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Autophagy Volume 18, 2022 - Issue 2
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Research Paper

Autophagy induction during stem cell activation plays a key role in salivary gland self-renewal

Idil Orhona Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsView further author information
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Cecilia Rocchia Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;b Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsView further author information
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Beatriz Villarejo-Zoric Department of Cellular and Molecular Biology, Centro De Investigaciones Biológicas Margarita Salas, CSIC, Madrid, SpainView further author information
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Paola Serrano Martineza Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;b Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsView further author information
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Mirjam Baanstraa Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;b Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsView further author information
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Uilke Brouwera Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;b Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsView further author information
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Patricia Boyac Department of Cellular and Molecular Biology, Centro De Investigaciones Biológicas Margarita Salas, CSIC, Madrid, SpainCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-3045-951XView further author information
ORCID Icon,
Rob Coppesa Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;b Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-5503-1064View further author information
ORCID Icon &
Fulvio Reggioria Department of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-2652-2686View further author information
ORCID Icon show all
Pages 293-308 | Received 31 Jan 2020, Accepted 27 Apr 2021, Published online: 19 May 2021

References

  • Clevers H, Cells STEM. What is an adult stem cell? Science. 2015;350:1319–1320.
  • Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008;132:598–611.
  • Zhou W, Choi M, Margineantu D, et al. HIF1alpha induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J. 2012;31:2103–2116.
  • Kubli DA, Sussman MA. Eat, breathe, ROS: controlling stem cell fate through metabolism. Expert Rev Cardiovasc Ther. 2017;15:345–356.
  • Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nat Cell Biol. 2013;15:713–720.
  • Rodolfo C, Di Bartolomeo S, Cecconi F. Autophagy in stem and progenitor cells. Cell Mol Life Sci. 2016;73:475–496.
  • Kuma A, Komatsu M, Mizushima N. Autophagy-monitoring and autophagy-deficient mice. Autophagy. 2017;13:1619–1628.
  • Boya P, Codogno P, Rodriguez-Muela N. Autophagy in stem cells: repair, remodelling and metabolic reprogramming. Development. 2018;145:dev146506.
  • Garcia-Prat L, Martinez-Vicente M, Perdiguero E, et al. Autophagy maintains stemness by preventing senescence. Nature. 2016;529:37–42.
  • Leeman DS, Hebestreit K, Ruetz T, et al. Lysosome activation clears aggregates and enhances quiescent neural stem cell activation during aging. Science. 2018;359:1277–1283.
  • Liu P, Liu K, Gu H, et al. High autophagic flux guards ESC identity through coordinating autophagy machinery gene program by FOXO1. Cell Death Differ. 2017;24:1672–1680.
  • Ho TT, Warr MR, Adelman ER, et al. Autophagy maintains the metabolism and function of young and old stem cells. Nature. 2017;543:205–210.
  • Salemi S, Yousefi S, Constantinescu MA, et al. Autophagy is required for self-renewal and differentiation of adult human stem cells. Cell Res. 2012;22:432–435.
  • Donnelly H, Salmeron-Sanchez M, Dalby MJ. Designing stem cell niches for differentiation and self-renewal. J R Soc Interface. 2018;15:20180388.
  • Yin X, Mead BE, Safaee H, et al. Engineering stem cell organoids. Cell Stem Cell. 2016;18:25–38.
  • Murrow LM, Weber RJ, Gartner ZJ. Dissecting the stem cell niche with organoid models: an engineering-based approach. Development. 2017;144:998–1007.
  • Clevers H, Watt FM. Defining adult stem cells by function, not by phenotype. Annu Rev Biochem. 2018;87:1015–1027.
  • Weng PL, Aure MH, Maruyama T, et al. Limited regeneration of adult salivary glands after severe injury involves cellular plasticity. Cell Rep. 2018;24:1464–1470.
  • Luitje ME, Israel AK, Cummings MA, et al. Long-term maintenance of acinar cells in human submandibular glands after radiation therapy. Int J Radiat Oncol Biol Phys. 2021;109:1028–1039.
  • Aure MH, Konieczny SF, Ovitt CE. Salivary gland homeostasis is maintained through acinar cell self-duplication. Dev Cell. 2015;33:231–237.
  • Vissink A, Mitchell JB, Baum BJ, et al. Clinical management of salivary gland hypofunction and xerostomia in head-and-neck cancer patients: successes and barriers. Int J Radiat Oncol Biol Phys. 2010;78:983–991.
  • Lombaert I, Movahednia MM, Adine C, et al. Concise review: salivary gland regeneration: therapeutic approaches from stem cells to tissue organoids. Stem Cells. 2017;35:97–105.
  • Pringle S, Van Os R, Coppes RP. Concise review: adult salivary gland stem cells and a potential therapy for xerostomia. Stem Cells. 2013;31:613–619.
  • Jensen SB, Vissink A, Limesand KH, et al. Salivary gland hypofunction and xerostomia in head and neck radiation patients. J Natl Cancer Inst Monogr. 2019;2019:lgz016.
  • Pringle S, Maimets M, Van Der Zwaag M, et al. Human salivary gland stem cells functionally restore radiation damaged salivary glands. Stem Cells. 2016;34:640–652.
  • Nanduri LS, Maimets M, Pringle SA, et al. Regeneration of irradiated salivary glands with stem cell marker expressing cells. Radiother Oncol. 2011;99:367–372.
  • Maimets M, Rocchi C, Bron R, et al. Long-term in vitro expansion of salivary gland stem cells driven by wnt signals. Stem Cell Reports. 2016;6:150–162.
  • Feng J, Van Der Zwaag M, Stokman MA, et al. Isolation and characterization of human salivary gland cells for stem cell transplantation to reduce radiation-induced hyposalivation. Radiother Oncol. 2009;92:466–471.
  • Pringle S, Nanduri LS, Van Der Zwaag M, et al. Isolation of mouse salivary gland stem cells. J Vis Exp. 2011;8:2484.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
  • Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol. 2010;22:124–131.
  • Emmerson E, Knox SM. Salivary gland stem cells: a review of development, regeneration and cancer. Genesis. 2018;56:e23211.
  • Shoji-Kawata S, Sumpter R, Leveno M, et al. Identification of a candidate therapeutic autophagy-inducing peptide. Nature. 2013;494:201–206.
  • May AJ, Cruz-Pacheco N, Emmerson E, et al. Diverse progenitor cells preserve salivary gland ductal architecture after radiation-induced damage. Development. 2018;145:dev166363.
  • Kulkarni RS, Bajaj MS, Kale VP. Induction and detection of autophagy in aged hematopoietic stem cells by exposing them to microvesicles secreted by HSC-supportive mesenchymal stromal cells. Methods Mol Biol. 2019;1854:21–34.
  • Kulkarni A, Dong A, Kulkarni VV, et al. Differential regulation of autophagy during metabolic stress in astrocytes and neurons. Autophagy. 2019;16:1651–1667.
  • Kohli L, Passegue E. Surviving change: the metabolic journey of hematopoietic stem cells. Trends Cell Biol. 2014;24:479–487.
  • Nguyen-mccarty M, Klein PS. Autophagy is a signature of a signaling network that maintains hematopoietic stem cells. PLoS One. 2017;12:e0177054.
  • Jung HE, Shim YR, Oh JE, et al. The autophagy protein Atg5 plays a crucial role in the maintenance and reconstitution ability of hematopoietic stem cells. Immune Netw. 2019;19:e12.
  • Regmi S, Raut PK, Pathak S, et al. Enhanced viability and function of mesenchymal stromal cell spheroids is mediated via autophagy induction. Autophagy. 2020;7. in press.
  • Pennings S, Liu KJ, Qian H. The stem cell niche: interactions between stem cells and their environment. Stem Cells Int. 2018;2018:4879379.
  • Esteban-Martinez L, Boya P. BNIP3L/NIX-dependent mitophagy regulates cell differentiation via metabolic reprogramming. Autophagy. 2018;14:915–917.
  • Esteban-Martinez L, Sierra-Filardi E, McGreal RS, et al. Programmed mitophagy is essential for the glycolytic switch during cell differentiation. EMBO J. 2017;36:1688–1706.
  • Gopinath SD, Webb AE, Brunet A, et al. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Reports. 2014;2:414–426.
  • Cai WF, Wang L, Liu GS, et al. Manipulating the Hippo-Yap signal cascade in stem cells for heart regeneration. Ann Palliat Med. 2016;5:125–134.
  • Moya IM, Halder G. Hippo-YAP/TAZ signalling in organ regeneration and regenerative medicine. Nat Rev Mol Cell Biol. 2019;20:211–226.
  • Totaro A, Zhuang Q, Panciera T, et al. Cell phenotypic plasticity requires autophagic flux driven by YAP/TAZ mechanotransduction. Proc Natl Acad Sci U S A. 2019;116:17848–17857.
  • Wu X, Fleming A, Ricketts T, et al. Autophagy regulates Notch degradation and modulates stem cell development and neurogenesis. Nat Commun. 2016;7:10533.
  • Wang S, Xia P, Ye B, et al. Transient activation of autophagy via Sox2-mediated suppression of mTOR is an important early step in reprogramming to pluripotency. Cell Stem Cell. 2013;13:617–625.
  • Von Bultzingslowen I, Sollecito TP, Fox PC, et al. Salivary dysfunction associated with systemic diseases: systematic review and clinical management recommendations. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007 Mar;103(Suppl):S57 e1–15.
  • Morgan-Bathke M, Lin HH, Chibly AM, et al. Deletion of ATG5 shows a role of autophagy in salivary homeostatic control. J Dent Res. 2013;92:911–917.
  • Morgan-Bathke M, Hill GA, Harris ZI, et al. Autophagy correlates with maintenance of salivary gland function following radiation. Sci Rep. 2014;4:5206.
  • Van Luijk P, Pringle S, Deasy JO, et al. Sparing the region of the salivary gland containing stem cells preserves saliva production after radiotherapy for head and neck cancer. Sci Transl Med. 2015;7:305ra147.
  • Thellung S, Corsaro A, Nizzari M, et al. Autophagy activator drugs: a new opportunity in neuroprotection from misfolded protein toxicity. Int J Mol Sci. 2019 Feb 19;20:901.
  • Towers CG, Thorburn A. Therapeutic targeting of autophagy. EBioMedicine. 2016;14:15–23.
  • Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004;432:1032–1036.

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