Multi-omics profiling of calcium-induced human keratinocytes differentiation reveals modulation of unfolded protein response signaling pathways

References

• Fuchs E. Epidermal differentiation: the bare essentials. J Cell Biol. 1990;111:2807–2814.
   PubMed Web of Science ®Google Scholar
• Polakowska RR, Haake AR. Apoptosis: the skin from a new perspective. Cell Death Differ. 1994;1:19–31.
   PubMedGoogle Scholar
• Candi E, Schmidt R, Melino G. The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol. 2005;6:328–340.
   PubMed Web of Science ®Google Scholar
• Amoh Y, Hoffman R. Hair follicle-associated-pluripotent (HAP) stem cells. Cell Cycle. 2017;16:2169–2175.
   PubMed Web of Science ®Google Scholar
• Tohgi N, Obara K, Yashiro M, et al. Human hair-follicle associated pluripotent (hHAP) stem cells differentiate to cardiac-muscle cells. Cell Cycle. 2017;16:95–99.
   PubMed Web of Science ®Google Scholar
• Bikle DD, Xie Z, Tu CL. Calcium regulation of keratinocyte differentiation. Expert Rev Endocrinol Metab. 2012;7:461–472.
   PubMedGoogle Scholar
• Savini I, Catani MV, Rossi A, et al. Characterization of keratinocyte differentiation induced by ascorbic acid: protein kinase C involvement and vitamin C homeostasis. J Invest Dermatol. 2002;118:372–379.
   PubMed Web of Science ®Google Scholar
• Borowiec AS, Delcourt P, Dewailly E, et al. Optimal differentiation of in vitro keratinocytes requires multifactorial external control. PLoS One. 2013;8:e77507.
   PubMed Web of Science ®Google Scholar
• Seo EY, Namkung JH, Lee KM, et al. Analysis of calcium-inducible genes in keratinocytes using suppression subtractive hybridization and cDNA microarray. Genomics. 2005;86:528–538.
   PubMed Web of Science ®Google Scholar
• Palombo R, Savini I, Avigliano L, et al. Luteolin-7-glucoside inhibits IL-22/STAT3 pathway, reducing proliferation, acanthosis, and inflammation in keratinocytes and in mouse psoriatic model. Cell Death Dis. 2016;7:e2344-e2344.
   PubMed Web of Science ®Google Scholar
• Elsholz F, Harteneck C, Muller W, et al. Calcium - A central regulator of keratinocyte differentiation in health and disease. Eur J Dermatol. 2014;24(6):650–661
   PubMed Web of Science ®Google Scholar
• Candi E, Cipollone R, Rivetti di Val Cervo P, et al. p63 in epithelial development. Cell Mol Life Sci. 2008;65:3126–3133.
   PubMed Web of Science ®Google Scholar
• Eckhart L, Lippens S, Tschachler E, et al. Cell death by cornification. Biochim Biophys Acta Mol Cell Res. 2013;1833:3471–3480.
   Web of Science ®Google Scholar
• Yuspa SH, Ben T, Hennings H. The induction of epidermal transglutaminase and terminal differentiation by tumor promoters in cultured epidermal cells. Carcinogenesis. 1983;4:1413–1418.
   PubMed Web of Science ®Google Scholar
• Yuspa SH, Kilkenny AE, Steinert PM, et al. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro. J Cell Biol. 1989;109:1207–1217.
   PubMed Web of Science ®Google Scholar
• Wikramanayake TC, Stojadinovic O, Tomic-Canic M. Epidermal differentiation in barrier maintenance and wound healing. Adv Wound Care. 2014;3:272–280.
   Google Scholar
• Sugiura K. Unfolded protein response in keratinocytes: impact on normal and abnormal keratinization. J Dermatol Sci. 2013;69:181–186.
   Web of Science ®Google Scholar
• Sugiura K, Muro Y, Nishizawa Y, et al. LEDGF/DFS70, a major autoantigen of atopic dermatitis, is a component of keratohyalin granules. J Invest Dermatol. 2007;127:75–80.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89–102.
   PubMed Web of Science ®Google Scholar
• Sabnis AJ, Bivona TG. HSP70 dependence in rhabdomyosarcoma: seed or soil? Cell Cycle. 2017;16:147–148.
   PubMed Web of Science ®Google Scholar
• Xia D, Ji W, Xu C, et al. Knockout of MARCH2 inhibits the growth of HCT116 colon cancer cells by inducing endoplasmic reticulum stress. Cell Death Dis. 2017;8:e2957.
   PubMed Web of Science ®Google Scholar
• Kindås-Mügge I, Trautinger F. Increased expression of the M(r) 27,000 heat shock protein (hsp27) in in vitro differentiated normal human keratinocytes. Cell Growth Differ. 1994;5(7):777–781
   PubMedGoogle Scholar
• Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature. 2008;454:455–462.
   Web of Science ®Google Scholar
• Gardner BM, Pincus D, Gotthardt K, et al. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol. 2013;5(3):a013169
   PubMed Web of Science ®Google Scholar
• Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334(6059):1081–1086
   Web of Science ®Google Scholar
• Aubrey BJ, Kelly GL, Janic A, et al. How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death Differ. 2018;25:104–113.
   PubMed Web of Science ®Google Scholar
• Baugh EH, Ke H, Levine AJ, et al. Why are there hotspot mutations in the TP53 gene in human cancers? Cell Death Differ. 2018;25:154–160.
   PubMed Web of Science ®Google Scholar
• Sullivan KD, Galbraith MD, Andrysik Z, et al. Mechanisms of transcriptional regulation by p53. Cell Death Differ. 2018;25:133–143.
   PubMed Web of Science ®Google Scholar
• Wu D, Prives C. Relevance of the p53-MDM2 axis to aging. Cell Death Differ. 2018;25:169–179.
   PubMed Web of Science ®Google Scholar
• Charni M, Aloni-Grinstein R, Molchadsky A, et al. P53 on the crossroad between regeneration and cancer. Cell Death Differ. 2017;8–14.
   PubMed Web of Science ®Google Scholar
• Engeland K. Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death Differ. 2018;25:114–132.
   PubMed Web of Science ®Google Scholar
• Furth N, Aylon Y, Oren M. P53 shades of Hippo. Cell Death Differ. 2018;25:81–92.
   PubMed Web of Science ®Google Scholar
• Furth N, Aylon Y. The LATS1 and LATS2 tumor suppressors: beyond the hippo pathway. Cell Death Differ. 2017;24:1488–1501.
   PubMed Web of Science ®Google Scholar
• Kaiser AM, Attardi LD. Deconstructing networks of p53-mediated tumor suppression in vivo. Cell Death Differ. 2018;25:93–103.
   PubMed Web of Science ®Google Scholar
• Kim MP, Lozano G. Mutant p53 partners in crime. Cell Death Differ. 2018;25:161–168.
   PubMed Web of Science ®Google Scholar
• Nemajerova A, Amelio I, Gebel J, et al. Non-oncogenic roles of TAp73: from multiciliogenesis to metabolism. Cell Death Differ. 2018;25:144–153.
   PubMed Web of Science ®Google Scholar
• Parrales A, Thoenen E, Iwakuma T. The interplay between mutant p53 and the mevalonate pathway. Cell Death Differ. 2018;25:460–470.
   PubMed Web of Science ®Google Scholar
• Adams JM, Cory S. The BCL-2 arbiters of apoptosis and their growing role as cancer targets. Cell Death Differ. 2018;25:27–36.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Vitale I, Aaronson SA, et al. Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. Cell Death Differ. 2018;25:486–541.
   PubMed Web of Science ®Google Scholar
• Kale J, Osterlund EJ, Andrews DW. BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ. 2018;25:65–80.
   PubMed Web of Science ®Google Scholar
• Kalkavan H, Green DR. MOMP, cell suicide as a BCL-2 family business. Cell Death Differ. 2018;25:46–55.
   PubMed Web of Science ®Google Scholar
• Montero J, Letai A. Why do BCL-2 inhibitorswork and where should we use them in the clinic? Cell Death Differ. 2018;25:56–64.
   PubMed Web of Science ®Google Scholar
• Mukherjee A, Williams DW. More alive than dead: non-apoptotic roles for caspases in neuronal development, plasticity and disease. Cell Death Differ. 2017;24:1411–1421.
   PubMed Web of Science ®Google Scholar
• Opferman JT, Kothari A. Anti-apoptotic BCL-2 family members in development. Cell Death Differ. 2018;25:37–45.
   PubMed Web of Science ®Google Scholar
• Pihán P, Carreras-Sureda A, Hetz C. BCL-2 family: integrating stress responses at the ER to control cell demise. Cell Death Differ. 2017;24:1478–1487.
   PubMed Web of Science ®Google Scholar
• Strasser A, Vaux DL. Viewing BCL2 and cell death control from an evolutionary perspective. Cell Death Differ. 2018;25:13–20.
   PubMed Web of Science ®Google Scholar
• Pekarsky Y, Balatti V, Croce CM. BCL2 and miR-15/16: from gene discovery to treatment. Cell Death Differ. 2018;25:21–26.
   PubMed Web of Science ®Google Scholar
• Schröder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res. 2005;569:29–63.
   PubMed Web of Science ®Google Scholar
• Bertolotti A, Zhang Y, Hendershot LM, et al. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol. 2000;2:326–332.
   PubMed Web of Science ®Google Scholar
• Okamura K, Kimata Y, Higashio H, et al. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem Biophys Res Commun. 2000;279:445–450.
   PubMed Web of Science ®Google Scholar
• Shen J, Chen X, Hendershot L, et al. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of golgi localization signals. Dev Cell. 2002;3:99–111.
   PubMed Web of Science ®Google Scholar
• Ron D, Harding HP, Zhang Y. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999;397:271–274.
   PubMed Web of Science ®Google Scholar
• Lee A-H, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23:7448–7459.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Sato T, Matsui T, et al. Transcriptional Induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev Cell. 2007;13:365–376.
   PubMed Web of Science ®Google Scholar
• Shoulders MD, Ryno LM, Genereux JC, et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. 2013;3:1279–1292.
   PubMed Web of Science ®Google Scholar
• Adachi Y, Yamamoto K, Okada T, et al. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct. 2008;33:75–89.
   PubMed Web of Science ®Google Scholar
• Hegde RS, Ploegh HL. Quality and quantity control at the endoplasmic reticulum. Curr Opin Cell Biol. 2010;22:437–446.
   PubMed Web of Science ®Google Scholar
• Shevchenko A, Wilm M, Vorm O, et al. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem. 1996;68:850–858.
   PubMed Web of Science ®Google Scholar
• Smirnov A, Lena AM, Cappello A, et al. ZNF185 is a p63 target gene critical for epidermal differentiation and squamous cell carcinoma development. Oncogene. 2018;38(10):1625–1638
   PubMed Web of Science ®Google Scholar
• Dunham I, Kundaje A, Aldred SF, et al.; ENCODE. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57–74.
   PubMed Web of Science ®Google Scholar
• Corley SM, Mendoza-reinoso V, Giles N, et al. Plau and Tgfbr3 are YAP-regulated genes that promote keratinocyte proliferation. Cell Death Dis. 2018;9:1106.
   PubMed Web of Science ®Google Scholar
• Goldie SJ, Cottle DL, Tan FH, et al. Loss of GRHL3 leads to TARC/CCL17-mediated keratinocyte proliferation in the epidermis. Cell Death Dis. 2018;9(11):1072.
   Web of Science ®Google Scholar
• Peng L, Li Q, Wang H, et al. Fn14 deficiency ameliorates psoriasis-like skin disease in a murine model. Cell Death Dis. 2018;9(8):801.
   Web of Science ®Google Scholar
• Bigas J, Sevilla LM, Carceller E, et al. Epidermal glucocorticoid and mineralocorticoid receptors act cooperatively to regulate epidermal development and counteract skin inflammation article. Cell Death Dis. 2018;9(6):588.
   Web of Science ®Google Scholar
• Gutowska-Owsiak D, De La Serna JB, Fritzsche M, et al. Orchestrated control of filaggrin-actin scaffolds underpins cornification. Cell Death Dis. 2018;9(4):412.
   Web of Science ®Google Scholar
• Carreras-Sureda A, Pihán P, Hetz C. Calcium signaling at the endoplasmic reticulum: fine-tuning stress responses. Cell Calcium. 2018;70:24–31.
   PubMed Web of Science ®Google Scholar
• Higgins R, JM G, Rising L, et al. The unfolded protein response triggers site-specific regulatory ubiquitylation of 40s ribosomal proteins. Mol Cell. 2015;59:35–49.
   PubMed Web of Science ®Google Scholar
• Chen FW, Ioannou YA. Ribosomal proteins in cell proliferation and apoptosis. Int Rev Immunol. 1999;18:429–448.
   PubMedGoogle Scholar
• Wang X, Eno CO, Altman BJ, et al. ER stress modulates cellular metabolism. Biochem J. 2011;435:285–296.
   PubMed Web of Science ®Google Scholar
• Venkatesh S, Suzuki CK. HSP60 takes a hit: inhibition of mitochondrial protein folding. Cell Chem Biol. 2017;24:543–545.
   PubMed Web of Science ®Google Scholar
• Zhao L, Ackerman S. Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol. 2006;18:444–452.
   PubMed Web of Science ®Google Scholar
• Zhao L, Rosales C, Seburn K, et al. Alteration of the unfolded protein response modifies neurodegeneration in a mouse model of Marinesco-Sjögren syndrome. Hum Mol Genet. 2010;19:25–35.
   PubMed Web of Science ®Google Scholar
• Spector DL, Ochs RL, Busch H. Silver staining, immunofluorescence, and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma. 1984;90:139–148.
   PubMed Web of Science ®Google Scholar
• Szegedi K, Göblös A, Bacsa S, et al. Expression and functional studies on the noncoding RNA, PRINS. Int J Mol Sci. 2013;14:205–225.
   Web of Science ®Google Scholar
• Feuerstein N, Spiegel S, Mond JJ. The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody. J Cell Biol. 1988;107:1629–1642.
   PubMed Web of Science ®Google Scholar
• Feuerstein N, Chan PK, Mond JJ. Identification of numatrin, the nuclear matrix protein associated with induction of mitogenesis, as the nucleolar protein B23. Implication for the role of the nucleolus in early transduction of mitogenic signals. J Biol Chem. 1988;263:10608–10612.
   PubMed Web of Science ®Google Scholar
• Sasikumar AN, Perez WB, Kinzy TG. The many roles of the eukaryotic elongation factor 1 complex. Wiley Interdiscip Rev RNA. 2012;3:543–555.
   PubMed Web of Science ®Google Scholar
• Kaitsuka T, Matsushita M. Regulation of translation factor EEF1D gene function by alternative splicing. Int J Mol Sci. 2015;16:3970–3979.
   PubMed Web of Science ®Google Scholar
• Ni M, Zhang Y, Lee AS. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem J. 2011;434:181–188.
   PubMed Web of Science ®Google Scholar
• Misra UK, Deedwania R, Pizzo SV. Activation and cross-talk between Akt, NF-κB, and unfolded protein response signaling in 1-LN prostate cancer cells consequent to ligation of cell surface-associated GRP78. J Biol Chem. 2006;281:13694–13707.
   PubMed Web of Science ®Google Scholar
• Kelber JA, Panopoulos AD, Shani G, et al. Blockade of Cripto binding to cell surface GRP78 inhibits oncogenic Cripto signaling via MAPK/PI3K and Smad2/3 pathways. Oncogene. 2009;28:2324–2336.
   PubMed Web of Science ®Google Scholar
• Davidson DJ, Haskell C, Majest S, et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res. 2005;65:4663–4672.
   PubMed Web of Science ®Google Scholar
• Higashi K, Hasegawa M, Yokoyama C, et al. Dermokine-β impairs ERK signaling through direct binding to GRP78. FEBS Lett. 2012;586:2300–2305.
   PubMed Web of Science ®Google Scholar
• Gardner BM, Walter P. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science. 2011;333:1891–1894.
   PubMed Web of Science ®Google Scholar
• Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32:805–818.
   PubMed Web of Science ®Google Scholar
• Tsai YL, Zhang Y, Tseng CC, et al. Characterization and mechanism of stress-induced translocation of 78-kilodalton glucose-regulated protein (GRP78) to the cell surface. J Biol Chem. 2015;290:8049–8064.
   PubMed Web of Science ®Google Scholar
• Ehren JL, Maher P. Concurrent regulation of the transcription factors Nrf2 and ATF4 mediates the enhancement of glutathione levels by the flavonoid fisetin. Biochem Pharmacol. 2013;85:1816–1826.
   PubMed Web of Science ®Google Scholar
• Li Z, Wang Y, Wu H, et al. GRP78 enhances the glutamine metabolism to support cell survival from glucose deficiency by modulating the b-catenin signaling. Oncotarget. 2014;5.
   Google Scholar
• Zhang L, Li Z, Shi T, et al. Design, purification and assessment of GRP78 binding peptide-linked Subunit A of Subtilase cytotoxic for targeting cancer cells. BMC Biotechnol. 2016;16.
   Web of Science ®Google Scholar
• Matsunaga R, Abe R, Ishii D, et al. Bidirectional binding property of high glycine-tyrosine keratin-associated protein contributes to the mechanical strength and shape of hair. J Struct Biol. 2013;183:484–494.
   PubMed Web of Science ®Google Scholar
• Braakman I, Bulleid NJ. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem. 2011;80:71–99.
   PubMed Web of Science ®Google Scholar
• Ellgaard L, Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005;6:28–32.
   PubMed Web of Science ®Google Scholar
• Onda Y, Kobori Y. Differential activity of rice protein disulfide isomerase family members for disulfide bond formation and reduction. FEBS Open Bio. 2014;4:730–734.
   PubMed Web of Science ®Google Scholar
• Chakravarthi S, Jessop CE, Bulleid NJ. The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep. 2006;7:271–275.
   PubMed Web of Science ®Google Scholar
• Chen L, Zhao M, Li J, et al. Critical role of X-box binding protein 1 in NADPH oxidase 4-triggered cardiac hypertrophy is mediated by receptor interacting protein kinase 1. Cell Cycle. 2017;16:348–359.
   PubMed Web of Science ®Google Scholar
• Kranz P, Neumann F, Wolf A, et al. PDI is an essential redox-sensitive activator of PERK during the unfolded protein response (UPR). Cell Death Dis. 2017;8:e2986.
   PubMed Web of Science ®Google Scholar
• Appenzeller-Herzog C, Riemer J, Zito E, et al. Disulphide production by Ero1α-PDI relay is rapid and effectively regulated. Embo J. 2010;29:3318–3329.
   PubMed Web of Science ®Google Scholar
• Viticchiè G, Agostini M, Lena AM, et al. p63 supports aerobic respiration through hexokinase II. Proc Natl Acad Sci. 2015;112:11577–11582.
   PubMed Web of Science ®Google Scholar
• D’Alessandro A, Amelio I, Berkers CR, et al. Metabolic effect of TAp63 enhanced glycolysis and pentose phosphate pathway, resulting in increased antioxidant defense. Oncotarget. 2014;5(17):7722–7733.
   Google Scholar
• Giacobbe A, Bongiorno-Borbone L, Bernassola F, et al. P63 regulates glutaminase 2 expression. Cell Cycle. 2013;12:1395–1405.
   PubMed Web of Science ®Google Scholar
• Rivetti di Val Cervo P, AM L, Nicoloso M, et al. p63-microRNA feedback in keratinocyte senescence. Proc Natl Acad Sci. 2012;109:1133–1138.
   PubMed Web of Science ®Google Scholar
• Candi E, Smirnov A, Panatta E, et al. Metabolic pathways regulated by p63. Biochem Biophys Res Commun. 2017;482(3):440–444.
   PubMed Web of Science ®Google Scholar
• Dodson M, Darley-Usmar V, Zhang J. Cellular metabolic and autophagic pathways: traffic control by redox signaling. Free Radic Biol Med. 2013;63:207–221.
   PubMed Web of Science ®Google Scholar
• Dantuma NP, Heinen C, Hoogstraten D. The ubiquitin receptor Rad23: at the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair (Amst). 2009;8:449–460.
   PubMed Web of Science ®Google Scholar
• Oh DH, Yeh K. Differentiating human keratinocytes are deficient in p53 but retain global nucleotide excision repair following ultraviolet radiation. DNA Repair (Amst). 2005;4:1149–1159.
   PubMed Web of Science ®Google Scholar
• de Pedro I, Alonso-Lecue P, Sanz-Gómez N, et al. Sublethal UV irradiation induces squamous differentiation via a p53-independent, DNA damage-mitosis checkpoint. Cell Death Dis. 2018;9(11):1094.
   Web of Science ®Google Scholar
• Messenger Z, Hall J, Jima D, et al. C/EBPβ deletion in oncogenic Ras skin tumors is a synthetic lethal event. Cell Death Dis. 2018;9:1054.
   PubMed Web of Science ®Google Scholar
• Singh TP, Vieyra-Garcia PA, Wagner K, et al. Cbl-b deficiency provides protection against UVB-induced skin damage by modulating inflammatory gene signature. Cell Death Dis. 2018;9(8):835.
   Web of Science ®Google Scholar
• Singh B, Schoeb TR, Bajpai P, et al. Reversing wrinkled skin and hair loss in mice by restoring mitochondrial function. Cell Death Dis. 2018;9(7):735.
   Web of Science ®Google Scholar