Regulation of B1 Cell Migration by Signals Through Toll-like Receptors

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2006 Oct 25

PMID 17060475

Citations 157

Authors

Seon-Ah Ha

Masayuki Tsuji

Keiichiro Suzuki

Bob Meek

Nobutaka Yasuda

Tsuneyasu Kaisho

Sidonia Fagarasan

Affiliations

Soon will be listed here.

Abstract

Peritoneal B1 cells are known to generate large amounts of antibodies outside their residential site. These antibodies play an important role in the early defense against bacteria and viruses, before the establishment of adaptive immune responses. Although many stimuli, including antigen, lipopolysaccharide, or cytokines, have been shown to activate B1 cells and induce their differentiation into plasma cells, the molecular signals required for their egress from the peritoneal cavity are not understood. We demonstrate here that direct signals through Toll-like receptors (TLRs) induce specific, rapid, and transient down-regulation of integrins and CD9 on B1 cells, which is required for detachment from local matrix and a high velocity movement of cells in response to chemokines. Thus, we revealed an unexpected role for TLRs in governing the interplay between integrins, tetraspanins, and chemokine receptors required for B1 cell egress and, as such, in facilitating appropriate transition from innate to adaptive immune responses.

Citing Articles

Neutrophil extracellular traps promote pre-metastatic niche formation in the omentum by expanding innate-like B cells that express IL-10.

Lee W, Ko S, Akasaka H, Weigert M, Lengyel E, Naora H Cancer Cell. 2025; 43(1):69-85.e11.

PMID: 39753138 PMC: 11732717. DOI: 10.1016/j.ccell.2024.12.004.

Regional immune mechanisms enhance efficacy of an autologous cellular cancer vaccine with intraperitoneal administration.

Marwedel B, Medina L, De May H, Adogla J, Kennedy E, Flores E Oncoimmunology. 2024; 13(1):2421029.

PMID: 39625271 PMC: 11540083. DOI: 10.1080/2162402X.2024.2421029.

Effects of dietary Lactobacillus postbiotics and bacitracin on the modulation of mucosa-associated microbiota and pattern recognition receptors affecting immunocompetence of jejunal mucosa in pigs challenged with enterotoxigenic F18 Escherichia....

Duarte M, Deng Z, Kim S J Anim Sci Biotechnol. 2024; 15(1):139.

PMID: 39390608 PMC: 11468193. DOI: 10.1186/s40104-024-01098-1.

The immunology of B-1 cells: from development to aging.

Mattos M, Vandendriessche S, Waisman A, Marques P Immun Ageing. 2024; 21(1):54.

PMID: 39095816 PMC: 11295433. DOI: 10.1186/s12979-024-00455-y.

Tipping the Scale: Atheroprotective IgM-Producing B Cells in Atherosclerosis.

Ransegnola B, Pattarabanjird T, McNamara C Arterioscler Thromb Vasc Biol. 2024; 44(9):1906-1915.

PMID: 39022832 PMC: 11338718. DOI: 10.1161/ATVBAHA.124.319847.

References

Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F . Requirement of CD9 on the egg plasma membrane for fertilization. Science. 2000; 287(5451):321-4. DOI: 10.1126/science.287.5451.321. View

Haas K, Poe J, Steeber D, Tedder T . B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity. 2005; 23(1):7-18. DOI: 10.1016/j.immuni.2005.04.011. View

Fagarasan S, Shinkura R, Kamata T, Nogaki F, Ikuta K, Tashiro K . Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med. 2000; 191(9):1477-86. PMC: 2213441. DOI: 10.1084/jem.191.9.1477. View

Macpherson A, Gatto D, Sainsbury E, Harriman G, Hengartner H, Zinkernagel R . A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 2000; 288(5474):2222-6. DOI: 10.1126/science.288.5474.2222. View

Potocnik A, Brakebusch C, Fassler R . Fetal and adult hematopoietic stem cells require beta1 integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity. 2000; 12(6):653-63. DOI: 10.1016/s1074-7613(00)80216-2. View

Baumgarth N, Herman O, Jager G, Brown L, Herzenberg L, Chen J . B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J Exp Med. 2000; 192(2):271-80. PMC: 2193249. DOI: 10.1084/jem.192.2.271. View

Arroyo A, Taverna D, Whittaker C, Strauch U, Bader B, Rayburn H . In vivo roles of integrins during leukocyte development and traffic: insights from the analysis of mice chimeric for alpha 5, alpha v, and alpha 4 integrins. J Immunol. 2000; 165(8):4667-75. DOI: 10.4049/jimmunol.165.8.4667. View

Miyake M, Inufusa H, Adachi M, Ishida H, Hashida H, Tokuhara T . Suppression of pulmonary metastasis using adenovirally motility related protein-1 (MRP-1/CD9) gene delivery. Oncogene. 2000; 19(46):5221-6. DOI: 10.1038/sj.onc.1203919. View

Martin F, Kearney J . B1 cells: similarities and differences with other B cell subsets. Curr Opin Immunol. 2001; 13(2):195-201. DOI: 10.1016/s0952-7915(00)00204-1. View

10.

Schnare M, BARTON G, Holt A, Takeda K, Akira S, Medzhitov R . Toll-like receptors control activation of adaptive immune responses. Nat Immunol. 2001; 2(10):947-50. DOI: 10.1038/ni712. View

11.

Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T . In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature. 2001; 413(6856):639-43. DOI: 10.1038/35098100. View

12.

Berditchevski F . Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci. 2001; 114(Pt 23):4143-51. DOI: 10.1242/jcs.114.23.4143. View

13.

Ansel K, Harris R, Cyster J . CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity. 2002; 16(1):67-76. DOI: 10.1016/s1074-7613(01)00257-6. View

14.

Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T . Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity. 1999; 11(4):443-51. DOI: 10.1016/s1074-7613(00)80119-3. View

15.

Ochsenbein A, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H . Control of early viral and bacterial distribution and disease by natural antibodies. Science. 1999; 286(5447):2156-9. DOI: 10.1126/science.286.5447.2156. View

16.

Hardy R, Hayakawa K . B cell development pathways. Annu Rev Immunol. 2001; 19:595-621. DOI: 10.1146/annurev.immunol.19.1.595. View

17.

Kaisho T, Takeuchi O, Kawai T, Hoshino K, Akira S . Endotoxin-induced maturation of MyD88-deficient dendritic cells. J Immunol. 2001; 166(9):5688-94. DOI: 10.4049/jimmunol.166.9.5688. View

18.

Martin F, Oliver A, Kearney J . Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity. 2001; 14(5):617-29. DOI: 10.1016/s1074-7613(01)00129-7. View

19.

Bendelac A, Bonneville M, Kearney J . Autoreactivity by design: innate B and T lymphocytes. Nat Rev Immunol. 2002; 1(3):177-86. DOI: 10.1038/35105052. View

20.

Won W, Kearney J . CD9 is a unique marker for marginal zone B cells, B1 cells, and plasma cells in mice. J Immunol. 2002; 168(11):5605-11. DOI: 10.4049/jimmunol.168.11.5605. View