Poster Presentation 12th International Meeting on AMPK 2023

Exploring the impact of AMPK signaling on the plasticity and differentiation of intestinal stem cells (#70)

Brittany Ellis Jewell 1 , Debbie Ross 1 , Dannielle Engle 2 , Daniel E. Frigo 3 4 5 6 , Reuben J. Shaw 1
  1. Molecular and Cell Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California, United States
  2. Regulatory Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California, USA
  3. Department of Genitourinary Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas, USA
  4. Center for Nuclear Receptors and Cell Signaling, University of Houston, Houston, Texas, USA
  5. Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA
  6. Department of Cancer Systems Imaging, MD Anderson Cancer Center, Houston, Texas, USA

Intestinal stem cell plasticity and differentiation are known to impact nutrient absorption, water reabsorption, and overall digestive health, however the molecular metabolic signaling that contributes to these processes is poorly understood1. Under nutrient limited conditions, the key metabolic regulator AMPK is activated and inhibits the mechanistic target of mTORC1 pathway, preventing cell growth2.  While mTOR has been studied as a nutrient-sensitive regulator of epithelial differentiation of ISCs3, AMPK’s role in nutrient-sensitive control of cell growth or stem cell fate is unknown. We sought to define the role(s) of AMPK in intestinal stem cell maintenance and differentiation, first employing a model of AMPK a1/a2 conditional knockout in Lgr5+ intestinal stem cells (ISCs) and, separately, in transit amplifying cells using Lrig1-creER. Studies demonstrate that AMPK mediates effects on transcriptional rewiring of metabolism under nutrient- and energy-deprived cells. When and where AMPK is endogenously activated in various intestinal cell populations remains to be defined and is under examination. To unbiasedly define the role of AMPK in intestinal stem cell populations, we will combine single-cell RNA sequencing with Lgr5-creER and Lrig1-creER dependent AMPK knockout to define those genes reliant on intact AMPK signaling, and to specifically examine transcriptional targets that contribute to ISC niche maintenance. Complementary experiments will utilize small and large intestinal organoids. Together, results from these experiments begin to establish the roles of AMPK in the small intestine and colon, defining its impact on growth, metabolism, and stem cell function.

  1. Wang D, Odle J, Liu Y. Metabolic Regulation of Intestinal Stem Cell Homeostasis. Trends Cell Biol. 2021 May;31(5):325-327. doi: 10.1016/j.tcb.2021.02.001. Epub 2021 Feb 26. PMID: 33648839.
  2. Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol. 2018;19(2):121-35. Epub 2017/10/05. doi: 10.1038/nrm.2017.95. PubMed PMID: 28974774; PMCID: PMC5780224.
  3. Yilmaz, Ö., Katajisto, P., Lamming, D. et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486, 490–495 (2012). https://doi.org/10.1038/nature11163
  4. Malik N, Ferreira BI, Hollstein PE, Curtis SD, Trefts E, Weiser Novak S, Yu J, Gilson R, Hellberg K, Fang L, Sheridan A, Hah N, Shadel GS, Manor U, Shaw RJ. Induction of lysosomal and mitochondrial biogenesis by AMPK phosphorylation of FNIP1. Science. 2023 Apr 21;380(6642):eabj5559. doi: 10.1126/science.abj5559. Epub 2023 Apr 21. PMID: 37079666.
  5. Joung J, Ma S, Tay T, Geiger-Schuller KR, Kirchgatterer PC, Verdine VK, Guo B, Arias-Garcia MA, Allen WE, Singh A, Kuksenko O, Abudayyeh OO, Gootenberg JS, Fu Z, Macrae RK, Buenrostro JD, Regev A, Zhang F. A transcription factor atlas of directed differentiation. Cell. 2023 Jan 5;186(1):209-229.e26. doi: 10.1016/j.cell.2022.11.026. PMID: 36608654.