Advertisement

Molecular and Cellular Biochemistry

, Volume 461, Issue 1–2, pp 103–118 | Cite as

G protein-coupled receptor kinase 5 modifies cancer cell resistance to paclitaxel

  • Joann Lagman
  • Paula Sayegh
  • Christina S. Lee
  • Sarah M. Sulon
  • Alec Z. Jacinto
  • Vanessa Sok
  • Natalie Peng
  • Deniz Alp
  • Jeffrey L. Benovic
  • Christopher H. SoEmail author
Article

Abstract

G protein-coupled receptor kinases (GRKs) phosphorylate the activated forms of G protein-coupled receptors (GPCRs), leading to receptor desensitization and internalization. In addition, GRKs can modify the activity of many non-GPCR-signaling pathways as well, controlling other cellular functions beyond that directly associated with a GPCR. In this report, we show that cervical cancer HeLa cells and breast cancer MDA MB 231 cells with reduced GRK5 expression display increased sensitivity to the apoptotic effects of paclitaxel (Taxol). This effect in cancer cells with low GRK5 levels could be because of blunted histone deacetylase 6 (HDAC6) activity that leads to an increase in α-tubulin acetylation levels, which augments paclitaxel sensitivity. We demonstrate that GRK5 and HDAC6 form a signaling complex in cells and in vitro. GRK5 phosphorylates HDAC6 at Ser-21 to promote its deacetylase activity. Therefore, the GRK5–HDAC6 interaction may contribute to paclitaxel resistance in cancer cells.

Keywords

G protein-coupled receptor kinase Paclitaxel Histone deacetylase Acetylation Cancer 

Abbreviations

GRK

G protein-coupled receptor kinase

GPCR

G protein-coupled receptors

HDAC

Histone deacetylase

P

Phosphorylation

PLK1

Polo-like kinase 1

Notes

Compliance with ethical standards

Conflict of interest

Authors declare that there are no competing interests associated with the manuscript.

References

  1. 1.
    Long HJ (1994) Paclitaxel (Taxol): a novel anticancer chemotherapeutic drug. Mayo Clin Proc 69:341–345CrossRefGoogle Scholar
  2. 2.
    Frederiks CN, Lam SW, Guchelaar HJ, Boven E (2015) Genetic polymorphisms and paclitaxel- or docetaxel-induced toxicities: a systematic review. Cancer Treat Rev 41:935–950.  https://doi.org/10.1016/j.ctrv.2015.10.010 CrossRefPubMedGoogle Scholar
  3. 3.
    Gelmon K (1994) The taxoids: paclitaxel and docetaxel. Lancet 344:1267–1272CrossRefGoogle Scholar
  4. 4.
    Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP (2003) Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116:2987–2998.  https://doi.org/10.1242/jcs.00612 CrossRefPubMedGoogle Scholar
  5. 5.
    Kavallaris M (2010) Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer 10:194–204.  https://doi.org/10.1038/nrc2803 CrossRefPubMedGoogle Scholar
  6. 6.
    Yagi H, Yotsumoto F, Sonoda K, Kuroki M, Mekada E, Miyamoto S (2009) Synergistic anti-tumor effect of paclitaxel with CRM197, an inhibitor of HB-EGF, in ovarian cancer. Int J Cancer 124:1429–1439.  https://doi.org/10.1002/ijc.24031 CrossRefPubMedGoogle Scholar
  7. 7.
    Moore CA, Milano SK, Benovic JL (2007) Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 69:451–482.  https://doi.org/10.1146/annurev.physiol.69.022405.154712 CrossRefPubMedGoogle Scholar
  8. 8.
    Cant SH, Pitcher JA (2005) G protein-coupled receptor kinase 2-mediated phosphorylation of ezrin is required for G protein-coupled receptor-dependent reorganization of the actin cytoskeleton. Mol Biol Cell 16:3088–3099.  https://doi.org/10.1091/mbc.E04-10-0877 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Martini JS, Raake P, Vinge LE, DeGeorge BR, DeGeorge B, Chuprun JK, Harris DM, Gao E, Eckhart AD, Pitcher JA, Koch WJ (2008) Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc Natl Acad Sci USA 105:12457–12462.  https://doi.org/10.1073/pnas.0803153105 CrossRefPubMedGoogle Scholar
  10. 10.
    Carman CV, Som T, Kim CM, Benovic JL (1998) Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J Biol Chem 273:20308–20316CrossRefGoogle Scholar
  11. 11.
    Barthet G, Carrat G, Cassier E, Barker B, Gaven F, Pillot M, Framery B, Pellissier LP, Augier J, Kang DS, Claeysen S, Reiter E, Baneres JL, Benovic JL, Marin P, Bockaert J, Dumuis A (2009) Beta-arrestin1 phosphorylation by GRK5 regulates G protein-independent 5-HT4 receptor signalling. EMBO J 28:2706–2718.  https://doi.org/10.1038/emboj.2009.215 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Barker BL, Benovic JL (2011) G protein-coupled receptor kinase 5 phosphorylation of hip regulates internalization of the chemokine receptor CXCR12. Biochemistry 50:6933–6941.  https://doi.org/10.1021/bi2005202 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Pronin AN, Morris AJ, Surguchov A, Benovic JL (2000) Synucleins are a novel class of substrates for G protein-coupled receptor kinases. J Biol Chem 275:26515–26522.  https://doi.org/10.1074/jbc.M003542200 CrossRefPubMedGoogle Scholar
  14. 14.
    Chen X, Zhu H, Yuan M, Fu J, Zhou Y, Ma L (2010) G-protein-coupled receptor kinase 5 phosphorylates p53 and inhibits DNA damage-induced apoptosis. J Biol Chem 285:12823–12830.  https://doi.org/10.1074/jbc.M109.094243 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ruiz-Gomez A, Humrich J, Murga C, Quitterer U, Lohse MJ, Mayor F Jr (2000) Phosphorylation of phosducin and phosducin-like protein by G protein-coupled receptor kinase 2. J Biol Chem 275:29724–29730.  https://doi.org/10.1074/jbc.M001864200 CrossRefPubMedGoogle Scholar
  16. 16.
    Peregrin S, Jurado-Pueyo M, Campos PM, Sanz-Moreno V, Ruiz-Gomez A, Crespo P, Mayor F, Murga C (2006) Phosphorylation of p38 by GRK2 at the docking groove unveils a novel mechanism for inactivating p38MAPK. Curr Biol 16:2042–2047.  https://doi.org/10.1016/j.cub.2006.08.083 CrossRefPubMedGoogle Scholar
  17. 17.
    Patial S, Luo J, Porter KJ, Benovic JL, Parameswaran N (2009) G-protein-coupled-receptor kinases mediate TNFalpha-induced NFkappaB signalling via direct interaction with and phosphorylation of IkappaBalpha. Biochem J 425:169–178.  https://doi.org/10.1042/bj20090908 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Parameswaran N, Pao CS, Leonhard KS, Kang DS, Kratz M, Ley SC, Benovic JL (2006) Arrestin-2 and G protein-coupled receptor kinase 5 interact with NFkappaB1 p105 and negatively regulate lipopolysaccharide-stimulated ERK1/2 activation in macrophages. J Biol Chem 281:34159–34170.  https://doi.org/10.1074/jbc.M605376200 CrossRefPubMedGoogle Scholar
  19. 19.
    So CH, Michal A, Komolov KE, Luo J, Benovic JL (2013) G protein-coupled receptor kinase 2 (GRK2) is localized to centrosomes and mediates epidermal growth factor-promoted centrosomal separation. Mol Biol Cell 24:2795–2806.  https://doi.org/10.1091/mbc.E13-01-0013 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Chakraborty PK, Zhang Y, Coomes AS, Kim WJ, Stupay R, Lynch LD, Atkinson T, Kim JI, Nie Z, Daaka Y (2014) G protein-coupled receptor kinase GRK5 phosphorylates moesin and regulates metastasis in prostate cancer. Cancer Res 74:3489–3500.  https://doi.org/10.1158/0008-5472.CAN-13-2708 CrossRefPubMedGoogle Scholar
  21. 21.
    Ruiz-Gomez A, Mellstrom B, Tornero D, Morato E, Savignac M, Holguin H, Aurrekoetxea K, Gonzalez P, Gonzalez-Garcia C, Cena V, Mayor F Jr, Naranjo JR (2007) G protein-coupled receptor kinase 2-mediated phosphorylation of downstream regulatory element antagonist modulator regulates membrane trafficking of Kv4.2 potassium channel. J Biol Chem 282:1205–1215.  https://doi.org/10.1074/jbc.M607166200 CrossRefPubMedGoogle Scholar
  22. 22.
    Singhmar P, Huo X, Eijkelkamp N, Berciano SR, Baameur F, Mei FC, Zhu Y, Cheng X, Hawke D, Mayor F Jr, Murga C, Heijnen CJ, Kavelaars A (2016) Critical role for Epac1 in inflammatory pain controlled by GRK2-mediated phosphorylation of Epac1. Proc Natl Acad Sci USA 113:3036–3041.  https://doi.org/10.1073/pnas.1516036113 CrossRefPubMedGoogle Scholar
  23. 23.
    Ohba Y, Nakaya M, Watari K, Nagasaka A, Kurose H (2015) GRK6 phosphorylates IκBα at Ser(32)/Ser(36) and enhances TNF-α-induced inflammation. Biochem Biophys Res Commun 461:307–313.  https://doi.org/10.1016/j.bbrc.2015.04.027 CrossRefPubMedGoogle Scholar
  24. 24.
    Penela P, Rivas V, Salcedo A, Mayor F (2010) G protein-coupled receptor kinase 2 (GRK2) modulation and cell cycle progression. Proc Natl Acad Sci USA 107:1118–1123.  https://doi.org/10.1073/pnas.0905778107 CrossRefPubMedGoogle Scholar
  25. 25.
    Fu X, Koller S, Abd Alla J, Quitterer U (2013) Inhibition of G-protein-coupled receptor kinase 2 (GRK2) triggers the growth-promoting mitogen-activated protein kinase (MAPK) pathway. J Biol Chem 288:7738–7755.  https://doi.org/10.1074/jbc.M112.428078 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Sang M, Hulsurkar M, Zhang X, Song H, Zheng D, Zhang Y, Li M, Xu J, Zhang S, Ittmann M, Li W (2016) GRK3 is a direct target of CREB activation and regulates neuroendocrine differentiation of prostate cancer cells. Oncotarget 7:45171–45185.  https://doi.org/10.18632/oncotarget.9359 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Theccanat T, Philip JL, Razzaque AM, Ludmer N, Li J, Xu X, Akhter SA (2016) Regulation of cellular oxidative stress and apoptosis by G protein-coupled receptor kinase-2; the role of NADPH oxidase 4. Cell Signal 28:190–203.  https://doi.org/10.1016/j.cellsig.2015.11.013 CrossRefPubMedGoogle Scholar
  28. 28.
    Métayé T, Levillain P, Kraimps JL, Perdrisot R (2008) Immunohistochemical detection, regulation and antiproliferative function of G-protein-coupled receptor kinase 2 in thyroid carcinomas. J Endocrinol 198:101–110.  https://doi.org/10.1677/JOE-07-0562 CrossRefPubMedGoogle Scholar
  29. 29.
    Métayé T, Menet E, Guilhot J, Kraimps JL (2002) Expression and activity of g protein-coupled receptor kinases in differentiated thyroid carcinoma. J Clin Endocrinol Metab 87:3279–3286.  https://doi.org/10.1210/jcem.87.7.8618 CrossRefPubMedGoogle Scholar
  30. 30.
    Billard MJ, Fitzhugh DJ, Parker JS, Brozowski JM, McGinnis MW, Timoshchenko RG, Serafin DS, Lininger R, Klauber-Demore N, Sahagian G, Truong YK, Sassano MF, Serody JS, Tarrant TK (2016) G protein coupled receptor kinase 3 regulates breast cancer migration, invasion, and metastasis. PLoS ONE 11:e0152856.  https://doi.org/10.1371/journal.pone.0152856 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Kaur G, Kim J, Kaur R, Tan I, Bloch O, Sun MZ, Safaee M, Oh MC, Sughrue M, Phillips J, Parsa AT (2013) G-protein coupled receptor kinase (GRK)-5 regulates proliferation of glioblastoma-derived stem cells. J Clin Neurosci 20:1014–1018.  https://doi.org/10.1016/j.jocn.2012.10.008 CrossRefPubMedGoogle Scholar
  32. 32.
    Woerner BM, Luo J, Brown KR, Jackson E, Dahiya SM, Mischel P, Benovic JL, Piwnica-Worms D, Rubin JB (2012) Suppression of G-protein-coupled receptor kinase 3 expression is a feature of classical GBM that is required for maximal growth. Mol Cancer Res 10:156–166.  https://doi.org/10.1158/1541-7786.MCR-11-0411 CrossRefPubMedGoogle Scholar
  33. 33.
    Nogues L, Reglero C, Rivas V, Salcedo A, Lafarga V, Neves M, Ramos P, Mendiola M, Berjon A, Stamatakis K, Zhou XZ, Lu KP, Hardisson D, Mayor F Jr, Penela P (2016) G protein-coupled receptor kinase 2 (GRK2) promotes breast tumorigenesis through a HDAC6-Pin1 axis. EBioMedicine 13:132–145.  https://doi.org/10.1016/j.ebiom.2016.09.030 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    So CH, Michal AM, Mashayekhi R, Benovic JL (2012) G protein-coupled receptor kinase 5 phosphorylates nucleophosmin and regulates cell sensitivity to polo-like kinase 1 inhibition. J Biol Chem 287:17088–17099.  https://doi.org/10.1074/jbc.M112.353854 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Michal AM, So CH, Beeharry N, Shankar H, Mashayekhi R, Yen TJ, Benovic JL (2012) G Protein-coupled receptor kinase 5 is localized to centrosomes and regulates cell cycle progression. J Biol Chem 287:6928–6940.  https://doi.org/10.1074/jbc.M111.298034 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Catalano MG, Poli R, Pugliese M, Fortunati N, Boccuzzi G (2007) Valproic acid enhances tubulin acetylation and apoptotic activity of paclitaxel on anaplastic thyroid cancer cell lines. Endocr Relat Cancer 14:839–845.  https://doi.org/10.1677/erc-07-0096 CrossRefPubMedGoogle Scholar
  37. 37.
    Lafarga V, Aymerich I, Tapia O, Mayor F Jr, Penela P (2012) A novel GRK2/HDAC6 interaction modulates cell spreading and motility. EMBO J 31:856–869.  https://doi.org/10.1038/emboj.2011.466 CrossRefPubMedGoogle Scholar
  38. 38.
    Du Y, Seibenhener ML, Yan J, Jiang J, Wooten MC (2015) aPKC phosphorylation of HDAC6 results in increased deacetylation activity. PLoS ONE 10:e0123191.  https://doi.org/10.1371/journal.pone.0123191 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Kunapuli P, Benovic JL (1993) Cloning and expression of GRK5: a member of the G protein-coupled receptor kinase family. Proc Natl Acad Sci USA 90:5588–5592.  https://doi.org/10.1073/pnas.90.12.5588 CrossRefPubMedGoogle Scholar
  40. 40.
    Spencer ML, Theodosiou M, Noonan DJ (2004) NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J Biol Chem 279:37069–37078.  https://doi.org/10.1074/jbc.M402507200 CrossRefPubMedGoogle Scholar
  41. 41.
    Skoufias DA, Wilson L (1992) Mechanism of inhibition of microtubule polymerization by colchicine: inhibitory potencies of unliganded colchicine and tubulin-colchicine complexes. Biochemistry 31:738–746CrossRefGoogle Scholar
  42. 42.
    Vasquez RJ, Howell B, Yvon AM, Wadsworth P, Cassimeris L (1997) Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol Biol Cell 8:973–985CrossRefGoogle Scholar
  43. 43.
    Xu R, Sato N, Yanai K, Akiyoshi T, Nagai S, Wada J, Koga K, Mibu R, Nakamura M, Katano M (2009) Enhancement of paclitaxel-induced apoptosis by inhibition of mitogen-activated protein kinase pathway in colon cancer cells. Anticancer Res 29:261–270PubMedGoogle Scholar
  44. 44.
    Sallmann FR, Bourassa S, Saint-Cyr J, Poirier GG (1997) Characterization of antibodies specific for the caspase cleavage site on poly(ADP-ribose) polymerase: specific detection of apoptotic fragments and mapping of the necrotic fragments of poly(ADP-ribose) polymerase. Biochem Cell Biol 75:451–456CrossRefGoogle Scholar
  45. 45.
    Dumka D, Puri P, Carayol N, Lumby C, Balachandran H, Schuster K, Verma AK, Terada LS, Platanias LC, Parmar S (2009) Activation of the p38 Map kinase pathway is essential for the antileukemic effects of dasatinib. Leuk Lymphoma 50:2017–2029.  https://doi.org/10.3109/10428190903147637 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Aslan Kosar P, Tuncer H, Cihangir Uguz A, Espino Palma J, Darici H, Onaran I, Cig B, Kosar A, Rodriguez Moratinos AB (2015) The efficiency of poly(ADP-Ribose) polymerase (PARP) cleavage on detection of apoptosis in an experimental model of testicular torsion. Int J Exp Pathol 96:294–300.  https://doi.org/10.1111/iep.12137 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Liu X, Erikson RL (2003) Polo-like kinase (Plk)1 depletion induces apoptosis in cancer cells. Proc Natl Acad Sci USA 100:5789–5794.  https://doi.org/10.1073/pnas.1031523100 CrossRefPubMedGoogle Scholar
  48. 48.
    Butch ER, Guan KL (1996) Characterization of ERK1 activation site mutants and the effect on recognition by MEK1 and MEK2. J Biol Chem 271:4230–4235CrossRefGoogle Scholar
  49. 49.
    Hu J, Zhang NA, Wang R, Huang F, Li G (2015) Paclitaxel induces apoptosis and reduces proliferation by targeting epidermal growth factor receptor signaling pathway in oral cavity squamous cell carcinoma. Oncol Lett 10:2378–2384.  https://doi.org/10.3892/ol.2015.3499 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Perdiz D, Mackeh R, Pous C, Baillet A (2011) The ins and outs of tubulin acetylation: more than just a post-translational modification? Cell Signal 23:763–771.  https://doi.org/10.1016/j.cellsig.2010.10.014 CrossRefPubMedGoogle Scholar
  51. 51.
    Sobue S, Mizutani N, Aoyama Y, Kawamoto Y, Suzuki M, Nozawa Y, Ichihara M, Murate T (2016) Mechanism of paclitaxel resistance in a human prostate cancer cell line, PC3-PR, and its sensitization by cabazitaxel. Biochem Biophys Res Commun 479:808–813.  https://doi.org/10.1016/j.bbrc.2016.09.128 CrossRefPubMedGoogle Scholar
  52. 52.
    Blagosklonny MV, Robey R, Sackett DL, Du L, Traganos F, Darzynkiewicz Z, Fojo T, Bates SE (2002) Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol Cancer Ther 1:937–941PubMedGoogle Scholar
  53. 53.
    Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417:455–458.  https://doi.org/10.1038/417455a CrossRefPubMedGoogle Scholar
  54. 54.
    Chen S, Owens GC, Makarenkova H, Edelman DB (2010) HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS ONE 5:e10848.  https://doi.org/10.1371/journal.pone.0010848 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Williams KA, Zhang M, Xiang S, Hu C, Wu JY, Zhang S, Ryan M, Cox AD, Der CJ, Fang B, Koomen J, Haura E, Bepler G, Nicosia SV, Matthias P, Wang C, Bai W, Zhang X (2013) Extracellular signal-regulated kinase (ERK) phosphorylates histone deacetylase 6 (HDAC6) at serine 1035 to stimulate cell migration. J Biol Chem 288:33156–33170.  https://doi.org/10.1074/jbc.M113.472506 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Scharer CD, Laycock N, Osunkoya AO, Logani S, McDonald JF, Benigno BB, Moreno CS (2008) Aurora kinase inhibitors synergize with paclitaxel to induce apoptosis in ovarian cancer cells. J Transl Med 6:79.  https://doi.org/10.1186/1479-5876-6-79 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Bello E, Taraboletti G, Colella G, Zucchetti M, Forestieri D, Licandro SA, Berndt A, Richter P, D’Incalci M, Cavalletti E, Giavazzi R, Camboni G, Damia G (2013) The tyrosine kinase inhibitor E-3810 combined with paclitaxel inhibits the growth of advanced-stage triple-negative breast cancer xenografts. Mol Cancer Ther 12:131–140.  https://doi.org/10.1158/1535-7163.mct-12-0275-t CrossRefPubMedGoogle Scholar
  58. 58.
    Homan KT, Waldschmidt HV, Glukhova A, Cannavo A, Song J, Cheung JY, Koch WJ, Larsen SD, Tesmer JJ (2015) Crystal structure of G protein-coupled receptor kinase 5 in complex with a rationally designed inhibitor. J Biol Chem 290:20649–20659.  https://doi.org/10.1074/jbc.M115.647370 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Schumacher SM, Gao E, Zhu W, Chen X, Chuprun JK, Feldman AM, Tesmer JJ, Koch WJ (2015) Paroxetine-mediated GRK2 inhibition reverses cardiac dysfunction and remodeling after myocardial infarction. Sci Transl Med 7:277ra31.  https://doi.org/10.1126/scitranslmed.aaa0154 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Howes SC, Alushin GM, Shida T, Nachury MV, Nogales E (2014) Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol Biol Cell 25:257–266.  https://doi.org/10.1091/mbc.E13-07-0387 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Liu W, Fan LX, Zhou X, Sweeney WE Jr, Avner ED, Li X (2012) HDAC6 regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation in renal epithelial cells. PLoS ONE 7:e49418.  https://doi.org/10.1371/journal.pone.0049418 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Liu Y, Peng L, Seto E, Huang S, Qiu Y (2012) Modulation of histone deacetylase 6 (HDAC6) nuclear import and tubulin deacetylase activity through acetylation. J Biol Chem 287:29168–29174.  https://doi.org/10.1074/jbc.M112.371120 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Palazzo A, Ackerman B, Gundersen GG (2003) Cell biology: tubulin acetylation and cell motility. Nature 421:230.  https://doi.org/10.1038/421230a CrossRefPubMedGoogle Scholar
  64. 64.
    Yagi Y, Fushida S, Harada S, Kinoshita J, Makino I, Oyama K, Tajima H, Fujita H, Takamura H, Ninomiya I, Fujimura T, Ohta T, Yashiro M, Hirakawa K (2010) Effects of valproic acid on the cell cycle and apoptosis through acetylation of histone and tubulin in a scirrhous gastric cancer cell line. J Exp Clin Cancer Res 29:149.  https://doi.org/10.1186/1756-9966-29-149 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Kim SH, Juhnn YS, Song YS (2007) Akt involvement in paclitaxel chemoresistance of human ovarian cancer cells. Ann N Y Acad Sci 1095:82–89.  https://doi.org/10.1196/annals.1397.012 CrossRefPubMedGoogle Scholar
  66. 66.
    Bae T, Weon KY, Lee JW, Eum KH, Kim S, Choi JW (2015) Restoration of paclitaxel resistance by CDK1 intervention in drug-resistant ovarian cancer. Carcinogenesis 36:1561–1571.  https://doi.org/10.1093/carcin/bgv140 CrossRefPubMedGoogle Scholar
  67. 67.
    Shi X, Sun X (2017) Regulation of paclitaxel activity by microtubule-associated proteins in cancer chemotherapy. Cancer Chemother Pharmacol 80:909–917.  https://doi.org/10.1007/s00280-017-3398-2 CrossRefPubMedGoogle Scholar
  68. 68.
    Fujioka H, Sakai A, Tanaka S, Kimura K, Miyamoto A, Iwamoto M, Uchiyama K (2017) Comparative proteomic analysis of paclitaxel resistance-related proteins in human breast cancer cell lines. Oncol Lett 13:289–295.  https://doi.org/10.3892/ol.2016.5455 CrossRefPubMedGoogle Scholar
  69. 69.
    Kramer OH, Mahboobi S, Sellmer A (2014) Drugging the HDAC6-HSP90 interplay in malignant cells. Trends Pharmacol Sci 35:501–509.  https://doi.org/10.1016/j.tips.2014.08.001 CrossRefPubMedGoogle Scholar
  70. 70.
    Di Fulvio S, Azakir BA, Therrien C, Sinnreich M (2011) Dysferlin interacts with histone deacetylase 6 and increases alpha-tubulin acetylation. PLoS ONE 6:e28563.  https://doi.org/10.1371/journal.pone.0028563 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Wu Y, Song SW, Sun J, Bruner JM, Fuller GN, Zhang W (2010) IIp45 inhibits cell migration through inhibition of HDAC6. J Biol Chem 285:3554–3560.  https://doi.org/10.1074/jbc.M109.063354 CrossRefPubMedGoogle Scholar
  72. 72.
    Lernoux M, Schnekenburger M, Dicato M, Diederich M (2017) Anti-cancer effects of naturally derived compounds targeting histone deacetylase 6-related pathways. Pharmacol Res.  https://doi.org/10.1016/j.phrs.2017.11.004 CrossRefPubMedGoogle Scholar
  73. 73.
    Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A, Koomen J, Olashaw N, Parsons JT, Yang XJ, Dent SR, Yao TP, Lane WS, Seto E (2007) HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell 27:197–213.  https://doi.org/10.1016/j.molcel.2007.05.033 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP (2005) HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 18:601–607.  https://doi.org/10.1016/j.molcel.2005.04.021 CrossRefPubMedGoogle Scholar
  75. 75.
    Garmpis N, Damaskos C, Garmpi A, Dimitroulis D, Spartalis E, Margonis GA, Schizas D, Deskou I, Doula C, Magkouti E, Andreatos N, Antoniou EA, Nonni A, Kontzoglou K, Mantas D (2017) Targeting histone deacetylases in malignant melanoma: a future therapeutic agent or just great expectations? Anticancer Res 37:5355–5362.  https://doi.org/10.21873/anticanres.11961 CrossRefPubMedGoogle Scholar
  76. 76.
    Glozak MA, Seto E (2007) Histone deacetylases and cancer. Oncogene 26:5420–5432.  https://doi.org/10.1038/sj.onc.1210610 CrossRefPubMedGoogle Scholar
  77. 77.
    Komolov KE, Du Y, Duc NM, Betz RM, Rodrigues J, Leib RD, Patra D, Skiniotis G, Adams CM, Dror RO, Chung KY, Kobilka BK, Benovic JL (2017) Structural and functional analysis of a beta2-adrenergic receptor complex with grk5. Cell 169:407–421.e16.  https://doi.org/10.1016/j.cell.2017.03.047 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Liebmann JE, Cook JA, Lipschultz C, Teague D, Fisher J, Mitchell JB (1993) Cytotoxic studies of paclitaxel (taxol) in human tumour cell lines. Br J Cancer 68:1104–1109.  https://doi.org/10.1038/bjc.1993.488 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Karabulut B, Erten C, Gul MK, Cengiz E, Karaca B, Kucukzeybek Y, Gorumlu G, Atmaca H, Uzunoglu S, Sanli UA, Baran Y, Uslu R (2009) Docetaxel/zoledronic acid combination triggers apoptosis synergistically through downregulating antiapoptotic Bcl-2 protein level in hormone-refractory prostate cancer cells. Cell Biol Int 33:239–246.  https://doi.org/10.1016/j.cellbi.2008.11.011 CrossRefPubMedGoogle Scholar
  80. 80.
    Low SY, Rennie MJ, Taylor PM (1997) Involvement of integrins and the cytoskeleton in modulation of skeletal muscle glycogen synthesis by changes in cell volume. FEBS Lett 417:101–103CrossRefGoogle Scholar
  81. 81.
    Blajeski AL, Phan VA, Kottke TJ, Kaufmann SH (2002) G(1) and G(2) cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J Clin Invest 110:91–99.  https://doi.org/10.1172/jci13275 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Joann Lagman
    • 1
  • Paula Sayegh
    • 1
  • Christina S. Lee
    • 1
  • Sarah M. Sulon
    • 2
  • Alec Z. Jacinto
    • 1
  • Vanessa Sok
    • 1
  • Natalie Peng
    • 1
  • Deniz Alp
    • 1
  • Jeffrey L. Benovic
    • 2
  • Christopher H. So
    • 1
    Email author
  1. 1.Roseman University of Health Sciences School of PharmacyHendersonUSA
  2. 2.Department of Biochemistry and Molecular BiologyThomas Jefferson UniversityPhiladelphiaUSA

Personalised recommendations