Rapamycin and chloroquine: The In Vitro and In Vivo effects of autophagy-modifying drugs show promising results in Valosin containing protein multisystem proteinopathy

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Nalbandian, Angèle ^a,b   Llewellyn, Katrina J ^a,b   Nguyen, Christopher ^a   Yazdi, Puya G ^b,c   Kimonis, Virginia E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Systomic Health LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; OPTINEURIN; PROTEIN P62; RAPAMYCIN; TAR DNA BINDING PROTEIN; UBIQUITIN; VALOSIN CONTAINING PROTEIN; DNA BINDING PROTEIN; EYE PROTEIN; OPTN PROTEIN, MOUSE; PEPTIDE; TARGET OF RAPAMYCIN KINASE; VALOSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DRUG HALF LIFE; DRUG MECHANISM; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MUSCLE FUNCTION; MUSCLE STRENGTH; MYOBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; QUADRICEPS FEMORIS MUSCLE; SIGNAL TRANSDUCTION; TDP 43 PROTEINOPATHY; TREATMENT DURATION; TREATMENT RESPONSE; ANIMAL; CELL LINE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; FRONTOTEMPORAL DEMENTIA; GENE TARGETING; GENETICS; METABOLISM; PAGET BONE DISEASE; PATHOLOGY; SKELETAL MUSCLE;

MUS;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE; CHLOROQUINE; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EYE PROTEINS; FRONTOTEMPORAL DEMENTIA; GENE KNOCK-IN TECHNIQUES; HUMANS; MALE; MICE; MUSCLE, SKELETAL; MYOBLASTS; OSTEITIS DEFORMANS; PEPTIDES; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; UBIQUITIN;

EID: 84929492880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122888     Document Type: Article

References (65)

1. Kimonis VE, Kovach MJ, Waggoner B, Leal S, Salam A, Rimer L, et al. Clinical and molecular studies in a unique family with autosomal dominant limb-girdle muscular dystrophy and Paget disease of bone. Genet Med. 2000; 2(4):232-41. PMID: 11252708.
2. Kovach MJ, Waggoner B, Leal SM, Gelber D, Khardori R, Levenstien MA, et al. Clinical delineation and localization to chromosome 9p13.3-p12 of a unique dominant disorder in four families: hereditary inclusion body myopathy, Paget disease of bone, and frontotemporal dementia. Molecular genetics and metabolism. 2001; 74(4):458-75. doi: 10.1006/mgme.2001.3256 PMID: 11749051.
3. Watts GD, Thorne M, Kovach MJ, Pestronk A, Kimonis VE. Clinical and genetic heterogeneity in chromosome 9p associated hereditary inclusion body myopathy: exclusion of GNE and three other candidate genes. Neuromuscul Disord. 2003; 13(7-8):559-67. PMID: 12921793.
4. Watts GD, Wymer J, Kovach MJ, Mehta SG, Mumm S, Darvish D, et al. Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nature genetics. 2004; 36(4):377-81. PMID: 15034582.
5. Kimonis VE, Mehta SG, Fulchiero EC, Thomasova D, Pasquali M, Boycott K, et al. Clinical studies in familial VCP myopathy associated with Paget disease of bone and frontotemporal dementia. American journal of medical genetics. 2008; 146(6):745-57. PMID: 18260132.
6. Kimonis VE, Fulchiero E, Vesa J, Watts G. VCP disease associated with myopathy, paget disease of bone and frontotemporal dementia: Review of a unique disorder. Biochimica et biophysica acta. 2008. PMID: 18845250.
7. Kimonis V, Donkervoort S, Watts G. Inclusion Body Myopathy Associated with Paget Disease of Bone and/or Frontotemporal Dementia Gene [Review]. 2011. Available: http://www.ncbi.nlm.nih.gov/pubmed/20301649.
8. Kimonis VE, Watts GD. Autosomal dominant inclusion body myopathy, Paget disease of bone, and frontotemporal dementia. Alzheimer disease and associated disorders. 2005; 19 Suppl 1:S44-7. PMID: 16317258.
9. Schroder R, Watts GD, Mehta SG, Evert BO, Broich P, Fliessbach K, et al. Mutant valosin-containing protein causes a novel type of frontotemporal dementia. Annals of neurology. 2005; 57(3):457-61. PMID: 15732117.
10. Djamshidian A, Schaefer J, Haubenberger D, Stogmann E, Zimprich F, Auff E, et al. A novel mutation in the VCP gene (G157R) in a German family with inclusion-body myopathy with Paget disease of bone and frontotemporal dementia. Muscle & nerve. 2009; 39(3):389-91. PMID: 19208399.
11. Guyant-Marechal L, Laquerriere A, Duyckaerts C, Dumanchin C, Bou J, Dugny F, et al. Valosin-containing protein gene mutations: clinical and neuropathologic features. Neurology. 2006; 67(4):644-51. PMID: 16790606.
12. Haubenberger D, Bittner RE, Rauch-Shorny S, Zimprich F, Mannhalter C, Wagner L, et al. Inclusion body myopathy and Paget disease is linked to a novel mutation in the VCP gene. Neurology. 2005; 65(8):1304-5. PMID: 16247064.
13. Bersano A, Del Bo R, Lamperti C, Ghezzi S, Fagiolari G, Fortunato F, et al. Inclusion body myopathy and frontotemporal dementia caused by a novel VCP mutation. Neurobiology of aging. 2007. PMID: 17889967.
14. Viassolo V, Previtali SC, Schiatti E, Magnani G, Minetti C, Zara F, et al. Inclusion body myopathy, Paget's disease of the bone and frontotemporal dementia: recurrence of the VCP R155H mutation in an Italian family and implications for genetic counselling. Clinical genetics. 2008. PMID: 18341608.
15. Miller TD, Jackson AP, Barresi R, Smart CM, Eugenicos M, Summers D, et al. Inclusion body myopathy with Paget disease and frontotemporal dementia (IBMPFD): clinical features including sphincter disturbance in a large pedigree. Journal of neurology, neurosurgery, and psychiatry. 2009; 80(5):583-4. PMID: 19372299. doi: 10.1136/jnnp.2008.148676
16. Kumar KR, Needham M, Mina K, Davis M, Brewer J, Staples C, et al. Two Australian families with inclusion-body myopathy, Paget's disease of bone and frontotemporal dementia: novel clinical and genetic findings. Neuromuscul Disord. 2010; 20(5):330-4. Epub 2010/03/26. doi: S0960-8966(10)00107-0 [pii] doi: 10.1016/j.nmd.2010.03.002 PMID: 20335036.
17. Fanganiello RD, Kimonis V, Nitrini R, Passos-Bueno MR. A Brazilian family with IBMPFD caused by p. R93C mutation in the VCP gene and literature review for genotype-phenotype correlations. Experimental Brain Research - Manuscript ID EBR-10-0487 2011.
18. Kim EJ, Park YE, Kim DS, Ahn BY, Kim HS, Chang YH, et al. Inclusion body myopathy with Paget disease of bone and frontotemporal dementia linked to VCP p.Arg155Cys in a Korean family. Archives of neurology. 2011; 68(6):787-96. Epub 2011/02/16. doi: archneurol.2010.376 [pii] doi: 10.1001/archneurol.2010.376 PMID: 21320982.
19. Komatsu J, Iwasa K, Yanase D, Yamada M. Inclusion body myopathy with Paget disease of the bone and frontotemporal dementia associated with a novel G156S mutation in the VCP gene. Muscle & nerve. 2013. doi: 10.1002/mus.23960 PMID: 23868359.
20. Spina S, Van Laar A, Murrell JR, de Courten-Myers G, Hamilton RL, Farlow MR, et al. Frontotemporal dementia associated with a Valosin-Containing Protein mutation: report of three families. The FASEB Journal 2008; 22: 58.4.
21. Watts GD, Thomasova D, Ramdeen SK, Fulchiero EC, Mehta SG, Drachman DA, et al. Novel VCP mutations in inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia. Clinical genetics. 2007; 72(5):420-6. Epub 2007/10/16. doi: CGE887 [pii] doi: 10.1111/j.1399-0004.2007.00887.x PMID: 17935506.
22. Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, Trojanowski JQ, et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron. 2010; 68(5):857-64. Epub 2010/12/15. doi: S0896-6273(10)00978-5 [pii] doi: 10.1016/j.neuron.2010.11.036 PMID: 21145000.
23. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nature neuroscience. 13(7):805-11. PMID: 20581817. doi: 10.1038/nn.2575
24. Komatsu M, Kominami E, Tanaka K. Autophagy and neurodegeneration. Autophagy. 2006; 2(4):315-7. PMID: 16874063.
25. Malicdan MC, Nishino I. Autophagy in lysosomal myopathies. Brain pathology (Zurich, Switzerland). 2012; 22(1):82-8. Epub 2011/12/14. doi: 10.1111/j.1750-3639.2011.00543.x. PMID: 22150923.
26. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008; 132(1):27-42. Epub 2008/01/15. doi: S0092-8674(07)01685-6 [pii] doi: 10.1016/j.cell.2007.12.018 PMID: 18191218; PubMed Central PMCID: PMC2696814.
27. Tung YT, Wang BJ, Hu MK, Hsu WM, Lee H, Huang WP, et al. Autophagy: a double-edged sword in Alzheimer's disease. J Biosci. 2012; 37(1):157-65. Epub 2012/02/24. PMID: 22357213.
28. DeLaBarre B, Christianson JC, Kopito RR, Brunger AT. Central pore residues mediate the p97/VCP activity required for ERAD. Molecular cell. 2006; 22(4):451-62. PMID: 16713576.
29. Nalbandian A, Llewellyn K, Badadani M, Yin H, Nguyen C, Katheria V, et al. A Progressive Translational Mouse Model of Human VCP Disease: The VCP R155H/+ Mouse. Muscle & nerve. 2012;(in press).
30. Yin HZ, Nalbandian A, Hsu CI, Li S, Llewellyn KJ, Mozaffar T, et al. Slow development of ALS-like spinal cord pathology in mutant valosin-containing protein gene knock-in mice. Cell Death Dis. 2012; 3: e374. Epub 2012/08/18. doi: cddis2012115 [pii] doi: 10.1038/cddis.2012.115 PMID: 22898872; PubMed Central PMCID: PMC3434652.
31. Nalbandian A, Llewellyn KJ, Kitazawa M, Yin HZ, Badadani M, Khanlou N, et al. The Homozygote VCP (R155H/R155H) Mouse Model Exhibits Accelerated Human VCP-Associated Disease Pathology. PLoS ONE. 2012; 7(9):e46308. Epub 2012/10/03. doi: 10.1371/journal.pone.0046308 PONE-D-12-17339 [pii]. PMID: 23029473; PubMed Central PMCID: PMC3460820.
32. Badadani M, Nalbandian A, Watts GD, Vesa J, Kitazawa M, Su H, et al. VCP associated inclusion body myopathy and paget disease of bone knock-in mouse model exhibits tissue pathology typical of human disease. PloS one. 2010; 5(10). PMID: 20957154.
33. Vesa J, Su H, Watts GD, Krause S, Walter MC, Martin B, et al. Valosin containing protein associated inclusion body myopathy: abnormal vacuolization, autophagy and cell fusion in myoblasts. Neuromuscul Disord. 2009; 19(11):766-72. PMID: 19828315. doi: 10.1016/j.nmd.2009.08.003
34. Llewellyn K NA, Kwang-Mook J, Nguyen C, Avandesian A, Mozaffar T, Piomelli D, Kimonis VE. Lipid-enriched diet rescues lethality and slows down progression in a murine model of VCP-associated disease. Human molecular genetics. 2013. Epub 2013.
35. Bays NW, Hampton RY. Cdc48-Ufd1-Npl4: stuck in the middle with Ub. Curr Biol. 2002; 12(10):R366-71. PMID: 12015140.
36. Dai RM, Li CC. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nature cell biology. 2001; 3(8):740-4. PMID: 11483959.
37. Fu X, Ng C, Feng D, Liang C. Cdc48p is required for the cell cycle commitment point at Start via degradation of the G1-CDK inhibitor Far1p. The Journal of cell biology. 2003; 163(1):21-6. PMID: 14557244.
38. Richly H, Rape M, Braun S, Rumpf S, Hoege C, Jentsch S. A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell. 2005; 120(1):73-84. PMID: 15652483.
39. Ye Y, Meyer HH, Rapoport TA. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature. 2001; 414(6864):652-6. PMID: 11740563.
40. Frohlich KU, Fries HW, Rudiger M, Erdmann R, Botstein D, Mecke D. Yeast cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation, and gene expression. The Journal of cell biology. 1991; 114(3):443-53. PMID: 1860879.
41. Lamb JR, Fu V, Wirtz E, Bangs JD. Functional analysis of the trypanosomal AAA protein TbVCP with trans-dominant ATP hydrolysis mutants. The Journal of biological chemistry. 2001; 276(24):21512-20. PMID: 11279035.
42. Leon A, McKearin D. Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Molecular biology of the cell. 1999; 10(11):3825-34. PMID: 10564274.
43. Wojcik C, Yano M, DeMartino GN. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. Journal of cell science. 2004; 117(Pt 2):281-92. PMID: 14657277.
44. Ju JS, Fuentealba RA, Miller SE, Jackson E, Piwnica-Worms D, Baloh RH, et al. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. The Journal of cell biology. 2009; 187(6):875-88. PMID: 20008565. doi: 10.1083/jcb.200908115
45. Ju JS, Miller SE, Hanson PI, Weihl CC. Impaired protein aggregate handling and clearance underlie the pathogenesis of p97/VCP-associated disease. The Journal of biological chemistry. 2008; 283(44):30289-99. PMID: 18715868. doi: 10.1074/jbc.M805517200
46. Ju JS, Weihl CC. p97/VCP at the intersection of the autophagy and the ubiquitin proteasome system. Autophagy. 6(2). PMID: 20083896.
47. Ching JK, Elizabeth SV, Ju JS, Lusk C, Pittman SK, Weihl CC. mTOR dysfunction contributes to vacuolar pathology and weakness in valosin-containing protein associated inclusion body myopathy. Human molecular genetics. 2013; 22(6):1167-79. doi: 10.1093/hmg/dds524 PMID: 23250913.
48. Kawai T, Murakami S, Nishiyama H, Kishino M, Sakuda M, Fuchihata H. Diagnostic imaging for a case of maxillary myxoma with a review of the magnetic resonance images of myxoid lesions. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 1997; 84(4):449-54. PMID: 9347513.
49. Li J, Kim SG, Blenis J. Rapamycin: One Drug, Many Effects. Cell Metab. 2014. doi: 10.1016/j.cmet.2014.01.001 PMID: 24508508.
50. Ghosh I, Arun I, Sen S, Mishra L. Metastatic perivascular epithelioid cell tumor responding to mammalian target of rapamycin inhibition. Indian journal of medical and paediatric oncology: official journal of Indian Society of Medical & Paediatric Oncology. 2014; 35(1):99-102. doi: 10.4103/0971-5851.133733 PMID: 25006296; PubMed Central PMCID: PMC4080675.
51. Muzic JG, Kindle SA, Tollefson MM. Successful Treatment of Subungual Fibromas of Tuberous Sclerosis With Topical Rapamycin. JAMA dermatology. 2014. doi: 10.1001/jamadermatol.2014.87 PMID: 24919623.
52. Peng ZF, Yang L, Wang TT, Han P, Liu ZH, Wei Q. Efficacy and safety of sirolimus for renal angiomyolipoma in patients with tuberous sclerosis complex or sporadic lymphangioleiomyomatosis: a systematic review. The Journal of urology. 2014. doi: 10.1016/j.juro.2014.04.096 PMID: 24813310.
53. Bove J, Martinez-Vicente M, Vila M. Fighting neurodegeneration with rapamycin: mechanistic insights. Nature reviews Neuroscience. 2011; 12(8):437-52. doi: 10.1038/nrn3068 PMID: 21772323.
54. Caccamo A, De Pinto V, Messina A, Branca C, Oddo S. Genetic reduction of mammalian target of rapamycin ameliorates Alzheimer's disease-like cognitive and pathological deficits by restoring hippocampal gene expression signature. J Neurosci. 2014; 34(23):7988-98. doi: 10.1523/JNEUROSCI.0777-14.2014 PMID: 24899720; PubMed Central PMCID: PMC4044255.
55. De Palma C, Morisi F, Cheli S, Pambianco S, Cappello V, Vezzoli M, et al. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis. 2012; 3:e418. doi: 10.1038/cddis.2012.159 PMID: 23152054; PubMed Central PMCID: PMC3542595.
56. Johnson SC, Yanos ME, Kayser EB, Quintana A, Sangesland M, Castanza A, et al. mTOR inhibition alleviates mitochondrial disease in a mouse model of Leigh syndrome. Science (New York, NY. 2013; 342(6165):1524-8. doi: 10.1126/science.1244360 PMID: 24231806.
57. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009; 460(7253):392-5. doi: 10.1038/nature08221 PMID: 19587680; PubMed Central PMCID: PMC2786175.
58. Kaeberlein M, PowersRW 3rd, Steffen KK, Westman EA, Hu D, Dang N, et al. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science (New York, NY. 2005; 310(5751):1193-6. doi: 10.1126/science.1115535 PMID: 16293764.
59. Powers RW 3rd, Kaeberlein M, Caldwell SD, Kennedy BK, Fields S. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes & development. 2006; 20(2):174-84. doi: 10.1101/gad.1381406 PMID: 16418483; PubMed Central PMCID: PMC1356109.
60. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, Orosz L, Muller F. Genetics: influence of TOR kinase on lifespan in C. elegans. Nature. 2003; 426(6967):620. doi: 10.1038/426620a PMID: 14668850.
61. Nalbandian A, Llewellyn KJ, Badadani M, Yin HZ, Nguyen C, Katheria V, et al. A progressive translational mouse model of human valosin-containing protein disease: the VCP(R155H/+) mouse. Muscle & nerve. 2013; 47(2):260-70. doi: 10.1002/mus.23522 PMID: 23169451; PubMed Central PMCID: PMC3556223.
62. Rodriguez-Caruncho C, Bielsa Marsol I. Antimalarials in dermatology: mechanism of action, indications, and side effects. Actas dermo-sifiliograficas. 2014; 105(3):243-52. doi: 10.1016/j.adengl.2012.10.021 PMID: 24656224.
63. Jiang D, Chen K, Lu X, Gao HJ, Qin ZH, Lin F. Exercise ameliorates the detrimental effect of chloroquine on skeletal muscles in mice via restoring autophagy flux. Acta pharmacologica Sinica. 2014; 35(1):135-42. doi: 10.1038/aps.2013.144 PMID: 24335841.
64. Ching JK, Weihl CC. Rapamycin-induced autophagy aggravates pathology and weakness in a mouse model of VCP-associated myopathy. Autophagy. 2013; 9(5):799-800. doi: 10.4161/auto.23958 PMID: 23439279; PubMed Central PMCID: PMC3669194.
65. Bibee KP, Cheng YJ, Ching JK, Marsh JN, Li AJ, Keeling RM, et al. Rapamycin nanoparticles target defective autophagy in muscular dystrophy to enhance both strength and cardiac function. FASEB J. 2014; 28(5):2047-61. doi: 10.1096/fj.13-237388 PMID: 24500923; PubMed Central PMCID: PMC3986846.