Home LiteratureArticle Details
PMID: 19581584 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons.

Simons JP, Al-Shawi R, Minogue S, Waugh MG, Wiedemann C, Evangelou S, Loesch A, Sihra TS, King R, Warner TT, Hsuan JJ

Abstract

Phosphoinositide (PI) lipids are intracellular membrane signaling intermediates and effectors produced by localized PI kinase and phosphatase activities. Although many signaling roles of PI kinases have been identified in cultured cell lines, transgenic animal studies have produced unexpected insight into the in vivo functions of specific PI 3- and 5-kinases, but no mammalian PI 4-kinase (PI4K) knockout has previously been reported. Prior studies using cultured cells implicated the PI4K2alpha isozyme in diverse functions, including receptor signaling, ion channel regulation, endosomal trafficking, and regulated secretion. We now show that despite these important functions, mice lacking PI4K2alpha kinase activity initially appear normal. However, adult Pi4k2a(GT/GT) animals develop a progressive neurological disease characterized by tremor, limb weakness, urinary incontinence, and premature mortality. Histological analysis of aged Pi4k2a(GT/GT) animals revealed lipofuscin-like deposition and gliosis in the cerebellum, and loss of Purkinje cells. Peripheral nerves are essentially normal, but massive axonal degeneration was found in the spinal cord in both ascending and descending tracts. These results reveal a previously undescribed role for aberrant PI signaling in neurological disease that resembles autosomal recessive hereditary spastic paraplegia.

MeSH Terms
Alanine Transaminase/blood Animals Aspartate Aminotransferases/blood Axons/metabolism,pathology Blood Chemical Analysis Mice Mice, Knockout Minor Histocompatibility Antigens Nerve Degeneration/metabolism Phosphotransferases (Alcohol Group Acceptor)/deficiency Signal Transduction/genetics,physiology Spinal Cord/cytology,pathology
Chemicals
Minor Histocompatibility Antigens Aspartate Aminotransferases Alanine Transaminase Phosphotransferases (Alcohol Group Acceptor) phosphatidylinositol phosphate 4-kinase
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Simons J Paul
Division of Medicine, Royal Free Centre for Biomedical Science, University College London Medical School, University College London, London NW3 2PF, United Kingdom.
Al-Shawi Raya
Minogue Shane
Waugh Mark G
Wiedemann Claudia
Evangelou Stylianos
Loesch Andrzej
Sihra Talvinder S
King Rosalind
Warner Thomas T
Hsuan J Justin
References (38)
38 references, click to expand
  1. The Saccharomyces cerevisiae LSB6 gene encodes phosphatidylinositol 4-kinase activity.
    J Biol Chem. 2002 Dec 6;277(49):47709-18 PMID: 12361950
  2. Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue.
    J Histochem Cytochem. 1999 Jun;47(6):719-30 PMID: 10330448
  3. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking.
    Nature. 2004 Sep 23;431(7007):415-22 PMID: 15386003
  4. Physiological roles of clathrin adaptor AP complexes: lessons from mutant animals.
    J Biochem. 2006 Jun;139(6):943-8 PMID: 16788044
  5. Wnt3a-mediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation.
    Science. 2008 Sep 5;321(5894):1350-3 PMID: 18772438
  6. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor.
    J Cell Sci. 2006 Feb 1;119(Pt 3):571-81 PMID: 16443754
  7. Neuronal and non-neuronal functions of the AP-3 sorting machinery.
    J Cell Sci. 2007 Feb 15;120(Pt 4):531-41 PMID: 17287392
  8. Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3995-4000 PMID: 12646710
  9. Molecular anatomy of a trafficking organelle.
    Cell. 2006 Nov 17;127(4):831-46 PMID: 17110340
  10. A WASp-binding type II phosphatidylinositol 4-kinase required for actin polymerization-driven endosome motility.
    J Cell Biol. 2005 Oct 10;171(1):133-42 PMID: 16216926
  11. A public gene trap resource for mouse functional genomics.
    Nat Genet. 2004 Jun;36(6):543-4 PMID: 15167922
  12. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments.
    J Biol Chem. 2002 May 31;277(22):20041-50 PMID: 11923287
  13. Actin-based motility during endocytosis in budding yeast.
    Mol Biol Cell. 2006 Mar;17(3):1354-63 PMID: 16394096
  14. Newly synthesized phosphatidylinositol phosphates are required for synaptic norepinephrine but not glutamate or gamma-aminobutyric acid (GABA) release.
    J Biol Chem. 1998 Aug 21;273(34):21451-4 PMID: 9705272
  15. Phosphatidylinositol-4-kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic.
    Mol Biol Cell. 2008 Apr;19(4):1415-26 PMID: 18256276
  16. Properties of synaptic vesicle pools in mature central nerve terminals.
    J Biol Chem. 2005 Nov 4;280(44):37278-88 PMID: 16148008
  17. Milk composition and lactation of beta-casein-deficient mice.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6138-42 PMID: 8016126
  18. Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms.
    Lancet Neurol. 2008 Dec;7(12):1127-38 PMID: 19007737
  19. Signalling by PI3K isoforms: insights from gene-targeted mice.
    Trends Biochem Sci. 2005 Apr;30(4):194-204 PMID: 15817396
  20. Estrogen increases retrograde labeling of motoneurons: evidence of a nongenomic mechanism.
    Am J Physiol Cell Physiol. 2004 Aug;287(2):C320-6 PMID: 15044155
  21. Phosphatidylinositol 4-kinases: old enzymes with emerging functions.
    Trends Cell Biol. 2006 Jul;16(7):351-61 PMID: 16793271
  22. An essential role for a small synaptic vesicle-associated phosphatidylinositol 4-kinase in neurotransmitter release.
    J Neurosci. 1998 Aug 1;18(15):5594-602 PMID: 9671651
  23. Phosphatidylinositol kinase enzymes regulate the retrograde axonal transport of NT-3 and NT-4 in sympathetic and sensory neurons.
    J Neurosci Res. 2002 Apr 15;68(2):169-75 PMID: 11948662
  24. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport.
    J Clin Invest. 2004 Jan;113(2):231-42 PMID: 14722615
  25. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi.
    Cell. 2003 Aug 8;114(3):299-310 PMID: 12914695
  26. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling.
    Neuron. 2006 Jul 6;51(1):71-84 PMID: 16815333
  27. PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal.
    Mol Biol Cell. 2007 Jul;18(7):2646-55 PMID: 17494868
  28. Molecular determinants of activation and membrane targeting of phosphoinositol 4-kinase IIbeta.
    Biochem J. 2008 Jan 15;409(2):501-9 PMID: 17927563
  29. Evidence for phosphatidylinositol 4-kinase and actin involvement in the regulation of 125I-beta-nerve growth factor retrograde axonal transport.
    J Neurochem. 1999 Jul;73(1):87-95 PMID: 10386958
  30. The role of ZFYVE27/protrudin in hereditary spastic paraplegia.
    Am J Hum Genet. 2008 Jul;83(1):127-8; author reply 128-30 PMID: 18606302
  31. You say lipofuscin, we say ceroid: defining autofluorescent storage material.
    Neurobiol Aging. 2006 Apr;27(4):576-88 PMID: 16455164
  32. Molecular motors and mechanisms of directional transport in neurons.
    Nat Rev Neurosci. 2005 Mar;6(3):201-14 PMID: 15711600
  33. Hermansky-Pudlak syndrome protein complexes associate with phosphatidylinositol 4-kinase type II alpha in neuronal and non-neuronal cells.
    J Biol Chem. 2009 Jan 16;284(3):1790-802 PMID: 19010779
  34. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment.
    Mamm Genome. 1997 Oct;8(10):711-3 PMID: 9321461
  35. PIP5KI gamma is required for cardiovascular and neuronal development.
    Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11748-53 PMID: 17609388
  36. A multi-exonic SPG4 duplication underlies sex-dependent penetrance of hereditary spastic paraplegia in a large Brazilian pedigree.
    Eur J Hum Genet. 2007 Dec;15(12):1276-9 PMID: 17895902
  37. Loss of PIP5KIbeta demonstrates that PIP5KI isoform-specific PIP2 synthesis is required for IP3 formation.
    Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):14064-9 PMID: 18772378
  38. Regulation of anaphylactic responses by phosphatidylinositol phosphate kinase type I {alpha}.
    J Exp Med. 2005 Mar 21;201(6):859-70 PMID: 15767368
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-07-14
Epub
2009-00-06
Pages
11535-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2710652
Subset
IM
Grants
Cancer Research UK · C25540/A8562 · United Kingdom
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]