Mutations in cytoplasmic dynein lead to a Huntington's disease-like defect in energy metabolism of brown and white adipose tissues

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 1, 2011, Pages 59-69

  Eschbach, Judith ^a,b   Fergani, Anissa ^a,b   Oudart, Hugues ^c   Robin, Jean Patrice ^c   Rene, Frédérique ^a,b   Gonzalez de Aguilar, Jose Luis ^a,b   Larmet, Yves ^a,b   Zoll, Joffrey ^b,d   Hafezparast, Majid ^e   Schwalenstocker, Birgit ^f   Loeffler, Jean Philippe ^a,b   Ludolph, Albert C ^f   Dupuis, Luc ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c IPHC   (France)

^d HÔPITAL CIVIL   (France)

^e UNIVERSITY OF SUSSEX   (United Kingdom)

^f UNIVERSITY OF ULM   (Germany)

Author keywords

Brown adipose tissue; Huntington's disease; Lipid droplets; Lipolysis; Molecular motors; Thermogenesis; White adipose tissue

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; HUNTINGTIN; NORADRENALIN; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; ENERGY METABOLISM; HUNTINGTON CHOREA; LIPID METABOLISM; LIPOLYSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; THERMOGENESIS; WHITE ADIPOSE TISSUE;

ANIMALIA; MUS;

EID: 78650299647     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.09.009     Document Type: Article

References (46)

1. Chevalier-Larsen E., Holzbaur E.L. Axonal transport and neurodegenerative disease. Biochim. Biophys. Acta 2006, 1762:1094-1108.
2. Zheng Y., Wildonger J., Ye B., Zhang Y., Kita A., Younger S.H., Zimmerman S., Jan L.Y., Jan Y.N. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 2008, 10:1172-1180.
3. Harada A., Takei Y., Kanai Y., Tanaka Y., Nonaka S., Hirokawa N. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol. 1998, 141:51-59.
4. Hafezparast M., Klocke R., Ruhrberg C., Marquardt A., Ahmad-Annuar A., Bowen S., Lalli G., Witherden A.S., Hummerich H., Nicholson S., Morgan P.J., Oozageer R., Priestley J.V., Averill S., King V.R., Ball S., Peters J., Toda T., Yamamoto A., Hiraoka Y., Augustin M., Korthaus D., Wattler S., Wabnitz P., Dickneite C., Lampel S., Boehme F., Peraus G., Popp A., Rudelius M., Schlegel J., Fuchs H., Hrabe de Angelis M., Schiavo G., Shima D.T., Russ A.P., Stumm G., Martin J.E., Fisher E.M. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 2003, 300:808-812.
5. Perlson E., Jeong G.B., Ross J.L., Dixit R., Wallace K.E., Kalb R.G., Holzbaur E.L. A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J. Neurosci. 2009, 29:9903-9917.
6. Ilieva H.S., Yamanaka K., Malkmus S., Kakinohana O., Yaksh T., Marsala M., Cleveland D.W. Mutant dynein (Loa) triggers proprioceptive axon loss that extends survival only in the SOD1 ALS model with highest motor neuron death. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12599-12604.
7. Dupuis L., Fergani A., Braunstein K.E., Eschbach J., Holl N., Rene F., Gonzalez De Aguilar J.L., Zoerner B., Schwalenstocker B., Ludolph A.C., Loeffler J.P. Mice with a mutation in the dynein heavy chain 1 gene display sensory neuropathy but lack motor neuron disease. Exp. Neurol. 2009, 215:146-152.
8. Chen X.J., Levedakou E.N., Millen K.J., Wollmann R.L., Soliven B., Popko B. Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic Dynein heavy chain 1 gene. J. Neurosci. 2007, 27:14515-14524.
9. Caviston J.P., Ross J.L., Antony S.M., Tokito M., Holzbaur E.L. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10045-10050.
10. 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., Saudou F. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 2004, 118:127-138.
11. Braunstein K.E., Eschbach J., Rona-Voros K., Soylu R., Mikrouli E., Larmet Y., Rene F., Gonzalez De Aguilar J.L., Loeffler J.P., Muller H.P., Bucher S., Kaulisch T., Niessen H.G., Tillmanns J., Fischer K., Schwalenstocker B., Kassubek J., Pichler B., Stiller D., Petersen A., Ludolph A.C., Dupuis L. A point mutation in the dynein heavy chain gene leads to striatal atrophy and compromises neurite outgrowth of striatal neurons. Hum. Mol. Genet. 2010, 10.1093/hmg/ddq1361.
12. Petersen A., Bjorkqvist M. Hypothalamic-endocrine aspects in Huntington's disease. Eur. J. Neurosci. 2006, 24:961-967.
13. Weydt P., Pineda V.V., Torrence A.E., Libby R.T., Satterfield T.F., Lazarowski E.R., Gilbert M.L., Morton G.J., Bammler T.K., Strand A.D., Cui L., Beyer R.P., Easley C.N., Smith A.C., Krainc D., Luquet S., Sweet I.R., Schwartz M.W., La Spada A.R. Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab. 2006, 4:349-362.
14. Fain J.N., Del Mar N.A., Meade C.A., Reiner A., Goldowitz D. Abnormalities in the functioning of adipocytes from R6/2 mice that are transgenic for the Huntington's disease mutation. Hum. Mol. Genet. 2001, 10:145-152.
15. Dupuis L., Oudart H., Rene F., Gonzalez de Aguilar J.L., Loeffler J.P. Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11159-11164.
16. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
17. W.S. Rasband, ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, U.S.A., 1997-2008. http://rsb.info.nih.gov/ij/.
18. Langin D., Dicker A., Tavernier G., Hoffstedt J., Mairal A., Ryden M., Arner E., Sicard A., Jenkins C.M., Viguerie N., van Harmelen V., Gross R.W., Holm C., Arner P. Adipocyte lipases and defect of lipolysis in human obesity. Diabetes 2005, 54:3190-3197.
19. Ravikumar B., Acevedo-Arozena A., Imarisio S., Berger Z., Vacher C., O'Kane C.J., Brown S.D., Rubinsztein D.C. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet. 2005, 37:771-776.
20. Ekstrom P., Kanje M. Inhibition of fast axonal transport by erythro-9-[3-(2-hydroxynonyl)]adenine. J. Neurochem. 1984, 43:1342-1345.
21. Krieger-Brauer H.I., Medda P.K., Sattel B., Kather H. Inhibitory effect of isoproterenol on NADPH-dependent H(2)O(2) generation in human adipocyte plasma membranes is mediated by betagamma-subunits derived from G(s). J. Biol. Chem. 2000, 275:2486-2490.
22. Moniri N.H., Daaka Y. Agonist-stimulated reactive oxygen species formation regulates beta2-adrenergic receptor signal transduction. Biochem. Pharmacol. 2007, 74:64-73.
23. 2 and the sulfonylurea drug, glimepiride, in rat adipocytes depends on cAMP degradation by lipid droplets. Biochemistry 2008, 47:1259-1273.
24. Gauthier M.S., Miyoshi H., Souza S.C., Cacicedo J.M., Saha A.K., Greenberg A.S., Ruderman N.B. AMP-activated protein kinase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J. Biol. Chem. 2008, 283:16514-16524.
25. Alexandre J., Hu Y., Lu W., Pelicano H., Huang P. Novel action of paclitaxel against cancer cells: bystander effect mediated by reactive oxygen species. Cancer Res. 2007, 67:3512-3517.
26. Jang H.J., Hwang S., Cho K.Y., Kim do K., Chay K.O., Kim J.K. Taxol induces oxidative neuronal cell death by enhancing the activity of NADPH oxidase in mouse cortical cultures. Neurosci. Lett. 2008, 443:17-22.
27. Furukawa S., Fujita T., Shimabukuro M., Iwaki M., Yamada Y., Nakajima Y., Nakayama O., Makishima M., Matsuda M., Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 2004, 114:1752-1761.
28. Phan J., Hickey M.A., Zhang P., Chesselet M.F., Reue K. Adipose tissue dysfunction tracks disease progression in two Huntington's disease mouse models. Hum. Mol. Genet. 2009, 18:1006-1016.
29. van der Burg J.M., Bacos K., Wood N.I., Lindqvist A., Wierup N., Woodman B., Wamsteeker J.I., Smith R., Deierborg T., Kuhar M.J., Bates G.P., Mulder H., Erlanson-Albertsson C., Morton A.J., Brundin P., Petersen A., Bjorkqvist M. Increased metabolism in the R6/2 mouse model of Huntington's disease. Neurobiol. Dis. 2008, 29:41-51.
30. Engelender S., Sharp A.H., Colomer V., Tokito M.K., Lanahan A., Worley P., Holzbaur E.L., Ross C.A. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 1997, 6:2205-2212.
31. Li X.J., Li S.H., Sharp A.H., Nucifora F.C., Schilling G., Lanahan A., Worley P., Snyder S.H., Ross C.A. A huntingtin-associated protein enriched in brain with implications for pathology. Nature 1995, 378:398-402.
32. Andersson L., Bostrom P., Ericson J., Rutberg M., Magnusson B., Marchesan D., Ruiz M., Asp L., Huang P., Frohman M.A., Boren J., Olofsson S.O. PLD1 and ERK2 regulate cytosolic lipid droplet formation. J. Cell Sci. 2006, 119:2246-2257.
33. Bostrom P., Andersson L., Rutberg M., Perman J., Lidberg U., Johansson B.R., Fernandez-Rodriguez J., Ericson J., Nilsson T., Boren J., Olofsson S.O. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat. Cell Biol. 2007, 9:1286-1293.
34. Bostrom P., Rutberg M., Ericsson J., Holmdahl P., Andersson L., Frohman M.A., Boren J., Olofsson S.O. Cytosolic lipid droplets increase in size by microtubule-dependent complex formation. Arterioscler. Thromb. Vasc. Biol. 2005, 25:1945-1951.
35. Gross S.P., Welte M.A., Block S.M., Wieschaus E.F. Dynein-mediated cargo transport in vivo. A switch controls travel distance. J. Cell Biol. 2000, 148:945-956.
36. Guo Y., Walther T.C., Rao M., Stuurman N., Goshima G., Terayama K., Wong J.S., Vale R.D., Walter P., Farese R.V. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 2008, 453:657-661.
37. Tansey J.T., Sztalryd C., Gruia-Gray J., Roush D.L., Zee J.V., Gavrilova O., Reitman M.L., Deng C.X., Li C., Kimmel A.R., Londos C. Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6494-6499.
38. Cohen A.W., Razani B., Schubert W., Williams T.M., Wang X.B., Iyengar P., Brasaemle D.L., Scherer P.E., Lisanti M.P. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 2004, 53:1261-1270.
39. Gong K., Li Z., Xu M., Du J., Lv Z., Zhang Y. A novel protein kinase A-independent, beta-arrestin-1-dependent signaling pathway for p38 mitogen-activated protein kinase activation by beta2-adrenergic receptors. J. Biol. Chem. 2008, 283:29028-29036.
40. Sachdev P., Menon S., Kastner D.B., Chuang J.Z., Yeh T.Y., Conde C., Caceres A., Sung C.H., Sakmar T.P. G protein beta gamma subunit interaction with the dynein light-chain component Tctex-1 regulates neurite outgrowth. EMBO J. 2007, 26:2621-2632.
41. Jung Y., Kim H., Min S.H., Rhee S.G., Jeong W. Dynein light chain LC8 negatively regulates NF-kappaB through the redox-dependent interaction with IkappaBalpha. J. Biol. Chem. 2008, 283:23863-23871.
42. Stefanska J., Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm. 2008, 2008:106507.
43. Ferrante R.J. Mouse models of Huntington's disease and methodological considerations for therapeutic trials. Biochim. Biophys. Acta 2009, 1792:506-520.
44. Petersen A., Hult S., Kirik D. Huntington's disease-new perspectives based on neuroendocrine changes in rodent models. Neurodegener. Dis. 2009, 6:154-164.
45. Sassone J., Colciago C., Cislaghi G., Silani V., Ciammola A. Huntington's disease: the current state of research with peripheral tissues. Exp. Neurol. 2009, 219:385-397.
46. van der Burg J.M., Bjorkqvist M., Brundin P. Beyond the brain: widespread pathology in Huntington's disease. Lancet Neurol. 2009, 8:765-774.