Nuclear envelope lamin-A as a coordinator of T cell activation

Nucleus

Volumn 5, Issue 5, 2014, Pages 396-401

  Rocha Perugini, Vera ^a,b   González Granado, José M ^b  

^a Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

Immune synapse; Immune system; Lamin A C; Nuclear envelope proteins; T cell activation

Indexed keywords

CD69 ANTIGEN; F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTERLEUKIN 2 RECEPTOR ALPHA; LAMIN A; NUCLEAR PROTEIN; CHROMATIN;

ACTIN POLYMERIZATION; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL NUCLEUS MEMBRANE; DENDRITIC CELL; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; FIBROBLAST; GENE; GRANULOCYTE; HUMAN; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MICROTUBULE ORGANIZING CENTER; MONOCYTE; NEUTROPHIL; NONHUMAN; PHOSPHORYLATION; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; CELL NUCLEUS; CHROMATIN; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY;

CELL DIFFERENTIATION; CELL NUCLEUS; CHROMATIN; HUMANS; IMMUNE SYSTEM; LAMIN TYPE A; LYMPHOCYTE ACTIVATION; NUCLEAR ENVELOPE; T-LYMPHOCYTES;

EID: 84908219205     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.36361     Document Type: Article

References (42)

1. Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006; 86:967-1008; PMID:16816143; http://dx.doi.org/10.1152/physrev.00047.2005
2. Andrés V, González JM. Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol 2009; 187:945-57; PMID:20038676; http://dx.doi.org/10.1083/jcb.200904124
3. González-Granado JM, Silvestre-Roig C, Rocha- Perugini V, Trigueros-Motos L, Cibrián D, Morlino G, Blanco-Berrocal M, Osorio FG, Freije JM, López-Otín C, et al. Nuclear envelope lamin-A couples actin dynamics with immunological synapse architecture and T cell activation. Sci Signal 2014; 7:ra37; PMID:24757177; http://dx.doi.org/10.1126/ scisignal.2004872
4. Kumari S, Curado S, Mayya V, Dustin ML. T cell antigen receptor activation and actin cytoskeleton remodeling. Biochim Biophys Acta 2014; 1838:546-56; PMID:23680625; http://dx.doi.org/10.1016/j. bbamem.2013.05.004
5. Martín-Cófreces NB, Baixauli F, Sánchez-Madrid F. Immune synapse: conductor of orchestrated organelle movement. Trends Cell Biol 2014; 24:61-72; PMID:24119664; http://dx.doi.org/10.1016/j. tcb.2013.09.005
6. Guilly MN, Bensussan A, Bourge JF, Bornens M, Courvalin JC. A human T lymphoblastic cell line lacks lamins A and C. EMBO J 1987; 6:3795-9; PMID:3501373
7. Röber RA, Sauter H, Weber K, Osborn M. Cells of the cellular immune and hemopoietic system of the mouse lack lamins A/C: distinction versus other somatic cells. J Cell Sci 1990; 95:587-98; PMID:2200797
8. Röber RA, Gieseler RK, Peters JH, Weber K, Osborn M. Induction of nuclear lamins A/C in macrophages in in vitro cultures of rat bone marrow precursor cells and human blood monocytes, and in macrophages elicited in vivo by thioglycollate stimulation. Exp Cell Res 1990; 190:185-94; PMID:2209722; http://dx.doi.org/10.1016/0014-4827(90)90184-C
9. Jansen MP, Machiels BM, Hopman AH, Broers JL, Bot FJ, Arends JW, Ramaekers FC, Schouten HC. Comparison of A and B-type lamin expression in reactive lymph nodes and nodular sclerosing Hodgkin’s disease. Histopathology 1997; 31:304-12; PMID:9363444; http://dx.doi.org/10.1046/j.1365-2559.1997.2820881.x
10. Stadelmann B, Khandjian E, Hirt A, Lüthy A, Weil R, Wagner HP. Repression of nuclear lamin A and C gene expression in human acute lymphoblastic leukemia and non-Hodgkin’s lymphoma cells. Leuk Res 1990; 14:815-21; PMID:2232854; http://dx.doi.org/10.1016/0145-2126(90)90076-L
11. Wheeler LA, Trifonova R, Vrbanac V, Basar E, McKernan S, Xu Z, Seung E, Deruaz M, Dudek T, Einarsson JI, et al. Inhibition of HIV transmission in human cervicovaginal explants and humanized mice using CD4 aptamer-siRNA chimeras. J Clin Invest 2011; 121:2401-12; PMID:21576818; http://dx.doi.org/10.1172/JCI45876
12. Moir RD, Yoon M, Khuon S, Goldman RD. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 2000; 151:1155-68; PMID:11121432; http://dx.doi.org/10.1083/jcb.151.6.1155
13. Bauer B, Baier G. Protein kinase C and AKT/protein kinase B in CD4+ T-lymphocytes: new partners in TCR/CD28 signal integration. Mol Immunol 2002; 38:1087-99; PMID:12044776; http://dx.doi.org/10.1016/S0161-5890(02)00011-1
14. Bertacchini J, Beretti F, Cenni V, Guida M, Gibellini F, Mediani L, Marin O, Maraldi NM, de Pol A, Lattanzi G, et al. The protein kinase Akt/ PKB regulates both prelamin A degradation and Lmna gene expression. FASEB J 2013; 27:2145-55; PMID:23430973; http://dx.doi.org/10.1096/ fj.12-218214
15. Zuo B, Yang J, Wang F, Wang L, Yin Y, Dan J, Liu N, Liu L. Influences of lamin A levels on induction of pluripotent stem cells. Biol Open 2012; 1:1118-27; PMID:23213392; http://dx.doi.org/10.1242/ bio.20121586
16. Hale JS, Frock RL, Mamman SA, Fink PJ, Kennedy BK. Cell-extrinsic defective lymphocyte development in Lmna(-/-) mice. PLoS One 2010; 5:e10127; PMID:20405040; http://dx.doi.org/10.1371/journal.pone.0010127
17. Honda T, Egawa G, Grabbe S, Kabashima K. Update of immune events in the murine contact hypersensitivity model: toward the understanding of allergic contact dermatitis. J Invest Dermatol 2013; 133:303-15; PMID:22931926; http://dx.doi.org/10.1038/ jid.2012.284
18. Cimo AM, Ahmed Z, McIntyre BW, Lewis DE, Ladbury JE. CD25 and CD69 induction by α4β1 outside-in signalling requires TCR early signalling complex proteins. Biochem J 2013; 454:109-21; PMID:23758320; http://dx.doi.org/10.1042/ BJ20130485
19. Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 2010; 26:421-44; PMID:20507227; http://dx.doi.org/10.1146/annurev-cellbio-100109-104037
20. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 2011; 286:26743-53; PMID:21652697; http://dx.doi.org/10.1074/jbc. M111.233700
21. Yi J, Wu X, Chung AH, Chen JK, Kapoor TM, Hammer JA. Centrosome repositioning in T cells is biphasic and driven by microtubule end-on capture-shrinkage. J Cell Biol 2013; 202:779-92; PMID:23979719; http://dx.doi.org/10.1083/ jcb.201301004
22. Lui-Roberts WW, Stinchcombe JC, Ritter AT, Akhmanova A, Karakesisoglou I, Griffiths GM. Cytotoxic T lymphocyte effector function is independent of nucleus-centrosome dissociation. Eur J Immunol 2012; 42:2132-41; PMID:22736282; http://dx.doi.org/10.1002/eji.201242525
23. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 2005; 171:799-810; PMID:16330710; http://dx.doi.org/10.1083/ jcb.200506083
24. Geerts D, Fontao L, Nievers MG, Schaapveld RQ, Purkis PE, Wheeler GN, Lane EB, Leigh IM, Sonnenberg A. Binding of integrin alpha6beta4 to plectin prevents plectin association with F-actin but does not interfere with intermediate filament binding. J Cell Biol 1999; 147:417-34; PMID:10525545; http://dx.doi.org/10.1083/jcb.147.2.417
25. Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10:75-82; PMID:19197334; http://dx.doi.org/10.1038/nrm2594
26. Judokusumo E, Tabdanov E, Kumari S, Dustin ML, Kam LC. Mechanosensing in T lymphocyte activation. Biophys J 2012; 102:L5-7; PMID:22339876; http://dx.doi.org/10.1016/j.bpj.2011.12.011
27. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol 2010; 28:445-89; PMID:20192806; http://dx.doi.org/10.1146/annurev-immunol-030409-101212
28. Broers JL, Machiels BM, Kuijpers HJ, Smedts F, van den Kieboom R, Raymond Y, Ramaekers FC. A- and B-type lamins are differentially expressed in normal human tissues. Histochem Cell Biol 1997; 107:505-17; PMID:9243284; http://dx.doi.org/10.1007/ s004180050138
29. Agrelo R, Setien F, Espada J, Artiga MJ, Rodriguez M, Pérez-Rosado A, Sanchez-Aguilera A, Fraga MF, Piris MA, Esteller M. Inactivation of the lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma. J Clin Oncol 2005; 23:3940-7; PMID:15867203; http://dx.doi.org/10.1200/JCO.2005.11.650
30. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 2013; 152:584-98; PMID:23374351; http://dx.doi.org/10.1016/j. cell.2013.01.009
31. Busslinger M, Tarakhovsky A. Epigenetic control of immunity. Cold Spring Harb Perspect Biol 2014; 6:6; PMID:24890513; http://dx.doi.org/10.1101/cshperspect.a019307
32. Bru T, Clarke C, McGrew MJ, Sang HM, Wilmut I, Blow JJ. Rapid induction of pluripotency genes after exposure of human somatic cells to mouse ES cell extracts. Exp Cell Res 2008; 314:2634-42; PMID:18571647; http://dx.doi.org/10.1016/j. yexcr.2008.05.009
33. Houben F, Willems CH, Declercq IL, Hochstenbach K, Kamps MA, Snoeckx LH, Ramaekers FC, Broers JL. Disturbed nuclear orientation and cellular migration in A-type lamin deficient cells. Biochim Biophys Acta 2009; 1793:312-24; PMID:19013199; http://dx.doi.org/10.1016/j.bbamcr.2008.10.003
34. Prechtel AT, Turza NM, Theodoridis AA, Kummer M, Steinkasserer A. Small interfering RNA (siRNA) delivery into monocyte-derived dendritic cells by electroporation. J Immunol Methods 2006; 311:139-52; PMID:16556448; http://dx.doi.org/10.1016/j. jim.2006.01.021
35. Gieseler RK, Röber RA, Kuhn R, Weber K, Osborn M, Peters JH. Dendritic accessory cells derived from rat bone marrow precursors under chemically defined conditions in vitro belong to the myeloid lineage. Eur J Cell Biol 1991; 54:171-81; PMID:1851701
36. Gieseler RK, Xu H, Schlemminger R, Peters JH. Serum-free differentiation of rat and human dendritic cells, accompanied by acquisition of the nuclear lamins A/C as differentiation markers. Adv Exp Med Biol 1993; 329:287-91; PMID:8379383; http://dx.doi.org/10.1007/978-1-4615-2930-9_48
37. Jin D, Ojcius DM, Sun D, Dong H, Luo Y, Mao Y, Yan J. Leptospira interrogans induces apoptosis in macrophages via caspase-8- and caspase-3-dependent pathways. Infect Immun 2009; 77:799-809; PMID:19029301; http://dx.doi.org/10.1128/ IAI.00914-08
38. Müller PR, Meier R, Hirt A, Bodmer JJ, Janic D, Leibundgut K, Lüthy AR, Wagner HP. Nuclear lamin expression reveals a surprisingly high growth fraction in childhood acute lymphoblastic leukemia cells. Leukemia 1994; 8:940-5; PMID:8207988
39. Collard JF, Senécal JL, Raymond Y. Redistribution of nuclear lamin A is an early event associated with differentiation of human promyelocytic leukemia HL-60 cells. J Cell Sci 1992; 101:657-70; PMID:1522148
40. Olins AL, Zwerger M, Herrmann H, Zentgraf H, Simon AJ, Monestier M, Olins DE. The human granulocyte nucleus: Unusual nuclear envelope and heterochromatin composition. Eur J Cell Biol 2008; 87:279-90; PMID:18396345; http://dx.doi.org/10.1016/j.ejcb.2008.02.007
41. Olins AL, Ernst A, Zwerger M, Herrmann H, Olins DE. An in vitro model for Pelger-Huët anomaly: stable knockdown of lamin B receptor in HL-60 cells. Nucleus 2010; 1:506-12; PMID:21327094
42. Rowat AC, Jaalouk DE, Zwerger M, Ung WL, Eydelnant IA, Olins DE, Olins AL, Herrmann H, Weitz DA, Lammerding J. Nuclear envelope composition determines the ability of neutrophil-type cells to passage through micron-scale constrictions. J Biol Chem 2013; 288:8610-8; PMID:23355469; http://dx.doi.org/10.1074/jbc.M112.441535