Reactive nucleolar and Cajal body responses to proteasome inhibition in sensory ganglion neurons

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 6, 2014, Pages 848-859

  Palanca, Ana ^a,b   Casafont, Iñigo ^a,b   Berciano, María T ^a,b   Lafarga, Miguel ^a,b  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Bortezomib; Cajal body; Nucleolus; Proteasome inhibitor; Proteotoxic stress; Sensory ganglia neuron

Indexed keywords

BORTEZOMIB; FIBRILLARIN; FLUOROURIDINE; POLYADENYLATED RNA; PROTEASOME; RIBOSOME RNA; RNA 45S; RNA PRECURSOR; TIFENAMIL; UNCLASSIFIED DRUG; BORONIC ACID DERIVATIVE; PYRAZINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL STRESS; CELLULAR STRESS RESPONSE; COILED BODY; CONTROLLED STUDY; DOSE RESPONSE; MALE; NEUROTOXICITY; NONHUMAN; NUCLEAR SIZE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SENSORY GANGLION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ANIMAL; CELL CYCLE CHECKPOINT; CELL NUCLEUS; CYTOPLASM; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NEURODEGENERATIVE DISEASES; NUCLEOLUS; PATHOLOGY; SENSORY NERVE CELL;

RATTUS;

ANIMALS; BORONIC ACIDS; CELL CYCLE CHECKPOINTS; CELL NUCLEOLUS; CELL NUCLEUS; COILED BODIES; CYTOPLASM; GANGLIA, SENSORY; HUMANS; NEURODEGENERATIVE DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; RATS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION;

EID: 84897072085     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.11.016     Document Type: Article

References (72)

1. Schwartz A.L., Ciechanover A. Targeting protein for destruction by the ubiquitin system: implications for human pathobiology. Annu. Rev. Pharmacol. Toxicol. 2009, 49:73-96.
2. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Ann. Rev. Biochem. 2009, 78:477-513.
3. Adams J. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 2004, 5:417-421.
4. von Mikecz A. The nuclear ubiquitin-proteasome system. J. Cell Sci. 2006, 119:1977-1984.
5. Lafarga M., Berciano M.T., Pena E., Mayo I., Castano J.G., Bohmann D., Rodrigues J.P., Tavanez J.P., Carmo-Fonseca M. Clastosome: a subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin, and protein substrates of proteasome. Mol. Biol. Cell 2002, 13:2771-2782.
6. Rockel T.D., Stuhlmann D., von Mikecz A. Proteasomes degrade proteins in focal subdomains of the human cell nucleus. J. Cell Sci. 2005, 118:5231-5242.
7. Scharf A., Rockel T.D., von Mikecz A. Localization of proteasomes and proteasomal proteolysis in the mammalian interphase cell nucleus by systematic application of immunocytochemistry. Histochem. Cell Biol. 2007, 127:591-601.
8. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
9. Richardson P.G., Mitsiades C., Hideshima T., Anderson K.C. Bortezomib: proteasome inhibition as an effective anticancer therapy. Annu. Rev. Med. 2006, 57:33-47.
10. McConkey D.J., Zhu K. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist. Updat. 2008, 11:164-179.
11. Cavaletti G., Gilardini A., Canta A., Rigamonti L., Rodriguez-Menendez V., Ceresa C., Marmiroli P., Bossi M., Oggioni N., DD́Incalci M., De Coster R. Bortezomib-induced peripheral neurotoxicity: a neurophysiological and pathological study in the rat. Exp. Neurol. 2007, 204:317-325.
12. Argyriou A.A., Bruna J., Marmiroli P., Cavaletti G. Chemotherapy-induced peripheral neurotoxicity (CIPN): an update. Crit. Rev. Oncol. Hematol. 2012, 8:51-77.
13. Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 2003, 17:1691-1702.
14. Raska I., Shaw P., Cmarko D. New insights into nucleolar architecture and activity. Int. Rev. Cytol. 2006, 255:177-235.
15. Boisvert F.M., van Koninggsbruggen A.I.S., Navascues J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
16. Hernandez-Verdun D., Roussel P., Thiry M., Sirri V., Lafontaine D.L. The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdiscip. Rev. RNA 2010, 3:415-431.
17. Olson M.O. Sensing cellular stress: another new function for the nucleolus?. Sci. STKE 2004, pe10.
18. Boulon S., Westman B.J., Hutten S., Boisvert F.M., Lamond A.I. The nucleolus under stress. Mol. Cell 2010, 40:216-227.
19. Moore H.M., Bai B., Matilainen O., Colis L., Peltonen K., Laiho M. Proteasome activity influences UV-mediated subnuclear localization changes of NPM. PLoS One 2013, 8:e59096. 10.1371/journal.pone.0059096.
20. Mattsson K., Pokrovskaja K., Kiss C., Klein G., Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1012-1017.
21. Stavreva D.A., Kawasaki M., Dundr M., Koberna K., Müller W.G., Tsujimura-Takahashi T., Komatsu W., Hayano T., Isobe T., Raska I., Misteli T., Takahashi N., McNally J.G. Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell. Biol. 2006, 26:5131-5145.
22. Latonen L., Moore H.M., Bai B., Jäämaa S., Laiho M. Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 2011, 30:790-805.
23. Crespo D., Viadero C.F., Villegas J., Lafarga M. Nucleoli numbers and neuronal growth in supraoptic nucleus neurons during postnatal development in the rat. Brain Res. Dev. Brain Res. 1988, 56:151-155.
24. Lafarga M., Andres M.A., Berciano M.T., Maquiera E. Organization of nucleoli and nuclear bodies in osmotically stimulated supraoptic neurons of the rat. J. Comp. Neurol. 1991, 308:329-339.
25. Kinderman N.B., Jones K.J. Testosterone enhancement of the nerve cell body response to injury: evidence using in situ hybridization and ribosomal DNA probes. J. Neurosci. 1993, 13:1523-1532.
26. Berciano M.T., Novell M., Villagra N.T., Casafont I., Bengoechea R., Val-Bernal J.F., Lafarga M. Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons. J. Struct. Biol. 2007, 158:410-420.
27. Jordan B.A., Fernholz B.D., Khatri L., Ziff E.B. Activity-dependent AIDA-1 nuclear signaling regulates nucleolar numbers and protein synthesis in neurons. Nat. Neurosci. 2007, 10:427-435.
28. Hetman M., Pietrzak M. Emerging roles of the neuronal nucleolus. Trends Neurosci. 2012, 35:305-314.
29. Hetman M., Vashishta A., Rempala G. Neurotoxic mechanisms of DNA damage: focus on transcriptional inhibition. J. Neurochem. 2010, 114:1537-1549.
30. Baltanas F.C., Casafont I., Weruaga E., Alonso J.R., Berciano M.T., Lafarga M. Nucleolar disruption and Cajal body disassembly are nuclear hallmarks of DNA damage-induced neurodegeneration in Purkinje cells. Brain Pathol. 2011, 21:374-388.
31. Parlato R., Kreiner G. Nucleolar activity in neurodegenerative diseases: a missing piece of the puzzle?. J. Mol. Med. 2013, 91:541-547.
32. Lafarga M., Casafont I., Bengoechea R., Tapia O., Berciano M.T. Cajal's contribution to the knowledge of the neuronal cell nucleus. Chromosoma 2009, 18:437-443.
33. Gall J.G. Cajal bodies: the first 100years. Annu. Rev. Cell Dev. Biol. 2000, 16:273-300.
34. Cioce M., Lamond A.I. Cajal bodies: a long history of discovery. Annu. Rev. Cell Dev. Biol. 2005, 21:105-131.
35. Nizami Z., Deryusheva S., Gall J.G. The Cajal body and histone locus body. Cold Spring Harb. Perspect. Biol. 2010, 2:a000653.
36. Machyna M., Heyn P., Neugebauer K.M. Cajal bodies: where form meets function. Wiley Interdiscip. Rev. RNA 2013, 4:17-34.
37. Lafarga M., Berciano M.T., Garcia-Segura L.M., Carmo-Fonseca M. Acute osmotic/stress stimuli induce a transient decrease of transcriptional activity in the neurosecretory neurons of supraoptic nuclei. J. Neurocytol. 1998, 27:205-217.
38. Pena E., Berciano M.T., Fernandez R., Ojeda J.L., Lafarga M. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J. Comp. Neurol. 2001, 430:250-263.
39. Casafont I., Berciano M.T., Lafarga M. Bortezomib induces the formation of nuclear poly(A) RNA granules enriched in Sam68 and PABPN1 in sensory ganglia neurons. Neurotox. Res. 2010, 17:167-178.
40. Carozzi V.A., Canta A., Oggioni N., Sala B., Chiorazzi A., Meregalli C., Bossi M., Marmiroli P., Cavaletti G. Neurophysiological and neuropathological characterization of new murine models of chemotherapy-induced chronic peripheral neuropathies. Exp. Neurol. 2010, 226:301-309.
41. Jansen R.P., Hurt E.C., Kern H., Lehtonen H., Carmo-Fonseca M., Lapeyre B., Tollervey D. Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J. Cell Biol. 1991, 113:715-729.
42. Casafont I., Navascues J., Pena E., Lafarga M., Berciano M.T. Nuclear organization and dynamics of transcription sites in rat sensory ganglia neurons detected by incorporation of 5'-fluorouridine into nascent RNA. Neuroscience 2006, 140:453-462.
43. Murayama A., Ohmori K., Fujimura A., Minami H., Yasuzawa-Tanaka K., Kuroda T., Oie S., Daitoku H., Okuwaki M., Nagata K., Fukamizu A., Kimura K., Shimizu T., Yanagisawa J. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 2008, 133:627-639.
44. Ren Y., Busch R.K., Perlaky L., Busch H. The 58-kDa microspherule protein (MSP58), a nucleolar protein, interacts with nucleolar protein p120. Eur. J. Biochem. 1998, 3:734-742.
45. Casafont I., Bengoechea R., Navascues J., Pena E., Berciano M.T., Lafarga M. The giant fibrillar center: a nucleolar structure enriched in upstream binding factor (UBF) that appears in transcriptionally more active sensory ganglion neurons. J. Struct. Biol. 2007, 159:451-461.
46. Jordan P., Mannervik M., Tora L., Carmo-Fonseca M. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase I when rRNA synthesis is either active or inactive. J. Cell Biol. 1996, 133:225-234.
47. Kalita K., Makonchuk D., Gomes C., Zheng J.J., Hetman M. Inhibition of nucleolar transcription as a trigger for neuronal apoptosis. J. Neurochem. 2008, 105:2286-2299.
48. Mayer C., Bierhoff H., Grummt I. The nucleolus as a stress sensor: JNK2 inactivates the transcription factor TIF-IA and downregulates rRNA synthesis. Genes Dev. 2005, 19:933-941.
49. Grandori C., Gomez-Roman N., Felton-Edkins Z.A., Ngouenet C., Galloway D.A., Eisenman R.N., White R.J. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 2005, 7:311-318.
50. van Riggelen J., Yetil A., Felsher D.W. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 2010, 10:301-309.
51. Zhai W., Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol. 2000, 20:5930-5938.
52. Verheggen C., Mouaikel J., Thiry M., Blanchard J.M., Tollervey D., Bordonné R., Lafontaine D.L., Bertrand E. Box C/D small nucleolar RNA trafficking involves small nucleolar RNP proteins, nucleolar factors and a novel nuclear domain. EMBO J. 2001, 19:5480-5490.
53. Gilder A.S., Do P.M., Carrero Z.I., Cosman A.M., Broome H.J., Velma V., Martinez L.A., Hebert M.D. Coilin participates in suppression of RNA polymerase I in response to cisplatin-induced DNA damage. Mol. Biol. Cell 2011, 7:1070-1079.
54. Gilder A.S., Hebert M. Relationship of the Cajal body to the nucleolus. The Nucleolus 2011, Springer-Science. M.O.J. Olson (Ed.).
55. Tapia O., Bengoechea R., Palanca A., Arteaga R., Val-Bernal J.F., Tizzano E.F., Berciano M.T., Lafarga M. Reorganization of Cajal bodies and nucleolar targeting of coilin in motor neurons of type I spinal muscular atrophy. Histochem. Cell Biol. 2012, 137:657-667.
56. Raska I., Ochs R.L., Andrade L.E.C., Chan E.K.L., Burlingame R., Peebles C., Gruol D., Tan E.M. Association between the nucleolus and the coiled body. J. Struct. Biol. 1990, 104:120-127.
57. Tucker K.E., Berciano M.T., Jacobs E.Y., LePage D.F., Shpargel K.B., Rossire J.J., Chan E.K., Lafarga M., Colon R.A., Matera A.G. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J. Cell Biol. 2001, 154(2001):293-307.
58. Strzelecka M., Trowitzsch S., Weber G., Lührmann R., Oates A.C., Neugebauer K.M. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat. Struct. Biol. 2010, 17:403-409.
59. Bruna J., Udina E., Alé A., Vilches J.J., Vynckier A., Monbaliu J., Silverman L., Navarro X. Neurophysiological, histological and immunohistochemical characterization of bortezomib-induced neuropathy in mice. Exp. Neurol. 2010, 223:599-608.
60. Schwarzacher H.G., Wachtler F. The nucleolus. Anat. Embryol. 1993, 188:515-536.
61. Garcia Moreno L.M., Cimadevilla J.M., Gonzalez Pardo H., Zahonero M.C., Arias J.L. NOR activity in hippocampal areas during the postnatal develioment and aging. Mech. Ageing Dev. 1997, 97:173-181.
62. Parlato R., Kreimer G., Erdmann G., Rieker C., Stotz S., Savenkova E., Berger S., Grummt I., Schutz G. Activation of an endogenous suicide response after perturbation of rRNA synthesis leads to neurodegeneration in mice. J. Neurosci. 2008, 28:12759-12764.
63. Mann D.M., Marcyniuk B., Yates P.O., Neary D., Snowden J.S. The progression of the pathological changes of Alzheimer's disease in frontal and temporal neocortex examined both at biopsy and autopsy. Neuropathol. Appl. Neurobiol. 1988, 14:177-195.
64. Iacono D., O'Brien R., Resnick S.M., Zonderman A.B., Pletnikova O., Rudow G., An Y., West M.J. Neuronal hypertrophy in asymptomatic Alzheimer disease. J. Neuropathol. Exp. Neurol. 2008, 67:578-589.
65. Wells M.R., Vaidya U. RNA transcription in axotomized dorsal root ganglion neurons. Brain Res. Mol. Brain Res. 1994, 27:163-166.
66. McIlwain D.L., Hoke V.B. The role of the cytoskeleton in cell body enlargement, increased nuclear eccentricity and chromatolysis in axotomized spinal motor neurons. BMC Neurosci. 2005, 17:6-19.
67. Kreiner G., Bierhoff H., Armentano M., Rodriguez-Parkitna J., Sowodniok S., Naranjo J.R., Bonfanti L., Liss B., Schütz G., Grummt I., Parlato R. A neuroprotective phase precedes striatal degeneration upon nucleolar stress. Cell Death Differ. 2013, 10.1038/cdd.2013.66.
68. Yuan X., Zhou Y., Casanova E., Chai M., Kiss E., Grone H.J., Schtz G., Grummt I. Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol. Cell 2005, 19:77-87.
69. Cioce M., Boulon S., Matera A.G., Lamond A.I. UV-induced fragmentation of Cajal bodies. J. Cell Biol. 2006, 175:401-413.
70. Chen F.-T., Yang C.-M., Yang C.-H. The protective effects of the proteasome inhibitor bortezomib (Velcade) on ischemia-reperfusion injury in the rat retina. PLoS One 2013, 8:e64262.
71. Casafont I., Palanca A., Lafarga V., Berciano M.T., Lafarga M. Effect of ionizing radiation in sensory ganglion neurons: organization and dynamics of nuclear compartments of DNA damage/repair and their relationship with transcription and cell cycle. Acta Neuropathol. 2011, 122:481-493.
72. Steffen J., Seeger M., Koch A., Krüger E. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 2010, 40:147-158.