Piwil2 Inhibits Keratin 8 Degradation through Promoting p38-Induced Phosphorylation To Resist Fas-Mediated Apoptosis

REFERENCES

• Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. 1998. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12:3715–3727. http://dx.doi.org/10.1101/gad.12.23.3715.
   PubMed Web of Science ®Google Scholar
• Farazi TA, Juranek SA, Tuschl T. 2008. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135:1201–1214. http://dx.doi.org/10.1242/dev.005629.
   PubMed Web of Science ®Google Scholar
• Houwing S, Berezikov E, Ketting RF. 2008. Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J. 27:2702–2711. http://dx.doi.org/10.1038/emboj.2008.204.
   PubMed Web of Science ®Google Scholar
• Seto AG, Kingston RE, Lau NC. 2007. The coming of age for Piwi proteins. Mol. Cell 26:603–609. http://dx.doi.org/10.1016/j.molcel.2007.05.021.
   PubMed Web of Science ®Google Scholar
• Lee JH, Engel W, Nayernia K. 2006. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol. Reprod. Dev. 73:173–179. http://dx.doi.org/10.1002/mrd.20391.
   PubMedGoogle Scholar
• Sun H, Li D, Chen S, Liu Y, Liao X, Deng W, Li N, Zeng M, Tao D, Ma Y. 2010. Zili inhibits transforming growth factor-beta signaling by interacting with Smad4. J. Biol. Chem. 285:4243–4250. http://dx.doi.org/10.1074/jbc.M109.079533.
   PubMedGoogle Scholar
• Smulders-Srinivasan TK, Szakmary A, Lin H. 2010. A Drosophila chromatin factor interacts with the Piwi-interacting RNA mechanism in niche cells to regulate germline stem cell self-renewal. Genetics 186:573–583. http://dx.doi.org/10.1534/genetics.110.119081.
   PubMedGoogle Scholar
• Szakmary A, Cox DN, Wang Z, Lin H. 2005. Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr. Biol. 15:171–178. http://dx.doi.org/10.1016/j.cub.2005.01.005.
   PubMed Web of Science ®Google Scholar
• Sasaki T, Shiohama A, Minoshima S, Shimizu N. 2003. Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics 82:323–330. http://dx.doi.org/10.1016/S0888-7543(03)00129-0.
   PubMed Web of Science ®Google Scholar
• Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, Draper BW, Ketting RF. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129:69–82. http://dx.doi.org/10.1016/j.cell.2007.03.026.
   PubMed Web of Science ®Google Scholar
• Lee JH, Schutte D, Wulf G, Fuzesi L, Radzun HJ, Schweyer S, Engel W, Nayernia K. 2006. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet. 15:201–211. http://dx.doi.org/10.1093/hmg/ddi430.
   PubMed Web of Science ®Google Scholar
• Lu Y, Zhang K, Li C, Yao Y, Tao D, Liu Y, Zhang S, Ma Y. 2012. Piwil2 suppresses p53 by inducing phosphorylation of signal transducer and activator of transcription 3 in tumor cells. PLoS One 7:e30999. http://dx.doi.org/10.1371/journal.pone.0030999.
   PubMed Web of Science ®Google Scholar
• Zhang K, Lu Y, Yang P, Li C, Sun H, Tao D, Liu Y, Zhang S, Ma Y. 2012. HILI inhibits TGF-beta signaling by interacting with Hsp90 and promoting TbetaR degradation. PLoS One 7:e41973. http://dx.doi.org/10.1371/journal.pone.0041973.
   PubMedGoogle Scholar
• Lee JH, Jung C, Javadian-Elyaderani P, Schweyer S, Schutte D, Shoukier M, Karimi-Busheri F, Weinfeld M, Rasouli-Nia A, Hengstler JG, Mantilla A, Soleimanpour-Lichaei HR, Engel W, Robson CN, Nayernia K. 2010. Pathways of proliferation and antiapoptosis driven in breast cancer stem cells by stem cell protein piwil2. Cancer Res. 70:4569–4579. http://dx.doi.org/10.1158/0008-5472.CAN-09-2670.
   PubMed Web of Science ®Google Scholar
• Yin DT, Wang Q, Chen L, Liu MY, Han C, Yan Q, Shen R, He G, Duan W, Li JJ, Wani A, Gao JX. 2011. Germline stem cell gene PIWIL2 mediates DNA repair through relaxation of chromatin. PLoS One 6:e27154. http://dx.doi.org/10.1371/journal.pone.0027154.
   PubMed Web of Science ®Google Scholar
• Wang QE, Han C, Milum K, Wani AA. 2011. Stem cell protein Piwil2 modulates chromatin modifications upon cisplatin treatment. Mutat. Res. 708:59–68. http://dx.doi.org/10.1016/j.mrfmmm.2011.02.001.
   PubMed Web of Science ®Google Scholar
• Nagata S, Golstein P. 1995. The Fas death factor. Science 267:1449–1456. http://dx.doi.org/10.1126/science.7533326.
   PubMed Web of Science ®Google Scholar
• Muzio M. 1998. Signalling by proteolysis: death receptors induce apoptosis. Int. J. Clin. Lab. Res. 28:141–147. http://dx.doi.org/10.1007/s005990050035.
   PubMedGoogle Scholar
• Reichmann E. 2002. The biological role of the Fas/FasL system during tumor formation and progression. Semin. Cancer Biol. 12:309–315. http://dx.doi.org/10.1016/S1044-579X(02)00017-2.
   PubMed Web of Science ®Google Scholar
• Kim S, Wong P, Coulombe PA. 2006. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 441:362–365. http://dx.doi.org/10.1038/nature04659.
   PubMed Web of Science ®Google Scholar
• Ku NO, Michie S, Resurreccion EZ, Broome RL, Omary MB. 2002. Keratin binding to 14-3-3 proteins modulates keratin filaments and hepatocyte mitotic progression. Proc. Natl. Acad. Sci. U. S. A. 99:4373–4378. http://dx.doi.org/10.1073/pnas.072624299.
   PubMed Web of Science ®Google Scholar
• Inada H, Izawa I, Nishizawa M, Fujita E, Kiyono T, Takahashi T, Momoi T, Inagaki M. 2001. Keratin attenuates tumor necrosis factor-induced cytotoxicity through association with TRADD. J. Cell Biol. 155:415–426. http://dx.doi.org/10.1083/jcb.200103078.
   PubMed Web of Science ®Google Scholar
• Ku NO, Toivola DM, Strnad P, Omary MB. 2010. Cytoskeletal keratin glycosylation protects epithelial tissue from injury. Nat. Cell Biol. 12:876–885. http://dx.doi.org/10.1038/ncb2091.
   PubMed Web of Science ®Google Scholar
• Gilbert S, Loranger A, Daigle N, Marceau N. 2001. Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J. Cell Biol. 154:763–773. http://dx.doi.org/10.1083/jcb.200102130.
   PubMed Web of Science ®Google Scholar
• Long HA, Boczonadi V, McInroy L, Goldberg M, Maatta A. 2006. Periplakin-dependent re-organisation of keratin cytoskeleton and loss of collective migration in keratin-8-downregulated epithelial sheets. J. Cell Sci. 119:5147–5159. http://dx.doi.org/10.1242/jcs.03304.
   PubMed Web of Science ®Google Scholar
• Buhler H, Schaller G. 2005. Transfection of keratin 18 gene in human breast cancer cells causes induction of adhesion proteins and dramatic regression of malignancy in vitro and in vivo. Mol. Cancer Res. 3:365–371. http://dx.doi.org/10.1158/1541-7786.MCR-04-0117.
   PubMedGoogle Scholar
• Schaller G, Fuchs I, Pritze W, Ebert A, Herbst H, Pantel K, Weitzel H, Lengyel E. 1996. Elevated keratin 18 protein expression indicates a favorable prognosis in patients with breast cancer. Clin. Cancer Res. 2:1879–1885.
   PubMedGoogle Scholar
• Bianchi N, Depianto D, McGowan K, Gu C, Coulombe PA. 2005. Exploiting the keratin 17 gene promoter to visualize live cells in epithelial appendages of mice. Mol. Cell. Biol. 25:7249–7259. http://dx.doi.org/10.1128/MCB.25.16.7249-7259.2005.
   PubMedGoogle Scholar
• Oshima RG. 2002. Apoptosis and keratin intermediate filaments. Cell Death Differ. 9:486–492. http://dx.doi.org/10.1038/sj.cdd.4400988.
   PubMed Web of Science ®Google Scholar
• Alam CM, Silvander JS, Daniel EN, Tao GZ, Kvarnstrom SM, Alam P, Omary MB, Hanninen A, Toivola DM. 2013. Keratin 8 modulates beta-cell stress responses and normoglycaemia. J. Cell Sci. 126:5635–5644. http://dx.doi.org/10.1242/jcs.132795.
   PubMed Web of Science ®Google Scholar
• Gilbert S, Loranger A, Marceau N. 2004. Keratins modulate c-Flip/extracellular signal-regulated kinase 1 and 2 antiapoptotic signaling in simple epithelial cells. Mol. Cell. Biol. 24:7072–7081. http://dx.doi.org/10.1128/MCB.24.16.7072-7081.2004.
   PubMedGoogle Scholar
• Jaitovich A, Mehta S, Na N, Ciechanover A, Goldman RD, Ridge KM. 2008. Ubiquitin-proteasome-mediated degradation of keratin intermediate filaments in mechanically stimulated A549 cells. J. Biol. Chem. 283:25348–25355. http://dx.doi.org/10.1074/jbc.M801635200.
   PubMed Web of Science ®Google Scholar
• Ku NO, Omary MB. 1997. Phosphorylation of human keratin 8 in vivo at conserved head domain serine 23 and at epidermal growth factor-stimulated tail domain serine 431. J. Biol. Chem. 272:7556–7564. http://dx.doi.org/10.1074/jbc.272.11.7556.
   PubMed Web of Science ®Google Scholar
• Ku NO, Omary MB. 2000. Keratins turn over by ubiquitination in a phosphorylation-modulated fashion. J. Cell Biol. 149:547–552. http://dx.doi.org/10.1083/jcb.149.3.547.
   PubMed Web of Science ®Google Scholar
• Ku NO, Azhar S, Omary MB. 2002. Keratin 8 phosphorylation by p38 kinase regulates cellular keratin filament reorganization: modulation by a keratin 1-like disease causing mutation. J. Biol. Chem. 277:10775–10782. http://dx.doi.org/10.1074/jbc.M107623200.
   PubMed Web of Science ®Google Scholar
• Ye Y, Yin DT, Chen L, Zhou Q, Shen R, He G, Yan Q, Tong Z, Issekutz AC, Shapiro CL, Barsky SH, Lin H, Li JJ, Gao JX. 2010. Identification of Piwil2-like (PL2L) proteins that promote tumorigenesis. PLoS One 5:e13406. http://dx.doi.org/10.1371/journal.pone.0013406.
   PubMed Web of Science ®Google Scholar
• Fortier AM, Asselin E, Cadrin M. 2013. Keratin 8 and 18 loss in epithelial cancer cells increases collective cell migration and cisplatin sensitivity through claudin1 up-regulation. J. Biol. Chem. 288:11555–11571. http://dx.doi.org/10.1074/jbc.M112.428920.
   PubMed Web of Science ®Google Scholar
• Gilbert S, Loranger A, Lavoie JN, Marceau N. 2012. Cytoskeleton keratin regulation of FasR signaling through modulation of actin/ezrin interplay at lipid rafts in hepatocytes. Apoptosis 17:880–894. http://dx.doi.org/10.1007/s10495-012-0733-2.
   PubMedGoogle Scholar
• Ridge KM, Linz L, Flitney FW, Kuczmarski ER, Chou YH, Omary MB, Sznajder JI, Goldman RD. 2005. Keratin 8 phosphorylation by protein kinase C delta regulates shear stress-mediated disassembly of keratin intermediate filaments in alveolar epithelial cells. J. Biol. Chem. 280:30400–30405. http://dx.doi.org/10.1074/jbc.M504239200.
   PubMedGoogle Scholar
• Ku NO, Omary MB. 1997. Phosphorylation of human keratin 8 in vivo at conserved head domain serine 23 and at epidermal growth factor-stimulated tail domain serine 431. J. Biol. Chem. 272:7556–7564. http://dx.doi.org/10.1074/jbc.272.11.7556.
   PubMed Web of Science ®Google Scholar
• Park MK, Lee HJ, Shin J, Noh M, Kim SY, Lee CH. 2011. Novel participation of transglutaminase-2 through c-Jun N-terminal kinase activation in sphingosylphosphorylcholine-induced keratin reorganization of PANC-1 cells. Biochim. Biophys. Acta 1811:1021–1029. http://dx.doi.org/10.1016/j.bbalip.2011.07.007.
   PubMedGoogle Scholar
• Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJJr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845–6854. http://dx.doi.org/10.1093/emboj/18.23.6845.
   PubMed Web of Science ®Google Scholar
• Koul HK, Pal M, Koul S. 2013. Role of p38 MAP kinase signal transduction in solid tumors. Genes Cancer 4:342–359. http://dx.doi.org/10.1177/1947601913507951.
   PubMedGoogle Scholar
• Tao GZ, Looi KS, Toivola DM, Strnad P, Zhou Q, Liao J, Wei Y, Habtezion A, Omary MB. 2009. Keratins modulate the shape and function of hepatocyte mitochondria: a mechanism for protection from apoptosis. J. Cell Sci. 122:3851–3855. http://dx.doi.org/10.1242/jcs.051862.
   PubMed Web of Science ®Google Scholar
• Farley N, Pedraza-Alva G, Serrano-Gomez D, Nagaleekar V, Aronshtam A, Krahl T, Thornton T, Rincon M. 2006. p38 mitogen-activated protein kinase mediates the Fas-induced mitochondrial death pathway in CD8+ T cells. Mol. Cell. Biol. 26:2118–2129. http://dx.doi.org/10.1128/MCB.26.6.2118-2129.2006.
   PubMedGoogle Scholar
• Merritt C, Enslen H, Diehl N, Conze D, Davis RJ, Rincon M. 2000. Activation of p38 mitogen-activated protein kinase in vivo selectively induces apoptosis of CD8(+) but not CD4(+) T cells. Mol. Cell. Biol. 20:936–946. http://dx.doi.org/10.1128/MCB.20.3.936-946.2000.
   PubMed Web of Science ®Google Scholar
• Ronkina N, Kotlyarov A, Dittrich-Breiholz O, Kracht M, Hitti E, Milarski K, Askew R, Marusic S, Lin LL, Gaestel M, Telliez JB. 2007. The mitogen-activated protein kinase (MAPK)-activated protein kinases MK2 and MK3 cooperate in stimulation of tumor necrosis factor biosynthesis and stabilization of p38 MAPK. Mol. Cell. Biol. 27:170–181. http://dx.doi.org/10.1128/MCB.01456-06.
   PubMed Web of Science ®Google Scholar
• Kwong J, Chen M, Lv D, Luo N, Su W, Xiang R, Sun P. 2013. Induction of p38delta expression plays an essential role in oncogenic ras-induced senescence. Mol. Cell. Biol. 33:3780–3794. http://dx.doi.org/10.1128/MCB.00784-13.
   PubMed Web of Science ®Google Scholar
• Tournier C, Whitmarsh AJ, Cavanagh J, Barrett T, Davis RJ. 1999. The MKK7 gene encodes a group of c-Jun NH2-terminal kinase kinases. Mol. Cell. Biol. 19:1569–1581.
   PubMed Web of Science ®Google Scholar
• Ku NO, Omary MB. 2006. A disease- and phosphorylation-related nonmechanical function for keratin 8. J. Cell Biol. 174:115–125. http://dx.doi.org/10.1083/jcb.200602146.
   PubMed Web of Science ®Google Scholar