Cutting Edge: NLRP12 Controls Dendritic and Myeloid Cell Migration to Affect Contact Hypersensitivity

Overview

Journal J Immunol

Specialty Allergy & Immunology

Date 2010 Sep 24

PMID 20861349

Citations 77

Authors

Janelle C Arthur

John D Lich

Zhengmao Ye

Irving C Allen

Denis Gris

Justin E Wilson

Monika Schneider

Kelly E Roney

Brian P OConnor

Chris B Moore

Amy Morrison

Fayyaz S Sutterwala

John Bertin

Beverly H Koller

Zhi Liu

Jenny P-Y Ting

Affiliations

Soon will be listed here.

Abstract

Nucleotide-binding domain leucine-rich repeat (NLR) proteins are regulators of inflammation and immunity. Although first described 8 y ago, a physiologic role for NLRP12 has remained elusive until now. We find that murine Nlrp12, an NLR linked to atopic dermatitis and hereditary periodic fever in humans, is prominently expressed in dendritic cells (DCs) and neutrophils. Nlrp12-deficient mice exhibit attenuated inflammatory responses in two models of contact hypersensitivity that exhibit features of allergic dermatitis. This cannot be attributed to defective Ag processing/presentation, inflammasome activation, or measurable changes in other inflammatory cytokines. Rather, Nlrp12(-/-) DCs display a significantly reduced capacity to migrate to draining lymph nodes. Both DCs and neutrophils fail to respond to chemokines in vitro. These findings indicate that NLRP12 is important in maintaining neutrophils and peripheral DCs in a migration-competent state.

Citing Articles

Clinical heterogeneity of NLRP12-associated autoinflammatory diseases.

Li Y, Deng M, Li Y, Mao X, Yan S, Tang X Genes Dis. 2023; 10(3):1090-1100.

PMID: 37396539 PMC: 10308098. DOI: 10.1016/j.gendis.2022.05.012.

deficiency alters gut microbiota and ameliorates -mediated systemic autoimmunity in male mice.

Abdelhamid L, Mao J, Cabana-Puig X, Zhu J, Swartwout B, Edwards M Front Immunol. 2023; 14:1120958.

PMID: 36969209 PMC: 10036793. DOI: 10.3389/fimmu.2023.1120958.

Pathogenesis of allergic diseases and implications for therapeutic interventions.

Wang J, Zhou Y, Zhang H, Hu L, Liu J, Wang L Signal Transduct Target Ther. 2023; 8(1):138.

PMID: 36964157 PMC: 10039055. DOI: 10.1038/s41392-023-01344-4.

NLRP12-expressing dendritic cells mediate both dissemination of infection and adaptive immune responses in visceral leishmaniasis.

Valadares D, Clay O, Chen Y, Scorza B, Cassel S, Sutterwala F iScience. 2023; 26(3):106163.

PMID: 36879824 PMC: 9985045. DOI: 10.1016/j.isci.2023.106163.

mA demethylase ALKBH5 is required for antibacterial innate defense by intrinsic motivation of neutrophil migration.

Liu Y, Song R, Zhao L, Lu Z, Li Y, Zhan X Signal Transduct Target Ther. 2022; 7(1):194.

PMID: 35764614 PMC: 9240034. DOI: 10.1038/s41392-022-01020-z.

References

Wang L, Manji G, Grenier J, Al-Garawi A, Merriam S, Lora J . PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing. J Biol Chem. 2002; 277(33):29874-80. DOI: 10.1074/jbc.M203915200. View

Wong A, Brickey W, Taxman D, van Deventer H, Reed W, Gao J . CIITA-regulated plexin-A1 affects T-cell-dendritic cell interactions. Nat Immunol. 2003; 4(9):891-8. DOI: 10.1038/ni960. View

Thomas W, Edwards A, Watkins M, Asherson G . Distribution of immunogenic cells after painting with the contact sensitizers fluorescein isothiocyanate and oxazolone. Different sensitizers form immunogenic complexes with different cell populations. Immunology. 1980; 39(1):21-7. PMC: 1457785. View

Kabashima K, Shiraishi N, Sugita K, Mori T, Onoue A, Kobayashi M . CXCL12-CXCR4 engagement is required for migration of cutaneous dendritic cells. Am J Pathol. 2007; 171(4):1249-57. PMC: 1988874. DOI: 10.2353/ajpath.2007.070225. View

Martin S, Jakob T . From innate to adaptive immune responses in contact hypersensitivity. Curr Opin Allergy Clin Immunol. 2008; 8(4):289-93. DOI: 10.1097/ACI.0b013e3283088cf9. View

Sangaletti S, Gioiosa L, Guiducci C, Rotta G, Rescigno M, Stoppacciaro A . Accelerated dendritic-cell migration and T-cell priming in SPARC-deficient mice. J Cell Sci. 2005; 118(Pt 16):3685-94. DOI: 10.1242/jcs.02474. View

Meixenberger K, Pache F, Eitel J, Schmeck B, Hippenstiel S, Slevogt H . Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3. J Immunol. 2009; 184(2):922-30. DOI: 10.4049/jimmunol.0901346. View

Jeru I, Duquesnoy P, Fernandes-Alnemri T, Cochet E, Yu J, Lackmy-Port-Lis M . Mutations in NALP12 cause hereditary periodic fever syndromes. Proc Natl Acad Sci U S A. 2008; 105(5):1614-9. PMC: 2234193. DOI: 10.1073/pnas.0708616105. View

Itano A, McSorley S, Reinhardt R, Ehst B, Ingulli E, Rudensky A . Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 2003; 19(1):47-57. DOI: 10.1016/s1074-7613(03)00175-4. View

10.

Asherson G, Ptak W . Contact and delayed hypersensitivity in the mouse. I. Active sensitization and passive transfer. Immunology. 1968; 15(3):405-16. PMC: 1409462. View

11.

Muruve D, Petrilli V, Zaiss A, White L, Clark S, Ross P . The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature. 2008; 452(7183):103-7. DOI: 10.1038/nature06664. View

12.

Williams K, Lich J, Duncan J, Reed W, Rallabhandi P, Moore C . The CATERPILLER protein monarch-1 is an antagonist of toll-like receptor-, tumor necrosis factor alpha-, and Mycobacterium tuberculosis-induced pro-inflammatory signals. J Biol Chem. 2005; 280(48):39914-24. PMC: 4422647. DOI: 10.1074/jbc.M502820200. View

13.

Boxio R, Bossenmeyer-Pourie C, Steinckwich N, Dournon C, Nusse O . Mouse bone marrow contains large numbers of functionally competent neutrophils. J Leukoc Biol. 2003; 75(4):604-11. DOI: 10.1189/jlb.0703340. View

14.

Johnson C, Kitz D, Little J . A method for the derivation and continuous propagation of cloned murine bone marrow macrophages. J Immunol Methods. 1983; 65(3):319-32. DOI: 10.1016/0022-1759(83)90127-8. View

15.

Lich J, Williams K, Moore C, Arthur J, Davis B, Taxman D . Monarch-1 suppresses non-canonical NF-kappaB activation and p52-dependent chemokine expression in monocytes. J Immunol. 2007; 178(3):1256-60. DOI: 10.4049/jimmunol.178.3.1256. View

16.

Ting J, Duncan J, Lei Y . How the noninflammasome NLRs function in the innate immune system. Science. 2010; 327(5963):286-90. PMC: 3943909. DOI: 10.1126/science.1184004. View

17.

Tertian G, Yung Y, Moore M . Long-term in vitro culture of murine mast cells. I. Description of a growth factor-dependent culture technique. J Immunol. 1981; 127(2):788-94. View

18.

Macaluso F, Nothnagel M, Parwez Q, Petrasch-Parwez E, Bechara F, Epplen J . Polymorphisms in NACHT-LRR (NLR) genes in atopic dermatitis. Exp Dermatol. 2007; 16(8):692-8. DOI: 10.1111/j.1600-0625.2007.00589.x. View

19.

Dieu M, Vanbervliet B, Vicari A, Bridon J, OLDHAM E, Briere F . Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med. 1998; 188(2):373-86. PMC: 2212459. DOI: 10.1084/jem.188.2.373. View

20.

Ruocco M, Maeda S, Park J, Lawrence T, Hsu L, Cao Y . I{kappa}B kinase (IKK){beta}, but not IKK{alpha}, is a critical mediator of osteoclast survival and is required for inflammation-induced bone loss. J Exp Med. 2005; 201(10):1677-87. PMC: 2212920. DOI: 10.1084/jem.20042081. View