Invited Speaker 11th International Symposium on Autophagy 2025

BECLIN1 as a gatekeeper of intestinal resilience (129866)

Erinna F Lee 1 2 3 , Juliani Juliani 1 2 3 , Sharon Tran 1 , Tiffany J Harris 1 , Aysha H Al-Ani 4 , Peter de Cruz 5 , Alpha S Yap 6 , John M Mariadason 1 , Britt Christensen 7 , Andre L Samson 4 , James M Murphy 4 , Doug Fairlie 1 2 3
  1. Olivia Newton-John Cancer Research Institute, Heidelberg, VIC, Australia
  2. La Trobe Institute for Molecular Science, La Trobe University, Australia
  3. La Trobe University, Heidelberg, VIC, Australia
  4. Walter and Eliza Hall Institute, Parkville, VIC, Australia
  5. Austin Health, Melbourne
  6. Institute for Molecular Bioscience, Brisbane
  7. Royal Melbourne Hospital, Parkville

BECLIN1 is a central component of Class III phosphatidylinositol 3-kinase complexes, coordinating autophagy initiation and endocytic trafficking to maintain intestinal epithelial integrity. Complete, intestinal-specific BECLIN1 deletion in adult mice caused rapid, fatal enteritis with extensive epithelial apoptosis, impaired autophagy, organelle stress, and loss of barrier function. These effects were not recapitulated by ATG7 deletion, revealing autophagy-independent functions for BECLIN1. Mechanistically, BECLIN1 deficiency led to E-CADHERIN mislocalisation linked to abnormal endocytic trafficking, providing a pathway by which barrier integrity is disrupted.

To model more clinically relevant states, we generated mice with inducible monoallelic Becn1 deletion. Partial BECLIN1 loss did not cause overt disease under homeostasis but produced subtle epithelial changes, including shortened small intestines, reduced crypt length, altered cell architecture, impaired goblet cell maturation, and reduced mucin content. These alterations were associated with cytoskeletal reorganisation, redistribution of E-CADHERIN, and modest changes in early endosome dynamics without overt autophagy defects. When challenged with dextran sulphate sodium, mice heterozygous for BECLIN1 developed more severe colitis, greater epithelial injury, and depletion of protective neutral mucins.

Together, these findings reveal that both complete and partial BECLIN1 loss compromise mucosal homeostasis through distinct mechanisms, positioning BECLIN1 as a pivotal determinant of gut barrier resilience and inflammatory disease susceptibility.

 

  1. Juliani J, Tran S, Harris TJ, De Cruz P, Ellis SL, Gleeson PA, Mariadason JM, Duszyc K, Yap AS, Lee EF, Fairlie WD. BECLIN-1 is essential for the maintenance of gastrointestinal epithelial integrity by regulating endocytic trafficking, F-actin organization, and lysosomal function. Autophagy Rep. 2025 Apr 3;4(1):2484494. doi: 10.1080/27694127.2025.2484494. PMID: 40395982; PMCID: PMC11980461.
  2. Tran S, Juliani J, Harris TJ, Evangelista M, Ratcliffe J, Ellis SL, Baloyan D, Reehorst CM, Nightingale R, Luk IY, Jenkins LJ, Ghilas S, Yakou MH, Inguanti C, Johnson C, Buchert M, Lee JC, De Cruz P, Duszyc K, Gleeson PA, Kile BT, Mielke LA, Yap AS, Mariadason JM, Fairlie WD, Lee EF. BECLIN1 is essential for intestinal homeostasis involving autophagy-independent mechanisms through its function in endocytic trafficking. Commun Biol. 2024 Feb 20;7(1):209. doi: 10.1038/s42003-024-05890-7. PMID: 38378743; PMCID: PMC10879175.