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ER proteins decipher the tubulin code to regulate organelle distribution

Author

Listed:
  • Pengli Zheng

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health)

  • Christopher J. Obara

    (Howard Hughes Medical Institute)

  • Ewa Szczesna

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health)

  • Jonathon Nixon-Abell

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health
    Howard Hughes Medical Institute
    Cambridge Institute for Medical Research)

  • Kishore K. Mahalingan

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health)

  • Antonina Roll-Mecak

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health
    Lung and Blood Institute, National Institutes of Health)

  • Jennifer Lippincott-Schwartz

    (Howard Hughes Medical Institute)

  • Craig Blackstone

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health
    Massachusetts General Hospital
    Massachusetts General Hospital and Harvard Medical School)

Abstract

Organelles move along differentially modified microtubules to establish and maintain their proper distributions and functions1,2. However, how cells interpret these post-translational microtubule modification codes to selectively regulate organelle positioning remains largely unknown. The endoplasmic reticulum (ER) is an interconnected network of diverse morphologies that extends promiscuously throughout the cytoplasm3, forming abundant contacts with other organelles4. Dysregulation of endoplasmic reticulum morphology is tightly linked to neurologic disorders and cancer5,6. Here we demonstrate that three membrane-bound endoplasmic reticulum proteins preferentially interact with different microtubule populations, with CLIMP63 binding centrosome microtubules, kinectin (KTN1) binding perinuclear polyglutamylated microtubules, and p180 binding glutamylated microtubules. Knockout of these proteins or manipulation of microtubule populations and glutamylation status results in marked changes in endoplasmic reticulum positioning, leading to similar redistributions of other organelles. During nutrient starvation, cells modulate CLIMP63 protein levels and p180–microtubule binding to bidirectionally move endoplasmic reticulum and lysosomes for proper autophagic responses.

Suggested Citation

  • Pengli Zheng & Christopher J. Obara & Ewa Szczesna & Jonathon Nixon-Abell & Kishore K. Mahalingan & Antonina Roll-Mecak & Jennifer Lippincott-Schwartz & Craig Blackstone, 2022. "ER proteins decipher the tubulin code to regulate organelle distribution," Nature, Nature, vol. 601(7891), pages 132-138, January.
  • Handle: RePEc:nat:nature:v:601:y:2022:i:7891:d:10.1038_s41586-021-04204-9
    DOI: 10.1038/s41586-021-04204-9
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    Cited by:

    1. Patrick A. Sandoz & Robin A. Denhardt-Eriksson & Laurence Abrami & Luciano A. Abriata & Gard Spreemann & Catherine Maclachlan & Sylvia Ho & Béatrice Kunz & Kathryn Hess & Graham Knott & Francisco S. M, 2023. "Dynamics of CLIMP-63 S-acylation control ER morphology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. William Y. C. Huang & Xianrui Cheng & James E. Ferrell, 2022. "Cytoplasmic organization promotes protein diffusion in Xenopus extracts," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Cátia Silva Janota & Andreia Pinto & Anna Pezzarossa & Pedro Machado & Judite Costa & Pedro Campinho & Cláudio A. Franco & Edgar R. Gomes, 2022. "Shielding of actin by the endoplasmic reticulum impacts nuclear positioning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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