The hippo kinase STK38 ensures functionality of XPO1

References

• Dobzhansky T. Nothing in biology makes sense except in the light of evolution. Am Biol Teach. 1973;35:125–129.
   Web of Science ®Google Scholar
• Apple’s Jobs to Obama: ‘jobs aren’t coming back’ to U.S. - News - Sarasota Herald-Tribune, Sarasota, FL.
   Google Scholar
• Supply Chain 4.0 – the next-generation digital supply chain | McKinsey.
   Google Scholar
• CALLAN HG, RANDALL JT, TOMLIN SG. An electron microscope study of the nuclear membrane. Nature. 1949;163:280.
   PubMed Web of Science ®Google Scholar
• Huang R, Xu Y, Wan W, et al. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell. 2015;57:456–466.
   PubMed Web of Science ®Google Scholar
• Martin AP, Jacquemyn M, Lipecka J, et al. STK38 kinase acts as XPO1 gatekeeper regulating the nuclear export of autophagy proteins and other cargoes. EMBO Rep. 2019;20:e48150.
   PubMed Web of Science ®Google Scholar
• Burke B, Stewart CL. The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol. 2013;14:13–24.
   PubMed Web of Science ®Google Scholar
• Solovei I, Wang AS, Thanisch K, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell. 2013;152:584–598.
   PubMed Web of Science ®Google Scholar
• Mattout A, Pike BL, Towbin BD, et al. An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr Biol. 2011;21:1603–1614.
   PubMed Web of Science ®Google Scholar
• Kind J, van Steensel B. Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol. 2010;22:320–325.
   PubMed Web of Science ®Google Scholar
• Dauer WT, Worman HJ. The nuclear envelope as a signaling node in development and disease. Dev Cell. 2009;17:626–638.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Bravo V, Pippa R, Song W-M, et al. Nuclear pores promote lethal prostate cancer by increasing POM121-driven E2F1, MYC, and AR nuclear import. Cell. 2018;174:1200–1215.e20.
   PubMed Web of Science ®Google Scholar
• Heessen S, Fornerod M. The inner nuclear envelope as a transcription factor resting place. EMBO Rep. 2007;8:914–919.
   PubMed Web of Science ®Google Scholar
• Görlich D, Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol. 1999;15:607–660.
   PubMed Web of Science ®Google Scholar
• BARNES BG, DAVIS JM. The structure of nuclear pores in mammalian tissue. J Ultrastruct Res. 1959;3:131–146.
   PubMedGoogle Scholar
• Fahrenkrog B, Aebi U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat Rev Mol Cell Biol. 2003;4:757–766.
   PubMed Web of Science ®Google Scholar
• Callan HG, Tomlin SG. Experimental studies on amphibian oocyte nuclei. I. Investigation of the structure of the nuclear membrane by means of the electron microscope. 1950;137:367–378. Proc R Soc London Ser B, Biol Sci.
   PubMed Web of Science ®Google Scholar
• Goldstein L. Localization of nucleusspecific protein as shown by transplantation experiments in Amoeba proteus. Exp Cell Res. 1958;15:635–637.
   PubMed Web of Science ®Google Scholar
• Borer RA, Lehner CF, Eppenberger HM, et al. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 1989;56:379–390.
   PubMed Web of Science ®Google Scholar
• Beck M, Hurt E. The nuclear pore complex: understanding its function through structural insight. Nat Rev Mol Cell Biol. 2016;18:73–89.
   PubMed Web of Science ®Google Scholar
• Schwartz TU. Modularity within the architecture of the nuclear pore complex. Curr Opin Struct Biol. 2005;15:221–226.
   PubMed Web of Science ®Google Scholar
• Cautain B, Hill R, De Pedro N, et al. Components and regulation of nuclear transport processes. Febs J. 2015;282:445–462.
   PubMed Web of Science ®Google Scholar
• Grossman E, Medalia O, Zwerger M. Functional architecture of the nuclear pore complex. Annu Rev Biophys. 2012;41:557–584.
   PubMed Web of Science ®Google Scholar
• Neumann N, Lundin D, Poole AM. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One. 2010;5:e13241.
   PubMed Web of Science ®Google Scholar
• Hoelz A, Debler EW, Blobel G. The structure of the nuclear pore complex. Annu Rev Biochem. 2011;80:613–643.
   PubMed Web of Science ®Google Scholar
• Fu X, Liang C, Li F, et al. The rules and functions of nucleocytoplasmic shuttling proteins. Int J Mol Sci. 2018;19:1445.
   Web of Science ®Google Scholar
• Benarroch EE. Nucleocytoplasmic transport: mechanisms and involvement in neurodegenerative disease. Neurology. 2019;92:757–764.
   PubMed Web of Science ®Google Scholar
• Mor A, White MA, Fontoura BMA. Nuclear trafficking in health and disease. Curr Opin Cell Biol. 2014;28:28–35.
   PubMed Web of Science ®Google Scholar
• Hung MC, Link W. Protein localization in disease and therapy. J Cell Sci. 2011;124:3381–3392.
   PubMed Web of Science ®Google Scholar
• Hill R, Cautain B, De Pedro N, et al. Targeting nucleocytoplasmic transport in cancer therapy. Oncotarget. 2014;5:11–28.
   PubMedGoogle Scholar
• Boehringer A, Bowser R. RNA nucleocytoplasmic transport defects in neurodegenerative diseases. In: Advances in neurobiology. Cham: Springer; 2018. p. 85–101.
   Google Scholar
• Fahrenkrog B, Harel A. Perturbations in traffic: aberrant nucleocytoplasmic transport at the heart of neurodegeneration. Cells. 2018;7:232.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Taylor JP. Lost in transportation: nucleocytoplasmic transport defects in ALS and other neurodegenerative diseases. Neuron. 2017;96:285–297.
   PubMed Web of Science ®Google Scholar
• Veldman MB, Yang XW. Huntington’s disease: nuclear gatekeepers under attack. Neuron. 2017;94:1–4.
   PubMed Web of Science ®Google Scholar
• Stade K, Ford CS, Guthrie C, et al. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell. 1997;90:1041–1050.
   PubMed Web of Science ®Google Scholar
• Fukuda M, Asano S, Nakamura T, et al. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature. 1997;390:308–311.
   PubMed Web of Science ®Google Scholar
• Adachi Y, Yanagida M. Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J Cell Biol. 1989;108:1195–1207.
   PubMed Web of Science ®Google Scholar
• Dong X, Biswas A, Süel KE, et al. Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature. 2009;458:1136–1141.
   PubMed Web of Science ®Google Scholar
• Andrade MA, Bork P. HEAT repeats in the Huntington’s disease protein. Nat Genet. 1995;11:115–116.
   PubMed Web of Science ®Google Scholar
• Fox AM, Ciziene D, McLaughlin SH, et al. Electrostatic interactions involving the extreme C terminus of nuclear export factor CRM1 modulate its affinity for cargo. J Biol Chem. 2011;286:29325–29335.
   PubMed Web of Science ®Google Scholar
• Dong X, Biswas A, Chook YM. Structural basis for assembly and disassembly of the CRM1 nuclear export complex. Nat Struct Mol Biol. 2009;16:558–560.
   PubMed Web of Science ®Google Scholar
• Güttler T, Madl T, Neumann P, et al. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat Struct Mol Biol. 2010;17:1367–1376.
   PubMed Web of Science ®Google Scholar
• Monecke T, Güttler T, Neumann P, et al. Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science. 2009;324:1087–1091.
   PubMed Web of Science ®Google Scholar
• Dian C, Bernaudat F, Langer K, et al. Structure of a truncation mutant of the nuclear export factor CRM1 provides insights into the auto-inhibitory role of its C-terminal helix. Structure. 2013;21:1338–1349.
   PubMed Web of Science ®Google Scholar
• Benzeno S, Lu F, Guo M, et al. Identification of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene. 2006;25:6291–6303.
   PubMed Web of Science ®Google Scholar
• Sasaki T, Kojima H, Kishimoto R, et al. Spatiotemporal regulation of c-Fos by ERK5 and the E3 ubiquitin ligase UBR1, and its biological role. Mol Cell. 2006;24:63–75.
   PubMed Web of Science ®Google Scholar
• Hutten S, Kehlenbach RH. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol. 2007;17:193–201.
   PubMed Web of Science ®Google Scholar
• Nemergut ME, Lindsay ME, Brownawell AM, et al. Ran-binding protein 3 links Crm1 to the Ran guanine nucleotide exchange factor. J Biol Chem. 2002;277:17385–17388.
   PubMedGoogle Scholar
• Lindsay ME, Holaska JM, Welch K, et al. Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J Cell Biol. 2001;153:1391–1402.
   PubMed Web of Science ®Google Scholar
• Englmeier L, Fornerod M, Bischoff FR, et al. RanBP3 influences interactions between CRM1 and its nuclear protein export substrates. EMBO Rep. 2001;2:926–932.
   PubMed Web of Science ®Google Scholar
• Hutten S, Kehlenbach RH. Nup214 is required for CRM1-dependent nuclear protein export in vivo. Mol Cell Biol. 2006;26:6772–6785.
   PubMed Web of Science ®Google Scholar
• Walther TC, Pickersgill HS, Cordes VC, et al. The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J Cell Biol. 2002;158:63–77.
   PubMed Web of Science ®Google Scholar
• Kehlenbach RH, Dickmanns A, Kehlenbach A, et al. A role for RanBP1 in the release of CRM1 from the nuclear pore complex in a terminal step of nuclear export. J Cell Biol. 1999;145:645–657.
   PubMed Web of Science ®Google Scholar
• Gravina GL, Senapedis W, McCauley D, et al. Nucleo-cytoplasmic transport as a therapeutic target of cancer. J Hematol Oncol. 2014;7:85.
   PubMed Web of Science ®Google Scholar
• Kudo N, Matsumori N, Taoka H, et al. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci U S A. 1999;96:9112–9117.
   PubMed Web of Science ®Google Scholar
• Lapalombella R, Sun Q, Williams K, et al. Selective inhibitors of nuclear export show that CRM1/XPO1 is a target in chronic lymphocytic leukemia. Blood. 2012;120:4621–4634.
   PubMed Web of Science ®Google Scholar
• Conforti F, Wang Y, Rodriguez JA, et al. Molecular pathways: anticancer activity by inhibition of nucleocytoplasmic shuttling. Clin Cancer Res. 2015;21:4508–4513.
   PubMed Web of Science ®Google Scholar
• Moon S, Yeon Park S, Woo Park H. Regulation of the Hippo pathway in cancer biology. Cell Mol Life Sci. 2018;75:2303–2319.
   PubMed Web of Science ®Google Scholar
• Yu FX, Guan KL. The Hippo pathway: regulators and regulations. Genes Dev. 2013;27:355–371.
   PubMed Web of Science ®Google Scholar
• Hergovich A, Stegert MR, Schmitz D, et al. NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol. 2006;7:253–264.
   PubMed Web of Science ®Google Scholar
• Moroishi T, Hansen CG, Guan KL. The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer. 2015;15:73–79.
   PubMed Web of Science ®Google Scholar
• Hong W, Guan KL. The YAP and TAZ transcription co-activators: key downstream effectors of the mammalian Hippo pathway. Semin Cell Dev Biol. 2012;23:785–793.
   PubMed Web of Science ®Google Scholar
• Meng Z, Moroishi T, Guan K-L. Mechanisms of Hippo pathway regulation. Genes Dev. 2016;30:1–17.
   PubMed Web of Science ®Google Scholar
• Meng Z, Moroishi T, Mottier-Pavie V, et al. MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat Commun. 2015;6. DOI:10.1038/ncomms9357.
   Web of Science ®Google Scholar
• Zhang L, Tang F, Terracciano L, et al. NDR functions as a physiological YAP1 kinase in the intestinal epithelium. Curr Biol. 2015;25:296–305.
   PubMed Web of Science ®Google Scholar
• Bichsel SJ, Tamaskovic R, Stegert MR, et al. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J Biol Chem. 2004;279:35228–35235.
   PubMed Web of Science ®Google Scholar
• Tamaskovic R, Bichsel SJ, Rogniaux H, et al. Mechanism of Ca2+-mediated regulation of NDR protein kinase through autophosphorylation and phosphorylation by an upstream kinase. J Biol Chem. 2003;278:6710–6718.
   PubMed Web of Science ®Google Scholar
• Stegert MR, Tamaskovic R, Bichsel SJ, et al. Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calcium-binding protein. J Biol Chem. 2004;279:23806–23812.
   PubMedGoogle Scholar
• Stegert MR, Hergovich A, Tamaskovic R, et al. Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol Cell Biol. 2005;25:11019–11029.
   PubMed Web of Science ®Google Scholar
• Hergovich A. The roles of NDR protein kinases in hippo signalling. Genes (Basel). 2016;7:21.
   PubMed Web of Science ®Google Scholar
• Hergovich A. Regulation and functions of mammalian LATS/NDR kinases: looking beyond canonical Hippo signalling. Cell Biosci. 2013;3:32.
   PubMed Web of Science ®Google Scholar
• Selimoglu R, Bettoun A, Joffre C, et al. RalA GTPase and MAP4K4 function through NDR1 activation in stress response and apoptotic signaling. HSOA J Cell Biol Cell Metab. 2014;1: 1–11.
   Google Scholar
• Cook D, Hoa LY, Gomez V, et al. Constitutively active NDR1-PIF kinase functions independent of MST1 and hMOB1 signalling. Cell Signal. 2014;26:1657–1667.
   PubMed Web of Science ®Google Scholar
• Johnson LN, Noble MEM, Owen DJ. Active and inactive protein kinases: structural basis for regulation. Cell. 1996;85:149–158.
   PubMed Web of Science ®Google Scholar
• Hergovich A, Lamla S, Nigg EA, et al. Centrosome-associated NDR kinase regulates centrosome duplication. Mol Cell. 2007;25:625–634.
   PubMed Web of Science ®Google Scholar
• Cornils H, Kohler RS, Hergovich A, et al. Downstream of human NDR kinases: impacting on c-myc and p21 protein stability to control cell cycle progression. Cell Cycle. 2011;10:1897–1904.
   PubMed Web of Science ®Google Scholar
• Du Z, Tong X, Ye X. Cyclin D1 promotes cell cycle progression through enhancing NDR1/2 kinase activity independent of cyclin-dependent kinase. J Biol Chem. 2013;288:26678–26687.
   PubMed Web of Science ®Google Scholar
• Fukasawa T, Enomoto A, Miyagawa K. Serine-threonine kinase 38 regulates CDC25A stability and the DNA damage-induced G2/M checkpoint. Cell Signal. 2015;27:1569–1575.
   PubMed Web of Science ®Google Scholar
• Shi DD, Shi H, Lu D, et al. NDR1/STK38 potentiates NF-kB activation by its kinase activity. Cell Biochem Funct. 2012;30:664–670.
   PubMed Web of Science ®Google Scholar
• Joffre C, Dupont N, Hoa L, et al. The pro-apoptotic STK38 kinase is a new beclin1 partner positively regulating autophagy. Curr Biol. 2015;25:1–14.
   Web of Science ®Google Scholar
• Bettoun A, Joffre C, Parrini MC, et al. Mitochondrial clearance by the STK38 kinase supports oncogenic Ras-induced cell transformation. Oncotarget. 2016;7(28):44142–44160. .
   PubMedGoogle Scholar
• Rhee H-W, Zou P, Udeshi ND, et al. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science. 2013;339:1328–1331.
   Google Scholar
• Hung V, Udeshi ND, Lam SS, et al. Spatially resolved proteomic mapping in living cells with the engineered peroxidase APEX2. Nat Protoc. 2016;11:456–475.
   PubMed Web of Science ®Google Scholar
• Beausoleil SA, Jedrychowski M, Schwartz D, et al. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci. 2004;101:12130–12135.
   PubMed Web of Science ®Google Scholar
• Mertins P, Mani DR, Ruggles KV, et al. Proteogenomics connects somatic mutations to signalling in breast cancer. Nature. 2016;534:55–62.
   PubMed Web of Science ®Google Scholar
• Mertins P, Yang F, Liu T, et al. Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol Cell Proteomics. 2014;13:1690–1704.
   PubMed Web of Science ®Google Scholar
• Sharma K, D’Souza RCJ, Tyanova S, et al. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014;8:1583–1594.
   PubMed Web of Science ®Google Scholar
• Fung HYJ, Chook YM. Atomic basis of CRM1-cargo recognition, release and inhibition. Semin Cancer Biol. 2014;27:52–61.
   PubMed Web of Science ®Google Scholar
• Kirli K, Karaca S, Dehne HJ, et al. A deep proteomics perspective on CRM1-mediated nuclear export and nucleocytoplasmic partitioning. Elife. 2015;4:1–28.
   Web of Science ®Google Scholar
• Poon IKH, Jans DA. Regulation of nuclear transport: central role in development and transformation? Traffic. 2005;6:173–186.
   PubMed Web of Science ®Google Scholar
• Craig E, Zhang Z-K, Davies KP, et al. A masked NES in INI1/hSNF5 mediates hCRM1-dependent nuclear export: implications for tumorigenesis. Embo J. 2002;21:31–42.
   PubMed Web of Science ®Google Scholar
• Zhao X, Gan L, Pan H, et al. Multiple elements regulate nuclear/cytoplasmic shuttling of FOXO1: characterization of phosphorylation- and 14-3-3-dependent and -independent mechanisms. Biochem J. 2004;378:839–849.
   PubMed Web of Science ®Google Scholar
• Neggers JE, Vercruysse T, Jacquemyn M, et al. Identifying drug-target selectivity of small-molecule CRM1/XPO1 inhibitors by CRISPR/Cas9 genome editing. Chem Biol. 2015;22:107–116.
   PubMedGoogle Scholar