hoque, Ashfaqul, Shea, Gabrielle, Ngoei, Kevin R. W., Yu, Dingyi, Murray-Segal, Lisa, Scott, John W., Galic, Sandra, Kemp, Bruce E., Petersen, Janni and Oakhill, Jonathan S.. (2022). An AMPKa2-specific phospho-switch controls lysosomal targeting for activation. Cell Reports. 38(7), p. Article 110365. https://doi.org/10.1016/j.celrep.2022.110365
Personalized phosphoproteomics identifies functional signaling
Needham, Elise J., Hingst, Janne R., Parker, Benjamin L., Morrison, Kaitlin R., Yang, Guang, Onslev, Johan, Kristensen, Jonas M., Højlund, Kurt, Ling, Naomi, Oakhill, Jonathan X. Y., Richter, Erik A., Kiens, Bente, Petersen, Janni, Pehmøller, Christian, James, David E., Wojtaszewski, Jørgen F. P. and Humphrey, Sean J.. (2022). Personalized phosphoproteomics identifies functional signaling. Nature Biotechnology. 40(4), pp. 576-584. https://doi.org/10.1038/s41587-021-01099-9
A novel small molecule inhibitor of human Drp1
Rosdah, Ayeshah A., Abbott, Belinda M., Langendorf, Christopher G., Deng, Yali, Truong, Jia Q., Waddell, Helen M. M., Ling, Naomi X. Y., Smiles, William J., Delbridge, Lea M. D., Liu, Guei-Sheung, Oakhill, Jonathan S., Lim, Shiang Y. and Holien, Jessica K.. (2022). A novel small molecule inhibitor of human Drp1. Scientific Reports. 12(1), p. Article 21531. https://doi.org/10.1038/s41598-022-25464-z
Blocking AMPK β1 myristoylation enhances AMPK activity and protects mice from high-fat diet-induced obesity and hepatic steatosis
Neopane, Katyayanee, Kozlov, Natalie, Negoita, Florentina, Murray-Segal, Lisa, Brink, Robert, Hoque, Ashfaqul, Ovens, Ashley J., Tjin, Gavin, McAloon, Luke M., Yu, Dingyi, Ling, Naomi X. Y., Sanders, Matthew J., Oakhill, Jonathan S., Scott, John W., Steinberg, Gregory R., Loh, Kim, Kemp, Bruce E., Sakamoto, Kei and Galic, Sandra. (2022). Blocking AMPK β1 myristoylation enhances AMPK activity and protects mice from high-fat diet-induced obesity and hepatic steatosis. Cell Reports. 41(12), pp. 1-16. https://doi.org/10.1016/j.celrep.2022.111862
Structure-function analysis of the AMPK activator SC4 and identification of a potent pan AMPK activator
Ovens, Ashley J., Gee, Yi Sing, Ling, Naomi X. Y., Yu, Dingyi, Hardee, Justin P., Chung, Jin D., Ngoei, Kevin R. W., Waters, Nicholas J., Hoffman, Nolan J., Scott, John W., Loh, Kim, Spengler, Katrin, Heller, Regine, Parker, Michael W., Lynch, Gordon S., Huang, Fei, Galic, Sandra, Kemp, Bruce E., Baell, Jonathan B., ... Langendorf, Christopher G.. (2022). Structure-function analysis of the AMPK activator SC4 and identification of a potent pan AMPK activator. Biochemical Journal. 479(11), pp. 1181-1204. https://doi.org/10.1042/BCJ20220067
Systemic ablation of Camkk2 impairs metastatic colonization and improves insulin sensitivity in TRAMP mice : Evidence for cancer cell-extrinsic CAMKK2 functions in prostate cancer
Pulliam, Thomas L., Awad, Dominik, Han, Jenny J., Murray, Mollianne M., Ackroyd, Jeffrey J., Goli, Pavithr, Oakhill, Jonathan S., Scott, John W., Ittmann, Michael M. and Frigo, Daniel E.. (2022). Systemic ablation of Camkk2 impairs metastatic colonization and improves insulin sensitivity in TRAMP mice : Evidence for cancer cell-extrinsic CAMKK2 functions in prostate cancer. Cells. 11(12), p. Article 1890. https://doi.org/10.3390/cells11121890
Genetic impairment of succinate metabolism disrupts bioenergetic sensing in adrenal neuroendocrine cancer
Gupta, Priyanka, Strange, Keehn, Telange, Rahul, Guo, Ailan, Hatch, Heather, Sobh, Amin, Elie, Jonathan, Carter, Angela M., Totenhagen, John, Tan, Chunfeng, Sonawane, Yogesh A., Neuzil, Jiri, Natarajan, Amarnath, Ovens, Ashley J., Oakhill, Jonathan S., Wiederhold, Thorsten, Pacak, Karel, Ghayee, Hans K., Meijer, Laurent, ... Bibb, James A.. (2022). Genetic impairment of succinate metabolism disrupts bioenergetic sensing in adrenal neuroendocrine cancer. Cell Reports. 40(7), p. Article 111218. https://doi.org/10.1016/j.celrep.2022.111218
Phosphoproteomics of three exercise modalities identifies canonical signaling and C180RF25 as an AMPK substrate regulating skeletal muscle function
Blazev, Ronnie, Carl, Christian S., Ng, Yaan-Kit, Molendijk, Jeffrey, Voldstedlund, Christian T., Zhao, Yuanyuan, Xiao, Di, Kueh, Andrew J., Miotto, Paula M., Haynes, Vanessa R., Hardee, Justin P., Chung, Jin D., MacNamara, James W., Qian, Hongwei, Gregorevic, Paul, Oakhill, Jonathan S., Herold, Marco J., Jensen, Thomas E., Lisowski, Leszek, ... Parker, Benjamin L.. (2022). Phosphoproteomics of three exercise modalities identifies canonical signaling and C180RF25 as an AMPK substrate regulating skeletal muscle function. Cell Metabolism. 34, pp. 1561-1577.e9. https://doi.org/10.1016/j.cmet.2022.07.003
Regulation of pancreatic β-cell function by the NPY system
Yang, Chieh-Hsin, Onda, Danise-Ann, Oakhill, Jonathan S., Scott, John W., Galic, Sandra and Loh, Kim. (2021). Regulation of pancreatic β-cell function by the NPY system. Endocrinology. 162(8), pp. 1-8. https://doi.org/10.1210/endocr/bqab070
Post-translational modifications of the energy guardian AMP-activated protein kinase
Ovens, Ashley J., Scott, John W., Langendorf, Christopher G., Kemp, Bruce E., Oakhill, Jonathan S. and Smiles, William J.. (2021). Post-translational modifications of the energy guardian AMP-activated protein kinase. International Journal of Molecular Sciences. 22(3), p. Article 1229. https://doi.org/10.3390/ijms22031229
Molecular mechanisms underlying the beneficial effects of exercise on brain function and neurological disorders
Nay, Kévin, Smiles, William J., Kaiser, Jacqueline, McAloon, Luke M., Loh, Kim, Galic, Sandra, Oakhill, Jonathan S., Gundlach, Andrew L. and Scott, John W.. (2021). Molecular mechanisms underlying the beneficial effects of exercise on brain function and neurological disorders. International Journal of Molecular Sciences. 22, p. Article 4052. https://doi.org/10.3390/ijms22084052
Hinge binder scaffold hopping identifies potent calcium/calmodulin-dependent protein kinase kinase 2 (CAMKK2) inhibitor chemotypes
Eduful, Benjamin J., O'Byrne, Sean N., Temme, Louisa, Asquith, Christopher R. M., Liang, Yi, Picado, Alfredo, Pilotte, Joseph R., Hossain, Mohammad Anwar, Wells, Carrow I., Zuercher, William J., Catta-Preta, Carolina M.C, Ramos, Priscila, de S. Santiago, André, Counago, Rafael M., Langendorf, Christopher G., Nay, Kevin, Oakhill, Jonathan S., Pulliam, Thomas L., Lin, Chenchu, ... Drewry, David H.. (2021). Hinge binder scaffold hopping identifies potent calcium/calmodulin-dependent protein kinase kinase 2 (CAMKK2) inhibitor chemotypes. Journal of Medicinal Chemistry. 64(15), pp. 10849-10877. https://doi.org/10.1021/acs.jmedchem.0c02274
Compound- and fiber type-selective requirement of AMPKγ3 for insulin-independent glucose uptake in skeletal muscle
Rhein, Philipp, Desjardins, Eric M., Rong, Ping, Ahwazi, Danial, Bonhoure, Nicolas, Stolte, Jens, Santos, Matthieu D., Ovens, Ashley J., Ehrlich, Amy M., Sanchez Garcia, José L., Ouyang, Qian, Yabut, Julian M., Kjolby, Mads, Membrez, Mathieu, Jessen, Niels, Oakhill, Jonathan S., Treebak, Jonas T., Maire, Pascal, Scott, John W., ... Sakamoto, Kei. (2021). Compound- and fiber type-selective requirement of AMPKγ3 for insulin-independent glucose uptake in skeletal muscle. Molecular Metabolism. 51, p. Article: 101228. https://doi.org/10.1016/j.molmet.2021.101228
New perspectives on the role of Drp1 isoforms in regulating mitochondrial pathophysiology
Rosdah, Ayeshah A., Smiles, William J., Oakhill, Jonathan S., Scott, John W., Langendorf, Christopher G., Delbridge, Lea M. D., Holien, Jessica K. and Lim, Shiang Y.. (2020). New perspectives on the role of Drp1 isoforms in regulating mitochondrial pathophysiology. Pharmacology and Therapeutics. 213, p. Article 107594. https://doi.org/10.1016/j.pharmthera.2020.107594
Functional analysis of an R311C variant of Ca2+-calmodulin-dependent protein kinase kinase-2 (CaMKK2) found as a de novo mutation in a patient with bipolar disorder
Xy Ling, Naomi, Langendorf, Christopher G., Hoque, Ashfaqul, Galic, Sandra, Loh, Kim, Kemp, Bruce E., Gundlach, Andrew L., Oakhill, Jonathan S. and Scott, John W.. (2020). Functional analysis of an R311C variant of Ca2+-calmodulin-dependent protein kinase kinase-2 (CaMKK2) found as a de novo mutation in a patient with bipolar disorder. Bipolar Disorders. 22(8), pp. 841-848. https://doi.org/10.1111/bdi.12901
CaMKK2 is inactivated by cAMP-PKA signaling and 14-3-3 adaptor proteins
Langendorf, Christopher G., O'Brien, Matthew T., Ngoei, Kevin R. W., McAloon, Luke M., Dhagat, Urmi, Hoque, Ashfaqul, Ling, Naomi X. Y., Dite, Toby A., Galic, Sandra, Loh, Kim, Parker, Michael W., Oakhill, Jonathan S., Kemp, Bruce E. and Scott, John W.. (2020). CaMKK2 is inactivated by cAMP-PKA signaling and 14-3-3 adaptor proteins. Journal of Biological Chemistry. 295(48), pp. 16239-16250. https://doi.org/10.1074/jbc.RA120.013756
DNA-dependent protein kinase regulates lysosomal AMP-dependent protein kinase activation and autophagy
Puustinen, Pietri, Keldsbo, Anne, Corcelle-Termeau, Elisabeth, Ngoei, Kevin, Sønder, Stine L., Farkas, Thomas, Kaae Andersen, Klaus, Oakhill, Jon S. and Jäättelä, Marja. (2020). DNA-dependent protein kinase regulates lysosomal AMP-dependent protein kinase activation and autophagy. Autophagy. 16(10), pp. 1871-1888. https://doi.org/10.1080/15548627.2019.1710430
The myokine meteorin-like (metrnl) improves glucose tolerance in both skeletal muscle cells and mice by targeting AMPKa2
Lee, Jung Ok, Byun, Won Seok, Kang, Min Ju, Han, Jeong Ah, Moon, Jiyoung, Shin, Min-Jeong, Lee, Ho Jun, Chung, Ji Hyung, Lee, Jin-Seok, Son, Chang-Gue, Song, Kwon-Ho, Kim, Tae Woo, Lee, Eun-Soo, Kim, Hong Min, Chung, Choon Hee, Ngoei, Kevin R. W., Ling, Naomi X. Y., Oakhill, Jonathan S., Galic, Sandra, ... Kim, Hyeon Soo. (2020). The myokine meteorin-like (metrnl) improves glucose tolerance in both skeletal muscle cells and mice by targeting AMPKa2. The FEBS Journal. 287(10), pp. 2087-2104. https://doi.org/10.1111/FEBS.15301
The eEF2 kinase-induced STAT3 inactivation inhibits lung cancer cell proliferation by phosphorylation of PKM2
Xiao, Min, Xie, Jianling, Wu, Yu, Wang, Genzhu, Qi, Xin, Liu, Zailiang, Wang, Yuying, Wang, Xuemin, Hoque, Ashfaqul, Oakhill, Jon, Proud, Christopher G. and Li, Jing. (2020). The eEF2 kinase-induced STAT3 inactivation inhibits lung cancer cell proliferation by phosphorylation of PKM2. Cell Communication and Signaling. 18(1), p. 25.
mTORC1 directly inhibits AMPK to promote cell proliferation under nutrient stress
Ling, Naomi X. Y., Kaczmarek, Adrian, Hoque, Ashfaqul, Davie, Elizabeth, Ngoei, Kevin R. W., Morrison, Kaitlin R., Smiles, William J., Forte, Gabriella M., Wang, Tingting, Lie, Shervi, Dite, Toby A., Langendorf, Christopher G., Scott, John W., Oakhill, Jonathan S. and Petersen, Janni. (2020). mTORC1 directly inhibits AMPK to promote cell proliferation under nutrient stress. Nature Metabolism. 2, pp. 41-49. https://doi.org/10.1038/s42255-019-0157-1
In depth analysis of kinase cross screening data to identify CaMKK2 inhibitory scaffolds
O’Byrne, Sean N., Scott, John W., Pilotte, Joseph R., Santiago, André da S., Langendorf, Christopher G., Oakhill, Jonathan S., Eduful, Benjamin J., Couñago, Rafael M., Wells, Carrow I., Zuercher, William J., Willson, Timothy M. and Drewry, David H.. (2020). In depth analysis of kinase cross screening data to identify CaMKK2 inhibitory scaffolds. Molecules. 25(2), pp. 1-19. https://doi.org/10.3390/molecules25020325
Genetic loss of AMPK-glycogen binding destabilizes AMPK and disrupts metabolism
Hoffman, Nolan J., Whitfield, Jamie, Janzen, Natalie R., Belhaj, Mehdi R., Galic, Sandra, Murray-Segal, Lisa, Smiles, William J., Ling, Naomi X. Y., Dite, Toby A., Scott, John W., Oakhill, Jonathan S., Brink, Robert, Kemp, Bruce E. and Hawley, John A.. (2020). Genetic loss of AMPK-glycogen binding destabilizes AMPK and disrupts metabolism. Molecular Metabolism. 41, pp. 1-13. https://doi.org/10.1016/j.molmet.2020.101048
Long-chain fatty acyl-CoA esters regulate metabolism via allosteric control of AMPK β1 isoforms
Pinkosky, Stephen L., Scott, John W., Desjardins, Eric M., Smith, Brennan K., Day, Emily A., Ford, Rebecca J., Langendorf, Christopher G., Ling, Naomi X. Y., Nero, Tracy L., Loh, Kim, Galic, Sandra, Hoque, Ashfaqul, Smiles, William J., Ngoei, Kevin R. W., Parker, Michael W., Yan, Yan, Melcher, Karsten, Kemp, Bruce E., Oakhill, Jonathan S. and Steinberg, Gregory R.. (2020). Long-chain fatty acyl-CoA esters regulate metabolism via allosteric control of AMPK β1 isoforms. Nature Metabolism. 2(9), pp. 873-881. https://doi.org/10.1038/s42255-020-0245-2
Transient expression of AMPK heterotrimer complexes in mammalian cells
Jon Oakhill, John Scott and Toby A. Dite. (2018). Transient expression of AMPK heterotrimer complexes in mammalian cells. In AMPK pp. 159-169 Humana Press, Inc.. https://doi.org/10.1007/978-1-4939-7598-3_10
Cyclin-dependent kinase-mediated phosphorylation of breast cancer metastasis suppressor 1 (BRMS1) affects cell migration
Roesley, Siti Nur Ain, Suryadinata, Randy, Morrish, Emma, Tan, Anthonius Ricardo, Issa, Samah M. A., Oakhill, Jon, Bernard, Ora, Welch, Danny R. and Sarcevic, Boris. (2016). Cyclin-dependent kinase-mediated phosphorylation of breast cancer metastasis suppressor 1 (BRMS1) affects cell migration. Cell Cycle. 15(1), pp. 137 - 151. https://doi.org/10.1080/15384101.2015.1121328
Metformin and salicylate synergistically activate liver AMPK, inhibit lipogenesis and improve insulin sensitivity
Ford, Rebecca, Fullerton, Morgan, Pinkosky, Stephen, Day, Emily, Scott, John, Oakhill, Jonathan, Bujak, Adam, Smith, Brennan, Crane, Justin, Blumer, Regje, Marcinko, Katarina, Kemp, Bruce, Gerstein, Hertzel and Steinberg, Gregory. (2015). Metformin and salicylate synergistically activate liver AMPK, inhibit lipogenesis and improve insulin sensitivity. Biochemical Journal. 468(1), pp. 125 - 132. https://doi.org/10.1042/BJ20150125
Inhibition of AMP-activated protein kinase at the allosteric drug-binding site promotes islet insulin release
Scott, John, Galic, Sandra, Graham, Kate, Foitzik, Richard, Ling, Naomi, Dite, Toby, Issa, Samah, Langendorf, Chris, Weng, Qing, Thomas, Helen, Kay, Thomas, Birnberg, Neal, Steinberg, Gregory, Kemp, Bruce and Oakhill, Jonathan. (2015). Inhibition of AMP-activated protein kinase at the allosteric drug-binding site promotes islet insulin release. Chemistry and Biology. 22(6), pp. 705 - 711. https://doi.org/10.1016/j.chembiol.2015.05.011
Autophosphorylation of CaMKK2 generates autonomous activity that is disrupted by a T85S mutation linked to anxiety and bipolar disorder
Scott, John, Park, Elizabeth, Rodriguiz, Ramona, Oakhill, Jonathan, Issa, Samah, O'Brien, Matthew, Dite, Toby, Langendorf, Christopher, Wetsel, William, Means, Anthony and Kemp, Bruce. (2015). Autophosphorylation of CaMKK2 generates autonomous activity that is disrupted by a T85S mutation linked to anxiety and bipolar disorder. Scientific Reports. 5, pp. 1 - 10. https://doi.org/10.1038/srep14436
ATP sensitive bi-quinoline activator of the AMP-activated protein kinase
Scott, John, Oakhill, Jonathan, Ling, Naomi, Langendorf, Christopher, Foitzik, Richard, Kemp, Bruce and Issinger, Olaf-Georg. (2014). ATP sensitive bi-quinoline activator of the AMP-activated protein kinase. Biochemical and Biophysical Research Communications. 443(2), pp. 435 - 440. https://doi.org/10.1016/j.bbrc.2013.11.130
Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling
Scott, John, Ling, Naomi, Issa, Samah, Dite, Toby, O'Brien, Matthew, Chen, Zhi-Ping, Galic, Sandra, Langendorf, Christopher, Steinberg, Gregory, Kemp, Bruce and Oakhill, Jonathan. (2014). Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling. Chemistry and Biology. 21(5), pp. 619 - 627. https://doi.org/10.1016/j.chembiol.2014.03.006
Ca 2+/calmodulin-dependent protein kinase kinase beta is regulated by multisite phosphorylation
Green, Michelle, Scott, John, Steel, Rohan, Oakhill, Jonathan, Kemp, Bruce and Means, Anthony. (2011). Ca 2+/calmodulin-dependent protein kinase kinase beta is regulated by multisite phosphorylation. Journal of Biological Chemistry. 286(32), pp. 28066 - 28079. https://doi.org/10.1074/jbc.M111.251504