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PMID: 19004782 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Altered functional properties of a TRPM2 variant in Guamanian ALS and PD.

Hermosura MC, Cui AM, Go RC, Davenport B, Shetler CM, Heizer JW, Schmitz C, Mocz G, Garruto RM, Perraud AL

Abstract

Two related neurodegenerative disorders, Western Pacific amyotrophic lateral sclerosis (ALS) and parkinsonism-dementia (PD), originally occurred at a high incidence on Guam, in the Kii peninsula of Japan, and in southern West New Guinea more than 50 years ago. These three foci shared a unique mineral environment characterized by the presence of severely low levels of Ca(2+) and Mg(2+), coupled with high levels of bioavailable transition metals in the soil and drinking water. Epidemiological studies suggest that genetic factors also contribute to the etiology of these disorders. Here, we report that a variant of the transient receptor potential melastatin 2 (TRPM2) gene may confer susceptibility to these diseases. TRPM2 encodes a calcium-permeable cation channel highly expressed in the brain that has been implicated in mediating cell death induced by oxidants. We found a heterozygous variant of TRPM2 in a subset of Guamanian ALS (ALS-G) and PD (PD-G) cases. This variant, TRPM2(P1018L), produces a missense change in the channel protein whereby proline 1018 (Pro(1018)) is replaced by leucine (Leu(1018)). Functional studies revealed that, unlike WT TRPM2, P1018L channels inactivate. Our results suggest that the ability of TRPM2 to maintain sustained ion influx is a physiologically important function and that its disruption may, under certain conditions, contribute to disease states.

MeSH Terms
Adenosine Diphosphate Ribose/pharmacology Amino Acid Sequence Amino Acids, Diamino/pharmacology Amyotrophic Lateral Sclerosis/metabolism Calcium/metabolism Calcium Signaling/drug effects Cell Membrane/drug effects,metabolism Conserved Sequence Cyanobacteria Toxins Evolution, Molecular Guam Humans Hydrogen Peroxide/pharmacology Ion Channel Gating/drug effects Leucine/genetics Magnesium/pharmacology Models, Molecular Molecular Sequence Data Mutant Proteins/metabolism Mutation/genetics Oxidative Stress/drug effects Parkinsonian Disorders/metabolism Proline/genetics TRPM Cation Channels/chemistry,genetics,metabolism Temperature
Chemicals
Amino Acids, Diamino Cyanobacteria Toxins Mutant Proteins TRPM Cation Channels TRPM2 protein, human beta-N-methylamino-L-alanine Adenosine Diphosphate Ribose Proline Hydrogen Peroxide Leucine Magnesium Calcium
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Hermosura Meredith C
Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA. meredith@pbrc.hawaii.edu
Cui Aaron M
Go Ramon Christopher V
Davenport Bennett
Shetler Cory M
Heizer Justin W
Schmitz Carsten
Mocz Gabor
Garruto Ralph M
Perraud Anne-Laure
References (32)
32 references, click to expand
  1. A critical role of TRPM2 in neuronal cell death by hydrogen peroxide.
    J Pharmacol Sci. 2006 May;101(1):66-76 PMID: 16651700
  2. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion.
    EMBO J. 2006 May 3;25(9):1804-15 PMID: 16601673
  3. TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration.
    Nat Med. 2008 Jul;14(7):738-47 PMID: 18542050
  4. Dynamic rearrangement of the outer mouth of a K+ channel during gating.
    Neuron. 1996 Apr;16(4):859-67 PMID: 8608004
  5. Magnesium deficiency over generations in rats with special references to the pathogenesis of the Parkinsonism-dementia complex and amyotrophic lateral sclerosis of Guam.
    Neuropathology. 2006 Apr;26(2):115-28 PMID: 16708544
  6. Chemotaxis of mouse bone marrow neutrophils and dendritic cells is controlled by adp-ribose, the major product generated by the CD38 enzyme reaction.
    J Immunol. 2007 Dec 1;179(11):7827-39 PMID: 18025229
  7. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology.
    Nature. 2001 May 31;411(6837):595-9 PMID: 11385575
  8. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis.
    Science. 2005 Jun 17;308(5729):1801-4 PMID: 15879175
  9. Endogenous ADP-ribose enables calcium-regulated cation currents through TRPM2 channels in neutrophil granulocytes.
    Biochem J. 2006 Sep 1;398(2):225-32 PMID: 16719842
  10. A TRPM7 variant shows altered sensitivity to magnesium that may contribute to the pathogenesis of two Guamanian neurodegenerative disorders.
    Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11510-5 PMID: 16051700
  11. Molecular determinants of voltage-dependent inactivation in calcium channels.
    Nature. 1994 Nov 3;372(6501):97-100 PMID: 7969428
  12. The contribution of mitochondrial dysfunction to a gene-environment model of Guamanian ALS and PD.
    Mitochondrion. 2008 Mar;8(2):109-16 PMID: 18054291
  13. Hydrogen peroxide and ADP-ribose induce TRPM2-mediated calcium influx and cation currents in microglia.
    Am J Physiol Cell Physiol. 2004 Jan;286(1):C129-37 PMID: 14512294
  14. Critical intracellular Ca2+ dependence of transient receptor potential melastatin 2 (TRPM2) cation channel activation.
    J Biol Chem. 2003 Mar 28;278(13):11002-6 PMID: 12529379
  15. Extracellular acid block and acid-enhanced inactivation of the Ca2+-activated cation channel TRPM5 involve residues in the S3-S4 and S5-S6 extracellular domains.
    J Biol Chem. 2005 May 27;280(21):20691-9 PMID: 15731110
  16. Evolutionary determinants of divergent calcium selectivity of TRPM channels.
    FASEB J. 2008 May;22(5):1540-51 PMID: 18073331
  17. The versatility and universality of calcium signalling.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):11-21 PMID: 11413485
  18. TRPM7 and TRPM2-Candidate susceptibility genes for Western Pacific ALS and PD?
    Biochim Biophys Acta. 2007 Aug;1772(8):822-35 PMID: 17395433
  19. Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin.
    Science. 1987 Jul 31;237(4814):517-22 PMID: 3603037
  20. Transient receptor potential cation channels in disease.
    Physiol Rev. 2007 Jan;87(1):165-217 PMID: 17237345
  21. Sites of the NUDT9-H domain critical for ADP-ribose activation of the cation channel TRPM2.
    J Biol Chem. 2004 Nov 5;279(45):46431-7 PMID: 15347676
  22. Immunocyte Ca2+ influx system mediated by LTRPC2.
    Science. 2001 Aug 17;293(5533):1327-30 PMID: 11509734
  23. The pathogenesis of amyotrophic lateral sclerosis.
    Lancet. 1972 Aug 12;2(7772):292-6 PMID: 4115029
  24. H2O 2-stimulated Ca2+ influx via TRPM2 is not the sole determinant of subsequent cell death.
    Pflugers Arch. 2008 Mar;455(6):1141-51 PMID: 18043941
  25. Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels.
    J Biol Chem. 2005 Feb 18;280(7):6138-48 PMID: 15561722
  26. Calcium and vitamin D metabolism in Guamanian Chamorros with amyotrophic lateral sclerosis and parkinsonism-dementia.
    Ann Neurol. 1984 Jan;15(1):42-8 PMID: 6546847
  27. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death.
    Mol Cell. 2002 Jan;9(1):163-73 PMID: 11804595
  28. Regulation of TRPM2 by extra- and intracellular calcium.
    J Gen Physiol. 2007 Oct;130(4):427-40 PMID: 17893195
  29. SnapShot: mammalian TRP channels.
    Cell. 2007 Apr 6;129(1):220 PMID: 17418797
  30. A polymorphism in CALHM1 influences Ca2+ homeostasis, Abeta levels, and Alzheimer's disease risk.
    Cell. 2008 Jun 27;133(7):1149-61 PMID: 18585350
  31. Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region.
    Neuron. 1991 Oct;7(4):547-56 PMID: 1931050
  32. A commentary on neuronal degeneration and cell death in Guam ALS and PD: an evolutionary process of understanding.
    Curr Alzheimer Res. 2006 Sep;3(4):397-401 PMID: 17017870
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
2008-11-18
Epub
2008-00-12
Pages
18029-34
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2584682
Subset
IM
Grants
NIAID NIH HHS · K08AI060926 · United States
NINDS NIH HHS · S11 NS043462 · United States
NIGMS NIH HHS · R01 GM068801-05 · United States
NIAID NIH HHS · K08 AI060926 · United States
NIGMS NIH HHS · R01 GM068801 · United States
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