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Autoinhibition of ankyrin-B/G membrane target bindings by intrinsically disordered segments from the tail regions.

Chen K, Li J, Wang C, Wei Z, Zhang M
Elife 6 (2017)
Related entries: 5y4e, 5y4f

Cited: 20 times
EuropePMC logo PMID: 28841137

Abstract

Ankyrins together with their spectrin partners are the master organizers of micron-scale membrane domains in diverse tissues. The 24 ankyrin (ANK) repeats of ankyrins bind to numerous membrane proteins, linking them to spectrin-based cytoskeletons at specific membrane microdomains. The accessibility of the target binding groove of ANK repeats must be regulated to achieve spatially defined functions of ankyrins/target complexes in different tissues, though little is known in this regard. Here we systemically investigated the autoinhibition mechanism of ankyrin-B/G by combined biochemical, biophysical and structural biology approaches. We discovered that the entire ANK repeats are inhibited by combinatorial and quasi-independent bindings of multiple disordered segments located in the ankyrin-B/G linkers and tails, suggesting a mechanistic basis for differential regulations of membrane target bindings by ankyrins. In addition to elucidating the autoinhibition mechanisms of ankyrins, our study may also shed light on regulations on target bindings by other long repeat-containing proteins.

Reviews - 5y4d mentioned but not cited (1)

  1. Diversity and function of arthropod endosymbiont toxins. Massey JH, Newton ILG. Trends Microbiol 30 185-198 (2022)

Articles - 5y4d mentioned but not cited (2)

  1. Usp9X Controls Ankyrin-Repeat Domain Protein Homeostasis during Dendritic Spine Development. Yoon S, Parnell E, Kasherman M, Forrest MP, Myczek K, Premarathne S, Sanchez Vega MC, Piper M, Burne THJ, Jolly LA, Wood SA, Penzes P. Neuron 105 506-521.e7 (2020)
  2. Autoinhibition of ankyrin-B/G membrane target bindings by intrinsically disordered segments from the tail regions. Chen K, Li J, Wang C, Wei Z, Zhang M. Elife 6 e29150 (2017)


Reviews citing this publication (3)

  1. Ankyrins: Roles in synaptic biology and pathology. Smith KR, Penzes P. Mol Cell Neurosci 91 131-139 (2018)
  2. The Mechanosensory Transduction Machinery in Inner Ear Hair Cells. Zheng W, Holt JR. Annu Rev Biophys 50 31-51 (2021)
  3. Cargo hold and delivery: Ankyrins, spectrins, and their functional patterning of neurons. Lorenzo DN. Cytoskeleton (Hoboken) 77 129-148 (2020)

Articles citing this publication (14)

  1. ANK2 autism mutation targeting giant ankyrin-B promotes axon branching and ectopic connectivity. Yang R, Walder-Christensen KK, Kim N, Wu D, Lorenzo DN, Badea A, Jiang YH, Yin HH, Wetsel WC, Bennett V. Proc Natl Acad Sci U S A 116 15262-15271 (2019)
  2. Mapping axon initial segment structure and function by multiplexed proximity biotinylation. Hamdan H, Lim BC, Torii T, Joshi A, Konning M, Smith C, Palmer DJ, Ng P, Leterrier C, Oses-Prieto JA, Burlingame AL, Rasband MN. Nat Commun 11 100 (2020)
  3. Neurodevelopmental mutation of giant ankyrin-G disrupts a core mechanism for axon initial segment assembly. Yang R, Walder-Christensen KK, Lalani S, Yan H, García-Prieto ID, Álvarez S, Fernández-Jaén A, Speltz L, Jiang YH, Bennett V. Proc Natl Acad Sci U S A 116 19717-19726 (2019)
  4. Architecture of the human erythrocyte ankyrin-1 complex. Vallese F, Kim K, Yen LY, Johnston JD, Noble AJ, Calì T, Clarke OB. Nat Struct Mol Biol 29 706-718 (2022)
  5. Mechanistic insights into the interactions of dynein regulator Ndel1 with neuronal ankyrins and implications in polarity maintenance. Ye J, Li J, Ye F, Zhang Y, Zhang M, Wang C. Proc Natl Acad Sci U S A 117 1207-1215 (2020)
  6. Giant ankyrin-B mediates transduction of axon guidance and collateral branch pruning factor sema 3A. Creighton BA, Afriyie S, Ajit D, Casingal CR, Voos KM, Reger J, Burch AM, Dyne E, Bay J, Huang JK, Anton ES, Fu MM, Lorenzo DN. Elife 10 e69815 (2021)
  7. Phosphorylation, Dephosphorylation, and Multiprotein Assemblies Regulate Dynamic Behavior of Neuronal Cytoskeleton: A Mini-Review. Kurochkina N, Bhaskar M, Yadav SP, Pant HC. Front Mol Neurosci 11 373 (2018)
  8. Giant ankyrin-B suppresses stochastic collateral axon branching through direct interaction with microtubules. Chen K, Yang R, Li Y, Zhou JC, Zhang M. J Cell Biol 219 e201910053 (2020)
  9. An unfolding role for ankyrin-G at the axon initial segment. Salzer JL. Proc Natl Acad Sci U S A 116 19228-19230 (2019)
  10. Crystal structure of Ankyrin-G in complex with a fragment of Neurofascin reveals binding mechanisms required for integrity of the axon initial segment. He L, Jiang W, Li J, Wang C. J Biol Chem 298 102272 (2022)
  11. A Rare Variant of ANK3 Is Associated With Intracranial Aneurysm. Liu J, Liao X, Zhou J, Li B, Xu L, Liu S, Li Y, Yuan D, Hu C, Jiang W, Yan J. Front Neurol 12 672570 (2021)
  12. Ankyrin B promotes developmental spine regulation in the mouse prefrontal cortex. Murphy KE, Duncan B, Sperringer JE, Zhang E, Haberman V, Wyatt EV, Maness P. Cereb Cortex 33 10634-10648 (2023)
  13. Connecting sequence features within the disordered C-terminal linker of Bacillus subtilis FtsZ to functions and bacterial cell division. Shinn MK, Cohan MC, Bullock JL, Ruff KM, Levin PA, Pappu RV. Proc Natl Acad Sci U S A 119 e2211178119 (2022)
  14. Dynamic interactions between E-cadherin and Ankyrin-G mediate epithelial cell polarity maintenance. Kong C, Qu X, Liu M, Xu W, Chen D, Zhang Y, Zhang S, Zhu F, Liu Z, Li J, Huang C, Wang C. Nat Commun 14 6860 (2023)


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