Home LiteratureArticle Details
PMID: 21289198 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Rescue of progranulin deficiency associated with frontotemporal lobar degeneration by alkalizing reagents and inhibition of vacuolar ATPase.

Capell A, Liebscher S, Fellerer K, Brouwers N, Willem M, Lammich S, Gijselinck I, Bittner T, Carlson AM, Sasse F, Kunze B, Steinmetz H, Jansen R, Dormann D, Sleegers K, Cruts M, Herms J, Van Broeckhoven C, Haass C

Abstract

Numerous loss-of-function mutations in the progranulin (GRN) gene cause frontotemporal lobar degeneration with ubiquitin and TAR-DNA binding protein 43-positive inclusions by reduced production and secretion of GRN. Consistent with the observation that GRN has neurotrophic properties, pharmacological stimulation of GRN production is a promising approach to rescue GRN haploinsufficiency and prevent disease progression. We therefore searched for compounds capable of selectively increasing GRN levels. Here, we demonstrate that four independent and highly selective inhibitors of vacuolar ATPase (bafilomycin A1, concanamycin A, archazolid B, and apicularen A) significantly elevate intracellular and secreted GRN. Furthermore, clinically used alkalizing drugs, including chloroquine, bepridil, and amiodarone, similarly stimulate GRN production. Elevation of GRN levels occurs via a translational mechanism independent of lysosomal degradation, autophagy, or endocytosis. Importantly, alkalizing reagents rescue GRN deficiency in organotypic cortical slice cultures from a mouse model for GRN deficiency and in primary cells derived from human patients with GRN loss-of-function mutations. Thus, alkalizing reagents, specifically those already used in humans for other applications, and vacuolar ATPase inhibitors may be therapeutically used to prevent GRN-dependent neurodegeneration.

MeSH Terms
Alkalies/pharmacology Amiodarone/pharmacology Animals Animals, Newborn Autophagy-Related Protein 5 Bepridil/pharmacology Blotting, Northern Bridged Bicyclo Compounds, Heterocyclic/pharmacology Cells, Cultured Cerebral Cortex/drug effects,metabolism Chloroquine/pharmacology Enzyme-Linked Immunosorbent Assay Female Fibroblasts/drug effects,metabolism Frontotemporal Lobar Degeneration/drug therapy,genetics,metabolism Granulins HEK293 Cells HeLa Cells Humans Intercellular Signaling Peptides and Proteins/deficiency,genetics,metabolism Macrolides/pharmacology Male Mice Microtubule-Associated Proteins/deficiency,genetics Mutation Neurons/drug effects,metabolism Progranulins RNA, Messenger/drug effects Reverse Transcriptase Polymerase Chain Reaction Thiazoles/pharmacology Vacuolar Proton-Translocating ATPases/antagonists & inhibitors
Chemicals
Alkalies Atg5 protein, mouse Autophagy-Related Protein 5 Bridged Bicyclo Compounds, Heterocyclic Granulins Grn protein, mouse Intercellular Signaling Peptides and Proteins Macrolides Microtubule-Associated Proteins Progranulins RNA, Messenger Thiazoles apicularen A archazolid B Bepridil concanamycin A Chloroquine bafilomycin A1 Vacuolar Proton-Translocating ATPases Amiodarone
Authors & Affiliations
19 authors, click to expand affiliations / ORCID
Capell Anja
German Center for Neurodegenerative Diseases, Ludwig Maximilians University, 80336 Munich, Germany. [email protected]
Liebscher Sabine
Fellerer Katrin
Brouwers Nathalie
Willem Michael
Lammich Sven
Gijselinck Ilse
Bittner Tobias
Carlson Aaron M
Sasse Florenz
Kunze Brigitte
Steinmetz Heinrich
Jansen Rolf
Dormann Dorothee
Sleegers Kristel
Cruts Marc
Herms Jochen
Van Broeckhoven Christine
Haass Christian
References (43)
43 references, click to expand
  1. Plasma progranulin levels predict progranulin mutation status in frontotemporal dementia patients and asymptomatic family members.
    Brain. 2009 Mar;132(Pt 3):583-91 PMID: 19158106
  2. Missense mutations in the progranulin gene linked to frontotemporal lobar degeneration with ubiquitin-immunoreactive inclusions reduce progranulin production and secretion.
    J Biol Chem. 2008 Jan 18;283(3):1744-1753 PMID: 17984093
  3. Frontotemporal dementia.
    Semin Neurol. 2007 Feb;27(1):48-57 PMID: 17226741
  4. Archazolid and apicularen: novel specific V-ATPase inhibitors.
    BMC Biochem. 2005 Aug 04;6:13 PMID: 16080788
  5. Granulin mutations associated with frontotemporal lobar degeneration and related disorders: an update.
    Hum Mutat. 2008 Dec;29(12):1373-86 PMID: 18543312
  6. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17.
    Nature. 2006 Aug 24;442(7105):916-9 PMID: 16862116
  7. Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21.
    Nature. 2006 Aug 24;442(7105):920-4 PMID: 16862115
  8. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis.
    Science. 2006 Oct 6;314(5796):130-3 PMID: 17023659
  9. Targeting vacuolar H+-ATPases as a new strategy against cancer.
    Cancer Res. 2007 Nov 15;67(22):10627-30 PMID: 18006801
  10. Immunohistochemical demonstration of the distribution of chloroquine (CQ) and its metabolites in CQ-poisoned mice.
    Arch Toxicol. 2007 Jul;81(7):471-8 PMID: 17593411
  11. Alteration of behavioural phenotype in mice by targeted disruption of the progranulin gene.
    Behav Brain Res. 2007 Dec 28;185(2):110-8 PMID: 17764761
  12. Alzheimer and Parkinson diagnoses in progranulin null mutation carriers in an extended founder family.
    Arch Neurol. 2007 Oct;64(10):1436-46 PMID: 17923627
  13. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology.
    Nat Rev Mol Cell Biol. 2007 Nov;8(11):917-29 PMID: 17912264
  14. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin.
    J Clin Invest. 2008 Jul;118(7):2438-47 PMID: 18568075
  15. Bepridil. A review of its pharmacological properties and therapeutic use in stable angina pectoris.
    Drugs. 1992 Nov;44(5):835-57 PMID: 1280569
  16. A gene network regulating lysosomal biogenesis and function.
    Science. 2009 Jul 24;325(5939):473-7 PMID: 19556463
  17. Expression of the Alzheimer protease BACE1 is suppressed via its 5'-untranslated region.
    EMBO Rep. 2004 Jun;5(6):620-5 PMID: 15167888
  18. Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-frontotemporal dementia phenotypes.
    J Neurol Neurosurg Psychiatry. 2007 Jul;78(7):754-6 PMID: 17371905
  19. Low plasma progranulin levels predict progranulin mutations in frontotemporal lobar degeneration.
    Neurology. 2008 Oct 14;71(16):1235-9 PMID: 18768919
  20. Exaggerated inflammation, impaired host defense, and neuropathology in progranulin-deficient mice.
    J Exp Med. 2010 Jan 18;207(1):117-28 PMID: 20026663
  21. Genetic variability in progranulin contributes to risk for clinically diagnosed Alzheimer disease.
    Neurology. 2008 Aug 26;71(9):656-64 PMID: 18565828
  22. Loss of progranulin function in frontotemporal lobar degeneration.
    Trends Genet. 2008 Apr;24(4):186-94 PMID: 18328591
  23. The granulin gene family: from cancer to dementia.
    Bioessays. 2009 Nov;31(11):1245-54 PMID: 19795409
  24. Amiodarone and bepridil inhibit anthrax toxin entry into host cells.
    Antimicrob Agents Chemother. 2007 Jul;51(7):2403-11 PMID: 17485504
  25. Bepridil and amiodarone simultaneously target the Alzheimer's disease beta- and gamma-secretase via distinct mechanisms.
    J Neurosci. 2010 Jun 30;30(26):8974-83 PMID: 20592218
  26. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies.
    Eur J Pharmacol. 2009 Dec 25;625(1-3):220-33 PMID: 19836374
  27. A new subtype of frontotemporal lobar degeneration with FUS pathology.
    Brain. 2009 Nov;132(Pt 11):2922-31 PMID: 19674978
  28. The bafilomycin/concanamycin binding site in subunit c of the V-ATPases from Neurospora crassa and Saccharomyces cerevisiae.
    J Biol Chem. 2004 Aug 6;279(32):33131-8 PMID: 15180988
  29. The dynamic nature of the Golgi complex.
    J Cell Biol. 1989 Feb;108(2):277-97 PMID: 2537312
  30. Pharmacokinetics of amiodarone in rats.
    J Cardiovasc Pharmacol. 1982 Mar-Apr;4(2):270-5 PMID: 6175811
  31. Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival.
    J Cell Biol. 2008 Apr 7;181(1):37-41 PMID: 18378771
  32. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes.
    Immunity. 2007 Jan;26(1):79-92 PMID: 17182262
  33. Molecular characterization of novel progranulin (GRN) mutations in frontotemporal dementia.
    Hum Mutat. 2008 Apr;29(4):512-21 PMID: 18183624
  34. Amiodarone: guidelines for use and monitoring.
    Am Fam Physician. 2003 Dec 1;68(11):2189-96 PMID: 14677664
  35. The novel membrane protein TMEM59 modulates complex glycosylation, cell surface expression, and secretion of the amyloid precursor protein.
    J Biol Chem. 2010 Jul 2;285(27):20664-74 PMID: 20427278
  36. Mutations other than null mutations producing a pathogenic loss of progranulin in frontotemporal dementia.
    Hum Mutat. 2007 Apr;28(4):416 PMID: 17345602
  37. Progranulin is a stress-response factor in fibroblasts subjected to hypoxia and acidosis.
    Growth Factors. 2007 Aug;25(4):280-5 PMID: 18092235
  38. The molecular genetics and neuropathology of frontotemporal lobar degeneration: recent developments.
    Neurogenetics. 2007 Nov;8(4):237-48 PMID: 17805587
  39. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells.
    J Cell Biol. 2001 Feb 19;152(4):657-68 PMID: 11266458
  40. Serum biomarker for progranulin-associated frontotemporal lobar degeneration.
    Ann Neurol. 2009 May;65(5):603-9 PMID: 19288468
  41. Progranulin is expressed within motor neurons and promotes neuronal cell survival.
    BMC Neurosci. 2009 Oct 27;10:130 PMID: 19860916
  42. Inhibitors of V-ATPases: old and new players.
    J Exp Biol. 2009 Feb;212(Pt 3):341-6 PMID: 19151208
  43. Organotypic entorhino-hippocampal slice cultures--a tool to study the molecular and cellular regulation of axonal regeneration and collateral sprouting in vitro.
    Methods Mol Biol. 2007;399:55-66 PMID: 18309925
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2011-02-02
Pages
1885-94
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6623716
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]