Efficient Homing of Antibody-secreting Cells to the Bone Marrow Requires RNA-binding Protein ZFP36L1

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2020 Dec 11

PMID 33306108

Citations 13

Authors

Alexander Saveliev

Sarah E Bell

Martin Turner

Affiliations

Soon will be listed here.

Abstract

Cell migration relies on coordinated activity of chemotactic and guidance receptors. Here, we report a specific role for the RNA-binding protein ZFP36L1 in limiting the abundance of molecules involved in the homing of antibody-secreting cells (ASCs) to the bone marrow (BM). In the absence of ZFP36L1, ASCs build up in the spleen and the liver and show diminished accumulation in the BM. ZFP36L1 facilitates migration by directly regulating G protein-coupled receptor kinase 2 (GRK2) and the integrin chains α4 and β1 in splenic ASCs. Expression of CXCR4 and of the integrins α4 and β1 is differentially regulated on ASCs produced at the early and late stages of the immune response. Consequently, deletion of the Zfp36l1 gene has a stronger effect on BM accumulation of high-affinity ASCs formed late in the response. Thus, ZFP36L1 is an integral part of the regulatory network controlling gene expression during ASC homing.

Citing Articles

Single-B cell analysis correlates high-lactate secretion with stress and increased apoptosis.

Bucheli O, Rodrigues D, Portmann K, Linder A, Thoma M, Halin C Sci Rep. 2024; 14(1):8507.

PMID: 38605071 PMC: 11009249. DOI: 10.1038/s41598-024-58868-0.

Inflammation as a driver of hematological malignancies.

Saluja S, Bansal I, Bhardwaj R, Beg M, Palanichamy J Front Oncol. 2024; 14:1347402.

PMID: 38571491 PMC: 10987768. DOI: 10.3389/fonc.2024.1347402.

Regulation of inflammatory diseases via the control of mRNA decay.

Yoshinaga M, Takeuchi O Inflamm Regen. 2024; 44(1):14.

PMID: 38491500 PMC: 10941436. DOI: 10.1186/s41232-024-00326-5.

Distinct transcriptomes and autocrine cytokines underpin maturation and survival of antibody-secreting cells in systemic lupus erythematosus.

Chen W, Hong S, Jenks S, Anam F, Tipton C, Woodruff M Nat Commun. 2024; 15(1):1899.

PMID: 38429276 PMC: 10907730. DOI: 10.1038/s41467-024-46053-w.

RNA helicase EIF4A1-mediated translation is essential for the GC response.

Screen M, Matheson L, Howden A, Strathdee D, Willis A, Bushell M Life Sci Alliance. 2023; 7(2).

PMID: 38011999 PMC: 10681908. DOI: 10.26508/lsa.202302301.

References

Lu E, Cyster J . G-protein coupled receptors and ligands that organize humoral immune responses. Immunol Rev. 2019; 289(1):158-172. PMC: 6464390. DOI: 10.1111/imr.12743. View

Grabovsky V, Feigelson S, Chen C, Bleijs D, Peled A, Cinamon G . Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med. 2000; 192(4):495-506. PMC: 2193239. DOI: 10.1084/jem.192.4.495. View

Peled A, Kollet O, Ponomaryov T, Petit I, Franitza S, Grabovsky V . The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood. 2000; 95(11):3289-96. View

Bowman E, Kuklin N, Youngman K, Lazarus N, Kunkel E, Pan J . The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med. 2002; 195(2):269-75. PMC: 2193602. DOI: 10.1084/jem.20010670. View

Park E, Rodrigo Mora J, Carman C, Chen J, Sasaki Y, Cheng G . Aberrant activation of integrin alpha4beta7 suppresses lymphocyte migration to the gut. J Clin Invest. 2007; 117(9):2526-38. PMC: 1952632. DOI: 10.1172/JCI31570. View

Kent W, Sugnet C, Furey T, Roskin K, Pringle T, Zahler A . The human genome browser at UCSC. Genome Res. 2002; 12(6):996-1006. PMC: 186604. DOI: 10.1101/gr.229102. View

Suan D, Sundling C, Brink R . Plasma cell and memory B cell differentiation from the germinal center. Curr Opin Immunol. 2017; 45:97-102. DOI: 10.1016/j.coi.2017.03.006. View

Klein U, Casola S, Cattoretti G, Shen Q, Lia M, Mo T . Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol. 2006; 7(7):773-82. DOI: 10.1038/ni1357. View

Imai Y, Park E, Peer D, Peixoto A, Cheng G, von Andrian U . Genetic perturbation of the putative cytoplasmic membrane-proximal salt bridge aberrantly activates alpha(4) integrins. Blood. 2008; 112(13):5007-15. PMC: 2597606. DOI: 10.1182/blood-2008-03-144543. View

10.

Newman R, Ahlfors H, Saveliev A, Galloway A, Hodson D, Williams R . Maintenance of the marginal-zone B cell compartment specifically requires the RNA-binding protein ZFP36L1. Nat Immunol. 2017; 18(6):683-693. PMC: 5438597. DOI: 10.1038/ni.3724. View

11.

Holl E, OConnor B, Holl T, Roney K, Zimmermann A, Jha S . Plexin-D1 is a novel regulator of germinal centers and humoral immune responses. J Immunol. 2011; 186(10):5603-11. PMC: 3771081. DOI: 10.4049/jimmunol.1003464. View

12.

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

13.

Vigorito E, Perks K, Abreu-Goodger C, Bunting S, Xiang Z, Kohlhaas S . microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007; 27(6):847-59. PMC: 4135426. DOI: 10.1016/j.immuni.2007.10.009. View

14.

Manz R, Thiel A, Radbruch A . Lifetime of plasma cells in the bone marrow. Nature. 1997; 388(6638):133-4. DOI: 10.1038/40540. View

15.

Chan J, Hyduk S, Cybulsky M . Chemoattractants induce a rapid and transient upregulation of monocyte alpha4 integrin affinity for vascular cell adhesion molecule 1 which mediates arrest: an early step in the process of emigration. J Exp Med. 2001; 193(10):1149-58. PMC: 2193331. DOI: 10.1084/jem.193.10.1149. View

16.

Corcoran L, Tarlinton D . Regulation of germinal center responses, memory B cells and plasma cell formation-an update. Curr Opin Immunol. 2016; 39:59-67. DOI: 10.1016/j.coi.2015.12.008. View

17.

Trapnell C, Williams B, Pertea G, Mortazavi A, Kwan G, van Baren M . Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28(5):511-5. PMC: 3146043. DOI: 10.1038/nbt.1621. View

18.

Otto F, Mathies M, Westermann J, Owen M, Hamann A, Hogg N . Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J Exp Med. 1999; 189(9):1467-78. PMC: 2193056. DOI: 10.1084/jem.189.9.1467. View

19.

Radbruch A, Muehlinghaus G, Luger E, Inamine A, Smith K, Dorner T . Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol. 2006; 6(10):741-50. DOI: 10.1038/nri1886. View

20.

Minnich M, Tagoh H, Bonelt P, Axelsson E, Fischer M, Cebolla B . Multifunctional role of the transcription factor Blimp-1 in coordinating plasma cell differentiation. Nat Immunol. 2016; 17(3):331-43. PMC: 5790184. DOI: 10.1038/ni.3349. View