Keywords

CaMKK, CaMKKα/1, CaMKKβ/2, CaMKI, CaMKIV, AMPK, PKA, calcium signaling, autophosphorylation, 14-3-3 proteins, kinase cascade, N-terminal regulatory domain


Reference

DOI: 10.3390/ijms231911025


Abstract Summary

  • CaMKK activates downstream kinases (CaMKI, CaMKIV, AMPK, Akt/PKB) via activation-loop phosphorylation in response to Ca²⁺/CaM binding.
  • CaMKK pathways regulate neuronal plasticity, transcription, autophagy, metabolism, and are implicated in diseases like cancer, metabolic syndrome, and mental disorders.
  • Review summarizes structural, functional, physiological aspects of CaMKK and pharmacological inhibitors.

1. Structural and Functional Overview of CaMKK Isoforms

IsoformKey Properties
CaMKKα/1Regulated by Ca²⁺/CaM and PKA phosphorylation (Thr108, Ser458), inhibited upon 14-3-3 binding (Ser74).
CaMKKβ/2Constitutively active (60-70%) via N-terminal regulatory domain (129–151). AutoP at Thr482 enhances activity. Phosphorylated by CDK5, GSK3, AMPK, PKA, modulating activity.

2. Ca²⁺/CaM-Dependent & Independent Mechanisms

  • CaMKKβ/2 N-terminal regulatory domain enables Ca²⁺/CaM-independent activity.
  • Ca²⁺/CaM binding displaces autoinhibitory segment, fully activating kinase.
  • Autophosphorylation (e.g., Thr482, Thr85) promotes autonomous activity but still modulated by external kinases (PKA, AMPK).

3. Regulatory Phosphorylation and Inhibitory Mechanisms

ModificationEffect on CaMKK Activity
PKA-mediated Thr108, Ser458 (α/1)↓ catalytic activity, ↓ CaM binding.
PKA-mediated Ser74 (α/1)Recruits 14-3-3, stabilizes inactive form.
PKA-mediated Ser495 (β/2)Impairs Ca²⁺/CaM activation, maintains autonomous activity.
PKA-mediated Ser100, Ser511 (β/2)14-3-3 recruitment prevents Ser495 dephosphorylation.
CDK5/GSK3: Ser-129, Ser-133, Ser-137 (β/2)↓ autonomous activity, maintain Ca²⁺/CaM dependence.
AMPK-mediated Thr144 (β/2)Converts to Ca²⁺/CaM-dependent form.
Autophosphorylation Thr482 (β/2)Partially disrupts autoinhibition, ↑ autonomous activity.
Autophosphorylation Thr85 (human β/2)Autonomous activity; linked to anxiety, bipolar disorder.

4. Functional and Biological Implications

  • Neuronal plasticity & morphogenesis: CaMKK-CaMKI/IV pathways.
  • Metabolic regulation: CaMKK-AMPK axis.
  • Pathophysiological roles: Cancer, neurodevelopmental disorders, stress responses.
  • Heat acclimation in C. elegans: CKK-1 phosphorylates CMK-1, regulates nuclear translocation and thermal avoidance behavior.

5. Structural Insights and Peptide Interactions

  • Fig 1B model: CaM anchors Trp444 and Phe459 of CaMKK peptide via hydrophobic pockets (N-/C-terminal), opposite orientation compared to CaMKII/MLCK.
  • CaMKKβ/2 dimerization/oligomerization potential via Arg311Cys mutant.
  • RP domain (Arg/Pro-rich segment): substrate-specific recognition and interaction site.
  • Ile441 critical for autoinhibition.

6. Substrate Preference and Structural Specificity

  • Tertiary structure preference: CaMKK phosphorylates full-length CaMKI/IV but not efficiently on linear peptides (e.g., KKKK-EHQVLMKTVCGTPGY).
  • Km for kinases (~1 μM) significantly lower than peptides, indicating conformation-specific phosphorylation.

Structural integrity of substrates crucial for effective phosphorylation.


7. Pharmacological Inhibition and Therapeutic Potential

  • Selective inhibitors of CaMKK under development for regulating AMPK pathway, neurological diseases, and cancer.
  • Importance of isoform-specific targeting due to distinct regulatory and autonomous activities.

8. Interesting Notes and Inspiration

  • Ca²⁺-induced nuclear translocation of CaMKK/CaMKIV may fine-tune transcriptional regulation.
  • Thermal stability of substrates critical: 5 min @ 60°C abolishes CaMKK-mediated phosphorylation, highlighting the need for native substrate conformation.
  • Peptide-based assays need caution—full-length proteins are more relevant for in vivo-like activity studies.
  • Insightful mention: “The amazing nature of regulatory complexity and fine-tuning of CaMKK activity.

RD’s Reflections

  • Impressively layered regulation of CaMKK — integrating Ca²⁺, phosphorylation, and scaffolding.
  • Constitutive vs inducible activation: evolutionary adaptation for different cellular roles (e.g., metabolic vs neural plasticity).
  • Extensive regulatory phospho-sites emphasize the precise tuning of CaMKK activity in response to multiple pathways.
  • Potential model for thinking about multi-modal kinase regulation in other signaling hubs.