Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding

Schwarz J, Schmidt S, Will O, Koudelka T, Koehler K, Boss M, Rabe B, Tholey A, Scheller J, Schmidt-Arras D, Schwake M, et al. (2014)
Journal of Biological Chemistry 289(5): 3080-3093.

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Abstract / Bemerkung
Background: The metalloprotease ADAM17 emerged as the main sheddase of several cytokines and cytokine receptors. Results: The acidophilic kinase PLK2 interacts with and phosphorylates ADAM17 in mammalian cells. Conclusion: PLK2 represents a novel cellular interaction partner of ADAM17 modulating its activity. Significance: Regulation of ADAM17 activity is essential for inflammatory responses. ADAM17 (a disintegrin and metalloprotease 17) controls pro- and anti-inflammatory signaling events by promoting ectodomain shedding of cytokine precursors and cytokine receptors. Despite the well documented substrate repertoire of ADAM17, little is known about regulatory mechanisms, leading to substrate recognition and catalytic activation. Here we report a direct interaction of the acidophilic kinase Polo-like kinase 2 (PLK2, also known as SNK) with the cytoplasmic portion of ADAM17 through the C-terminal noncatalytic region of PLK2 containing the Polo box domains. PLK2 activity leads to ADAM17 phosphorylation at serine 794, which represents a novel phosphorylation site. Activation of ADAM17 by PLK2 results in the release of pro-TNF and TNF receptors from the cell surface, and pharmacological inhibition of PLK2 leads to down-regulation of LPS-induced ADAM17-mediated shedding on primary macrophages and dendritic cells. Importantly, PLK2 expression is up-regulated during inflammatory conditions increasing ADAM17-mediated proteolytic events. Our findings suggest a new role for PLK2 in the regulation of inflammatory diseases by modulating ADAM17 activity.
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Journal of Biological Chemistry
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289
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5
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3080-3093
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Schwarz J, Schmidt S, Will O, et al. Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding. Journal of Biological Chemistry. 2014;289(5):3080-3093.
Schwarz, J., Schmidt, S., Will, O., Koudelka, T., Koehler, K., Boss, M., Rabe, B., et al. (2014). Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding. Journal of Biological Chemistry, 289(5), 3080-3093. doi:10.1074/jbc.M113.536847
Schwarz, J., Schmidt, S., Will, O., Koudelka, T., Koehler, K., Boss, M., Rabe, B., Tholey, A., Scheller, J., Schmidt-Arras, D., et al. (2014). Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding. Journal of Biological Chemistry 289, 3080-3093.
Schwarz, J., et al., 2014. Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding. Journal of Biological Chemistry, 289(5), p 3080-3093.
J. Schwarz, et al., “Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding”, Journal of Biological Chemistry, vol. 289, 2014, pp. 3080-3093.
Schwarz, J., Schmidt, S., Will, O., Koudelka, T., Koehler, K., Boss, M., Rabe, B., Tholey, A., Scheller, J., Schmidt-Arras, D., Schwake, M., Rose-John, S., Chalaris, A.: Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding. Journal of Biological Chemistry. 289, 3080-3093 (2014).
Schwarz, Jeanette, Schmidt, Stefanie, Will, Olga, Koudelka, Tomas, Koehler, Kaja, Boss, Melanie, Rabe, Bjoern, Tholey, Andreas, Scheller, Juergen, Schmidt-Arras, Dirk, Schwake, Michael, Rose-John, Stefan, and Chalaris, Athena. “Polo-like Kinase 2, a Novel ADAM17 Signaling Component, Regulates Tumor Necrosis Factor similar to Ectodomain Shedding”. Journal of Biological Chemistry 289.5 (2014): 3080-3093.

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Daten bereitgestellt von Europe PubMed Central.

Rutaecarpine prevents hypertensive cardiac hypertrophy involving the inhibition of Nox4-ROS-ADAM17 pathway.
Zeng SY, Yang L, Lu HQ, Yan QJ, Gao L, Qin XP., J Cell Mol Med 23(6), 2019
PMID: 30953402
Structural and Functional Analyses of the Shedding Protease ADAM17 in HoxB8-Immortalized Macrophages and Dendritic-like Cells.
Cabron AS, El Azzouzi K, Boss M, Arnold P, Schwarz J, Rosas M, Dobert JP, Pavlenko E, Schumacher N, Renné T, Taylor PR, Linder S, Rose-John S, Zunke F., J Immunol 201(10), 2018
PMID: 30355783
The emerging role of ADAM metalloproteinases in immunity.
Lambrecht BN, Vanderkerken M, Hammad H., Nat Rev Immunol 18(12), 2018
PMID: 30242265
The Transcriptome of Estrogen-Independent Mammary Growth in Female Mice Reveals That Not All Mammary Glands Are Created Equally.
Berryhill GE, Lemay DG, Trott JF, Aimo L, Lock AL, Hovey RC., Endocrinology 158(10), 2017
PMID: 28938404
Enhanced ADAM17 expression is associated with cardiac remodeling in rats with acute myocardial infarction.
Zheng DY, Zhao J, Yang JM, Wang M, Zhang XT., Life Sci 151(), 2016
PMID: 26944439
Expression of ADAM17 and ADAM10 in nasal polyps.
Bae WY, Park SK, Kim do H, Koh TK, Hur DY, Chueh HW., Int Forum Allergy Rhinol 6(7), 2016
PMID: 27012683
Phosphatidylserine exposure is required for ADAM17 sheddase function.
Sommer A, Kordowski F, Büch J, Maretzky T, Evers A, Andrä J, Düsterhöft S, Michalek M, Lorenzen I, Somasundaram P, Tholey A, Sönnichsen FD, Kunzelmann K, Heinbockel L, Nehls C, Gutsmann T, Grötzinger J, Bhakdi S, Reiss K., Nat Commun 7(), 2016
PMID: 27161080
A Disintegrin and Metalloprotease 17 in the Cardiovascular and Central Nervous Systems.
Xu J, Mukerjee S, Silva-Alves CR, Carvalho-Galvão A, Cruz JC, Balarini CM, Braga VA, Lazartigues E, França-Silva MS., Front Physiol 7(), 2016
PMID: 27803674
Structural analysis of the polo-box domain of human Polo-like kinase 2.
Kim JH, Ku B, Lee KS, Kim SJ., Proteins 83(7), 2015
PMID: 25846005
Expression profile of ADAM10 and ADAM17 in allergic rhinitis.
Chueh HW, Park SK, Hur DY, Bae WY., Int Forum Allergy Rhinol 5(11), 2015
PMID: 26250527
ADAM17 at the interface between inflammation and autoimmunity.
Lisi S, D'Amore M, Sisto M., Immunol Lett 162(1 pt a), 2014
PMID: 25171914
Amyloid precursor protein regulates migration and metalloproteinase gene expression in prostate cancer cells.
Miyazaki T, Ikeda K, Horie-Inoue K, Inoue S., Biochem Biophys Res Commun 452(3), 2014
PMID: 25218471
GSK3 and Polo-like kinase regulate ADAM13 function during cranial neural crest cell migration.
Abbruzzese G, Cousin H, Salicioni AM, Alfandari D., Mol Biol Cell 25(25), 2014
PMID: 25298404
Identification of the PLK2-dependent phosphopeptidome by quantitative proteomics [corrected].
Franchin C, Cesaro L, Pinna LA, Arrigoni G, Salvi M., PLoS One 9(10), 2014
PMID: 25338102
Identification of multiple DNA copy number alterations including frequent 8p11.22 amplification in conjunctival squamous cell carcinoma.
Asnaghi L, Alkatan H, Mahale A, Othman M, Alwadani S, Al-Hussain H, Jastaneiah S, Yu W, Maktabi A, Edward DP, Eberhart CG., Invest Ophthalmol Vis Sci 55(12), 2014
PMID: 25491297

64 References

Daten bereitgestellt von Europe PubMed Central.

Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme.
Reddy P, Slack JL, Davis R, Cerretti DP, Kozlosky CJ, Blanton RA, Shows D, Peschon JJ, Black RA., J. Biol. Chem. 275(19), 2000
PMID: 10799547
Systematic discovery of TLR signaling components delineates viral-sensing circuits.
Chevrier N, Mertins P, Artyomov MN, Shalek AK, Iannacone M, Ciaccio MF, Gat-Viks I, Tonti E, DeGrace MM, Clauser KR, Garber M, Eisenhaure TM, Yosef N, Robinson J, Sutton A, Andersen MS, Root DE, von Andrian U, Jones RB, Park H, Carr SA, Regev A, Amit I, Hacohen N., Cell 147(4), 2011
PMID: 22078882
Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates.
Elia AE, Cantley LC, Yaffe MB., Science 299(5610), 2003
PMID: 12595692
Silencing of the novel p53 target gene Snk/Plk2 leads to mitotic catastrophe in paclitaxel (taxol)-exposed cells.
Burns TF, Fei P, Scata KA, Dicker DT, El-Deiry WS., Mol. Cell. Biol. 23(16), 2003
PMID: 12897130
Role of Plk2 (Snk) in mouse development and cell proliferation.
Ma S, Charron J, Erikson RL., Mol. Cell. Biol. 23(19), 2003
PMID: 12972611
The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain.
Elia AE, Rellos P, Haire LF, Chao JW, Ivins FJ, Hoepker K, Mohammad D, Cantley LC, Smerdon SJ, Yaffe MB., Cell 115(1), 2003
PMID: 14532005
The crystal structure of the human polo-like kinase-1 polo box domain and its phospho-peptide complex.
Cheng KY, Lowe ED, Sinclair J, Nigg EA, Johnson LN., EMBO J. 22(21), 2003
PMID: 14592974
Polo-like kinases and the orchestration of cell division.
Barr FA, Sillje HH, Nigg EA., Nat. Rev. Mol. Cell Biol. 5(6), 2004
PMID: 15173822
polo, a mitotic mutant of Drosophila displaying abnormal spindle poles.
Sunkel CE, Glover DM., J. Cell. Sci. 89 ( Pt 1)(), 1988
PMID: 3417791
Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor.
Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM., J. Exp. Med. 176(6), 1992
PMID: 1460426
Multimerisation of A disintegrin and metalloprotease protein-17 (ADAM17) is mediated by its EGF-like domain.
Lorenzen I, Trad A, Grotzinger J., Biochem. Biophys. Res. Commun. 415(2), 2011
PMID: 22033402
Benchmarking a luciferase complementation assay for detecting protein complexes.
Cassonnet P, Rolloy C, Neveu G, Vidalain PO, Chantier T, Pellet J, Jones L, Muller M, Demeret C, Gaud G, Vuillier F, Lotteau V, Tangy F, Favre M, Jacob Y., Nat. Methods 8(12), 2011
PMID: 22127214
TACE activation by MAPK-mediated regulation of cell surface dimerization and TIMP3 association.
Xu P, Liu J, Sakaki-Yumoto M, Derynck R., Sci Signal 5(222), 2012
PMID: 22550340
The membrane-proximal domain of A Disintegrin and Metalloprotease 17 (ADAM17) is responsible for recognition of the interleukin-6 receptor and interleukin-1 receptor II.
Lorenzen I, Lokau J, Dusterhoft S, Trad A, Garbers C, Scheller J, Rose-John S, Grotzinger J., FEBS Lett. 586(8), 2012
PMID: 22575642
Investigation on PLK2 and PLK3 substrate recognition.
Salvi M, Trashi E, Cozza G, Franchin C, Arrigoni G, Pinna LA., Biochim. Biophys. Acta 1824(12), 2012
PMID: 22828320
Systemic overexpression of TNFα-converting enzyme does not lead to enhanced shedding activity in vivo.
Yoda M, Kimura T, Tohmonda T, Morioka H, Matsumoto M, Okada Y, Toyama Y, Horiuchi K., PLoS ONE 8(1), 2013
PMID: 23342154
ADAM17, shedding, TACE as therapeutic targets.
Rose-John S., Pharmacol. Res. 71(), 2013
PMID: 23415892
Regulated ADAM17-dependent EGF family ligand release by substrate-selecting signaling pathways.
Dang M, Armbruster N, Miller MA, Cermeno E, Hartmann M, Bell GW, Root DE, Lauffenburger DA, Lodish HF, Herrlich A., Proc. Natl. Acad. Sci. U.S.A. 110(24), 2013
PMID: 23720309
iRhom2 controls the substrate selectivity of stimulated ADAM17-dependent ectodomain shedding.
Maretzky T, McIlwain DR, Issuree PD, Li X, Malapeira J, Amin S, Lang PA, Mak TW, Blobel CP., Proc. Natl. Acad. Sci. U.S.A. 110(28), 2013
PMID: 23801765
Short-term TNFα shedding is independent of cytoplasmic phosphorylation or furin cleavage of ADAM17.
Schwarz J, Broder C, Helmstetter A, Schmidt S, Yan I, Muller M, Schmidt-Arras D, Becker-Pauly C, Koch-Nolte F, Mittrucker HW, Rabe B, Rose-John S, Chalaris A., Biochim. Biophys. Acta 1833(12), 2013
PMID: 24135057
Identification and cloning of a protein kinase-encoding mouse gene, Plk, related to the polo gene of Drosophila.
Clay FJ, McEwen SJ, Bertoncello I, Wilks AF, Dunn AR., Proc. Natl. Acad. Sci. U.S.A. 90(11), 1993
PMID: 8099445
Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing.
Mohler KM, Sleath PR, Fitzner JN, Cerretti DP, Alderson M, Kerwar SS, Torrance DS, Otten-Evans C, Greenstreet T, Weerawarna K., Nature 370(6486), 1994
PMID: 8028669
A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells.
Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, Nelson N, Boiani N, Schooley KA, Gerhart M, Davis R, Fitzner JN, Johnson RS, Paxton RJ, March CJ, Cerretti DP., Nature 385(6618), 1997
PMID: 9034190
Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha.
Moss ML, Jin SL, Milla ME, Bickett DM, Burkhart W, Carter HL, Chen WJ, Clay WC, Didsbury JR, Hassler D, Hoffman CR, Kost TA, Lambert MH, Leesnitzer MA, McCauley P, McGeehan G, Mitchell J, Moyer M, Pahel G, Rocque W, Overton LK, Schoenen F, Seaton T, Su JL, Becherer JD., Nature 385(6618), 1997
PMID: 9034191
Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk.
Lee KS, Grenfell TZ, Yarm FR, Erikson RL., Proc. Natl. Acad. Sci. U.S.A. 95(16), 1998
PMID: 9689075
An essential role for ectodomain shedding in mammalian development.
Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, Russell WE, Castner BJ, Johnson RS, Fitzner JN, Boyce RW, Nelson N, Kozlosky CJ, Wolfson MF, Rauch CT, Cerretti DP, Paxton RJ, March CJ, Black RA., Science 282(5392), 1998
PMID: 9812885
ADAMs: key components in EGFR signalling and development.
Blobel CP., Nat. Rev. Mol. Cell Biol. 6(1), 2005
PMID: 15688065
Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation.
Zhang Q, Thomas SM, Lui VW, Xi S, Siegfried JM, Fan H, Smithgall TE, Mills GB, Grandis JR., Proc. Natl. Acad. Sci. U.S.A. 103(18), 2006
PMID: 16641105
BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo.
Steegmaier M, Hoffmann M, Baum A, Lenart P, Petronczki M, Krssak M, Gurtler U, Garin-Chesa P, Lieb S, Quant J, Grauert M, Adolf GR, Kraut N, Peters JM, Rettig WJ., Curr. Biol. 17(4), 2007
PMID: 17291758
Molecular and structural basis of polo-like kinase 1 substrate recognition: Implications in centrosomal localization.
Garcia-Alvarez B, de Carcer G, Ibanez S, Bragado-Nilsson E, Montoya G., Proc. Natl. Acad. Sci. U.S.A. 104(9), 2007
PMID: 17307877
Structure of the catalytic domain of human polo-like kinase 1.
Kothe M, Kohls D, Low S, Coli R, Cheng AC, Jacques SL, Johnson TL, Lewis C, Loh C, Nonomiya J, Sheils AL, Verdries KA, Wynn TA, Kuhn C, Ding YH., Biochemistry 46(20), 2007
PMID: 17461553
Cutting edge: TNF-alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock.
Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y, Toyama Y, Blobel CP., J. Immunol. 179(5), 2007
PMID: 17709479
Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils.
Chalaris A, Rabe B, Paliga K, Lange H, Laskay T, Fielding CA, Jones SA, Rose-John S, Scheller J., Blood 110(6), 2007
PMID: 17567983
TPL2-mediated activation of ERK1 and ERK2 regulates the processing of pre-TNF alpha in LPS-stimulated macrophages.
Rousseau S, Papoutsopoulou M, Symons A, Cook D, Lucocq JM, Prescott AR, O'Garra A, Ley SC, Cohen P., J. Cell. Sci. 121(Pt 2), 2008
PMID: 18187448
Polo on the Rise-from Mitotic Entry to Cytokinesis with Plk1.
Petronczki M, Lenart P, Peters JM., Dev. Cell 14(5), 2008
PMID: 18477449
Polo-box domains confer target specificity to the Polo-like kinase family.
van de Weerdt BC, Littler DR, Klompmaker R, Huseinovic A, Fish A, Perrakis A, Medema RH., Biochim. Biophys. Acta 1783(6), 2008
PMID: 18359294
Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity.
Seeburg DP, Feliu-Mojer M, Gaiottino J, Pak DT, Sheng M., Neuron 58(4), 2008
PMID: 18498738
Phase I dose escalation and pharmacokinetic study of BI 2536, a novel Polo-like kinase 1 inhibitor, in patients with advanced solid tumors.
Mross K, Frost A, Steinbild S, Hedbom S, Rentschler J, Kaiser R, Rouyrre N, Trommeshauser D, Hoesl CE, Munzert G., J. Clin. Oncol. 26(34), 2008
PMID: 18955456
Polo-like kinases: conservation and divergence in their functions and regulation.
Archambault V, Glover DM., Nat. Rev. Mol. Cell Biol. 10(4), 2009
PMID: 19305416
Phosphorylation of synucleins by members of the Polo-like kinase family.
Mbefo MK, Paleologou KE, Boucharaba A, Oueslati A, Schell H, Fournier M, Olschewski D, Yin G, Zweckstetter M, Masliah E, Kahle PJ, Hirling H, Lashuel HA., J. Biol. Chem. 285(4), 2009
PMID: 19889641
ADAM-17: the enzyme that does it all.
Gooz M., Crit. Rev. Biochem. Mol. Biol. 45(2), 2010
PMID: 20184396
The inflammasomes.
Schroder K, Tschopp J., Cell 140(6), 2010
PMID: 20303873
In vivo role of leukocyte ADAM17 in the inflammatory and host responses during E. coli-mediated peritonitis.
Long C, Wang Y, Herrera AH, Horiuchi K, Walcheck B., J. Leukoc. Biol. 87(6), 2010
PMID: 20154226
Forced homo- and heterodimerization of all gp130-type receptor complexes leads to constitutive ligand-independent signaling and cytokine-independent growth.
Suthaus J, Tillmann A, Lorenzen I, Bulanova E, Rose-John S, Scheller J., Mol. Biol. Cell 21(15), 2010
PMID: 20554759
Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice.
Chalaris A, Adam N, Sina C, Rosenstiel P, Lehmann-Koch J, Schirmacher P, Hartmann D, Cichy J, Gavrilova O, Schreiber S, Jostock T, Matthews V, Hasler R, Becker C, Neurath MF, Reiss K, Saftig P, Scheller J, Rose-John S., J. Exp. Med. 207(8), 2010
PMID: 20603312
Plk2 attachment to NSF induces homeostatic removal of GluA2 during chronic overexcitation.
Evers DM, Matta JA, Hoe HS, Zarkowsky D, Lee SH, Isaac JT, Pak DT., Nat. Neurosci. 13(10), 2010
PMID: 20802490
ADAM17 is regulated by a rapid and reversible mechanism that controls access to its catalytic site.
Le Gall SM, Maretzky T, Issuree PD, Niu XD, Reiss K, Saftig P, Khokha R, Lundell D, Blobel CP., J. Cell. Sci. 123(Pt 22), 2010
PMID: 20980382
Deciphering the human platelet sheddome.
Fong KP, Barry C, Tran AN, Traxler EA, Wannemacher KM, Tang HY, Speicher KD, Blair IA, Speicher DW, Grosser T, Brass LF., Blood 117(1), 2010
PMID: 20962327
Requirement for Plk2 in orchestrated ras and rap signaling, homeostatic structural plasticity, and memory.
Lee KJ, Lee Y, Rozeboom A, Lee JY, Udagawa N, Hoe HS, Pak DT., Neuron 69(5), 2011
PMID: 21382555
TACE (ADAM17) inhibits Schwann cell myelination.
La Marca R, Cerri F, Horiuchi K, Bachi A, Feltri ML, Wrabetz L, Blobel CP, Quattrini A, Salzer JL, Taveggia C., Nat. Neurosci. 14(7), 2011
PMID: 21666671
ADAM17: a molecular switch to control inflammation and tissue regeneration.
Scheller J, Chalaris A, Garbers C, Rose-John S., Trends Immunol. 32(8), 2011
PMID: 21752713
Reactive oxygen species and p38 mitogen-activated protein kinase mediate tumor necrosis factor α-converting enzyme (TACE/ADAM-17) activation in primary human monocytes.
Scott AJ, O'Dea KP, O'Callaghan D, Williams L, Dokpesi JO, Tatton L, Handy JM, Hogg PJ, Takata M., J. Biol. Chem. 286(41), 2011
PMID: 21865167
Radiation-inducible hSNK gene is transcriptionally regulated by p53 binding homology element in human thyroid cells.
Shimizu-Yoshida Y, Sugiyama K, Rogounovitch T, Ohtsuru A, Namba H, Saenko V, Yamashita S., Biochem. Biophys. Res. Commun. 289(2), 2001
PMID: 11716500

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