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01, 2024;25 (1): e12921.

IST1 regulates select recycling pathways.

Amy K Clippinger, Teresa V Naismith, Wonjin Yoo, Silvia Jansen, David J Kast, Phyllis I Hanson
Author Information
  1. Amy K Clippinger: Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, Missouri, USA. ORCID
  2. Teresa V Naismith: Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, Missouri, USA.
  3. Wonjin Yoo: Department of Biological Chemistry, University of Michigan Medical School, Ann Arbor, Michigan, USA.
  4. Silvia Jansen: Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, Missouri, USA.
  5. David J Kast: Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, Missouri, USA.
  6. Phyllis I Hanson: Department of Cell Biology and Physiology, Washington University in St. Louis, St. Louis, Missouri, USA.
PMID: 37926552 DOI: 10.1111/tra.12921

Abstract

ESCRTs (Endosomal Sorting Complex Required for Transports) are a modular set of protein complexes with membrane remodeling activities that include the formation and release of intraluminal vesicles (ILVs) to generate multivesicular endosomes. While most of the 12 ESCRT-III proteins are known to play roles in ILV formation, IST1 has been associated with a wider range of endosomal remodeling events. Here, we extend previous studies of IST1 function in endosomal trafficking and confirm that IST1, along with its binding partner CHMP1B, contributes to scission of early endosomal carriers. Functionally, depleting IST1 impaired delivery of transferrin receptor from early/sorting endosomes to the endocytic recycling compartment and instead increased its rapid recycling to the plasma membrane via peripheral endosomes enriched in the clathrin adaptor AP-1. IST1 is also important for export of mannose 6-phosphate receptor from early/sorting endosomes. Examination of IST1 binding partners on endosomes revealed that IST1 interacts with the MIT domain-containing sorting nexin SNX15, a protein previously reported to regulate endosomal recycling. Our kinetic and spatial analyses establish that SNX15 and IST1 occupy a clathrin-containing subdomain on the endosomal perimeter distinct from those previously implicated in cargo retrieval or degradation. Using live-cell microscopy, we see that SNX15 and CHMP1B alternately recruit IST1 to this subdomain or the base of endosomal tubules. These findings indicate that IST1 contributes to a subset of recycling pathways from the early/sorting endosome.

Keywords

AP-1 clathrin endosomal sorting complex required for transport sorting nexin transferrin receptor

References

  1. Nat Struct Mol Biol. 2020 Apr;27(4):392-399 [PMID: 32251413]
  2. J Biol Chem. 2001 Feb 16;276(7):5074-84 [PMID: 11085978]
  3. J Cell Biol. 2005 Aug 29;170(5):769-79 [PMID: 16129785]
  4. Nat Methods. 2008 Jun;5(6):545-51 [PMID: 18454154]
  5. Methods Mol Biol. 2010;619:403-10 [PMID: 20419424]
  6. Dev Cell. 2009 Nov;17(5):712-23 [PMID: 19922875]
  7. Curr Biol. 2014 Jun 2;24(11):1187-98 [PMID: 24835460]
  8. Nat Cell Biol. 2007 Dec;9(12):1370-80 [PMID: 17994011]
  9. Nat Rev Mol Cell Biol. 2020 Jan;21(1):25-42 [PMID: 31705132]
  10. J Cell Biol. 2018 Jul 2;217(7):2549-2564 [PMID: 29891722]
  11. Proc Natl Acad Sci U S A. 2012 Apr 3;109(14):5311-5 [PMID: 22431626]
  12. Cell. 2014 Nov 20;159(5):1027-1041 [PMID: 25416943]
  13. Elife. 2022 Sep 15;11: [PMID: 36107470]
  14. J Cell Sci. 2016 Jul 1;129(13):2625-37 [PMID: 27206861]
  15. Nat Genet. 1999 Nov;23(3):296-303 [PMID: 10610178]
  16. FEBS J. 2014 Aug;281(16):3642-55 [PMID: 24953135]
  17. J Cell Biol. 2014 Apr 14;205(1):33-49 [PMID: 24711499]
  18. Traffic. 2008 Dec;9(12):2253-64 [PMID: 18817526]
  19. Dev Cell. 2002 Aug;3(2):271-82 [PMID: 12194857]
  20. J Cell Biol. 2017 Oct 2;216(10):3275-3290 [PMID: 28768685]
  21. Nat Rev Mol Cell Biol. 2009 Sep;10(9):597-608 [PMID: 19696797]
  22. Nat Rev Neurosci. 2011 Jan;12(1):31-42 [PMID: 21139634]
  23. Nature. 2012 May 23;485(7399):465-70 [PMID: 22622570]
  24. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9559-64 [PMID: 8790369]
  25. Mol Biol Cell. 2009 Mar;20(5):1374-87 [PMID: 19129480]
  26. J Cell Sci. 2015 Aug 1;128(15):2854-65 [PMID: 26092934]
  27. J Cell Biol. 2015 Oct 12;211(1):123-44 [PMID: 26459602]
  28. J Cell Biol. 1996 Jan;132(1-2):21-33 [PMID: 8567724]
  29. Traffic. 2013 Jan;14(1):97-106 [PMID: 22998223]
  30. Nat Protoc. 2014 Mar;9(3):586-96 [PMID: 24525752]
  31. PLoS Biol. 2011 Mar;9(3):e1000604 [PMID: 21445324]
  32. Mol Biol Cell. 2004 May;15(5):2410-22 [PMID: 15020713]
  33. Am J Hum Genet. 2020 Dec 3;107(6):1129-1148 [PMID: 33186545]
  34. Biophys J. 2008 Jan 1;94(1):230-40 [PMID: 17872962]
  35. Science. 2018 Apr 6;360(6384): [PMID: 29622626]
  36. PLoS One. 2014 Feb 28;9(2):e90384 [PMID: 24587345]
  37. Mol Biol Cell. 2009 Mar;20(5):1360-73 [PMID: 19129479]
  38. J Cell Sci. 2020 Jan 22;133(2): [PMID: 31843759]
  39. J Cell Biol. 2017 May 1;216(5):1337-1355 [PMID: 28389476]
  40. Dev Cell. 2008 Oct;15(4):578-89 [PMID: 18854142]
  41. J Cell Biol. 2013 Aug 5;202(3):527-43 [PMID: 23897888]
  42. Science. 2015 Dec 18;350(6267):1548-51 [PMID: 26634441]
  43. Nat Commun. 2017 Nov 13;8(1):1439 [PMID: 29129923]
  44. J Cell Sci. 2013 Nov 1;126(Pt 21):4885-99 [PMID: 23986476]
  45. Traffic. 2009 Dec;10(12):1868-80 [PMID: 19874558]
  46. J Cell Sci. 2015 Feb 15;128(4):755-67 [PMID: 25588841]
  47. Mol Biol Cell. 2009 Aug;20(15):3514-24 [PMID: 19477918]
  48. Mol Neurobiol. 2016 Aug;53(6):3690-3701 [PMID: 26115702]
  49. Nat Struct Mol Biol. 2008 Dec;15(12):1278-86 [PMID: 18997780]
  50. J Cell Biol. 2004 Apr;165(1):123-33 [PMID: 15078903]
  51. Mol Biol Cell. 2008 Feb;19(2):465-74 [PMID: 18032582]
  52. PLoS One. 2012;7(6):e39774 [PMID: 22737254]
  53. Cell. 2009 Jan 9;136(1):97-109 [PMID: 19135892]
  54. Curr Biol. 2012 Sep 25;22(18):1711-6 [PMID: 22902756]
  55. J Biol Chem. 2015 Dec 11;290(50):30053-65 [PMID: 26515066]
  56. Cell. 1992 Apr 3;69(1):129-38 [PMID: 1555237]
  57. Nat Commun. 2014 May 23;5:3891 [PMID: 24852344]
  58. J Cell Biol. 2019 Aug 5;218(8):2583-2599 [PMID: 31227594]
  59. J Cell Biol. 2021 Aug 2;220(8): [PMID: 34047770]
  60. EMBO J. 2001 Sep 3;20(17):5008-21 [PMID: 11532964]
  61. Cell Mol Life Sci. 2020 Jul;77(13):2641-2658 [PMID: 31587092]
  62. Nat Rev Mol Cell Biol. 2004 Feb;5(2):121-32 [PMID: 15040445]
  63. J Cell Biol. 1992 Jun;117(6):1171-9 [PMID: 1607381]
  64. J Cell Sci. 2007 Jun 15;120(Pt 12):2022-31 [PMID: 17550971]
  65. Dev Cell. 2004 Apr;6(4):525-38 [PMID: 15068792]
  66. Nat Genet. 2002 Aug;31(4):347-8 [PMID: 12134148]
  67. Plant Physiol. 2016 May;171(1):251-64 [PMID: 26983994]
  68. Nat Commun. 2018 Jul 26;9(1):2932 [PMID: 30050131]
  69. Cell. 2020 Sep 3;182(5):1140-1155.e18 [PMID: 32814015]
  70. Mol Biol Cell. 2010 Mar 15;21(6):1023-32 [PMID: 20089837]
  71. J Cell Biol. 2010 May 31;189(5):777-82 [PMID: 20513764]
  72. Mol Biol Cell. 2005 May;16(5):2554-65 [PMID: 15758025]
  73. Proc Natl Acad Sci U S A. 2022 Jul 19;119(29):e2204536119 [PMID: 35858336]
  74. Mol Biol Cell. 2008 Feb;19(2):475-84 [PMID: 18032584]
  75. Nat Struct Mol Biol. 2009 Jul;16(7):754-62 [PMID: 19525971]
  76. Proc Natl Acad Sci U S A. 2017 Jan 17;114(3):E307-E316 [PMID: 28053230]
  77. Mol Biol Cell. 2010 Oct 1;21(19):3293-303 [PMID: 20719964]
  78. Nat Rev Mol Cell Biol. 2018 Nov;19(11):679-696 [PMID: 30194414]
  79. J Cell Biol. 2022 Nov 7;221(11): [PMID: 36125415]
  80. Front Neurosci. 2019 Nov 08;13:1179 [PMID: 31787869]
  81. Nat Methods. 2008 Jul;5(7):605-7 [PMID: 18536722]
  82. Cold Spring Harb Protoc. 2011 May 01;2011(5):pdb.prot5623 [PMID: 21536757]
  83. Cell. 1998 Dec 11;95(6):847-58 [PMID: 9865702]
  84. Nat Cell Biol. 2017 Jul;19(7):787-798 [PMID: 28604678]
  85. FEBS Lett. 1994 Aug 1;349(2):173-80 [PMID: 7519568]
  86. J Cell Physiol. 1990 Jul;144(1):52-61 [PMID: 2365746]
  87. Cell Host Microbe. 2011 Mar 17;9(3):235-242 [PMID: 21396898]
  88. J Cell Biol. 2004 Apr;165(1):111-22 [PMID: 15078902]
  89. Nat Cell Biol. 2015 May;17(5):639-50 [PMID: 25799061]
  90. Cell Metab. 2013 Mar 5;17(3):343-52 [PMID: 23416069]

Grants

  1. R01GM122434/NIH HHS
  2. R01GM136925/NIH HHS
  3. R01 GM076686/NIGMS NIH HHS
  4. R01GM138448/NIH HHS
  5. R01 GM136925/NIGMS NIH HHS
  6. S10 OD021629/NIH HHS
  7. R01 GM138448/NIGMS NIH HHS
  8. R01 GM122434/NIGMS NIH HHS

MeSH Term

Endosomal Sorting Complexes Required for Transport
Protein Transport
Endosomes
Multivesicular Bodies
Biological Transport

Chemicals

Endosomal Sorting Complexes Required for Transport
Journal Article
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Word Cloud

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