Lmo4 Deficiency Enhances Susceptibility to Cisplatin-Induced Cochlear Apoptosis and Hearing Loss.

Adaptor Proteins, Signal Transducing / genetics Animals Apoptosis / drug effects Cisplatin / adverse effects Cochlea / pathology Evoked Potentials, Auditory, Brain Stem / drug effects Genetic Predisposition to Disease Hearing Loss / chemically induced LIM Domain Proteins / genetics Mice Mice, Knockout
Cisplatin Cochlea Hearing loss LMO4 Ototoxicity STAT3

Journal

Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963

Informations de publication

Date de publication:
May 2021
Historique:
received: 18 06 2020
accepted: 24 11 2020
pubmed: 8 1 2021
medline: 20 11 2021
entrez: 7 1 2021
Statut: ppublish

Résumé

Cisplatin, a potent chemotherapeutic drug, induces ototoxicity, which limits its clinical utility. Cisplatin-induced oxidative stress plays a causal role in cochlear apoptosis while the consequent nitrative stress leads to the nitration of LIM domain only 4 (LMO4), a transcriptional regulator, and decreases its cochlear expression levels. Here, we show a direct link between cochlear LMO4 and cisplatin-induced hearing loss by employing a Lmo4 conditional knockout mouse model (Lmo4

Identifiants

DOI: 10.1007/s12035-020-02226-4 PMID: 33411315 PMC: PMC8026651
pubmed: 33411315
doi: 10.1007/s12035-020-02226-4
pii: 10.1007/s12035-020-02226-4
pmc: PMC8026651
mid: NIHMS1661194
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
LIM Domain Proteins 0
Lmo4 protein, mouse 0
Cisplatin Q20Q21Q62J

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2019-2029

Subventions

Organisme : NIEHS NIH HHS
ID : K01 ES028750
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES020957
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC016835
Pays : United States
Organisme : Wayne State University
ID : Faculty Start-up

Références

Travis LB, Fossa SD, Sesso HD, Frisina RD, Herrmann DN, Beard CJ, Feldman DR, Pagliaro LC et al (2014) Chemotherapy-induced peripheral neurotoxicity and ototoxicity: new paradigms for translational genomics. J Natl Cancer Inst 106(5):dju044. https://doi.org/10.1093/jnci/dju044
doi: 10.1093/jnci/dju044 pubmed: 24623533 pmcid: 4568989
Breglio AM, Rusheen AE, Shide ED, Fernandez KA, Spielbauer KK, McLachlin KM, Hall MD, Amable L et al (2017) Cisplatin is retained in the cochlea indefinitely following chemotherapy. Nat Commun 8(1):1654. https://doi.org/10.1038/s41467-017-01837-1
doi: 10.1038/s41467-017-01837-1 pubmed: 29162831 pmcid: 5698400
Brock PR, Knight KR, Freyer DR, Campbell KC, Steyger PS, Blakley BW, Rassekh SR, Chang KW et al (2012) Platinum-induced ototoxicity in children: a consensus review on mechanisms, predisposition, and protection, including a new International Society of Pediatric Oncology Boston ototoxicity scale. J Clin Oncol 30(19):2408–2417. https://doi.org/10.1200/JCO.2011.39.1110
doi: 10.1200/JCO.2011.39.1110 pubmed: 22547603 pmcid: 3675696
Langer T, am Zehnhoff-Dinnesen A, Radtke S, Meitert J, Zolk O (2013) Understanding platinum-induced ototoxicity. Trends Pharmacol Sci 34(8):458–469. https://doi.org/10.1016/j.tips.2013.05.006
doi: 10.1016/j.tips.2013.05.006 pubmed: 23769626
Rybak LP, Whitworth CA, Mukherjea D, Ramkumar V (2007) Mechanisms of cisplatin-induced ototoxicity and prevention. Hear Res 226(1–2):157–167. https://doi.org/10.1016/j.heares.2006.09.015
doi: 10.1016/j.heares.2006.09.015 pubmed: 17113254
Ruhl D, Du TT, Wagner EL, Choi JH, Li S, Reed R, Kim K, Freeman M et al (2019) Necroptosis and apoptosis contribute to cisplatin and aminoglycoside ototoxicity. J Neurosci 39(15):2951–2964. https://doi.org/10.1523/JNEUROSCI.1384-18.2019
doi: 10.1523/JNEUROSCI.1384-18.2019 pubmed: 30733218 pmcid: 6462451
Jamesdaniel S (2014) Downstream targets of Lmo4 are modulated by cisplatin in the inner ear of Wistar rats. PLoS One 9(12):e115263. https://doi.org/10.1371/journal.pone.0115263
doi: 10.1371/journal.pone.0115263 pubmed: 25501662 pmcid: 4264883
Jamesdaniel S, Coling D, Hinduja S, Ding D, Li J, Cassidy L, Seigel GM, Qu J et al (2012) Cisplatin-induced ototoxicity is mediated by nitroxidative modification of cochlear proteins characterized by nitration of Lmo4. J Biol Chem 287(22):18674–18686. https://doi.org/10.1074/jbc.M111.297960
doi: 10.1074/jbc.M111.297960 pubmed: 22493493 pmcid: 3365719
Rosati R, Shahab M, Neumann WL, Jamesdaniel S (2019) Inhibition of protein nitration prevents cisplatin-induced inactivation of STAT3 and promotes anti-apoptotic signaling in organ of Corti cells. Exp Cell Res 381(1):105–111. https://doi.org/10.1016/j.yexcr.2019.05.008
doi: 10.1016/j.yexcr.2019.05.008 pubmed: 31078568 pmcid: 6546436
Rathinam R, Ghosh S, Neumann WL, Jamesdaniel S (2015) Cisplatin-induced apoptosis in auditory, renal, and neuronal cells is associated with nitration and downregulation of LMO4. Cell Death Discov 1. https://doi.org/10.1038/cddiscovery.2015.52
Deng M, Luo XJ, Pan L, Yang H, Xie X, Liang G, Huang L, Hu F et al (2014) LMO4 functions as a negative regulator of sensory organ formation in the mammalian cochlea. J Neurosci 34(30):10072–10077. https://doi.org/10.1523/JNEUROSCI.0352-14.2014
doi: 10.1523/JNEUROSCI.0352-14.2014 pubmed: 25057208 pmcid: 4107398
Chen HH, Schock SC, Xu J, Safarpour F, Thompson CS, Stewart AF (2007) Extracellular ATP-dependent upregulation of the transcription cofactor LMO4 promotes neuron survival from hypoxia. Exp Cell Res 313(14):3106–3116. https://doi.org/10.1016/j.yexcr.2007.04.026
doi: 10.1016/j.yexcr.2007.04.026 pubmed: 17524392
Tian Y, Wang N, Lu Z (2010) Repression of Lim only protein 4-activated transcription inhibits proliferation and induces apoptosis of normal mammary epithelial cells and breast cancer cells. Clin Exp Metastasis 27(7):455–463. https://doi.org/10.1007/s10585-010-9332-1
doi: 10.1007/s10585-010-9332-1 pubmed: 20526802
Jamesdaniel S, Rathinam R, Neumann WL (2016) Targeting nitrative stress for attenuating cisplatin-induced downregulation of cochlear LIM domain only 4 and ototoxicity. Redox Biol 10:257–265. https://doi.org/10.1016/j.redox.2016.10.016
doi: 10.1016/j.redox.2016.10.016 pubmed: 27821327 pmcid: 5099269
Rathinam R, Rosati R, Jamesdaniel S (2018) CRISPR/Cas9-mediated knockout of Lim-domain only four retards organ of Corti cell growth. J Cell Biochem 119(4):3545–3553. https://doi.org/10.1002/jcb.26529
doi: 10.1002/jcb.26529 pubmed: 29143984 pmcid: 6366322
Novotny-Diermayr V, Lin B, Gu L, Cao X (2005) Modulation of the interleukin-6 receptor subunit glycoprotein 130 complex and its signaling by LMO4 interaction. J Biol Chem 280(13):12747–12757. https://doi.org/10.1074/jbc.M500175200
doi: 10.1074/jbc.M500175200 pubmed: 15677447
Schock SC, Xu J, Duquette PM, Qin Z, Lewandowski AJ, Rai PS, Thompson CS, Seifert EL et al (2008) Rescue of neurons from ischemic injury by peroxisome proliferator-activated receptor-gamma requires a novel essential cofactor LMO4. J Neurosci 28(47):12433–12444. https://doi.org/10.1523/JNEUROSCI.2897-08.2008
doi: 10.1523/JNEUROSCI.2897-08.2008 pubmed: 19020036 pmcid: 2954187
Setogawa T, Shinozaki-Yabana S, Masuda T, Matsuura K, Akiyama T (2006) The tumor suppressor LKB1 induces p21 expression in collaboration with LMO4, GATA-6, and Ldb1. Biochem Biophys Res Commun 343(4):1186–1190. https://doi.org/10.1016/j.bbrc.2006.03.077
doi: 10.1016/j.bbrc.2006.03.077 pubmed: 16580634
Wang N, Lin KK, Lu Z, Lam KS, Newton R, Xu X, Yu Z, Gill GN et al (2007) The LIM-only factor LMO4 regulates expression of the BMP7 gene through an HDAC2-dependent mechanism, and controls cell proliferation and apoptosis of mammary epithelial cells. Oncogene 26(44):6431–6441. https://doi.org/10.1038/sj.onc.1210465
doi: 10.1038/sj.onc.1210465 pubmed: 17452977
Levano S, Bodmer D (2015) Loss of STAT1 protects hair cells from ototoxicity through modulation of STAT3, c-Jun, Akt, and autophagy factors. Cell Death Dis 6:e2019. https://doi.org/10.1038/cddis.2015.362
doi: 10.1038/cddis.2015.362 pubmed: 26673664 pmcid: 4720895
Schmitt NC, Rubel EW, Nathanson NM (2009) Cisplatin-induced hair cell death requires STAT1 and is attenuated by epigallocatechin gallate. J Neurosci 29(12):3843–3851. https://doi.org/10.1523/JNEUROSCI.5842-08.2009
doi: 10.1523/JNEUROSCI.5842-08.2009 pubmed: 19321781 pmcid: 2707781
Kaur T, Mukherjea D, Sheehan K, Jajoo S, Rybak LP, Ramkumar V (2011) Short interfering RNA against STAT1 attenuates cisplatin-induced ototoxicity in the rat by suppressing inflammation. Cell Death Dis 2:e180. https://doi.org/10.1038/cddis.2011.63
doi: 10.1038/cddis.2011.63 pubmed: 21776018 pmcid: 3199718
Stephanou A, Latchman DS (2005) Opposing actions of STAT-1 and STAT-3. Growth Factors 23(3):177–182. https://doi.org/10.1080/08977190500178745
doi: 10.1080/08977190500178745 pubmed: 16243709
Hu X, Ivashkiv LB (2009) Cross-regulation of signaling pathways by interferon-gamma: Implications for immune responses and autoimmune diseases. Immunity 31(4):539–550. https://doi.org/10.1016/j.immuni.2009.09.002
doi: 10.1016/j.immuni.2009.09.002 pubmed: 19833085 pmcid: 2774226
Deng M, Pan L, Xie X, Gan L (2010) Requirement for Lmo4 in the vestibular morphogenesis of mouse inner ear. Dev Biol 338(1):38–49. https://doi.org/10.1016/j.ydbio.2009.11.003
doi: 10.1016/j.ydbio.2009.11.003 pubmed: 19913004
Hughes AL, Hussain N, Pafford R, Parham K (2014) Dexamethasone otoprotection in a multidose cisplatin ototoxicity mouse model. Otolaryngol Head Neck Surg 150(1):115–120. https://doi.org/10.1177/0194599813511948
doi: 10.1177/0194599813511948 pubmed: 24233060
Berndtsson M, Hagg M, Panaretakis T, Havelka AM, Shoshan MC, Linder S (2007) Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int J Cancer 120(1):175–180. https://doi.org/10.1002/ijc.22132
doi: 10.1002/ijc.22132 pubmed: 17044026
More SS, Akil O, Ianculescu AG, Geier EG, Lustig LR, Giacomini KM (2010) Role of the copper transporter, CTR1, in platinum-induced ototoxicity. J Neurosci 30(28):9500–9509. https://doi.org/10.1523/JNEUROSCI.1544-10.2010
doi: 10.1523/JNEUROSCI.1544-10.2010 pubmed: 20631178 pmcid: 2949060
Thomas AJ, Hailey DW, Stawicki TM, Wu P, Coffin AB, Rubel EW, Raible DW, Simon JA et al (2013) Functional mechanotransduction is required for cisplatin-induced hair cell death in the zebrafish lateral line. J Neurosci 33(10):4405–4414. https://doi.org/10.1523/JNEUROSCI.3940-12.2013
doi: 10.1523/JNEUROSCI.3940-12.2013 pubmed: 23467357 pmcid: 3666553
Kaur T, Borse V, Sheth S, Sheehan K, Ghosh S, Tupal S, Jajoo S, Mukherjea D et al (2016) Adenosine A1 receptor protects against cisplatin ototoxicity by suppressing the NOX3/STAT1 inflammatory pathway in the cochlea. J Neurosci 36(14):3962–3977. https://doi.org/10.1523/JNEUROSCI.3111-15.2016
doi: 10.1523/JNEUROSCI.3111-15.2016 pubmed: 27053204 pmcid: 4821909
Park HJ, Kim MJ, Rothenberger C, Kumar A, Sampson EM, Ding D, Han C, White K et al (2019) GSTA4 mediates reduction of cisplatin ototoxicity in female mice. Nat Commun 10(1):4150. https://doi.org/10.1038/s41467-019-12073-0
doi: 10.1038/s41467-019-12073-0 pubmed: 31515474 pmcid: 6742643
Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH (2004) NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 279(44):46065–46072. https://doi.org/10.1074/jbc.M403046200
doi: 10.1074/jbc.M403046200 pubmed: 15326186
Li G, Liu W, Frenz D (2006) Cisplatin ototoxicity to the rat inner ear: A role for HMG1 and iNOS. Neurotoxicology 27(1):22–30. https://doi.org/10.1016/j.neuro.2005.05.010
doi: 10.1016/j.neuro.2005.05.010 pubmed: 16125245
Watanabe K, Inai S, Jinnouchi K, Bada S, Hess A, Michel O, Yagi T (2002) Nuclear-factor kappa B (NF-kappa B)-inducible nitric oxide synthase (iNOS/NOS II) pathway damages the stria vascularis in cisplatin-treated mice. Anticancer Res 22(6C):4081–4085
pubmed: 12553036
Jamesdaniel S, Ding D, Kermany MH, Davidson BA, Knight PR 3rd, Salvi R, Coling DE (2008) Proteomic analysis of the balance between survival and cell death responses in cisplatin-mediated ototoxicity. J Proteome Res 7(8):3516–3524. https://doi.org/10.1021/pr8002479
doi: 10.1021/pr8002479 pubmed: 18578524 pmcid: 2570323
Low IC, Loh T, Huang Y, Virshup DM, Pervaiz S (2014) Ser70 phosphorylation of Bcl-2 by selective tyrosine nitration of PP2A-B56delta stabilizes its antiapoptotic activity. Blood 124(14):2223–2234. https://doi.org/10.1182/blood-2014-03-563296
doi: 10.1182/blood-2014-03-563296 pubmed: 25082878
Joshi MS, Mihm MJ, Cook AC, Schanbacher BL, Bauer JA (2015) Alterations in connexin 43 during diabetic cardiomyopathy: Competition of tyrosine nitration versus phosphorylation. J Diabetes 7(2):250–259. https://doi.org/10.1111/1753-0407.12164
doi: 10.1111/1753-0407.12164 pubmed: 24796789
Franco MC, Ye Y, Refakis CA, Feldman JL, Stokes AL, Basso M, Melero Fernandez de Mera RM, Sparrow NA et al (2013) Nitration of Hsp90 induces cell death. Proc Natl Acad Sci U S A 110(12):E1102–E1111. https://doi.org/10.1073/pnas.1215177110
doi: 10.1073/pnas.1215177110 pubmed: 23487751 pmcid: 3607042
Venkatesan A, Uzasci L, Chen Z, Rajbhandari L, Anderson C, Lee MH, Bianchet MA, Cotter R et al (2011) Impairment of adult hippocampal neural progenitor proliferation by methamphetamine: Role for nitrotyrosination. Mol Brain 4:28. https://doi.org/10.1186/1756-6606-4-28
doi: 10.1186/1756-6606-4-28 pubmed: 21708025 pmcid: 3142219
Curry-McCoy TV, Osna NA, Donohue TM Jr (2009) Modulation of lysozyme function and degradation after nitration with peroxynitrite. Biochim Biophys Acta 1790(8):778–786. https://doi.org/10.1016/j.bbagen.2009.04.008
doi: 10.1016/j.bbagen.2009.04.008 pubmed: 19376194 pmcid: 2706308
Souza JM, Choi I, Chen Q, Weisse M, Daikhin E, Yudkoff M, Obin M, Ara J et al (2000) Proteolytic degradation of tyrosine nitrated proteins. Arch Biochem Biophys 380(2):360–366. https://doi.org/10.1006/abbi.2000.1940
doi: 10.1006/abbi.2000.1940 pubmed: 10933892
Sum EY, Peng B, Yu X, Chen J, Byrne J, Lindeman GJ, Visvader JE (2002) The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J Biol Chem 277(10):7849–7856. https://doi.org/10.1074/jbc.M110603200
doi: 10.1074/jbc.M110603200 pubmed: 11751867
Manetopoulos C, Hansson A, Karlsson J, Jonsson JI, Axelson H (2003) The LIM-only protein LMO4 modulates the transcriptional activity of HEN1. Biochem Biophys Res Commun 307(4):891–899. https://doi.org/10.1016/s0006-291x(03)01298-1
doi: 10.1016/s0006-291x(03)01298-1 pubmed: 12878195
Singh RR, Barnes CJ, Talukder AH, Fuqua SA, Kumar R (2005) Negative regulation of estrogen receptor alpha transactivation functions by LIM domain only 4 protein. Cancer Res 65(22):10594–10601. https://doi.org/10.1158/0008-5472.CAN-05-2268
doi: 10.1158/0008-5472.CAN-05-2268 pubmed: 16288053
Charitidi K, Meltser I, Tahera Y, Canlon B (2009) Functional responses of estrogen receptors in the male and female auditory system. Hear Res 252(1–2):71–78. https://doi.org/10.1016/j.heares.2008.12.009
doi: 10.1016/j.heares.2008.12.009 pubmed: 19450435
Yamamoto T, Matsuda T, Junicho A, Kishi H, Saatcioglu F, Muraguchi A (2000) Cross-talk between signal transducer and activator of transcription 3 and estrogen receptor signaling. FEBS Lett 486(2):143–148. https://doi.org/10.1016/s0014-5793(00)02296-1
doi: 10.1016/s0014-5793(00)02296-1 pubmed: 11113455
Garcia-Berrocal JR, Nevado J, Ramirez-Camacho R, Sanz R, Gonzalez-Garcia JA, Sanchez-Rodriguez C, Cantos B, Espana P et al (2007) The anticancer drug cisplatin induces an intrinsic apoptotic pathway inside the inner ear. Br J Pharmacol 152(7):1012–1020. https://doi.org/10.1038/sj.bjp.0707405
doi: 10.1038/sj.bjp.0707405 pubmed: 17906689 pmcid: 2095105

Auteurs

Rita Rosati (R)

Institute of Environmental Health Sciences, Wayne State University, 6135 Woodward Avenue, Detroit, MI, 48202, USA.

Monazza Shahab (M)

Institute of Environmental Health Sciences, Wayne State University, 6135 Woodward Avenue, Detroit, MI, 48202, USA.
Department of Pharmacology, Wayne State University, Detroit, MI, 48201, USA.

Vickram Ramkumar (V)

Department of Pharmacology, Southern Illinois University School of Medicine, Springfield, IL, 62794, USA.

Samson Jamesdaniel (S)

Institute of Environmental Health Sciences, Wayne State University, 6135 Woodward Avenue, Detroit, MI, 48202, USA. sjamesdaniel@wayne.edu.
Department of Pharmacology, Wayne State University, Detroit, MI, 48201, USA. sjamesdaniel@wayne.edu.
Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, MI, 48202, USA. sjamesdaniel@wayne.edu.
ORCID: 0000-0002-5269-9007

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Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines adaptatrices de la transduction du signal › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Eucaryotes › Animaux › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Mort cellulaire › Mort cellulaire régulée › Apoptose › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Produits chimiques inorganiques › Composés du platine › Cisplatine › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Organes des sens › Oreille › Oreille interne › Cochlée › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Excitabilité corticale › Potentiels évoqués › Potentiels évoqués auditifs › Potentiels évoqués auditifs du tronc cérébral › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Phénomènes génétiques › Génotype › Prédisposition génétique à une maladie › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › États, signes et symptômes pathologiques › Signes et symptômes › Manifestations neurologiques › Troubles sensitifs › Troubles de l'audition › Perte d'audition › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines à domaine LIM › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lmo4 Deficiency Enhances Susceptibility to...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souris transgéniques › Souris knockout › Lmo4 Deficiency Enhances Susceptibility to...