Home LiteratureArticle Details
PMID: 19509286 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A TIR domain variant of MyD88 adapter-like (Mal)/TIRAP results in loss of MyD88 binding and reduced TLR2/TLR4 signaling.

The Journal of biological chemistry ·Vol. 284 ·No. 38 ·2009-09-18 ·Pages 25742-8

Nagpal K, Plantinga TS, Wong J, Monks BG, Gay NJ, Netea MG, Fitzgerald KA, Golenbock DT

Abstract

The adapter protein MyD88 adapter-like (Mal), encoded by TIR-domain containing adapter protein (Tirap) (MIM 606252), is the most polymorphic of the five adapter proteins involved in Toll-like receptor signaling, harboring eight non-synonymous single nucleotide polymorphisms in its coding region. We screened reported mutations of Mal for activity in reporter assays to test the hypothesis that variants of Mal existed with altered signaling potential. A TIR domain variant, Mal D96N (rs8177400), was found to be inactive. In reconstituted cell lines, Mal D96N acted as a hypomorphic mutation, with impaired cytokine production and NF-kappaB activation upon lipopolysaccharide or PAM2CSK4 stimulation. Moreover, co-immunoprecipitation studies revealed that Mal D96N is unable to interact with MyD88, a prerequisite for downstream signaling to occur. Computer modeling data suggested that residue 96 resides in the MyD88 binding site, further supporting these findings. Genotyping of Mal D96N in three different cohorts suggested that it is a rare mutation. We, thus, describe a rare variant in Mal that exerts its effect via its inability to bind MyD88.

MeSH Terms
Amino Acid Substitution Binding Sites/physiology Cell Line Cohort Studies Computer Simulation Female Humans Lipopeptides/pharmacology Lipopolysaccharides/pharmacology Male Membrane Glycoproteins/genetics,metabolism Models, Molecular Mutation, Missense Myeloid Differentiation Factor 88/genetics,metabolism Polymorphism, Single Nucleotide Protein Binding/drug effects,physiology Protein Structure, Tertiary Receptors, Interleukin-1/genetics,metabolism Signal Transduction/drug effects,physiology Toll-Like Receptor 2/genetics,metabolism Toll-Like Receptor 4/genetics,metabolism
Chemicals
Lipopeptides Lipopolysaccharides MYD88 protein, human Membrane Glycoproteins Myeloid Differentiation Factor 88 Pam(3)CSK(4) peptide Receptors, Interleukin-1 TIRAP protein, human TLR2 protein, human TLR4 protein, human Toll-Like Receptor 2 Toll-Like Receptor 4
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Nagpal Kamalpreet
Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA.
Plantinga Theo S
Wong Joyce
Monks Brian G
Gay Nicholas J
Netea Mihai G
Fitzgerald Katherine A
Golenbock Douglas T
References (37)
37 references, click to expand
  1. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation.
    Nat Immunol. 2004 May;5(5):503-7 PMID: 15064760
  2. A dimer of the Toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins.
    PLoS One. 2007 Aug 29;2(8):e788 PMID: 17726518
  3. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF.
    J Exp Med. 2003 Oct 6;198(7):1043-55 PMID: 14517278
  4. NF-kappaB activation by the Toll-IL-1 receptor domain protein MyD88 adapter-like is regulated by caspase-1.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3372-7 PMID: 17360653
  5. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction.
    Nature. 2001 Sep 6;413(6851):78-83 PMID: 11544529
  6. Targeting toll-like receptor signaling pathways for design of novel immune therapeutics.
    Curr Drug Discov Technol. 2008 Mar;5(1):29-38 PMID: 18537565
  7. A structural bioinformatics approach to the analysis of nonsynonymous single nucleotide polymorphisms (nsSNPs) and their relation to disease.
    J Bioinform Comput Biol. 2007 Dec;5(6):1297-318 PMID: 18172930
  8. When signaling pathways collide: positive and negative regulation of toll-like receptor signal transduction.
    Immunity. 2008 Jul 18;29(1):12-20 PMID: 18631453
  9. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway.
    Nat Immunol. 2003 May;4(5):491-6 PMID: 12692549
  10. Prediction of the stability of protein mutants based on structural environment-dependent amino acid substitution and propensity tables.
    Protein Eng. 1997 Jan;10(1):7-21 PMID: 9051729
  11. Comparative protein modelling by satisfaction of spatial restraints.
    J Mol Biol. 1993 Dec 5;234(3):779-815 PMID: 8254673
  12. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties.
    J Mol Biol. 2001 Jun 29;310(1):243-57 PMID: 11419950
  13. The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor 7 signaling.
    J Biol Chem. 2005 Apr 29;280(17):17005-12 PMID: 15695821
  14. Pyogenic bacterial infections in humans with MyD88 deficiency.
    Science. 2008 Aug 1;321(5889):691-6 PMID: 18669862
  15. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains.
    Nature. 2000 Nov 2;408(6808):111-5 PMID: 11081518
  16. TLR-independent type I interferon induction in response to an extracellular bacterial pathogen via intracellular recognition of its DNA.
    Cell Host Microbe. 2008 Dec 11;4(6):543-54 PMID: 19064255
  17. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta.
    Nat Immunol. 2008 Aug;9(8):857-65 PMID: 18604209
  18. The expanding family of MyD88-like adaptors in Toll-like receptor signal transduction.
    Mol Immunol. 2004 Jul;41(6-7):577-82 PMID: 15219996
  19. Genetic association and expression studies indicate a role of toll-like receptor 8 in pulmonary tuberculosis.
    PLoS Genet. 2008 Oct;4(10):e1000218 PMID: 18927625
  20. Sequence variability and protein domain architectures for bovine Toll-like receptors 1, 5, and 10.
    Genomics. 2007 Oct;90(4):502-15 PMID: 17719743
  21. TIRAP: an adapter molecule in the Toll signaling pathway.
    Nat Immunol. 2001 Sep;2(9):835-41 PMID: 11526399
  22. Versatile retroviral vectors for potential use in gene therapy.
    Gene Ther. 1994 Mar;1(2):136-8 PMID: 7584069
  23. TLR9 signals after translocating from the ER to CpG DNA in the lysosome.
    Nat Immunol. 2004 Feb;5(2):190-8 PMID: 14716310
  24. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis.
    Nat Genet. 2007 Apr;39(4):523-8 PMID: 17322885
  25. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4.
    Nature. 2002 Nov 21;420(6913):324-9 PMID: 12447441
  26. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling.
    Cell. 2006 Jun 2;125(5):943-55 PMID: 16751103
  27. Cutting edge: A common polymorphism impairs cell surface trafficking and functional responses of TLR1 but protects against leprosy.
    J Immunol. 2007 Jun 15;178(12):7520-4 PMID: 17548585
  28. Sorting out Toll signals.
    Cell. 2006 Jun 2;125(5):834-6 PMID: 16751092
  29. TLR4 polymorphisms, infectious diseases, and evolutionary pressure during migration of modern humans.
    Proc Natl Acad Sci U S A. 2007 Oct 16;104(42):16645-50 PMID: 17925445
  30. Functional activity of MD-2 polymorphic variant is significantly different in soluble and TLR4-bound forms: decreased endotoxin binding by G56R MD-2 and its rescue by TLR4 ectodomain.
    J Immunol. 2008 May 1;180(9):6107-15 PMID: 18424732
  31. A polymorphism in Toll-interleukin 1 receptor domain containing adaptor protein is associated with susceptibility to meningeal tuberculosis.
    J Infect Dis. 2006 Oct 15;194(8):1127-1134 PMID: 16991088
  32. Pyogenic bacterial infections in humans with IRAK-4 deficiency.
    Science. 2003 Mar 28;299(5615):2076-9 PMID: 12637671
  33. TLRs: differential adapter utilization by toll-like receptors mediates TLR-specific patterns of gene expression.
    Mol Interv. 2003 Dec;3(8):466-77 PMID: 14993454
  34. Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response.
    J Biol Chem. 2008 May 23;283(21):14295-308 PMID: 18332133
  35. Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections.
    J Exp Med. 2003 Aug 18;198(4):521-31 PMID: 12925671
  36. Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis.
    Am J Respir Crit Care Med. 2008 Oct 1;178(7):710-20 PMID: 18635889
  37. Genomic variants of TLR1--it takes (TLR-)two to tango.
    Eur J Immunol. 2007 Aug;37(8):2059-62 PMID: 17654751
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2009-09-18
Epub
2009-00-09
Pages
25742-8
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2757976
Subset
IM
Grants
NIGMS NIH HHS · GM54060 · United States
Biotechnology and Biological Sciences Research Council · BB/G002797/1 · United Kingdom
NIGMS NIH HHS · R37 GM054060 · United States
NIAID NIH HHS · AI067497 · United States
Biotechnology and Biological Sciences Research Council · BB/G009295/1 · United Kingdom
NIAID NIH HHS · AI52455 · United States
Wellcome Trust · United Kingdom
Medical Research Council · G1000133 · United Kingdom
NIAID NIH HHS · R37 AI067497 · United States
NIAID NIH HHS · R56 AI052455 · United States
Medical Research Council · G0400007 · United Kingdom
NIAID NIH HHS · R01 AI067497 · United States
NIGMS NIH HHS · R01 GM054060 · United States
NIAID NIH HHS · R01 AI052455 · United States
NIAID NIH HHS · R56 AI067497 · United States
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]