Home LiteratureArticle Details
PMID: 18504603 Published · ppublish English Journal Article Review

The varitint-waddler mouse phenotypes and the TRPML3 ion channel mutation: cause and consequence.

Pflugers Archiv : European journal of physiology ·Vol. 457 ·No. 2 ·2008-11-00 ·Pages 463-73

Cuajungco MP, Samie MA

Abstract

The transient receptor potential mucolipins (TRPMLs) are the most recently discovered subfamily of TRP ion channel proteins. Positional cloning approach has identified two mutations in the TRPML3 (Mcoln3) gene that cause the varitint-waddler mouse phenotypes. Short for variable tint (diluted coat color), the varitint-waddler consists two phenotypes Va and Va ( J ). The mutation associated with the Va phenotype is an alanine to proline substitution at position 419 (A419P) within the predicted fifth transmembrane (TM5) domain of TRPML3. The second Va ( J ) mouse phenotype arose spontaneously from an isoleucine to threonine substitution at position 362 (I362T) that is proximal to the predicted TM3 domain in addition to the existing A419P mutation on TM5. Mice with the Va and Va ( J ) mutations exhibit a spectrum of disease phenotypes from diluted coat color to auditory and vestibular problems, depending on which alleles are present. It has been over 5 years since the discovery of these TRPML3 mutations, and it was just recently that the nature of these mutations has been characterized. In this review, we discuss the molecular and cell physiological effects of the two distinct TRPML3 mutations. We reveal the effects of proline substitution on transmembrane domain structure and channel function and discuss how the Va mutation confers its cytotoxicity, while the Va ( J ) mutation results in an apparent rescue phenotype. Finally, we briefly tackle molecular strategies that have been employed to neutralize the cytotoxic effect and constitutive channel activity of the Va mutation.

MeSH Terms
Alanine Animals Calcium/metabolism Genetic Predisposition to Disease Genotype Hair Color/genetics Hearing/genetics Hearing Disorders/genetics,metabolism Isoleucine Membrane Potentials Mice Mice, Mutant Strains Models, Molecular Mutation Phenotype Proline Protein Conformation Protein Structure, Tertiary Skin Pigmentation/genetics TRPM Cation Channels/chemistry,genetics,metabolism Threonine Transient Receptor Potential Channels
Chemicals
Mcoln3 protein, mouse TRPM Cation Channels Transient Receptor Potential Channels Isoleucine Threonine Proline Alanine Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cuajungco Math P
Department of Biological Science, California State University, Fullerton, CA 92831, USA. mcuajungco@fullerton.edu
Samie Mohammad A
References (49)
49 references, click to expand
  1. Two di-leucine motifs regulate trafficking of mucolipin-1 to lysosomes.
    Traffic. 2006 Mar;7(3):337-53 PMID: 16497227
  2. Proline-induced hinges in transmembrane helices: possible roles in ion channel gating.
    Proteins. 2001 Aug 1;44(2):63-72 PMID: 11391769
  3. Mucolipin-2 localizes to the Arf6-associated pathway and regulates recycling of GPI-APs.
    Traffic. 2007 Oct;8(10):1404-14 PMID: 17662026
  4. Neurochemical correlates of the waltzing-shaker syndrome in the Varitint-waddler mouse.
    Psychopharmacologia. 1972;24(3):384-96 PMID: 5064304
  5. TRP channels: a TR(I)P through a world of multifunctional cation channels.
    Pflugers Arch. 2005 Oct;451(1):1-10 PMID: 16012814
  6. Proline-induced distortions of transmembrane helices.
    J Mol Biol. 2002 Nov 8;323(5):951-60 PMID: 12417206
  7. The varitint-waddler (Va) deafness mutation in TRPML3 generates constitutive, inward rectifying currents and causes cell degeneration.
    Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):353-8 PMID: 18162548
  8. Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1.
    J Biol Chem. 2006 Jun 23;281(25):17517-17527 PMID: 16606612
  9. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels.
    Nature. 2004 Aug 12;430(7001):748-54 PMID: 15306801
  10. Genetic analyses of the mouse deafness mutations varitint-waddler (Va) and jerker (Espnje).
    J Assoc Res Otolaryngol. 2003 Mar;4(1):83-90 PMID: 12209292
  11. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents.
    Cell. 2006 Mar 24;124(6):1269-82 PMID: 16564016
  12. Functional links between mucolipin-1 and Ca2+-dependent membrane trafficking in mucolipidosis IV.
    Biochem Biophys Res Commun. 2004 Oct 1;322(4):1384-91 PMID: 15336987
  13. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel.
    Hum Mol Genet. 2000 Oct 12;9(17):2471-8 PMID: 11030752
  14. A novel mode of TRPML3 regulation by extracytosolic pH absent in the varitint-waddler phenotype.
    EMBO J. 2008 Apr 23;27(8):1197-205 PMID: 18369318
  15. Lysosomal exocytosis is impaired in mucolipidosis type IV.
    Mol Genet Metab. 2006 Dec;89(4):339-48 PMID: 16914343
  16. Permeation and selectivity of TRP channels.
    Annu Rev Physiol. 2006;68:685-717 PMID: 16460288
  17. Conformational changes of pore helix coupled to gating of TRPV5 by protons.
    EMBO J. 2005 Sep 21;24(18):3224-34 PMID: 16121193
  18. Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic.
    Traffic. 2006 Oct;7(10):1388-98 PMID: 16978393
  19. Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4483-8 PMID: 15070744
  20. Combined cochleo-saccular and neuroepithelial abnormalities in the Varitint-waddler-J (VaJ) mouse.
    Hear Res. 1998 Sep;123(1-2):125-36 PMID: 9745961
  21. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling.
    Electrophoresis. 1997 Dec;18(15):2714-23 PMID: 9504803
  22. Gain-of-function mutation in TRPML3 causes the mouse Varitint-Waddler phenotype.
    J Biol Chem. 2007 Dec 14;282(50):36138-42 PMID: 17962195
  23. TRPML cation channels regulate the specialized lysosomal compartment of vertebrate B-lymphocytes.
    Eur J Cell Biol. 2006 Dec;85(12):1253-64 PMID: 17050035
  24. Gating of shaker-type channels requires the flexibility of S6 caused by prolines.
    J Biol Chem. 2003 Dec 12;278(50):50724-31 PMID: 13679372
  25. Voltage sensor of Kv1.2: structural basis of electromechanical coupling.
    Science. 2005 Aug 5;309(5736):903-8 PMID: 16002579
  26. A helix-breaking mutation in TRPML3 leads to constitutive activity underlying deafness in the varitint-waddler mouse.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19583-8 PMID: 18048323
  27. T-Coffee: A novel method for fast and accurate multiple sequence alignment.
    J Mol Biol. 2000 Sep 8;302(1):205-17 PMID: 10964570
  28. Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14994-9 PMID: 12403827
  29. Identification of the gene causing mucolipidosis type IV.
    Nat Genet. 2000 Sep;26(1):118-23 PMID: 10973263
  30. Differential expression and molecular characterisation of Lmo7, Myo1e, Sash1, and Mcoln2 genes in Btk-defective B-cells.
    Cell Immunol. 2005 May;235(1):46-55 PMID: 16137664
  31. Defective B cell development and function in Btk-deficient mice.
    Immunity. 1995 Sep;3(3):283-99 PMID: 7552994
  32. On the distribution of amino acid residues in transmembrane alpha-helix bundles.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4577-81 PMID: 7753846
  33. TRP-ML1 is a lysosomal monovalent cation channel that undergoes proteolytic cleavage.
    J Biol Chem. 2005 Dec 30;280(52):43218-23 PMID: 16257972
  34. The TRP ion channel family.
    Nat Rev Neurosci. 2001 Jun;2(6):387-96 PMID: 11389472
  35. SWISS-MODEL: An automated protein homology-modeling server.
    Nucleic Acids Res. 2003 Jul 1;31(13):3381-5 PMID: 12824332
  36. Varitint-waddler: a double whammy for hearing.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14613-5 PMID: 12417743
  37. TRPML and lysosomal function.
    Biochim Biophys Acta. 2007 Aug;1772(8):851-8 PMID: 17306511
  38. Cation channel activity of mucolipin-1: the effect of calcium.
    Pflugers Arch. 2005 Oct;451(1):304-12 PMID: 16133264
  39. The TRP superfamily of cation channels.
    Sci STKE. 2005 Feb 22;2005(272):re3 PMID: 15728426
  40. TRP-ML1 regulates lysosomal pH and acidic lysosomal lipid hydrolytic activity.
    J Biol Chem. 2006 Mar 17;281(11):7294-301 PMID: 16361256
  41. Activating mutation in a mucolipin transient receptor potential channel leads to melanocyte loss in varitint-waddler mice.
    Proc Natl Acad Sci U S A. 2007 Nov 13;104(46):18321-6 PMID: 17989217
  42. Molecular pathophysiology of mucolipidosis type IV: pH dysregulation of the mucolipin-1 cation channel.
    Hum Mol Genet. 2004 Mar 15;13(6):617-27 PMID: 14749347
  43. The selectivity filter of the cation channel TRPM4.
    J Biol Chem. 2005 Jun 17;280(24):22899-906 PMID: 15845551
  44. Identification and characterization of the single channel function of human mucolipin-1 implicated in mucolipidosis type IV, a disorder affecting the lysosomal pathway.
    FEBS Lett. 2002 Dec 4;532(1-2):183-7 PMID: 12459486
  45. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells.
    Nature. 2004 Dec 9;432(7018):723-30 PMID: 15483558
  46. Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV.
    Am J Hum Genet. 2000 Nov;67(5):1110-20 PMID: 11013137
  47. Posttranslational cleavage and adaptor protein complex-dependent trafficking of mucolipin-1.
    J Biol Chem. 2006 May 5;281(18):12751-9 PMID: 16517607
  48. Outer pore topology of the ECaC-TRPV5 channel by cysteine scan mutagenesis.
    J Biol Chem. 2004 Feb 20;279(8):6853-62 PMID: 14630907
  49. TRP channels as candidates for hearing and balance abnormalities in vertebrates.
    Biochim Biophys Acta. 2007 Aug;1772(8):1022-7 PMID: 17300924
Article Info
Journal
Pflugers Archiv : European journal of physiology
Abbr.
Pflugers Arch
ISSN
0031-6768
Published
2008-11-00
Epub
2008-00-27
Pages
463-73
Language
English
Region
Germany
NLM ID
0154720
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: product@genelibs.com