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PMID: 18349142 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Loss of the inactive myotubularin-related phosphatase Mtmr13 leads to a Charcot-Marie-Tooth 4B2-like peripheral neuropathy in mice.

Robinson FL, Niesman IR, Beiswenger KK, Dixon JE

Abstract

Charcot-Marie-Tooth disease type 4B (CMT4B) is a severe, demyelinating peripheral neuropathy characterized by slowed nerve conduction velocity, axon loss, and distinctive myelin outfolding and infolding. CMT4B is caused by recessive mutations in either myotubularin-related protein 2 (MTMR2; CMT4B1) or MTMR13 (CMT4B2). Myotubularins are phosphoinositide (PI) 3-phosphatases that dephosphorylate phosphatidylinositol 3-phosphate (PtdIns3P) and PtdIns(3,5)P(2), two phosphoinositides that regulate endosomal-lysosomal membrane traffic. Interestingly, nearly half of the metazoan myotubularins are predicted to be catalytically inactive. Both active and inactive myotubularins have essential functions in mammals and in Caenorhabditis elegans. MTMR2 and MTMR13 are active and inactive PI 3-phosphatases, respectively, and the two proteins have been shown to directly associate, although the functional significance of this association is not well understood. To establish a mouse model of CMT4B2, we disrupted the Mtmr13 gene. Mtmr13-deficient mice develop a peripheral neuropathy characterized by reduced nerve conduction velocity and myelin outfoldings and infoldings. Dysmyelination is evident in Mtmr13-deficient nerves at 14 days and worsens throughout life. Thus, loss of Mtmr13 in mice leads to a peripheral neuropathy with many of the key features of CMT4B2. Although myelin outfoldings and infoldings occur most frequently at the paranode, our morphological analyses indicate that the ultrastructure of the node of Ranvier and paranode is intact in Mtmr13-deficient nerve fibers. We also found that Mtmr2 levels are decreased by approximately 50% in Mtmr13-deficient sciatic nerves, suggesting a mode of Mtmr2 regulation. Mtmr13-deficient mice will be an essential tool for studying how the loss of MTMR13 leads to CMT4B2.

MeSH Terms
Animals Charcot-Marie-Tooth Disease/enzymology Enzyme Activation Gene Deletion Mice Nerve Fibers/pathology,ultrastructure Peripheral Nerves/pathology,ultrastructure Protein Tyrosine Phosphatases, Non-Receptor/deficiency,genetics
Chemicals
Protein Tyrosine Phosphatases, Non-Receptor Sbf2 protein, mouse
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Robinson Fred L
Department of Pharmacology, University of California at San Diego, La Jolla, CA 92093, USA.
Niesman Ingrid R
Beiswenger Kristina K
Dixon Jack E
References (56)
56 references, click to expand
  1. Identification of a new locus for autosomal recessive Charcot-Marie-Tooth disease with focally folded myelin on chromosome 11p15.
    Genomics. 1999 Dec 15;62(3):344-9 PMID: 10644431
  2. Hereditary motor and sensory neuropathy with myelin folding and juvenile onset glaucoma.
    Neurology. 2000 Aug 8;55(3):392-7 PMID: 10932274
  3. Genetic heterogeneity in autosomal recessive hereditary motor and sensory neuropathy with focally folded myelin sheaths (CMT4B).
    Neurology. 1998 Mar;50(3):799-801 PMID: 9521281
  4. Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans.
    Mol Biol Cell. 2004 Jan;15(1):189-96 PMID: 14565969
  5. Characterization of MTMR3. an inositol lipid 3-phosphatase with novel substrate specificity.
    Curr Biol. 2001 Oct 16;11(20):1600-5 PMID: 11676921
  6. Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2.
    Nat Genet. 2000 May;25(1):17-9 PMID: 10802647
  7. Alterations in degradative pathways and protein aggregation in a neuropathy model based on PMP22 overexpression.
    Neurobiol Dis. 2006 Apr;22(1):153-64 PMID: 16326107
  8. An animal model for Charcot-Marie-Tooth disease type 4B1.
    Hum Mol Genet. 2005 Dec 1;14(23):3685-95 PMID: 16249189
  9. Association of frabin with the actin cytoskeleton is essential for microspike formation through activation of Cdc42 small G protein.
    J Biol Chem. 1999 Sep 3;274(36):25197-200 PMID: 10464238
  10. NF-M is an essential target for the myelin-directed "outside-in" signaling cascade that mediates radial axonal growth.
    J Cell Biol. 2003 Dec 8;163(5):1011-20 PMID: 14662745
  11. Phosphatidylinositol 3-phosphate indirectly activates KCa3.1 via 14 amino acids in the carboxy terminus of KCa3.1.
    Mol Biol Cell. 2006 Jan;17(1):146-54 PMID: 16251351
  12. The Cys(X)5Arg catalytic motif in phosphoester hydrolysis.
    Biochemistry. 1994 Dec 27;33(51):15266-70 PMID: 7803389
  13. Finding the causes of inherited neuropathies.
    Arch Neurol. 2006 Jun;63(6):812-6 PMID: 16769861
  14. Systematic analysis of myotubularins: heteromeric interactions, subcellular localisation and endosome related functions.
    J Cell Sci. 2006 Jul 15;119(Pt 14):2953-9 PMID: 16787938
  15. Protein tyrosine phosphatases: from genes, to function, to disease.
    Nat Rev Mol Cell Biol. 2006 Nov;7(11):833-46 PMID: 17057753
  16. The phosphoinositide-3-phosphatase MTMR2 associates with MTMR13, a membrane-associated pseudophosphatase also mutated in type 4B Charcot-Marie-Tooth disease.
    J Biol Chem. 2005 Sep 9;280(36):31699-707 PMID: 15998640
  17. The myotubularin family of lipid phosphatases.
    Traffic. 2005 Dec;6(12):1063-9 PMID: 16262718
  18. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast.
    Nat Genet. 1996 Jun;13(2):175-82 PMID: 8640223
  19. Peripheral nerve demyelination caused by a mutant Rho GTPase guanine nucleotide exchange factor, frabin/FGD4.
    Am J Hum Genet. 2007 Jul;81(1):158-64 PMID: 17564972
  20. PTEN and myotubularin phosphatases: from 3-phosphoinositide dephosphorylation to disease.
    Trends Cell Biol. 2002 Dec;12(12):579-85 PMID: 12495846
  21. Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases.
    Hum Mol Genet. 2003 Oct 15;12 Spec No 2:R285-92 PMID: 12925573
  22. Mutations in MTMR13, a new pseudophosphatase homologue of MTMR2 and Sbf1, in two families with an autosomal recessive demyelinating form of Charcot-Marie-Tooth disease associated with early-onset glaucoma.
    Am J Hum Genet. 2003 May;72(5):1141-53 PMID: 12687498
  23. SET binding factor 2 (SBF2) mutation causes CMT4B with juvenile onset glaucoma.
    Neurology. 2004 Aug 10;63(3):577-80 PMID: 15304601
  24. Disease mechanisms in inherited neuropathies.
    Nat Rev Neurosci. 2003 Sep;4(9):714-26 PMID: 12951564
  25. Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J.
    Nature. 2007 Jul 5;448(7149):68-72 PMID: 17572665
  26. Characterization of myotubularin-related protein 7 and its binding partner, myotubularin-related protein 9.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9768-73 PMID: 12890864
  27. Mtmr13/Sbf2-deficient mice: an animal model for CMT4B2.
    Hum Mol Genet. 2007 Dec 15;16(24):2991-3001 PMID: 17855448
  28. Autosomal recessive hereditary motor and sensory neuropathy with focally folded myelin sheaths: clinical, electrophysiologic, and genetic aspects of a large family.
    Neurology. 1996 May;46(5):1318-24 PMID: 8628474
  29. Identification of myotubularin as the lipid phosphatase catalytic subunit associated with the 3-phosphatase adapter protein, 3-PAP.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8660-5 PMID: 12847286
  30. Charcot-Marie-Tooth type 4B demyelinating neuropathy: deciphering the role of MTMR phosphatases.
    Expert Rev Mol Med. 2007 Sep 20;9(25):1-16 PMID: 17880751
  31. Essential role for the myotubularin-related phosphatase Ymr1p and the synaptojanin-like phosphatases Sjl2p and Sjl3p in regulation of phosphatidylinositol 3-phosphate in yeast.
    Mol Biol Cell. 2004 Aug;15(8):3567-79 PMID: 15169871
  32. Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain.
    Biochim Biophys Acta. 2006 Aug;1761(8):868-77 PMID: 16644267
  33. Loss of Mtmr2 phosphatase in Schwann cells but not in motor neurons causes Charcot-Marie-Tooth type 4B1 neuropathy with myelin outfoldings.
    J Neurosci. 2005 Sep 14;25(37):8567-77 PMID: 16162938
  34. Regulation of membrane traffic by phosphoinositide 3-kinases.
    J Cell Sci. 2006 Feb 15;119(Pt 4):605-14 PMID: 16467569
  35. Focally folded myelin in Charcot-Marie-Tooth type 1B disease is associated with Asn131Lys mutation in myelin protein zero gene: short report.
    Eur J Neurol. 2003 Sep;10(5):547-9 PMID: 12940837
  36. De- and remyelination in spinal roots during normal perinatal development in the cat: a brief summary of structural observations and a conceptual hypothesis.
    J Anat. 2002 Apr;200(4):391-403 PMID: 12090405
  37. Myotubularin, a phosphatase deficient in myotubular myopathy, acts on phosphatidylinositol 3-kinase and phosphatidylinositol 3-phosphate pathway.
    Hum Mol Genet. 2000 Sep 22;9(15):2223-9 PMID: 11001925
  38. Male infertility, impaired spermatogenesis, and azoospermia in mice deficient for the pseudophosphatase Sbf1.
    J Clin Invest. 2002 May;109(9):1165-72 PMID: 11994405
  39. Molecular mechanisms, diagnosis, and rational approaches to management of and therapy for Charcot-Marie-Tooth disease and related peripheral neuropathies.
    J Investig Med. 2003 Sep;51(5):261-83 PMID: 14577517
  40. The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology.
    Curr Opin Cell Biol. 2005 Aug;17(4):402-8 PMID: 15975782
  41. Regulation of myotubularin-related (MTMR)2 phosphatidylinositol phosphatase by MTMR5, a catalytically inactive phosphatase.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4492-7 PMID: 12668758
  42. Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis.
    J Cell Biol. 2004 Nov 22;167(4):711-21 PMID: 15557122
  43. Studies on the "incisures" of Schmidt and Lanterman.
    J Cell Sci. 1970 May;6(3):767-91 PMID: 5452094
  44. Mutations in FGD4 encoding the Rho GDP/GTP exchange factor FRABIN cause autosomal recessive Charcot-Marie-Tooth type 4H.
    Am J Hum Genet. 2007 Jul;81(1):1-16 PMID: 17564959
  45. Myotubularin phosphatases: policing 3-phosphoinositides.
    Trends Cell Biol. 2006 Aug;16(8):403-12 PMID: 16828287
  46. Mutation of the SBF2 gene, encoding a novel member of the myotubularin family, in Charcot-Marie-Tooth neuropathy type 4B2/11p15.
    Hum Mol Genet. 2003 Feb 1;12(3):349-56 PMID: 12554688
  47. Functional gap junctions in the schwann cell myelin sheath.
    J Cell Biol. 1998 Aug 24;142(4):1095-104 PMID: 9722620
  48. Focally folded myelin in Charcot-Marie-Tooth neuropathy type 1B with Ser49Leu in the myelin protein zero.
    Acta Neuropathol. 2000 Sep;100(3):299-304 PMID: 10965800
  49. Genetic analysis of the myotubularin family of phosphatases in Caenorhabditis elegans.
    J Biol Chem. 2003 Sep 5;278(36):34380-6 PMID: 12788949
  50. PTEN and myotubularins: families of phosphoinositide phosphatases.
    Methods Enzymol. 2003;366:43-56 PMID: 14674238
  51. Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions.
    Trends Biochem Sci. 2006 Jan;31(1):52-63 PMID: 16364647
  52. Autosomal recessive motor and sensory neuropathy with excessive myelin outfolding.
    Muscle Nerve. 1989 Jul;12(7):568-75 PMID: 2779605
  53. Therapeutic strategies for the inherited neuropathies.
    Neuromolecular Med. 2006;8(1-2):255-78 PMID: 16775380
  54. Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8910-5 PMID: 10900271
  55. Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions.
    J Cell Biol. 1995 Apr;129(1):189-202 PMID: 7698985
  56. Multi-level regulation of myotubularin-related protein-2 phosphatase activity by myotubularin-related protein-13/set-binding factor-2.
    Hum Mol Genet. 2006 Feb 15;15(4):569-79 PMID: 16399794
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
2008-03-25
Epub
2008-00-18
Pages
4916-21
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2290800
Subset
IM
Grants
NCI NIH HHS · CA100768 · United States
NIDDK NIH HHS · R37DK018024 · United States
NIDDK NIH HHS · R01 DK017780 · United States
NINDS NIH HHS · K99 NS057903 · United States
NCI NIH HHS · R01 CA100768 · United States
NIDDK NIH HHS · DK17780 · United States
NINDS NIH HHS · K99NS057903 · United States
NIDDK NIH HHS · R37 DK018024 · United States
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