Potential role of tubulin tyrosine ligase-like enzymes in tumorigenesis and cancer cell resistance

Cancer Letters

Volumn 350, Issue 1-2, 2014, Pages 1-4

  Das, Viswanath ^a   Kanakkanthara, Arun ^b   Chan, Ariane ^c   Miller, John H ^d  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b MAYO CLINIC   (United States)

^c Matakina Technology Limited   (New Zealand)

^d VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Cancer resistance; Microtubule; Polyglutamylation; Polyglutamylation inhibitors; Tumorigenesis

Indexed keywords

ALPHA TUBULIN; ANTINEOPLASTIC AGENT; BETA TUBULIN; LIGASE; LIGASE INHIBITOR; POLYGLUTAMYLASE; POLYGLUTAMYLASE INHIBITOR; TUBULIN TYROSINE LIGASE LIKE ENZYME; UNCLASSIFIED DRUG;

CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RESISTANCE; CANCER THERAPY; CARCINOGENESIS; DRUG RESISTANCE; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; NONHUMAN; POLYGLUTAMYLATION; PRIORITY JOURNAL; PROTEIN PROCESSING; SHORT SURVEY; SIGNAL TRANSDUCTION;

CANCER RESISTANCE; MICROTUBULE; POLYGLUTAMYLATION; POLYGLUTAMYLATION INHIBITORS; TUMORIGENESIS;

ANTINEOPLASTIC AGENTS; CARCINOGENESIS; DRUG RESISTANCE, NEOPLASM; HUMANS; MICROTUBULES; NEOPLASMS; PEPTIDE SYNTHASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TUBULIN; TYROSINE;

EID: 84901493793     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.04.022     Document Type: Review

References (46)

1. Janke C., Kneussel M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 2010, 33:362-372.
2. Souček K., Kamaid A., Phung A.D., Kubala L., Bulinski J.C., Harper R.W., Eiserich J.P. Normal and prostate cancer cells display distinct molecular profiles of α-tubulin posttranslational modifications. Prostate 2006, 66:954-965.
3. Kato C., Miyazaki K., Nakagawa A., Ohira M., Nakamura Y., Ozaki T., Imai T., Nakagawara A. Low expression of human tubulin tyrosine ligase and suppressed tubulin tyrosination/detyrosination cycle are associated with impaired neuronal differentiation in neuroblastomas with poor prognosis. Int. J. Cancer 2004, 112:365-375.
4. Eddé B., Rossier J., Le Caer J., Desbruyères E., Gros F., Denoulet P. Posttranslational glutamylation of alpha-tubulin. Science 1990, 247:83-85.
5. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2011, 12:773-786.
6. Bonnet C., Boucher D., Lazereg S., Pedrotti B., Islam K., Denoulet P., Larcher J.C. Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation. J. Biol. Chem. 2001, 276:12839-12848.
7. Kubo T., Yanagisawa H., Yagi T., Hirono M., Kamiya R. Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr. Biol. 2010, 20:441-445.
8. Backer C.B., Gutzman J.H., Pearson C.G., Cheeseman I.M. CSAP localizes to polyglutamylated microtubules and promotes proper cilia function and zebrafish development. Mol. Biol. Cell 2012, 23:2122-2130.
9. Janke C., Rogowski K., Wloga D., Regnard C., Kajava A.V., Strub J.-M., Temurak N., van Dijk J., Boucher D., van Dorsselaer A., Suryavanshi S., Gaertig J., Eddé B. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 2005, 308:1758-1762.
10. Kimura Y., Kurabe N., Ikegami K., Tsutsumi K., Konishi Y., Kaplan O.I., Kunitomo H., Iino Y., Blacque O.E., Setou M. Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J. Biol. Chem. 2010, 285:22936-22941.
11. Rogowski K., van Dijk J., Magiera M.M., Bosc C., Deloulme J.-C., Bosson A., Peris L., Gold N.D., Lacroix B., Grau M.B., Bec N., Larroque C., Desagher S., Holzer M., Andrieux A., Moutin M.-J., Janke C. A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 2010, 143:564-578.
12. Ikegami K., Heier R.L., Taruishi M., Takagi H., Mukai M., Shimma S., Taira S., Hatanaka K., Morone N., Yao I., Campbell P.K., Yuasa S., Janke C., MacGregor G.R., Setou M. Loss of α-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc. Natl. Acad. Sci. USA 2007, 104:3213-3218.
13. Ikegami K., Sato S., Nakamura K., Ostrowski L.E., Setou M. Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry. Proc. Natl. Acad. Sci. USA 2010, 107:10490-10495.
14. Regnard C., Desbruyères E., Huet J.-C., Beauvallet C., Pernollet J.-C., Eddé B. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 2000, 275:15969-15976.
15. van Dijk J., Miro J., Strub J.-M., Lacroix B., van Dorsselaer A., Edde B., Janke C. Polyglutamylation is a post-translational modification with a broad range of substrates. J. Biol. Chem. 2008, 283:3915-3922.
16. Lacroix B., van Dijk J., Gold N.D., Guizetti J., Aldrian-Herrada G., Rogowski K., Gerlich D.W., Janke C. Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J. Cell Biol. 2010, 189:945-954.
17. Dráberová E., Vinopal S., Morfini G., Liu P.S., Sládková V., Sulimenko T., Burns M.R., Solowska J., Kulandaivel K., de Chadarévian J.-P., Legido A., Mörk S.J., Janácek J., Baas P.W., Dráber P., Katsetos C.D. Microtubule-severing ATPase spastin in glioblastoma: increased expression in human glioblastoma cell lines and inverse roles in cell motility and proliferation. J. Neuropathol. Exp. Neurol. 2011, 70:811-826.
18. Zempel H., Luedtke J., Kumar Y., Biernat J., Dawson H., Mandelkow E., Mandelkow E.M. Amyloid-β oligomers induce synaptic damage via tau-dependent microtubule severing by TTLL6 and spastin. EMBO J. 2013, 32:2920-2937.
19. Massoner P., Lueking A., Goehler H., Höpfner A., Kowald A., Kugler K.G., Amersdorfer P., Horninger W., Bartsch G., Schulz-Knappe P., Klocker H. Serum-autoantibodies for discovery of prostate cancer specific biomarkers. Prostate 2012, 72:427-436.
20. Wasylyk C., Zambrano A., Zhao C., Brants J., Abecassis J., Schalken J.A., Rogatsch H., Schaefer G., Pycha A., Klocker H., Wasylyk B. Tubulin tyrosine ligase like 12 links to prostate cancer through tubulin posttranslational modification and chromosome ploidy. Int. J. Cancer 2010, 127:2542-2553.
21. Brants J., Semenchenko K., Wasylyk C., Robert A., Carles A., Zambrano A., Pradeau-Aubreton K., Birck C., Schalken J.A., Poch O., de Mey J., Wasylyk B. Tubulin tyrosine ligase like 12, a TTLL family member with SET- and TTL-like domains and roles in histone and tubulin modifications and mitosis. PLoS ONE 2012, 7:e51258. 10.1371/journal.pone.0051258.
22. E. Komlodi-Pasztor, D. Sackett, J. Wilkerson, T. Fojo, Mitosis is not a key target of microtubule agents in patient tumors. Nat Rev Clin Oncol. 8:244-50. Erratum. In: Nat Rev Clin Oncol. 8 (2011) 244-250 and Erratum.
23. Komlodi-Pasztor E., Sackett D.L., Fojo A.T. Inhibitors targeting mitosis: tales of how great drugs against a promising target were brought down by a flawed rationale. Clin Cancer Res. 2012, 18:51-63.
24. van Dijk J., Rogowski K., Miro J., Lacroix B., Eddé B., Janke C. A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol. Cell. 2007, 26:437-448.
25. Kashiwaya K., Nakagawa H., Hosokawa M., Mochizuki Y., Ueda K., Piao L., Chung S., Hamamoto R., Eguchi H., Ohigashi H., Ishikawa O., Janke C., Shinomura Y., Nakamura Y. Involvement of the tubulin tyrosine ligase-like family member 4 polyglutamylase in PELP1 polyglutamylation and chromatin remodeling in pancreatic cancer cells. Cancer Res. 2010, 70:4024-4033.
26. Wloga D., Dave D., Meagley J., Rogowski K., Jerka-Dziadosz M., Gaertig J. Hyperglutamylation of tubulin can either stabilize or destabilize microtubules in the same cell. Eukaryot. Cell 2010, 9:184-193.
27. Suryavanshi S., Eddé B., Fox L.A., Guerrero S., Hard R., Hennessey T., Kabi A., Malison D., Pennock D., Sale W.S., Wloga D., Gaertig J. Tubulin glutamylation regulates ciliary motility by altering inner dynein arm activity. Curr. Biol. 2010, 20:435-440.
28. Pathak N., Obara T., Mangos S., Liu Y., Drummond I.A. The zebrafish fleer gene encodes an essential regulator of cilia tubulin polyglutamylation. Mol. Biol. Cell 2007, 18:4353-4364.
29. Fliegauf M., Benzing T., Omran H. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 2007, 8:880-893.
30. Hassounah N.B., Bunch T.A., McDermott K.M. Molecular pathways: the role of primary cilia in cancer progression and therapeutics with a focus on Hedgehog signaling. Clin. Cancer Res. 2012, 18:2429-2435.
31. Sheikh A., Alvi A.A., Aslam H.M., Haseeb A. Hedgehog pathway inhibitors - current status and future prospects. Infect. Agent Cancer 2012, 7:29.
32. Wong S.Y., Seol A.D., So P.L., Ermilov A.N., Bichakjian C.K., Epstein E.H., Dlugosz A.A., Reiter J.F. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med. 2009, 15:1055-1061.
33. Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nat. Rev. Cancer 2010, 10:194-204.
34. Idriss H.T. Three steps to cancer: how phosphorylation of tubulin, tubulin tyrosine ligase and P-glycoprotein may generate and sustain cancer. Cancer Chemoth. Pharmacol. 2004, 54:101-104.
35. Lou B., Engler D., Dubinsky W., Wu J., Vigneswaran N. Acquiring metastatic competence by oral squamous cell carcinoma cells is associated with differential expression of α-tubulin isoforms. J. Oncol. 2012, 2012:491685. 10.1155/2012/491685.
36. Sangrajrang S., Denoulet P., Laing N.M., Tatoud R., Millot G., Calvo F., Tew K.D., Fellous A. Association of estramustine resistance in human prostatic carcinoma cells with modified patterns of tubulin expression. Biochem. Pharmacol. 1998, 55:325-331.
37. Sangrajrang S., Fellous A. Taxol resistance. Chemotherapy 2000, 46:327-334.
38. Alexander J.E., Hunt D.F., Lee M.K., Shabanowitz J., Michel H., Berlin S.C., MacDonald T.L., Sundberg R.J., Rebhun L.I., Frankfurter A. Characterization of posttranslational modifications in neuron-specific class III beta-tubulin by mass spectrometry. Proc. Natl. Acad. Sci. USA 1991, 88:4685-4689.
39. McCarroll J.A., Gan P.P., Liu M., Kavallaris M. βIII-tubulin is a multifunctional protein involved in drug sensitivity and tumorigenesis in non-small cell lung cancer. Cancer Res. 2010, 70:4995-5003.
40. Kanakkanthara A., Wilmes A., O'Brate A., Escuin D., Chan A., Gjyrezi A., Crawford J., Rawson P., Kivell B., Northcote P.T., Hamel E., Giannakakou P., Miller J.H. Peloruside- and laulimalide-resistant human ovarian carcinoma cells have βI-tubulin mutations and altered expression of βII- and βIII-tubulin isotypes. Mol. Cancer Ther. 2011, 10:1419-1429.
41. Ahmed A.A., Wang X., Lu Z., Goldsmith J., Le X.-F., Grandjean G., Bartholomeusz G., Broom B., Bast R.C. Modulating microtubule stability enhances the cytotoxic response of cancer cells to paclitaxel. Cancer Res. 2011, 71:5806-5817.
42. Dal Piaz F., Vassallo A., Lepore L., Tosco A., Bader A., De Tommasi N. Sesterterpenes as tubulin tyrosine ligase inhibitors. First insight of structure-activity relationships and discovery of new lead. J. Med. Chem. 2009, 52:3814-3828.
43. Lane A.A., Chabner B.A. Histone deacetylase inhibitors in cancer therapy. J. Clin. Oncol. 2009, 27:5459-5468.
44. Liu Y., Garnham C.P., Roll-Mecak A., Tanner M.E. Phosphinic acid-based inhibitors of tubulin polyglutamylases. Bioorg. Med. Chem. Lett. 2013, 23:4408-4412.
45. Ikegami K., Mukai M., Tsuchida J., Heier R.L., MacGregor G.R., Setou M. TTLL7 is a mammalian β-tubulin polyglutamylase required for growth of map2-positive neurites. J. Biol. Chem. 2006, 281:30707-30716.
46. Rüdiger M., Wehland J., Weber K. The carboxy-terminal peptide of detyrosinated alpha tubulin provides a minimal system to study the substrate specificity of tubulin-tyrosine ligase. Eur. J. Biochem. 1994, 220:309-320.