Mutant huntingtin causes defective actin remodeling during stress: Defining a new role for transglutaminase 2 in neurodegenerative disease

Human Molecular Genetics

Volumn 20, Issue 10, 2011, Pages 1937-1951

  Munsie, Lise ^a   Caron, Nicholas ^a   Atwal, Randy Singh ^a   Marsden, Ian ^b   Wild, Edward J ^c   Bamburg, James R ^b   Tabrizi, Sarah J ^c   Truant, Ray ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; HUNTINGTIN; MUTANT PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ACTIN REMODELING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL STRESS; COMPLEX FORMATION; CROSS LINKING; CYTOPLASM; DEGENERATIVE DISEASE; DISEASE COURSE; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEAT SHOCK; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; IMAGE ANALYSIS; LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; TISSUE CULTURE; WESTERN BLOTTING;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CELL LINE; CYTOSKELETAL PROTEINS; GENE EXPRESSION; GTP-BINDING PROTEINS; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; HUMANS; HUNTINGTON DISEASE; INTRACELLULAR SPACE; LYMPHOCYTES; MICE; MODELS, BIOLOGICAL; MUTATION; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; TRANSGLUTAMINASES;

EID: 79955456732     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr075     Document Type: Article

References (67)

1. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell, 72, 971-983.
2. Rawlins, M. (2010) Huntington's disease out of the closet? Lancet, 23, 1372-1373.
3. Andrade, M.A., Petosa, C., O'Donoghue, S.I., Muller, C.W. and Bork, P. (2001) Comparison of ARM and HEAT protein repeats. J. Mol. Biol., 309, 1-18.
4. Grinthal, A., Adamovic, I., Weiner, B., Karplus, M. and Kleckner, N. (2010) PR65, the HEAT-repeat scaffold of phosphatase PP2A, is an elastic connector that links force and catalysis. Proc. Natl Acad. Sci. USA, 107, 2467-2472.
5. Zuccato, C., Ciammola, A., Rigamonti, D., Leavitt, B.R., Goffredo, D., Conti, L., MacDonald, M.E., Friedlander, R.M., Silani, V., Hayden, M.R. et al. (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science, 293, 493-498.
6. Seong, I.S., Woda, J.M., Song, J.J., Lloret, A., Abeyrathne, P.D., Woo, C.J., Gregory, G., Lee, J.M., Wheeler, V.C., Walz, T. et al. (2010) Huntingtin facilitates polycomb repressive complex 2. Hum. Mol. Genet., 19, 573-583.
7. Benn, C.L., Sun, T., Sadri-Vakili, G., McFarland, K.N., DiRocco, D.P., Yohrling, G.J., Clark, T.W., Bouzou, B. and Cha, J.H. (2008) Huntingtin modulates transcription, occupies gene promoters in vivo, and binds directly to DNA in a polyglutamine-dependent manner. J. Neurosci., 28, 10720-10733.
8. Gauthier, L.R., Charrin, B.C., Borrell-Pages, M., Dompierre, J.P., Rangone, H., Cordelieres, F.P., De Mey, J., MacDonald, M.E., Lessmann, V., Humbert, S. and Saudou, F. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell, 118, 127-138.
9. Atwal, R.S., Xia, J., Pinchev, D., Taylor, J., Epand, R.M. and Truant, R. (2007) Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity. Hum. Mol. Genet., 16, 2600-2615.
10. Godin, J.D., Colombo, K., Molina-Calavita, M., Keryer, G., Zala, D., Charrin, B.C., Dietrich, P., Volvert, M.L., Guillemot, F., Dragatsis, I. et al. (2010) Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron, 67, 392-406.
11. Rockabrand, E., Slepko, N., Pantalone, A., Nukala, V.N., Kazantsev, A., Marsh, J.L., Sullivan, P.G., Steffan, J.S., Sensi, S.L. and Thompson, L.M. (2007) The first 17 amino acids of Huntingtin modulate its sub-cellular localization, aggregation and effects on calcium homeostasis. Hum. Mol. Genet., 16, 61-77.
12. Aiken, C.T., Steffan, J.S., Guerrero, C.M., Khashwji, H., Lukacsovich, T., Simmons, D., Purcell, J.M., Menhaji, K., Zhu, Y.Z., Green, K. et al. (2009) Phosphorylation of threonine 3: implications for Huntingtin aggregation and neurotoxicity. J. Biol. Chem., 284, 29427-29436.
13. Gu, X., Greiner, E.R., Mishra, R., Kodali, R., Osmand, A., Finkbeiner, S., Steffan, J.S., Thompson, L.M., Wetzel, R. and Yang, X.W. (2009) Serines 13 and 16 are critical determinants of full-length human mutant huntingtin induced disease pathogenesis in HD mice. Neuron, 64, 828-840.
14. Steffan, J.S., Agrawal, N., Pallos, J., Rockabrand, E., Trotman, L.C., Slepko, N., Illes, K., Lukacsovich, T., Zhu, Y.Z., Cattaneo, E. et al. (2004) SUMO modification of Huntingtin and Huntington's disease pathology. Science, 304, 100-104.
15. Trettel, F., Rigamonti, D., Hilditch-Maguire, P., Wheeler, V.C., Sharp, A.H., Persichetti, F., Cattaneo, E. and MacDonald, M.E. (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet., 9, 2799-2809.
16. Morimoto, R.I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev., 22, 1427-1438.
17. Drummond, I.A., McClure, S.A., Poenie, M., Tsien, R.Y. and Steinhardt, R.A. (1986) Large changes in intracellular pH and calcium observed during heat shock are not responsible for the induction of heat shock proteins in Drosophila melanogaster. Mol. Cell Biol., 6, 1767-1775.
18. Schroder, M. and Kaufman, R.J. (2005) ER stress and the unfolded protein response. Mutat. Res., 569, 29-63.
19. Gibson, G.E., Starkov, A., Blass, J.P., Ratan, R.R. and Beal, M.F. (2010) Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases. Biochim. Biophys. Acta, 1802, 122-134.
20. Hosoi, T. and Ozawa, K. (2010) Endoplasmic reticulum stress in disease: mechanisms and therapeutic opportunities. Clin. Sci. (Lond.), 118, 19-29.
21. Keller, J.N. (2006) Age-related neuropathology, cognitive decline, and Alzheimer's disease. Ageing Res. Rev., 5, 1-13.
22. Maloney, M.T. and Bamburg, J.R. (2007) Cofilin-mediated neurodegeneration in Alzheimer's disease and other amyloidopathies. Mol. Neurobiol., 35, 21-44.
23. Minamide, L.S., Striegl, A.M., Boyle, J.A., Meberg, P.J. and Bamburg, J.R. (2000) Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol., 2, 628-636.
24. Bamburg, J.R. and Wiggan, O.P. (2002) ADF/cofilin and actin dynamics in disease. Trends Cell Biol., 12, 598-605.
25. Bernstein, B.W., Chen, H., Boyle, J.A. and Bamburg, J.R. (2006) Formation of actin-ADF/cofilin rods transiently retards decline of mitochondrial potential and ATP in stressed neurons. Am. J. Physiol. Cell Physiol., 291, C828-C839.
26. Lesort, M., Chun, W., Tucholski, J. and Johnson, G.V. (2002) Does tissue transglutaminase play a role in Huntington's disease? Neurochem. Int., 40, 37-52.
27. Lesort, M., Chun, W., Johnson, G.V. and Ferrante, R.J. (1999) Tissue transglutaminase is increased in Huntington's disease brain. J. Neurochem., 73, 2018-2027.
28. Cariello, L., de Cristofaro, T., Zanetti, L., Cuomo, T., Di Maio, L., Campanella, G., Rinaldi, S., Zanetti, P., Di Lauro, R. and Varrone, S. (1996) Transglutaminase activity is related to CAG repeat length in patients with Huntington's disease. Hum. Genet., 98, 633-635.
29. Benchaar, S.A., Xie, Y., Phillips, M., Loo, R.R., Galkin, V.E., Orlova, A., Thevis, M., Muhlrad, A., Almo, S.C., Loo, J.A. et al. (2007) Mapping the interaction of cofilin with subdomain 2 on actin. Biochemistry, 46, 225-233.
30. Wallrabe, H. and Periasamy, A. (2005) Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol., 16, 19-27.
31. Hotulainen, P. and Hoogenraad, C.C. (2010) Actin in dendritic spines: connecting dynamics to function. J. Cell Biol., 189, 619-629.
32. Cattaneo, E. and Conti, L. (1998) Generation and characterization of embryonic striatal conditionally immortalized ST14A cells. J. Neurosci. Res., 53, 223-234.
33. Nishida, E., Iida, K., Yonezawa, N., Koyasu, S., Yahara, I. and Sakai, H. (1987) Cofilin is a component of intranuclear and cytoplasmic actin rods induced in cultured cells. Proc. Natl Acad. Sci. USA, 84, 5262-5266.
34. Iida, K., Matsumoto, S. and Yahara, I. (1992) The KKRKK sequence is involved in heat shock-induced nuclear translocation of the 18-kDa actin-binding protein, cofilin. Cell Struct. Funct., 17, 39-46.
35. Ohta, Y., Nishida, E., Sakai, H. and Miyamoto, E. (1989) Dephosphorylation of cofilin accompanies heat shock-induced nuclear accumulation of cofilin. J. Biol. Chem., 264, 16143-16148.
36. Endo, M., Ohashi, K. and Mizuno, K. (2007) LIM kinase and slingshot are critical for neurite extension. J. Biol. Chem., 282, 13692-13702.
37. Lim, M.K., Kawamura, T., Ohsawa, Y., Ohtsubo, M., Asakawa, S., Takayanagi, A. and Shimizu, N. (2007) Parkin interacts with LIM Kinase 1 and reduces its cofilin-phosphorylation activity via ubiquitination. Exp. Cell Res., 313, 2858-2874.
38. Mila, S., Albo, A.G., Corpillo, D., Giraudo, S., Zibetti, M., Bucci, E.M., Lopiano, L. and Fasano, M. (2009) Lymphocyte proteomics of Parkinson's disease patients reveals cytoskeletal protein dysregulation and oxidative stress. Biomark. Med., 3, 117-128.
39. Mannherz, H.G., Ballweber, E., Galla, M., Villard, S., Granier, C., Steegborn, C., Schmidtmann, A., Jaquet, K., Pope, B. and Weeds, A.G. (2007) Mapping the ADF/cofilin binding site on monomeric actin by competitive cross-linking and peptide array: evidence for a second binding site on monomeric actin. J. Mol. Biol., 366, 745-755.
40. Ruan, Q. and Johnson, G.V. (2007) Transglutaminase 2 in neurodegenerative disorders. Front Biosci., 12, 891-904.
41. Jeitner, T.M., Matson, W.R., Folk, J.E., Blass, J.P. and Cooper, A.J. (2008) Increased levels of gamma-glutamylamines in Huntington disease CSF. J. Neurochem., 106, 37-44.
42. Johnson, G.V., Cox, T.M., Lockhart, J.P., Zinnerman, M.D., Miller, M.L. and Powers, R.E. (1997) Transglutaminase activity is increased in Alzheimer's disease brain. Brain Res., 751, 323-329.
43. Wilhelmus, M.M., Grunberg, S.C., Bol, J.G., van Dam, A.M., Hoozemans, J.J., Rozemuller, A.J. and Drukarch, B. (2009) Transglutaminases and transglutaminase-catalyzed cross-links colocalize with the pathological lesions in Alzheimer's disease brain. Brain Pathol., 19, 612-622.
44. Norlund, M.A., Lee, J.M., Zainelli, G.M. and Muma, N.A. (1999) Elevated transglutaminase-induced bonds in PHF tau in Alzheimer's disease. Brain Res., 851, 154-163.
45. Mastroberardino, P.G., Iannicola, C., Nardacci, R., Bernassola, F., De Laurenzi, V., Melino, G., Moreno, S., Pavone, F., Oliverio, S., Fesus, L. and Piacentini, M. (2002) 'Tissue' transglutaminase ablation reduces neuronal death and prolongs survival in a mouse model of Huntington's disease. Cell Death Differ., 9, 873-880.
46. Kahlem, P., Terre, C., Green, H. and Djian, P. (1996) Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system. Proc. Natl Acad. Sci. USA, 93, 14580-14585.
47. Cooper, A.J., Sheu, K.F., Burke, J.R., Onodera, O., Strittmatter, W.J., Roses, A.D. and Blass, J.P. (1997) Polyglutamine domains are substrates of tissue transglutaminase: does transglutaminase play a role in expanded CAG/poly-Q neurodegenerative diseases? J. Neurochem., 69, 431-434.
48. Chun, W., Lesort, M., Tucholski, J., Ross, C.A. and Johnson, G.V. (2001) Tissue transglutaminase does not contribute to the formation of mutant huntingtin aggregates. J. Cell Biol., 153, 25-34.
49. Bailey, C.D. and Johnson, G.V. (2005) Tissue transglutaminase contributes to disease progression in the R6/2 Huntington's disease mouse model via aggregate-independent mechanisms. J. Neurochem., 92, 83-92.
50. McConoughey, S.J., Basso, M., Niatsetskaya, Z.V., Sleiman, S.F., Smirnova, N.A., Langley, B.C., Mahishi, L., Cooper, A.J., Antonyak, M.A., Cerione, R.A. et al. (2010) Inhibition of transglutaminase 2 mitigates transcriptional dysregulation in models of Huntington disease. EMBO Mol. Med., 2, 335-337.
51. Tang, T.S., Slow, E., Lupu, V., Stavrovskaya, I.G., Sugimori, M., Llinas, R., Kristal, B.S., Hayden, M.R. and Bezprozvanny, I. (2005) Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc. Natl Acad. Sci. USA, 102, 2602-2607.
52. Zhao, L. and Ackerman, S.L. (2006) Endoplasmic reticulum stress in health and disease. Curr. Opin. Cell Biol., 18, 444-452.
53. Angeli, S., Shao, J. and Diamond, M.I. (2010) F-actin binding regions on the androgen receptor and huntingtin increase aggregation and alter aggregate characteristics. PLoS ONE, 5, e9053.
54. Luthi-Carter, R. and Cha, J.H. (2003) Mechanisms of transcriptional dysregulation in Huntington's disease. Clin. Neurosci. Res., 3, 165-177.
55. Pal, A., Severin, F., Lommer, B., Shevchenko, A. and Zerial, M. (2006) Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington's disease. J. Cell Biol., 172, 605-618.
56. Gines, S., Seong, I.S., Fossale, E., Ivanova, E., Trettel, F., Gusella, J.F., Wheeler, V.C., Persichetti, F. and MacDonald, M.E. (2003) Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Hum. Mol. Genet., 12, 497-508.
57. Koroshetz, W.J., Jenkins, B.G., Rosen, B.R. and Beal, M.F. (1997) Energy metabolism defects in Huntington's disease and effects of coenzyme Q10. Ann. Neurol., 41, 160-165.
58. Seong, I.S., Ivanova, E., Lee, J.M., Choo, Y.S., Fossale, E., Anderson, M., Gusella, J.F., Laramie, J.M., Myers, R.H., Lesort, M. and MacDonald, M.E. (2005) HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Hum. Mol. Genet., 14, 2871-2880.
59. Richfield, E.K., Maguire-Zeiss, K.A., Vonkeman, H.E. and Voorn, P. (1995) Preferential loss of preproenkephalin versus preprotachykinin neurons from the striatum of Huntington's disease patients. Ann. Neurol., 38, 852-861.
60. Bernstein, B.W. and Bamburg, J.R. (2003) Actin-ATP hydrolysis is a major energy drain for neurons. J. Neurosci., 23, 1-6.
61. Shao, J., Welch, W.J., Diprospero, N.A. and Diamond, M.I. (2008) Phosphorylation of profilin by ROCK1 regulates polyglutamine aggregation. Mol. Cell Biol., 28, 5196-5208.
62. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science, 285, 895-898.
63. Li, M., Huang, Y., Ma, A.A., Lin, E. and Diamond, M.I. (2009) Y-27632 improves rotarod performance and reduces huntingtin levels in R6/2 mice. Neurobiol. Dis., 36, 413-420.
64. Agrawal, N., Pallos, J., Slepko, N., Apostol, B.L., Bodai, L., Chang, L.W., Chiang, A.S., Thompson, L.M. and Marsh, J.L. (2005) Identification of combinatorial drug regimens for treatment of Huntington's disease using Drosophila. Proc. Natl Acad. Sci. USA, 102, 3777-3781.
65. Kiraly, R., Csosz, E., Kurtan, T., Antus, S., Szigeti, K., Simon-Vecsei, Z., Korponay-Szabo, I.R., Keresztessy, Z. and Fesus, L. (2009) Functional significance of five noncanonical Ca2+-binding sites of human transglutaminase 2 characterized by site-directed mutagenesis. FEBS J., 276, 7083-7096.
66. Zhang, H., Li, Q., Graham, R.K., Slow, E., Hayden, M.R. and Bezprozvanny, I. (2008) Full length mutant huntingtin is required for altered Ca2+ signaling and apoptosis of striatal neurons in the YAC mouse model of Huntington's disease. Neurobiol. Dis., 31, 80-88.
67. Schaertl, S., Prime, M., Wityak, J., Dominguez, C., Munoz-Sanjuan, I., Pacifici, R.E., Courtney, S., Scheel, A. and Macdonald, D. (2010) A profiling platform for the characterization of transglutaminase 2 (TG2) inhibitors. J. Biomol. Screen., 15, 478-487.