Peptide P A comprise the MARK3 T-loop peptide phosphorylated at Thr211 and Ser215, and Peptides P B comprise the MARK3 T-loop peptide phosphorylated at Thr211. In combination with MALDI TOF–TOF mass spectrometry, this enabled the identification of the sites phosphorylated in each peptide. ( B) Peptide P A and P B were subjected to solid-phase sequencing and 32P-radioactivity was measured after each cycle of Edman degradation. Fractions containing the 32P-labelled T-loop tryptic peptide (peptides P A and P B) are shown. The 32P-labelled MARK3 proteins were digested with trypsin and the resulting 32P-labelled peptides were chromatographed on a C 18 column. ( A) Catalytically inactive MARK3 (KI), which cannot autophosphorylate, and the indicated mutants were incubated with the LKB1 complex for 30 min with Mg 2+-ATP and separated by electrophoresis on a polyacrylamide gel, which was then autoradiographed. All proteins migrated with the expected mobility, taking into account the epitope tags.Īnalysis of phosphorylation and activation of MARK kinases. Samples from each incubation were also analysed by Western blotting and probed using the indicated antibodies (from top to bottom): anti-GST to detect LKB1 anti-FLAG to detect STRADα and STRADβ and anti- myc to detect MO25α and MO25β. of assays carried out in triplicate and representative of two independent experiments. The results are expressed as specific activity employing the AMARA peptide as substrate. The complexes were tested for their ability to activate the catalytic domain of AMPKα1 or the indicated AMPK-related kinases. The indicated combinations of GST-tagged wild-type LKB1 (WT, lanes 1–9), or catalytically inactive (KI, D194A, lanes 10–13) LKB1, or GST alone (lane 14), FLAG-tagged STRADα or STRADβ, and myc-tagged MO25α or MO25β were coexpressed in HEK-293T cells and purified on glutathione–sepharose. Ø represents a large hydrophobic residue X, any amino acid s, n, g and a preferences for Ser, Asn, Gly and Ala, respectively.Įfficient activation of AMPK-related kinases by LKB1 requires STRAD and MO25 subunits. The suggested consensus sequence for optimal LKB1 phosphorylation is indicated. The error bars are only shown when larger than the size of the open squares. At the indicated times, the activity of the AMPK-related kinases was assayed with the AMARA peptide, and the results are expressed as specific activity. ( B) The indicated AMPK-related kinases were incubated with wild-type LKB1:STRAD:MO25 (open squares) or catalytically inactive LKB1:STRAD:MO25 (open circles) complexes in the presence of Mg 2+ and ATP. The T-loop Thr and Ser are indicated with an asterisk. The identical residues are shaded black and the conserved residues in grey. ( A) Dendrogram and T-loop sequences of AMPK subfamily of protein kinases (Manning et al, 2002). Between them, these kinases may mediate the physiological effects of LKB1, including its tumour suppressor function.Īctivation of AMPK-related kinases by LKB1. Our results show that LKB1 functions as a master upstream protein kinase, regulating AMPK-related kinases as well as AMPK. Neither LKB1 activity nor that of AMPK-related kinases was stimulated by phenformin or AICAR, which activate AMPK. Activities of endogenous NUAK2, QIK, QSK, SIK, MARK1, MARK2/3 and MARK4 were markedly reduced in LKB1-deficient cells. Mutation of the T-loop Thr phosphorylated by LKB1 to Ala prevented activation, while mutation to glutamate produced active forms of many of the AMPK-related kinases. LKB1 catalytic activity and the presence of MO25 and STRAD are required for activation. Here we demonstrate that LKB1 can phosphorylate the T-loop of all the members of this subfamily, apart from MELK, increasing their activity >50-fold. A total of 12 human kinases (NUAK1, NUAK2, BRSK1, BRSK2, QIK, QSK, SIK, MARK1, MARK2, MARK3, MARK4 and MELK) are related to AMPK. We recently demonstrated that the LKB1 tumour suppressor kinase, in complex with the pseudokinase STRAD and the scaffolding protein MO25, phosphorylates and activates AMP-activated protein kinase (AMPK).
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