Skip to main content

Advertisement

SpringerLink
Log in

ADP-heptose: a bacterial PAMP detected by the host sensor ALPK1

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The innate immune response constitutes the first line of defense against pathogens. It involves the recognition of pathogen-associated molecular patterns (PAMPs) by pathogen recognition receptors (PRRs), the production of inflammatory cytokines and the recruitment of immune cells to infection sites. Recently, ADP-heptose, a soluble intermediate of the lipopolysaccharide biosynthetic pathway in Gram-negative bacteria, has been identified by several research groups as a PAMP. Here, we recapitulate the evidence that led to this identification and discuss the controversy over the immunogenic properties of heptose 1,7-bisphosphate (HBP), another bacterial heptose previously defined as an activator of innate immunity. Then, we describe the mechanism of ADP-heptose sensing by alpha-protein kinase 1 (ALPK1) and its downstream signaling pathway that involves the proteins TIFA and TRAF6 and induces the activation of NF-κB and the secretion of inflammatory cytokines. Finally, we discuss possible delivery mechanisms of ADP-heptose in cells during infection, and propose new lines of thinking to further explore the roles of the ADP-heptose/ALPK1/TIFA axis in infections and its potential implication in the control of intestinal homeostasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ADP-heptose:

ADP-L-glycero-β-D-manno-heptose

ADP-heptose 7P:

ADP-heptose 7-phosphate

AIDA:

Adhesin involved in diffuse adherence

AKT:

AK strain-transforming protein/protein kinase B

ALPK1:

Alpha-protein kinase 1

CD:

Cluster of differentiation

CLR:

C-type lectin receptor

dsRNA:

Double-stranded RNA

FHA:

Forkhead-associated domain

GM-CSF:

Granulocyte–macrophage colony stimulating factor

HBP:

D-glycero-β-D-manno-heptose 1,7-bisphosphate

HEK:

Human embryonic kidney

HIV:

Human immunodeficiency virus

HMP1:

D-glycero-β-D-manno-heptose 1-monophosphate

IFN:

Interferon

IKK:

IκB kinase

IL:

Interleukin

IP:

Interferon-γ induced protein

IκB:

Inhibitor of κB

Kdo:

3-Deoxy-D-manno-oct-2-ulosonic acid

KIF:

Kinesin superfamily protein

LPS:

Lipopolysaccharide

MCP:

Monocyte chemoattractant protein

MIP:

Macrophage inflammatory protein

MS:

Mass spectrometry

NEMO:

NF-κB essential modulator

NF-κB:

Nuclear-factor kappa B

NLR:

NOD-like receptor

NLRP3:

NOD-, LRR- and pyrin domain-containing protein 3

NMNAT:

Nicotinamide mononucleotide adenylyltransferase

NOD:

Nucleotide-binding and oligomerization domain

NTD:

N-terminal domain

PAMP:

Pathogen-associated molecular pattern

PRR:

Pathogen recognition receptor

pT9:

Phospho-threonine 9

RANTES:

Regulated on activation, normal T-cell expressed and secreted

RIG:

Retinoid acid-inducible gene

RLK:

Receptor-like kinase

RLR:

RIG-like receptor

T3/4SS:

Type 3/4 secretion system

T9:

Threonine 9

TAB:

TAK-1-binding protein

TAK:

Transforming growth factor β-activated kinase 1

Th1:

Type 1 helper T cell

Th17:

Type 17 helper T cell

TIFA:

TRAF-interacting protein with FHA domain-containing protein A

TLR:

Toll-like receptor

TNFα:

Tumor necrosis factor alpha

TRAF:

Tumor necrosis factor receptor-associated factor

Treg:

Regulatory T cell

TRIM:

Tripartite motif

Wt:

Wild type

ZCCHC:

Zinc finger CCHC-type containing protein

References

  1. Creagh EM, O’Neill LAJ (2006) TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27:352–357. https://doi.org/10.1016/j.it.2006.06.003

    Article  CAS  PubMed  Google Scholar 

  2. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801. https://doi.org/10.1016/j.cell.2006.02.015

    Article  CAS  PubMed  Google Scholar 

  3. Baccala R, Gonzalez-Quintial R, Lawson BR et al (2009) Sensors of the innate immune system: their mode of action. Nat Rev Rheumatol 5:448–456. https://doi.org/10.1038/nrrheum.2009.136

    Article  CAS  PubMed  Google Scholar 

  4. Muñoz-Wolf N, Lavelle EC (2016) Innate immune receptors. Methods Mol Biol Clifton NJ 1417:1–43. https://doi.org/10.1007/978-1-4939-3566-6_1

    Article  CAS  Google Scholar 

  5. Poltorak A, He X, Smirnova I et al (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088. https://doi.org/10.1126/science.282.5396.2085

    Article  CAS  PubMed  Google Scholar 

  6. Gewirtz AT, Navas TA, Lyons S et al (1950) (2001) Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol Baltim Md 167:1882–1885. https://doi.org/10.4049/jimmunol.167.4.1882

    Article  Google Scholar 

  7. Brightbill HD, Libraty DH, Krutzik SR et al (1999) Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285:732–736. https://doi.org/10.1126/science.285.5428.732

    Article  CAS  PubMed  Google Scholar 

  8. Hirschfeld M, Kirschning CJ, Schwandner R et al (1950) (1999) Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol Baltim Md 163:2382–2386

    Google Scholar 

  9. Bauer S, Kirschning CJ, Häcker H et al (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A 98:9237–9242. https://doi.org/10.1073/pnas.161293498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ishii KJ, Coban C, Kato H et al (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 7:40–48. https://doi.org/10.1038/ni1282

    Article  CAS  PubMed  Google Scholar 

  11. Chamaillard M, Hashimoto M, Horie Y et al (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4:702–707. https://doi.org/10.1038/ni945

    Article  CAS  PubMed  Google Scholar 

  12. Girardin SE, Boneca IG, Carneiro LAM et al (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584–1587. https://doi.org/10.1126/science.1084677

    Article  CAS  PubMed  Google Scholar 

  13. Girardin SE, Boneca IG, Viala J et al (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869–8872. https://doi.org/10.1074/jbc.C200651200

    Article  CAS  PubMed  Google Scholar 

  14. Inohara N, Ogura Y, Fontalba A et al (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn’s disease. J Biol Chem 278:5509–5512. https://doi.org/10.1074/jbc.C200673200

    Article  CAS  PubMed  Google Scholar 

  15. Yoneyama M, Kikuchi M, Natsukawa T et al (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730–737. https://doi.org/10.1038/ni1087

    Article  CAS  PubMed  Google Scholar 

  16. Sato K, Yang X, Yudate T et al (2006) Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem 281:38854–38866. https://doi.org/10.1074/jbc.M606542200

    Article  CAS  PubMed  Google Scholar 

  17. Wells CA, Salvage-Jones JA, Li X et al (1950) (2008) The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol Baltim Md 180:7404–7413. https://doi.org/10.4049/jimmunol.180.11.7404

    Article  Google Scholar 

  18. Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216. https://doi.org/10.1146/annurev.immunol.20.083001.084359

    Article  CAS  PubMed  Google Scholar 

  19. García-Weber D, Dangeard AS, Cornil J, et al (2018) ADP-heptose is a newly identified pathogen-associated molecular pattern of Shigella flexneri. EMBO Rep https://doi.org/10.15252/embr.201846943

  20. Zhou P, She Y, Dong N et al (2018) Alpha-kinase 1 is a cytosolic innate immune receptor for bacterial ADP-heptose. Nature 561:122–126. https://doi.org/10.1038/s41586-018-0433-3

    Article  CAS  PubMed  Google Scholar 

  21. Pfannkuch L, Hurwitz R, Traulsen J et al (2019) ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori. FASEB J Off Publ Fed Am Soc Exp Biol. https://doi.org/10.1096/fj.201802555R

    Article  Google Scholar 

  22. Raetz CRH (1990) Biochemistry of endotoxins. Annu Rev Biochem 59:129–170. https://doi.org/10.1146/annurev.bi.59.070190.001021

    Article  CAS  PubMed  Google Scholar 

  23. Shi J, Zhao Y, Wang Y et al (2014) Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514:187–192. https://doi.org/10.1038/nature13683

    Article  CAS  PubMed  Google Scholar 

  24. Park BS, Lee J-O (2013) Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med 45:e66. https://doi.org/10.1038/emm.2013.97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kunin CM, Beard MV (1963) Serological studies of o antigens of Escherichia Coli by means of the hemagglutination test. J Bacteriol 85:541–548

    Article  CAS  Google Scholar 

  26. Endotoxin in Health and Disease. In: CRC Press. https://www.routledge.com/Endotoxin-in-Health-and-Disease/Brade/p/book/9780824719449. Accessed 11 June 2020

  27. Møller AK, Leatham MP, Conway T et al (2003) An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infect Immun 71:2142–2152. https://doi.org/10.1128/iai.71.4.2142-2152.2003

    Article  PubMed  PubMed Central  Google Scholar 

  28. Xu D, Zhang W, Zhang B et al (2016) Characterization of a biofilm-forming Shigella flexneri phenotype due to deficiency in Hep biosynthesis. PeerJ 4:e2178. https://doi.org/10.7717/peerj.2178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Martinić M, Hoare A, Contreras I, Álvarez SA (2011) Contribution of the lipopolysaccharide to resistance of Shigella flexneri 2a to extreme acidity. PLoS ONE. https://doi.org/10.1371/journal.pone.0025557

    Article  PubMed  PubMed Central  Google Scholar 

  30. Coleman WG, Deshpande KS (1985) New cysE-pyrE-linked rfa mutation in Escherichia coli K-12 that results in a heptoseless lipopolysaccharide. J Bacteriol 161:1209–1214

    Article  CAS  Google Scholar 

  31. Valvano MA, Marolda CL, Bittner M et al (2000) The rfaE gene from Escherichia coli encodes a bifunctional protein involved in biosynthesis of the lipopolysaccharide core precursor ADP-L-glycero-d-manno-heptose. J Bacteriol 182:488–497. https://doi.org/10.1128/jb.182.2.488-497.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gronow S, Brade H (2001) Lipopolysaccharide biosynthesis: which steps do bacteria need to survive? J Endotoxin Res 7:3–23

    CAS  PubMed  Google Scholar 

  33. Shih GC, Kahler CM, Carlson RW et al (2001) gmhX, a novel gene required for the incorporation of L-glycero-D-manno-heptose into lipooligosaccharide in Neisseria meningitidis. Microbiol Read Engl 147:2367–2377. https://doi.org/10.1099/00221287-147-8-2367

    Article  CAS  Google Scholar 

  34. Kneidinger B, Marolda C, Graninger M et al (2002) Biosynthesis pathway of ADP-L-glycero-beta-D-manno-heptose in Escherichia coli. J Bacteriol 184:363–369. https://doi.org/10.1128/jb.184.2.363-369.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Valvano MA, Messner P, Kosma P (2002) Novel pathways for biosynthesis of nucleotide-activated glycero-manno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides. Microbiol Read Engl 148:1979–1989. https://doi.org/10.1099/00221287-148-7-1979

    Article  CAS  Google Scholar 

  36. Kim C-H (2003) A Salmonella typhimurium rfaE mutant recovers invasiveness for human epithelial cells when complemented by wild type rfaE (controlling biosynthesis of ADP-L-glycero-D-mannoheptose-containing lipopolysaccharide). Mol Cells 15:226–232

    CAS  PubMed  Google Scholar 

  37. McArthur F, Andersson CE, Loutet S et al (2005) Functional analysis of the glycero-manno-heptose 7-phosphate kinase domain from the bifunctional HldE protein, which is involved in ADP-L-glycero-D-manno-heptose biosynthesis. J Bacteriol 187:5292–5300. https://doi.org/10.1128/JB.187.15.5292-5300.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Malott RJ, Keller BO, Gaudet RG et al (2013) Neisseria gonorrhoeae-derived heptose elicits an innate immune response and drives HIV-1 expression. Proc Natl Acad Sci U S A 110:10234–10239. https://doi.org/10.1073/pnas.1303738110

    Article  PubMed  PubMed Central  Google Scholar 

  39. Pokorny B, Kosma P (2016) Synthesis of 5-O-oligoglucosyl extended α-(2→4)-Kdo disaccharides corresponding to inner core fragments of Moraxellaceae lipopolysaccharides. Carbohydr Res 422:5–12. https://doi.org/10.1016/j.carres.2015.12.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kadrmas JL, Brozek KA, Raetz CR (1996) Lipopolysaccharide core glycosylation in Rhizobium leguminosarum. An unusual mannosyl transferase resembling the heptosyl transferase I of Escherichia coli. J Biol Chem 271:32119–32125

    Article  CAS  Google Scholar 

  41. Kay W, Petersen BO, Duus JØ et al (2006) Characterization of the lipopolysaccharide and beta-glucan of the fish pathogen Francisella victoria. FEBS J 273:3002–3013. https://doi.org/10.1111/j.1742-4658.2006.05311.x

    Article  CAS  PubMed  Google Scholar 

  42. Knirel YA, Moll H, Zähringer U (1996) Structural study of a highly O-acetylated core of Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr Res 293:223–234. https://doi.org/10.1016/0008-6215(96)00194-2

    Article  CAS  PubMed  Google Scholar 

  43. Moreno E, Pitt MW, Jones LM et al (1979) Purification and characterization of smooth and rough lipopolysaccharides from Brucella abortus. J Bacteriol 138:361–369

    Article  CAS  Google Scholar 

  44. Okan NA, Kasper DL (2013) The atypical lipopolysaccharide of Francisella. Carbohydr Res 378:79–83. https://doi.org/10.1016/j.carres.2013.06.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. de Vries SPW, Bootsma HJ, Hays JP, Hermans PWM (2009) Molecular aspects of Moraxella catarrhalis pathogenesis. Microbiol Mol Biol Rev MMBR 73:389–406. https://doi.org/10.1128/MMBR.00007-09

    Article  CAS  PubMed  Google Scholar 

  46. Hajjar AM, Harvey MD, Shaffer SA et al (2006) Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect Immun 74:6730–6738. https://doi.org/10.1128/IAI.00934-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tang W, Guo Z, Cao Z et al (2018) d-Sedoheptulose-7-phosphate is a common precursor for the heptoses of septacidin and hygromycin B. Proc Natl Acad Sci U S A 115:2818–2823. https://doi.org/10.1073/pnas.1711665115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gaudet RG, Sintsova A, Buckwalter CM et al (2015) Innate immunity. Cytosolic detection of the bacterial metabolite HBP activates TIFA-dependent innate immunity. Science 348:1251–1255. https://doi.org/10.1126/science.aaa4921

    Article  CAS  PubMed  Google Scholar 

  49. Milivojevic M, Dangeard A-S, Kasper CA et al (2017) ALPK1 controls TIFA/TRAF6-dependent innate immunity against heptose-1,7-bisphosphate of gram-negative bacteria. PLoS Pathog 13:e1006224. https://doi.org/10.1371/journal.ppat.1006224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Stein SC, Faber E, Bats SH et al (2017) Helicobacter pylori modulates host cell responses by CagT4SS-dependent translocation of an intermediate metabolite of LPS inner core heptose biosynthesis. PLoS Pathog 13:e1006514. https://doi.org/10.1371/journal.ppat.1006514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Gall A, Gaudet RG, Gray-Owen SD, Salama NR (2017) TIFA Signaling in Gastric Epithelial Cells Initiates the cag Type 4 Secretion System-Dependent Innate Immune Response to Helicobacter pylori Infection. mBio https://doi.org/10.1128/mBio.01168-17

  52. Zimmermann S, Pfannkuch L, Al-Zeer MA et al (2017) ALPK1- and TIFA-dependent innate immune response triggered by the Helicobacter pylori Type IV Secretion System. Cell Rep 20:2384–2395. https://doi.org/10.1016/j.celrep.2017.08.039

    Article  CAS  PubMed  Google Scholar 

  53. Adekoya IA, Guo CX, Gray-Owen SD et al (1950) (2018) d-Glycero-β-d-Manno-heptose 1-phosphate and d-glycero-β-d-manno-heptose 1,7-biphosphate are both innate immune agonists. J Immunol Baltim Md 201:2385–2391. https://doi.org/10.4049/jimmunol.1801012

    Article  Google Scholar 

  54. Kanamori M, Suzuki H, Saito R et al (2002) T2BP, a novel TRAF2 binding protein, can activate NF-kappaB and AP-1 without TNF stimulation. Biochem Biophys Res Commun 290:1108–1113. https://doi.org/10.1006/bbrc.2001.6315

    Article  CAS  PubMed  Google Scholar 

  55. Takatsuna H, Kato H, Gohda J et al (2003) Identification of TIFA as an adapter protein that links tumor necrosis factor receptor-associated factor 6 (TRAF6) to interleukin-1 (IL-1) receptor-associated kinase-1 (IRAK-1) in IL-1 receptor signaling. J Biol Chem 278:12144–12150. https://doi.org/10.1074/jbc.M300720200

    Article  CAS  PubMed  Google Scholar 

  56. Huang C-CF, Weng J-H, Wei T-YW et al (2012) Intermolecular binding between TIFA-FHA and TIFA-pT mediates tumor necrosis factor alpha stimulation and NF-κB activation. Mol Cell Biol 32:2664–2673. https://doi.org/10.1128/MCB.00438-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Weng J-H, Hsieh Y-C, Huang C-CF et al (2015) Uncovering the mechanism of forkhead-associated domain-mediated TIFA oligomerization that plays a central role in immune responses. Biochemistry 54:6219–6229. https://doi.org/10.1021/acs.biochem.5b00500

    Article  CAS  PubMed  Google Scholar 

  58. Ea C-K, Sun L, Inoue J-I, Chen ZJ (2004) TIFA activates IkappaB kinase (IKK) by promoting oligomerization and ubiquitination of TRAF6. Proc Natl Acad Sci U S A 101:15318–15323. https://doi.org/10.1073/pnas.0404132101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gaudet RG, Guo CX, Molinaro R et al (2017) Innate recognition of intracellular bacterial growth is driven by the TIFA-dependent cytosolic surveillance pathway. Cell Rep 19:1418–1430. https://doi.org/10.1016/j.celrep.2017.04.063

    Article  CAS  PubMed  Google Scholar 

  60. Carson D, Barry R, Hopkins EGD et al (2020) Citrobacter rodentium induces rapid and unique metabolic and inflammatory responses in mice suffering from severe disease. Cell Microbiol 22:e13126. https://doi.org/10.1111/cmi.13126

    Article  CAS  PubMed  Google Scholar 

  61. Hillier LW, Graves TA, Fulton RS et al (2005) Generation and annotation of the DNA sequences of human chromosomes 2 and 4. Nature 434:724–731. https://doi.org/10.1038/nature03466

    Article  CAS  PubMed  Google Scholar 

  62. Scheeff ED, Bourne PE (2005) Structural evolution of the protein kinase-like superfamily. PLoS Comput Biol 1:e49. https://doi.org/10.1371/journal.pcbi.0010049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351. https://doi.org/10.1016/j.it.2014.05.004

    Article  CAS  PubMed  Google Scholar 

  64. Greeff C, Roux M, Mundy J, Petersen M (2012) Receptor-like kinase complexes in plant innate immunity. Front Plant Sci 3:209. https://doi.org/10.3389/fpls.2012.00209

    Article  PubMed  PubMed Central  Google Scholar 

  65. Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2:e2. https://doi.org/10.1371/journal.ppat.0020002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Chattopadhyay S, Sen GC (2014) Tyrosine phosphorylation in toll-like receptor signaling. Cytokine Growth Factor Rev 25:533–541. https://doi.org/10.1016/j.cytogfr.2014.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Samuel CE (1993) The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J Biol Chem 268:7603–7606

    Article  CAS  Google Scholar 

  68. Balachandran S, Roberts PC, Brown LE et al (2000) Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13:129–141. https://doi.org/10.1016/s1074-7613(00)00014-5

    Article  CAS  PubMed  Google Scholar 

  69. Dey M, Mann BR, Anshu A, Mannan MA (2014) Activation of protein kinase PKR requires dimerization-induced cis-phosphorylation within the activation loop. J Biol Chem 289:5747–5757. https://doi.org/10.1074/jbc.M113.527796

    Article  CAS  PubMed  Google Scholar 

  70. Middelbeek J, Clark K, Venselaar H et al (2010) The alpha-kinase family: an exceptional branch on the protein kinase tree. Cell Mol Life Sci CMLS 67:875–890. https://doi.org/10.1007/s00018-009-0215-z

    Article  CAS  PubMed  Google Scholar 

  71. Lin T-Y, Wei T-YW, Li S et al (2016) TIFA as a crucial mediator for NLRP3 inflammasome. Proc Natl Acad Sci U S A 113:15078–15083. https://doi.org/10.1073/pnas.1618773114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wei T-YW, Wu P-Y, Wu T-J et al (2017) Aurora A and NF-κB survival pathway drive chemoresistance in acute myeloid leukemia via the TRAF-interacting protein TIFA. Cancer Res 77:494–508. https://doi.org/10.1158/0008-5472.CAN-16-1004

    Article  CAS  PubMed  Google Scholar 

  73. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12:695–708. https://doi.org/10.1038/ni.2065

    Article  CAS  PubMed  Google Scholar 

  74. Lee C-P, Chiang S-L, Ko AM-S et al (2016) ALPK1 phosphorylates myosin IIA modulating TNF-α trafficking in gout flares. Sci Rep 6:25740. https://doi.org/10.1038/srep25740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Matsumura T, Semba K, Azuma S et al (2004) TIFAB inhibits TIFA, TRAF-interacting protein with a forkhead-associated domain. Biochem Biophys Res Commun 317:230–234. https://doi.org/10.1016/j.bbrc.2004.03.030

    Article  CAS  PubMed  Google Scholar 

  76. Matsumura T, Kawamura-Tsuzuku J, Yamamoto T et al (2009) TRAF-interacting protein with a forkhead-associated domain B (TIFAB) is a negative regulator of the TRAF6-induced cellular functions. J Biochem (Tokyo) 146:375–381. https://doi.org/10.1093/jb/mvp080

    Article  CAS  Google Scholar 

  77. Minoda Y, Saeki K, Aki D et al (2006) A novel Zinc finger protein, ZCCHC11, interacts with TIFA and modulates TLR signaling. Biochem Biophys Res Commun 344:1023–1030. https://doi.org/10.1016/j.bbrc.2006.04.006

    Article  CAS  PubMed  Google Scholar 

  78. Huang W-C, Liao J-H, Hsiao T-C et al (2019) Binding and enhanced binding between key immunity proteins TRAF6 and TIFA. Chembiochem Eur J Chem Biol 20:140–146. https://doi.org/10.1002/cbic.201800436

    Article  CAS  Google Scholar 

  79. Yin Q, Lin S-C, Lamothe B et al (2009) E2 interaction and dimerization in the crystal structure of TRAF6. Nat Struct Mol Biol 16:658–666. https://doi.org/10.1038/nsmb.1605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Parsot C (2009) Shigella type III secretion effectors: how, where, when, for what purposes? Curr Opin Microbiol 12:110–116. https://doi.org/10.1016/j.mib.2008.12.002

    Article  CAS  PubMed  Google Scholar 

  81. Kuehl CJ, Dragoi A-M, Talman A, Agaisse H (2015) Bacterial spread from cell to cell: beyond actin-based motility. Trends Microbiol 23:558–566. https://doi.org/10.1016/j.tim.2015.04.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Kasper CA, Sorg I, Schmutz C et al (2010) Cell-cell propagation of NF-κB transcription factor and MAP kinase activation amplifies innate immunity against bacterial infection. Immunity 33:804–816. https://doi.org/10.1016/j.immuni.2010.10.015

    Article  CAS  PubMed  Google Scholar 

  83. Kawai T, Akira S (2007) Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med 13:460–469. https://doi.org/10.1016/j.molmed.2007.09.002

    Article  CAS  PubMed  Google Scholar 

  84. Platnich JM, Muruve DA (2019) NOD-like receptors and inflammasomes: A review of their canonical and non-canonical signaling pathways. Arch Biochem Biophys 670:4–14. https://doi.org/10.1016/j.abb.2019.02.008

    Article  CAS  PubMed  Google Scholar 

  85. Bleich A, Büchler G, Beckwith J et al (2010) Cdcs1 a major colitis susceptibility locus in mice; subcongenic analysis reveals genetic complexity. Inflamm Bowel Dis 16:765–775. https://doi.org/10.1002/ibd.21146

    Article  PubMed  PubMed Central  Google Scholar 

  86. Boulard O, Kirchberger S, Royston DJ et al (2012) Identification of a genetic locus controlling bacteria-driven colitis and associated cancer through effects on innate inflammation. J Exp Med 209:1309–1324. https://doi.org/10.1084/jem.20120239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Ryzhakov G, West NR, Franchini F et al (2018) Alpha kinase 1 controls intestinal inflammation by suppressing the IL-12/Th1 axis. Nat Commun 9:3797. https://doi.org/10.1038/s41467-018-06085-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Caruso R, Warner N, Inohara N, Núñez G (2014) NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41:898–908. https://doi.org/10.1016/j.immuni.2014.12.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Kuo T-M, Hsu H-T, Chung C-M et al (2016) Enhanced alpha-kinase 1 accelerates multiple early nephropathies in streptozotocin-induced hyperglycemic mice. Biochim Biophys Acta 1862:2034–2042. https://doi.org/10.1016/j.bbadis.2016.08.010

    Article  CAS  PubMed  Google Scholar 

  90. Strietz J, Stepputtis SS, Preca B-T, et al (2016) ERN1 and ALPK1 inhibit differentiation of bi-potential tumor-initiating cells in human breast cancer. Oncotarget 7:83278–83293. https://doi.org/10.18632/oncotarget.13086

  91. Li C, Kuang L, Zhu B et al (2017) Identification of prognostic risk factors of acute lymphoblastic leukemia based on mRNA expression profiling. Neoplasma 64:494–501. https://doi.org/10.4149/neo_2017_402

    Article  CAS  PubMed  Google Scholar 

  92. Ji C, Lin S, Yao D et al (2019) Identification of promising prognostic genes for relapsed acute lymphoblastic leukemia. Blood Cells Mol Dis 77:113–119. https://doi.org/10.1016/j.bcmd.2019.04.010

    Article  CAS  PubMed  Google Scholar 

  93. Chen P-K, Hua C-H, Hsu H-T et al (2019) ALPK1 expression is associated with lymph node metastasis and tumor growth in oral squamous cell carcinoma patients. Am J Pathol 189:190–199. https://doi.org/10.1016/j.ajpath.2018.09.003

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Anne-Sophie Dangeard and Veronica Teixeira for critically reviewing the manuscript.

Funding

We gratefully acknowledge financial support from the Agence Nationale de la Recherche (Grants no: ANR‐14‐ACHN‐0029‐01 and ANR‐17‐CE15‐0006, including postdoctoral fellowships to DGW) and from Fondation ARC pour la Recherche sur le Cancer (Grant No: ARC—PJA20171206187).

Author information

Authors and Affiliations

  1. INSERM, U1016, Institut Cochin, CNRS, UMR8104, Université de Paris, 22 rue Méchain, 75014, Paris, France

    Diego García-Weber & Cécile Arrieumerlou

Authors
  1. Diego García-Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cécile Arrieumerlou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cécile Arrieumerlou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Weber, D., Arrieumerlou, C. ADP-heptose: a bacterial PAMP detected by the host sensor ALPK1. Cell. Mol. Life Sci. 78, 17–29 (2021). https://doi.org/10.1007/s00018-020-03577-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-020-03577-w

Keywords

Search

Navigation