Bidirectional regulation of structural damage on autophagy in the C. elegans epidermis

References

• Fung C, Lock R, Gao S, et al. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell. 2008 Mar;19(3):797–806.
   PubMed Web of Science ®Google Scholar
• Chen N, Debnath J. IκB kinase complex (IKK) triggers detachment-induced autophagy in mammary epithelial cells independently of the PI3K-AKT-MTORC1 pathway. Autophagy. 2013 Aug;9(8):1214–1227.
   PubMed Web of Science ®Google Scholar
• Avivar-Valderas A, Bobrovnikova-Marjon E, Alan Diehl J, et al. Regulation of autophagy during ECM detachment is linked to a selective inhibition of mTORC1 by PERK. Oncogene. 2013 Oct 10 32(41):4932–4940.
   PubMed Web of Science ®Google Scholar
• Yoo BH, Zagryazhskaya A, Li Y, et al. Upregulation of ATG3 contributes to autophagy induced by the detachment of intestinal epithelial cells from the extracellular matrix, but promotes autophagy-independent apoptosis of the attached cells. Autophagy. 2015;11(8):1230–1246.
   PubMed Web of Science ®Google Scholar
• Vlahakis A, Debnath J. The interconnections between autophagy and integrin-Mediated cell adhesion. J Mol Biol. 2017 Feb 17; 429(4):515–530.
   PubMed Web of Science ®Google Scholar
• Kast DJ, Dominguez R. The cytoskeleton-autophagy connection. Curr Biol. 2017 Apr 24; 27(8):R318–r326.
   PubMed Web of Science ®Google Scholar
• Wang RC, Wei Y, An Z, et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science (New York, NY). 2012 Nov 16 338(6109):956–959.
   Google Scholar
• King JS, Veltman DM, Insall RH. The induction of autophagy by mechanical stress. Autophagy. 2011 Dec;7(12):1490–1499.
   PubMed Web of Science ®Google Scholar
• Orhon I, Dupont N, Zaidan M, et al. Primary-cilium-dependent autophagy controls epithelial cell volume in response to fluid flow. Nat Cell Biol. 2016 Jun;18(6):657–667.
   PubMed Web of Science ®Google Scholar
• Chisholm AD, Xu S. The Caenorhabditis elegans epidermis as a model skin. II: differentiation and physiological roles. WIRES Dev Biol. 2012 Nov-Dec;1(6):879–902.
   Web of Science ®Google Scholar
• Zhang Y, Li W, Li L, et al. Structural damage in the C. elegans epidermis causes release of STA-2 and induction of an innate immune response. Immunity. 2015 Feb 17 42(2):309–320.
   PubMed Web of Science ®Google Scholar
• Zhang H, Labouesse M. The making of hemidesmosome structures in vivo. Dev Dyn. 2010 May;239(5):1465–1476.
   PubMed Web of Science ®Google Scholar
• Xu S, Chisholm AD. A Gαq-Ca2; signaling pathway promotes actin-mediated epidermal wound closure in C. elegans. Curr Biol. 2011 Dec 6; 21(23):1960–1967.
   PubMed Web of Science ®Google Scholar
• Pujol N, Cypowyj S, Ziegler K, et al. Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol. 2008 Apr 8 18(7):481–489.
   PubMed Web of Science ®Google Scholar
• Zhang H, Chang JT, Guo B, et al. Guidelines for monitoring autophagy in Caenorhabditis elegans. Autophagy. 2015;11(1):9–27.
   PubMed Web of Science ®Google Scholar
• Kumsta C, Chang JT, Schmalz J, et al. Hormetic heat stress and HSF-1 induce autophagy to improve survival and proteostasis in C. elegans. Nat Commun. 2017 Feb 15;8:14337.
   PubMed Web of Science ®Google Scholar
• Bosher JM, Hahn BS, Legouis R, et al. The caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces. J Cell Biol. 2003 May 26 161(4):757–768.
   PubMed Web of Science ®Google Scholar
• Hong L, Elbl T, Ward J, et al. MUP-4 is a novel transmembrane protein with functions in epithelial cell adhesion in Caenorhabditis elegans. J Cell Biol. 2001 Jul 23 154(2):403–414.
   PubMed Web of Science ®Google Scholar
• Hresko MC, Schriefer LA, Shrimankar P, et al. Myotactin, a novel hypodermal protein involved in muscle-cell adhesion in caenorhabditis elegans. J Cell Biol. 1999 Aug 9 146(3):659–672.
   PubMed Web of Science ®Google Scholar
• Mullen GP, Rogalski TM, Bush JA, et al. Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in caenorhabditis elegans. Mol Biol Cell. 1999 Oct;10(10):3205–3221.
   PubMed Web of Science ®Google Scholar
• Rogalski TM, Mullen GP, Gilbert MM, et al. The UNC-112 gene in caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol. 2000 Jul 10 150(1):253–264.
   PubMed Web of Science ®Google Scholar
• Woo WM, Goncharov A, Jin Y, et al. Intermediate filaments are required for C. elegans epidermal elongation. Dev Biol. 2004 Mar 1 267(1):216–229.
   PubMed Web of Science ®Google Scholar
• Costa M, Draper BW, Priess JR. The role of actin filaments in patterning the caenorhabditis elegans cuticle. Dev Biol. 1997 Apr 15; 184(2):373–384.
   PubMed Web of Science ®Google Scholar
• Wang S, Wu D, Quintin S, et al. NOCA-1 functions with γ-tubulin and in parallel to Patronin to assemble non-centrosomal microtubule arrays in C. elegans. eLife. 2015 Sep 15;4:e08649.
   PubMed Web of Science ®Google Scholar
• Lints R, Hall DH. The cuticle. WormAtlas. 2009. 10.3908/wormatlas.1.12
   Google Scholar
• Tian Y, Li Z, Hu W, et al. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell. 2010 Jun 11 141(6):1042–1055.
   PubMed Web of Science ®Google Scholar
• Wang Z, Miao G, Xue X, et al. The vici syndrome protein EPG5 Is a Rab7 effector that determines the fusion specificity of autophagosomes with late endosomes/lysosomes. Mol Cell. 2016 Sep 1 63(5):781–795.
   PubMed Web of Science ®Google Scholar
• Guo B, Liang Q, Li L, et al. O-GlcNAc-modification of SNAP-29 regulates autophagosome maturation. Nat Cell Biol. 2014 Dec;16(12):1215–1226.
   PubMed Web of Science ®Google Scholar
• Palikaras K, Tavernarakis N. Assessing mitochondrial selective autophagy in the nematode caenorhabditis elegans. Methods Mol Biol. 2017;1567:349–361.
   PubMedGoogle Scholar
• Miao R, Li M, Zhang Q, et al. An ECM-to-Nucleus signaling pathway activates lysosomes for C. elegans larval development. Dev Cell. 2020 Jan 6 52(1):21–37.e5.
   PubMed Web of Science ®Google Scholar
• Norman KR, Cordes S, Qadota H, et al. UNC-97/PINCH is involved in the assembly of integrin cell adhesion complexes in caenorhabditis elegans body wall muscle. Dev Biol. 2007 Sep 1 309(1):45–55.
   PubMed Web of Science ®Google Scholar
• Lin X, Qadota H, Moerman DG, et al. C. elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr Biol. 2003 May 27 13(11):922–932.
   PubMed Web of Science ®Google Scholar
• Moerman DG, Williams BD. Sarcomere assembly in C. elegans muscle The C. elegans Research Community, WormBook . 2006 Jan;16:1–16.
   Google Scholar
• Lee CF, Melkani GC, Bernstein SI. The UNC-45 myosin chaperone: from worms to flies to vertebrates. Int Rev Cell Mol Biol. 2014;313:103–144.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011 Feb;13(2):132–141.
   PubMed Web of Science ®Google Scholar
• Dalla Costa AP, Clemente CF, Carvalho HF, et al. FAK mediates the activation of cardiac fibroblasts induced by mechanical stress through regulation of the mTOR complex. Cardiovasc Res. 2010 Jun 1 86(3):421–431.
   PubMed Web of Science ®Google Scholar
• Rosner M, Siegel N, Valli A, et al. mTOR phosphorylated at S2448 binds to raptor and rictor. Amino Acids. 2010 Jan;38(1):223–228.
   PubMed Web of Science ®Google Scholar
• Wang Q, Guo W, Hao B, et al. Mechanistic study of TRPM2-Ca(2+)-CAMK2-BECN1 signaling in oxidative stress-induced autophagy inhibition. Autophagy. 2016 Aug 2 12(8):1340–1354.
   PubMed Web of Science ®Google Scholar
• Chin RM, Fu X, Pai MY, et al. The metabolite α-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR. Nature. 2014 Jun 19 510(7505):397–401.
   PubMed Web of Science ®Google Scholar
• Zheng H, Yuan C, Zhang H, et al. The tissue- and developmental stage-specific involvement of autophagy genes in aggrephagy. Autophagy. 2020 Apr;16(4):589–599.
   PubMed Web of Science ®Google Scholar
• Espert L, Denizot M, Grimaldi M, et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest. 2006 Aug;116(8):2161–2172.
   PubMed Web of Science ®Google Scholar
• Chen Z, Nie SD, Qu ML, et al. The autophagic degradation of Cav-1 contributes to PA-induced apoptosis and inflammation of astrocytes. Cell Death Dis. 2018 Jul 10 9(7):771.
   PubMedGoogle Scholar
• Lant B, Derry WB. Methods for detection and analysis of apoptosis signaling in the C. elegans germline. Methods (San Diego. Calif). 2013 Jun 1;61(2):174–182.
   Google Scholar
• Tuloup-Minguez V, Hamaï A, Greffard A, et al. Autophagy modulates cell migration and β1 integrin membrane recycling. cell cycle (Georgetown, Tex). Cell Cycle (Georgetown, Tex.). 2013 Oct 15 12(20):3317–3328.
   PubMed Web of Science ®Google Scholar
• Edick MJ, Tesfay L, Lamb LE, et al. Inhibition of integrin-mediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol Biol Cell. 2007 Jul;18(7):2481–2490.
   PubMed Web of Science ®Google Scholar
• Ning L, Xu Z, Furuya N, et al. Perlecan inhibits autophagy to maintain muscle homeostasis in mouse soleus muscle. Matrix Biol. 2015 Oct;48:26–35.
   PubMed Web of Science ®Google Scholar
• Ko SH, Apple EC, Liu, Z et al. Age-dependent autophagy induction after injury promotes axon regeneration by limiting NOTCH. Autophagy. 2020 Nov;16(11):2052–2068.
   PubMed Web of Science ®Google Scholar
• Luo CL, Li BX, Li QQ, et al. Autophagy is involved in traumatic brain injury-induced cell death and contributes to functional outcome deficits in mice. Neuroscience. 2011 Jun 16;184:54–63.
   PubMed Web of Science ®Google Scholar
• Knöferle J, Koch JC, Ostendorf T, et al. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proceedings of the National Academy of Sciences of the United States of America. 2010 Mar 30;107 (13):6064–6069.
   Google Scholar
• Sarkar C, Zhao Z, Aungst S, et al. Impaired autophagy flux is associated with neuronal cell death after traumatic brain injury. Autophagy. 2014;10(12):2208–2222.
   PubMed Web of Science ®Google Scholar
• Liu S, Sarkar C, Dinizo M, et al. Disrupted autophagy after spinal cord injury is associated with ER stress and neuronal cell death. Cell Death Dis. 2015 Jan 8 6(1):e1582.
   PubMedGoogle Scholar
• Wang W, Zuidema A, Te Molder L, et al. Hemidesmosomes modulate force generation via focal adhesions. J Cell Biol. 2020 Feb 3;219(2). 10.1083/jcb.201904137.
   Google Scholar
• Rabanal-Ruiz Y, Byron A, Wirth A, et al. mTORC1 activity is supported by spatial association with focal adhesions. J Cell Biol. 2021 May 3;220(5). 10.1083/jcb.202004010.
   PubMedGoogle Scholar
• Zhang H, Landmann F, Zahreddine H, et al. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature. 2011 Mar 3 471(7336):99–103.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhang CF, Rossiter H, et al. Autophagy is induced by UVA and promotes removal of oxidized phospholipids and protein aggregates in epidermal keratinocytes. J Invest Dermatol. 2013 Jun;133(6):1629–1637.
   PubMed Web of Science ®Google Scholar
• Song X, Narzt MS, Nagelreiter IM, et al. Autophagy deficient keratinocytes display increased DNA damage, senescence and aberrant lipid composition after oxidative stress in vitro and in vivo. Redox Biol. 2017Apr;11:219–230.
   PubMed Web of Science ®Google Scholar
• Wang Q, Ye Y, Liu W, et al. Dual effects of silibinin treatment on autophagy-regulated dermal apoptosis retardation and epidermal apoptosis up-regulation in UVB-induced skin inflammation. J Asian Nat Prod Res. 2012;14(7):688–699.
   PubMed Web of Science ®Google Scholar
• Wang Q, Liu W, Zeng H, et al. p53-mediated autophagy adjustment is involved in the protection of silibinin against murine dermal inflammation and epidermal apoptosis induced by UVB irradiation. J Asian Nat Prod Res. 2013;15(2):117–129.
   PubMed Web of Science ®Google Scholar
• Qiang L, Wu C, Ming M, et al. Autophagy controls p38 activation to promote cell survival under genotoxic stress. J Biol Chem. 2013 Jan 18 288(3):1603–1611.
   PubMed Web of Science ®Google Scholar
• Chen YL, Tao J, Zhao PJ et al. Adiponectin receptor PAQR-2 signaling senses low temperature to promote C. elegans longevity by regulating autophagy. Nat Commun. 2019 Jun 13; 10(1):2602.
   PubMedGoogle Scholar
• Yang Y, Wang H, Wang S, et al. GSK3β signaling is involved in ultraviolet B-induced activation of autophagy in epidermal cells. Int J Oncol. 2012 Nov;41(5):1782–1788.
   PubMed Web of Science ®Google Scholar
• Moriyama M, Moriyama H, Uda J, et al. BNIP3 upregulation via stimulation of ERK and JNK activity is required for the protection of keratinocytes from UVB-induced apoptosis. Cell Death Dis. 2017 Feb 2 8(2):e2576.
   PubMedGoogle Scholar
• Mou K, Liu W, Han D, et al. HMGB1/RAGE axis promotes autophagy and protects keratinocytes from ultraviolet radiation-induced cell death. J Dermatol Sci. 2017 Mar;85(3):162–169.
   PubMed Web of Science ®Google Scholar
• Misovic M, Milenkovic D, Martinovic T, et al. Short-term exposure to UV-A, UV-B, and UV-C irradiation induces alteration in cytoskeleton and autophagy in human keratinocytes. Ultrastruct Pathol. 2013 Aug;37(4):241–248.
   PubMed Web of Science ®Google Scholar
• Chen Y, Leboutet R, Largeau C, et al. Autophagy facilitates mitochondrial rebuilding after acute heat stress via a DRP-1-dependent process. J Cell Biol. 2021 Apr 5;220(4). 10.1083/jcb.201909139.
   Google Scholar
• Deruy E, Gosselin K, Vercamer C, et al. MnSOD upregulation induces autophagic programmed cell death in senescent keratinocytes. PloS one. 2010 Sep 14 5(9):e12712.
   PubMed Web of Science ®Google Scholar
• Wu S, Pei Q, Ni W, et al. HSPA1A Protects Cells from Thermal Stress by Impeding ESCRT-0-Mediated Autophagic Flux in Epidermal Thermoresistance. J Invest Dermatol. 2021 Jan;141(1):48–58.e3.
   PubMed Web of Science ®Google Scholar
• Hawk MA, Gorsuch CL, Fagan P, et al. RIPK1-mediated induction of mitophagy compromises the viability of extracellular-matrix-detached cells. Nat Cell Biol. 2018 Mar;20(3):272–284.
   PubMed Web of Science ®Google Scholar
• Satyavarapu EM, Nath S, Mandal C. Desialylation of Atg5 by sialidase (Neu2) enhances autophagosome formation to induce Anchorage-dependent cell death in ovarian cancer cells. Cell Death Discov. 2021 Feb 1; 7(1):26.
   PubMed Web of Science ®Google Scholar
• Uekita T, Fujii S, Miyazawa Y, et al. Suppression of autophagy by CUB domain-containing protein 1 signaling is essential for Anchorage-independent survival of lung cancer cells. Cancer Sci. 2013 Jul;104(7):865–870.
   PubMed Web of Science ®Google Scholar
• Harada M, Hanada S, Toivola DM, et al. Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology. 2008 Jun;47(6):2026–2035.
   PubMed Web of Science ®Google Scholar
• Kongara S, Kravchuk O, Teplova I, et al. Autophagy regulates keratin 8 homeostasis in mammary epithelial cells and in breast tumors. Mol Cancer Res. 2010 Jun;8(6):873–884.
   PubMed Web of Science ®Google Scholar
• Gilbert S, Loranger A, Daigle N, et al. Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol. 2001 Aug 20 154(4):763–774.
   PubMed Web of Science ®Google Scholar
• Caulin C, Ware CF, Magin TM, et al. Keratin-dependent, epithelial resistance to tumor necrosis factor-induced apoptosis. J Cell Biol. 2000 Apr 3 149(1):17–22.
   PubMed Web of Science ®Google Scholar
• Wang C, Mendonsa GR, Symington JW, et al. Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo. Proceedings of the National Academy of Sciences of the United States of America. 2012 Jul 3;109 (27):11008–11013.
   Google Scholar
• Saitoh T, Fujita N, Hayashi T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proceedings of the National Academy of Sciences of the United States of America. 2009 Dec 8;106 (49):20842–20846.
   Google Scholar
• Saitoh T, Fujita N, Jang MH, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature. 2008 Nov 13 456(7219):264–268.
   PubMed Web of Science ®Google Scholar
• Martin PK, Marchiando A, Xu R, et al. Autophagy proteins suppress protective type I interferon signalling in response to the murine gut microbiota. Nat Microbiol. 2018 Oct;3(10):1131–1141.
   PubMed Web of Science ®Google Scholar
• Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94.
   PubMed Web of Science ®Google Scholar
• Mello CC, Kramer JM, Stinchcomb D, et al. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991 Dec;10(12):3959–3970.
   PubMed Web of Science ®Google Scholar
• Mariol MC, Walter L, Bellemin S, et al. A rapid protocol for integrating extrachromosomal arrays with high transmission rate into the C. elegans genome. J vis exp. 2013 Dec;9(82):e50773.
   Google Scholar
• Xu S, Chisholm AD. Methods for skin wounding and assays for wound responses in C. elegans. J vis exp. 2014 Dec 3;(94 51959).
   Web of Science ®Google Scholar
• Meléndez A, Levine, B. Autophagy in C. elegans. 2009 24 Aug 2009; The C. elegans Research Community, WormBook, http://dx.doi.org/10.1895/wormbook.1.147.1
   Google Scholar