2,331
Views
19
CrossRef citations to date
0
Altmetric
Review

Uncovering mechanisms of nuclear degradation in keratinocytes: A paradigm for nuclear degradation in other tissues

ORCID Icon, & ORCID Icon
Pages 56-64 | Received 17 Oct 2017, Accepted 24 Nov 2017, Published online: 03 Jan 2018

References

  • Alberts B, Johnson A, Lewis J, et al. Molecular Biology of the Cell. 4th edition. Garland Science: 2002.
  • Keerthivasan G, Wickrema A, Crispino JD. Erythroblast Enucleation. SAGE-Hindawi Access to Res Stem Cells Int. 2011;2011:139851:
  • Bassnett S.. On the mechanism of organelle degradation in the vertebrate lens. Exp Eye Res. 2009;88:133–9. doi:10.1016/j.exer.2008.08.017.
  • Eckhart L, Lippens S, Tschachler E, et al. Cell death by cornification. Biochim Biophys Acta – Mol Cell Res. 2013;1833:3471–80. doi:10.1016/j.bbamcr.2013.06.010.
  • Ji P. New Insights into the Mechanisms of Mammalian Erythroid Chromatin Condensation and Enucleation. Int Rev Cell Mol Biol. 2015;316:159–82. doi:10.1016/bs.ircmb.2015.01.006.
  • Mijaljica D, Devenish RJ. Nucleophagy at a glance. J Cell Sci. 2013;126:4325–30. doi:10.1242/jcs.133090.
  • Chen K, Huang C, Yuan J, et al. Long-term artificial selection reveals a role of TCTP in autophagy in mammalian cells. Mol Biol Evol. 2014;31:2194–211. doi:10.1093/molbev/msu181.
  • Peng H, Lavker RM. Nucleophagy: A New Look at Past Observations. J Invest Dermatol. 2016;136:1316–8. doi:10.1016/j.jid.2016.04.019.
  • Modak SP, Perdue SW. Terminal lens cell differentiation I. Histological and microspectrophotometric analysis of nuclear Degeneration. Exp Cell Res. 1970;59:43–56. doi:10.1016/0014-4827(70)90622-1.
  • Vrensen GF, Graw J, De Wolf A. Nuclear breakdown during terminal differentiation of primary lens fibres in mice: a transmission electron microscopic study. Exp Eye Res. 1991;52:647–59. doi:10.1016/0014-4835(91)90017-9.
  • Costello MJ, Brennan LA, Mohamed A, et al. Identification and ultrastructural characterization of a novel nuclear degradation complex in differentiating Lens Fiber cells. PLoS One. 2016;11:e0160785. doi:10.1371/journal.pone.0160785.
  • Dahm R, Gribbon C, Quinlan RA, et al. Changes in the nucleolar and coiled body compartments precede lamina and chromatin reorganization during fibre cell denucleation in the bovine lens. Eur J Cell Biol. 1998;75:237–46. doi:10.1016/S0171-9335(98)80118-0.
  • De Maria A, Bassnett S. DNase IIβ distribution and activity in the mouse lens. Investig Opthalmology Vis Sci. 2007;48:5638. doi:10.1167/iovs.07-0782.
  • Costello MJ, Mohamed A, Gilliland K, et al. High resolution confocal microscopy of potential newly described nuclear excisosomes in primate lenses. Invest Ophthalmol Vis Sci. 2017;58:1213.
  • Nishimoto S, Kawane K, Watanabe-Fukunaga R, et al. et al. Nuclear cataract caused by a lack of DNA degradation in the mouse eye lens. Nature. 2003;424:1071–4. doi:10.1038/nature01895.
  • Nakahara M, Nagasaka A, Koike M, et al. Degradation of nuclear DNA by DNase II-like acid DNase in cortical fiber cells of mouse eye lens. FEBS J. 2007;274:3055–64. doi:10.1111/j.1742-4658.2007.05836.x.
  • Zandy AJ, Lakhani S, Zheng T, et al. Role of the executioner caspases during lens development. J Biol Chem. 2005;280:30263–72. doi:10.1074/jbc.M504007200.
  • Matsui M, Yamamoto A, Kuma A, et al. Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem Biophys Res Commun. 2006;339:485–9. doi:10.1016/j.bbrc.2005.11.044.
  • Nishida Y, Arakawa S, Fujitani K, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature. 2009;461:654–8. doi:10.1038/nature08455.
  • Rowan S, Chang ML, Reznikov N, et al. Disassembly of the lens fiber cell nucleus to create a clear lens: The p27 descent. Exp Eye Res. 2017;156:72–8. doi:10.1016/j.exer.2016.02.011.
  • Girão H, Pereira P, Taylor A, et al. Subcellular redistribution of components of the ubiquitin-proteasome pathway during lens differentiation and maturation. Investig Ophthalmol Vis Sci. 2005;46:1386–92. doi:10.1167/iovs.04-0563.
  • Basu S, Rajakaruna S, Reyes B, et al. Suppression of MAPK/JNK-MTORC1 signaling leads to premature loss of organelles and nuclei by autophagy during terminal differentiation of lens fiber cells. Autophagy. 2014;10:1193–211. doi:10.4161/auto.28768.
  • Maeda A, Moriguchi T, Hamada M, et al. Transcription factor GATA-3 is essential for lens development. Dev Dyn. 2009;238:2280–91. doi:10.1002/dvdy.22035.
  • Cui X, Wang L, Zhang J, et al. et al. HSF4 regulates DLAD expression and promotes lens de-nucleation. Biochim Biophys Acta – Mol Basis Dis. 2013;1832:1167–72. doi:10.1016/j.bbadis.2013.03.007.
  • He S, Pirity MK, Wang W-L, et al. et al. Chromatin remodeling enzyme Brg1 is required for mouse lens fiber cell terminal differentiation and its denucleation. Epigenetics Chromatin. 2010;3:21. doi:10.1186/1756-8935-3-21.
  • Gao J, Sun X, Martinez-Wittinghan FJ, et al. Connections between connexins, calcium, and cataracts in the lens. J Gen Physiol. 2004;124:289–300. doi:10.1085/jgp.200409121.
  • Nandakumar SK, Ulirsch JC, Sankaran VG. Advances in understanding erythropoiesis: Evolving perspectives. Br J Haematol. 2016;173:206–18. doi:10.1111/bjh.13938.
  • Yoshida H, Kawane K, Koike M, et al. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature. 2005;437:754–8. doi:10.1038/nature03964.
  • Toda S, Nishi C, Yanagihashi Y, et al. Clearance of apoptotic cells and pyrenocytes. Curr Top Dev Biol. 2015;114:267–95. doi:10.1016/bs.ctdb.2015.07.017.
  • Palis J.. Primitive and definitive erythropoiesis in mammals. Front Physiol. 2014;5:3. doi:10.3389/fphys.2014.00003.
  • Muir AR, Kerr DNS. Erythropoiesis: an electron microscopical study. Q J Exp Physiol Cogn Med Sci. 1958;43:106–14.
  • McGrath KE, Catherman SC, Palis J. Delineating stages of erythropoiesis using imaging flow cytometry. Methods. 2017;112:68–74. doi:10.1016/j.ymeth.2016.08.012.
  • Krauss SW, Lo AJ, Short SA, et al. Nuclear substructure reorganization during late-stage erythropoiesis is selective and does not involve caspase cleavage of major nuclear substructural proteins. Blood. 2005;106:2200–5. doi:10.1182/blood-2005-04-1357.
  • Zhao B, Mei Y, Schipma MJ, et al. Nuclear condensation during mouse erythropoiesis requires caspase-3-mediated nuclear opening. Dev Cell. 2016;36:498–510. doi:10.1016/j.devcel.2016.02.001.
  • Simpson CF, Kling JM. The mechanism of denucleation in circulating erythroblasts. J Cell Biol. 1967;35:237–45. doi:10.1083/jcb.35.1.237.
  • Ji P, Yeh V, Ramirez T, et al. Histone deacetylase 2 is required for chromatin condensation and subsequent enucleation of cultured mouse fetal erythroblasts. Haematologica. 2010;95:2013–21. doi:10.3324/haematol.2010.029827.
  • Swartz KL, Wood SN, Murthy T, et al. E2F-2 promotes nuclear condensation and enucleation of terminally differentiated erythroblasts. Mol Cell Biol. 2017;37:e00274–16. doi:10.1128/MCB.00274-16.
  • Nowak RB, Papoin J, Gokhin DS, et al. Tropomodulin 1 controls erythroblast enucleation via regulation of F-actin in the enucleosome. Blood. 2017;130:1144–55. doi:10.1182/blood-2017-05-787051.
  • Konstantinidis DG, Pushkaran S, Johnson JF, et al. Signaling and cytoskeletal requirements in erythroblast enucleation. Blood. 2012;119:6118–27. doi:10.1182/blood-2011-09-379263.
  • Wölwer CB, Pase LB, Russell SM, et al. Calcium signaling is required for erythroid enucleation. PLoS One. 2016;11:1–12. doi:10.1371/journal.pone.0146201.
  • Lavker RM, Matoltsy AG. Formation of horny cells: the fate of cell organelles and differentiation products in ruminal epithelium. J Cell Biol. 1970;44:501–12. doi:10.1083/jcb.44.3.501.
  • Gdula MR, Poterlowicz K, Mardaryev AN, et al. Remodeling of three-dimensional organization of the nucleus during terminal keratinocyte differentiation in the epidermis. J Invest Dermatol. 2013;133:2191–201. doi:10.1038/jid.2013.66.
  • Akinduro O, Sully K, Patel A, et al. et al. Constitutive autophagy and nucleophagy during epidermal differentiation. J Invest Dermatol. 2016;136:1460–70. doi:10.1016/j.jid.2016.03.016.
  • Fischer H, Buchberger M, Napirei M, et al. Inactivation of DNase1L2 and DNase2 in keratinocytes suppresses DNA degradation during epidermal cornification and results in constitutive parakeratosis. Sci Rep. 2017;7:6433. doi:10.1038/s41598-017-06652-8.
  • Naeem AS, Zhu Y, Di WL, et al. AKT1-mediated Lamin A/C degradation is required for nuclear degradation and normal epidermal terminal differentiation. Cell Death Differ. 2015;22:2123–32. doi:10.1038/cdd.2015.62.
  • Yamamoto-Tanaka M, Makino T, Motoyama A, et al. Multiple pathways are involved in DNA degradation during keratinocyte terminal differentiation. Cell Death Dis. 2014;5:e1181. doi:10.1038/cddis.2014.145.
  • Manils J, Fischer H, Climent J, et al. et al. Double deficiency of Trex2 and DNase1L2 nucleases leads to accumulation of DNA in lingual cornifying keratinocytes without activating inflammatory responses. Sci Rep. 2017;7:11902. doi:10.1038/s41598-017-12308-4.
  • Manils J, Casas E, Viña-Vilaseca A, et al. et al. The Exonuclease Trex2 Shapes Psoriatic Phenotype. J Invest Dermatol. 2016;136:2345–55. doi:10.1016/j.jid.2016.05.122.
  • Lan Y, Londoño D, Bouley R, et al. Dnase2a deficiency uncovers lysosomal clearance of damaged nuclear DNA via autophagy. Cell Rep. 2014;9:180–92. doi:10.1016/j.celrep.2014.08.074.
  • Yang SH, Chang SY, Yin L, et al. An absence of both lamin B1 and lamin B2 in keratinocytes has no effect on cell proliferation or the development of skin and hair. Hum Mol Genet. 2011;20:3537–44. doi:10.1093/hmg/ddr266.
  • Rossiter H, König U, Barresi C, et al. et al. Epidermal keratinocytes form a functional skin barrier in the absence of Atg7 dependent autophagy. J Dermatol Sci. 2013;71:67–75. doi:10.1016/j.jdermsci.2013.04.015.
  • Sukseree S, Rossiter H, Mildner M, et al. Targeted deletion of Atg5 reveals differential roles of autophagy in keratin K5-expressing epithelia. Biochem Biophys Res Commun. 2013;430:689–94. doi:10.1016/j.bbrc.2012.11.090.
  • Huang R, Xu Y, Wan W, et al. et al. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell. 2015;57:456–67. doi:10.1016/j.molcel.2014.12.013.
  • Yan S, Liu L, Ren F, et al. Sunitinib induces genomic instability of renal carcinoma cells through affecting the interaction of LC3-II and PARP-1. Cell Death Dis. 2017;8:e2988. doi:10.1038/cddis.2017.387.
  • Wang Y, Zhang N, Zhang L, et al. et al. Autophagy regulates chromatin ubiquitination in DNA damage response through elimination of SQSTM1/p62. Mol Cell. 2016;63:34–48. doi:10.1016/j.molcel.2016.05.027.
  • Park YE, Hayashi YK, Bonne G, et al. Autophagic degradation of nuclear components in mammalian cells. Autophagy. 2009;5:795–804. doi:10.4161/auto.8901.
  • Chikh A, Sanza P, Raimondi C, et al. iASPP is a novel autophagy inhibitor in keratinocytes. J Cell Sci. 2014;127:3079–93. doi:10.1242/jcs.144816.
  • Naeem AS, Tommasi C, Cole C, et al. et al. A mechanistic target of rapamycin complex 1/2 (mTORC1)/V-Akt murine thymoma viral oncogene homolog 1 (AKT1)/cathepsin H axis controls filaggrin expression and processing in skin, a novel mechanism for skin barrier disruption in patients with atopic dermat. J Allergy Clin Immunol. 2017;139:1228–41. doi:10.1016/j.jaci.2016.09.052.
  • Morioka K, Takano-ohmuro H, Sameshima M, et al. Extinction of organelles in differentiating epidermis. Acta Histochem Cytochem. 1999;32:465–76. doi:10.1267/ahc.32.465.
  • Ney PA. Normal and disordered reticulocyte maturation. Curr Opin Hematol. 2011;18:152–7. doi:10.1097/MOH.0b013e328345213e.
  • Schweers RL, Zhang J, Randall MS, et al. et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A. 2007;104:19500–5. doi:10.1073/pnas.0708818104.
  • Rouzbeh S, Kobari L, Cambot M, et al. Molecular signature of erythroblast enucleation in human embryonic stem cells. Stem Cells. 2015;33:2431–41. doi:10.1002/stem.2027.
  • Vacaru AM, Isern J, Fraser ST, et al. Analysis of primitive erythroid cell proliferation and enucleation using a cyan fluorescent reporter in transgenic mice. Genesis. 2013;51:751–62. doi:10.1002/dvg.22420.
  • Wölwer CB, Pase LB, Pearson HB, et al. A chemical screening approach to identify novel key mediators of erythroid enucleation. PLoS One. 2015;10:e0142655. doi:10.1371/journal.pone.0142655.