FORMINS: THE MULTITASKING ACTIN NUCLEATORS IN DENDRITIC CELL BIOLOGY, A LITERATURE REVIEW
DOI:
https://doi.org/10.18554/acbiobras.v8i2.8483Palavras-chave:
Formins, Actin cytoskeleton , Immunotherapy, dendritic cells, Cell biologyResumo
Dendritic cells (DCs) are at the frontline of the immune defense. They are professional antigen-presenting cells capable of linking adaptive and innate Immune responses by interacting with T cells and by secreting cytokines. By performing such activities, they play an ambiguous role, either engaging the adequate immune response or initiating diseases, and thus, they pose as important therapeutic targets for immunotherapies. Such potential is even more significant if we consider the dynamics of the actin cytoskeleton remodeling to perform such roles. The Formin family of actin nucleators performs one of the three actin-regulatory networks. Formins play essential roles in virtually all eukaryotic cells, including DCs. In this way, we reviewed the most prominent functions of formins in DC biology. The most prominent formins playing roles were members of the Diaphanous and FHOS/FHOD subtypes, acting from pathogen recognition and uptaking, T-cell activation, formation of viral synapses/filopodia, migration stability to adhesion and could be considered as biomarkers of inactive and activated states of DCs. These important roles in DCs leave important open questions yet to be answered.
Referências
1. Jiménez-Cortegana C, Palomares F, Alba G, Santa-María C, de la Cruz-Merino L, Sánchez-Margalet V, López-Enríquez S. Dendritic cells: the yin and yang in disease progression. Front Immunol. 2024; (14): e1321051https://pubmed.ncbi.nlm.nih.gov/38239364/. DOI: https://doi.org/10.3389/fimmu.2023.1321051
2. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J Exp Med. 1974; 139 (2): 380-397. https://pubmed.ncbi.nlm.nih.gov/4589990/. DOI: https://doi.org/10.1084/jem.139.2.380
3. Collin, M, Bigley, V. Human dendritic cell subsets: an update. Immunology. 2018; 154 (1): 3-20.https://pubmed.ncbi.nlm.nih.gov/29313948/. DOI: https://doi.org/10.1111/imm.12888
4. Benze, D, Fekete, T, Pázmándi, K. Type I Interferon Production of Plasmacytoid Dendritic Cells under Control. International Journal of Molecular Sciences, 2021; 22 (8): 4190. https://pubmed.ncbi.nlm.nih.gov/33919546/. DOI: https://doi.org/10.3390/ijms22084190
5. Cruvinel W de M, Mesquita Júnior D, Araújo JAP, Catelan TTT, Souza AWS de, Silva NP da, et al.. Sistema imunitário: Parte I. Fundamentos da imunidade inata com ênfase nos mecanismos moleculares e celulares da resposta inflamatória. Rev Bras Reumatol, 2010; 50 (4): 434–447. https://doi.org/10.1590/S0482-50042010000400008. DOI: https://doi.org/10.1590/S0482-50042010000400008
6. Soto, J. A. The Role of Dendritic Cells During Infections Caused by Highly Prevalent Viruses. Frontiers in Immunology, 2020; (11). https://pubmed.ncbi.nlm.nih.gov/32765522/. DOI: https://doi.org/10.3389/fimmu.2020.01513
7. Moussion C, Delamarre L. Antigen cross-presentation by dendritic cells: A critical axis in cancer immunotherapy. Semin Immunol. 2024; (71). https://pubmed.ncbi.nlm.nih.gov/38035643/. DOI: https://doi.org/10.1016/j.smim.2023.101848
8. Domingues, B. A atuação das células dendríticas na manutenção da imunidade. Revista Multidisciplinar em Saúde, 2023; 4 (2). https://ime.events/conbrai2023/pdf/14357. DOI: https://doi.org/10.51161/iii-conbrai/14357
9. Jamal, ME, Shibli, F. Dendritic cell and co-stimulatory molecule targeted therapy for autoimmune diseases: a review of the newly implemented strategies. Exploratory Immunology, 2024; (4): 189–210. https://doi.org/10.37349/ei.2024.00136. DOI: https://doi.org/10.37349/ei.2024.00136
10. Conti, BJ, Santiago, KB, Sforcin, JM. Células dendríticas: mini-revisão. Biosaúde, 2014; 16 (1): 28-34. https://www.uel.br/revistas/uel/index.php/biosaude/article/view/24351/0.
11. Brooks JW, Tillu V, Eckert J, Verma S, Collins BM, Parton RG, Yap AS. Caveola mechanotransduction reinforces the cortical cytoskeleton to promote epithelial resilience. Mol Biol Cell. 2023; 34 (12) https://pubmed.ncbi.nlm.nih.gov/37672337/. DOI: https://doi.org/10.1091/mbc.E23-05-0163
12. Wang H, Hu J, Yi K, Ma Z, Song X, Lee Y, Kalab P, Bershadsky AD, Miao Y, Li R. Dual control of formin-nucleated actin assembly by the chromatin and ER in mouse oocytes. Curr Biol. 2022; 32 (18): 4013-4024. https://pubmed.ncbi.nlm.nih.gov/35981539/. DOI: https://doi.org/10.1016/j.cub.2022.07.058
13. Parisis N, Krasinska L, Harker B, Urbach S, Rossignol M, Camasses A, Dewar J, Morin N, Fisher D. Initiation of DNA replication requires actin dynamics and formin activity. EMBO J. 2017; 36 (21): 3212-3231. https://pubmed.ncbi.nlm.nih.gov/28982779/. DOI: https://doi.org/10.15252/embj.201796585
14. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB. Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol. 2003; 19: 541-564. https://pubmed.ncbi.nlm.nih.gov/14570581/. DOI: https://doi.org/10.1146/annurev.cellbio.19.050103.103356
15. Pruyne D. Revisiting the Phylogeny of the Animal Formins: Two New Subtypes, Relationships with Multiple Wing Hairs Proteins, and a Lost Human Formin. PLoS One. 2016; 11 (10): e0164067. https://pubmed.ncbi.nlm.nih.gov/27695129/. DOI: https://doi.org/10.1371/journal.pone.0164067
16. Valencia DA, Quinlan ME. Formins. Curr Biol. 2021; 31 (10): R517-R522. https://pubmed.ncbi.nlm.nih.gov/34033783/. DOI: https://doi.org/10.1016/j.cub.2021.02.047
17. Gutiérrez-Martínez E, Benet Garrabé S, Mateos N, Erkizia I, Nieto-Garai JA, Lorizate M, Borgman KJE, Manzo C, Campelo F, Izquierdo-Useros N, Martinez-Picado J, Garcia-Parajo MF. Actin-regulated Siglec-1 nanoclustering influences HIV-1 capture and virus-containing compartment formation in dendritic cells. Elife. 2023; 20 (12): e78836. https://pubmed.ncbi.nlm.nih.gov/36940134/. DOI: https://doi.org/10.7554/eLife.78836
18. Vargas P, Barbier L, Sáez PJ, Piel M.. Mechanisms for fast cell migration in complex environments. Current Opinion in Cell Biology 2017; 48:72–78. https://pubmed.ncbi.nlm.nih.gov/28641118/. DOI: https://doi.org/10.1016/j.ceb.2017.04.007
19. Descamps D, Evnouchidou I, Caillens V, Drajac C, Riffault S, van Endert P, Saveanu L. The Role of Insulin Regulated Aminopeptidase in Endocytic Trafficking and Receptor Signaling in Immune Cells. Front Mol Biosci. 2020; (7): e583556. https://pubmed.ncbi.nlm.nih.gov/33195428/. DOI: https://doi.org/10.3389/fmolb.2020.583556
20. Tojo H, Kaieda I, Hattori H, Katayama N, Yoshimura K, Kakimoto S, et al. The Formin family protein, formin homolog overexpressed in spleen, interacts with the insulin-responsive aminopeptidase and profilin IIa. Mol. Endocrinol. 2003; 17: 1216–1229. https://academic.oup.com/mend/article/17/7/1216/275643. DOI: https://doi.org/10.1210/me.2003-0056
21. Babdor J, Descamps D, Adiko, AC, Tohmé M, Maschalidi S, Evnouchidou I, et al. IRAP+ endosomes restrict TLR9 activation and signaling. Nat. Immunol. 2017; 18: 509–518.https://pubmed.ncbi.nlm.nih.gov/28319098/. DOI: https://doi.org/10.1038/ni.3711
22. Fernandez-Borja M, Janssen L, Verwoerd D, Hordijk P, Neefjes J. . RhoB regulates endosome transport by promoting actin assembly on endosomal membranes through Dia1. J. Cell. Sci. 2005; 118: 2661–2670. https://pubmed.ncbi.nlm.nih.gov/15944396/. DOI: https://doi.org/10.1242/jcs.02384
23. Weimershaus M, Mauvais FX, Saveanu L, Adiko C, Babdor J, Abramova A, et al. Innate immune signals induce anterograde endosome transport promoting MHC class I cross-presentation. Cell. Rep. 2018; 24: 3568–3581. https://pubmed.ncbi.nlm.nih.gov/30257216/. DOI: https://doi.org/10.1016/j.celrep.2018.08.041
24. Rezaei Z, Tahmasebi A, Pourabbas B. Using meta-analysis and machine learning to investigate the transcriptional response of immune cells to Leishmania infection. PLoS Negl Trop Dis. 2024; 18 (1): e0011892. https://pubmed.ncbi.nlm.nih.gov/38190401/. DOI: https://doi.org/10.1371/journal.pntd.0011892
25. Kushwaha R, Seth A, Jijumon A, Reshmi P, Dileep D, Datta R, et al.. Leishmania major formins are cytosolic actin bundlers play an important role in cell physiology. bioRxiv. 2021; 4 (12): .https://www.biorxiv.org/lookup/doi/10.1101/2021.04.12.439584.
26. Shrivastava A, Prasad A, Kuzontkoski PM, Yu J, Groopman JE. Slit2N Inhibits Transmission of HIV-1 from Dendritic Cells to T-cells by Modulating Novel Cytoskeletal Elements. Sci Rep. 2015; 5: https://pubmed.ncbi.nlm.nih.gov/26582347/. DOI: https://doi.org/10.1038/srep16833
27. Aggarwal A, Iemma TL, Shih, I, Newsome, TP, McAllery, S, Cunningham, AL, Turville, SG. Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog 2012; 8: e1002762, https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1002762.
28. Higashi T, Ikeda T, Murakami T, Shirakawa R, Kawato M, Okawa K, Furuse M, Kimura T, Kita T, Horiuchi H. Flightless-I (Fli-I) regulates the actin assembly activity of diaphanous-related formins (DRFs) Daam1 and mDia1 in cooperation with active Rho GTPase. J Biol Chem. 2010; 285 (21):16231-16238, https://pubmed.ncbi.nlm.nih.gov/20223827/. DOI: https://doi.org/10.1074/jbc.M109.079236
29. Ostrowski PP, Grinstein S, Freeman SA. Diffusion Barriers, Mechanical Forces, and the Biophysics of Phagocytosis. Dev Cell. 2016; 38 (2): 135-146. https://pubmed.ncbi.nlm.nih.gov/27459066/. DOI: https://doi.org/10.1016/j.devcel.2016.06.023
30. Lomakin AJ, Lee KC, Han SJ, Bui DA, Davidson M, Mogilner A, Danuser G. Competition for actin between two distinct F-actin networks defines a bistable switch for cell polarization. Nat Cell Biol. 2015; 17 (11): 1435-1445. https://pubmed.ncbi.nlm.nih.gov/26414403/. DOI: https://doi.org/10.1038/ncb3246
31. Vargas P, Maiuri P, Bretou M, Sáez PJ, Pierobon P, Maurin M, Chabaud M, Lankar D, Obino D, Terriac E, Raab M, Thiam HR, Brocker T, Kitchen-Goosen SM, Alberts AS, Sunareni P, Xia S, Li R, Voituriez R, Piel M, Lennon-Duménil AM. Innate control of actin nucleation determines two distinct migration behaviors in dendritic cells. Nat Cell Biol. 2016; 18 (1): 43-53. https://pubmed.ncbi.nlm.nih.gov/26641718/. DOI: https://doi.org/10.1038/ncb3284
32. Tanizaki H, Egawa G, Inaba K, Honda T, Nakajima S, Moniaga CS, Otsuka A, Ishizaki T, Tomura M, Watanabe T, Miyachi Y, Narumiya S, Okada T, Kabashima K. Rho-mDia1 pathway is required for adhesion, migration, and T-cell stimulation in dendritic cells. Blood. 2010; 116 (26): 5875-5884. https://pubmed.ncbi.nlm.nih.gov/20881208/. DOI: https://doi.org/10.1182/blood-2010-01-264150
33. Aggarwal A, Iemma TL, Shih I, Newsome TP, McAllery S, Cunningham AL, Turville SG. Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog. 2012; 8 (6): e1002762. https://pubmed.ncbi.nlm.nih.gov/22685410/. DOI: https://doi.org/10.1371/journal.ppat.1002762
34. Visweswaran SP, Nayab H, Hoffmann L, Gil M, Liu F, Kühne R, Maritzen T. Ena/VASP proteins at the crossroads of actin nucleation pathways in dendritic cell migration. Front Cell Dev Biol. 2022; 10: e1008898. https://pubmed.ncbi.nlm.nih.gov/36274843/. DOI: https://doi.org/10.3389/fcell.2022.1008898
35. Bruhmann, S, Ushakov, D S, Winterhoff, M, Dickinson, RB, Curth, U, Faix, J. Distinct VASP tetramers synergize in the processive elongation of individual actin filaments from clustered arrays. Proc. Natl. Acad. Sci. U. S. A. 2017; 114 (29): E5815–E5824. https://pubmed.ncbi.nlm.nih.gov/28667124/. DOI: https://doi.org/10.1073/pnas.1703145114
36. Chen XJ, Squarr AJ, Stephan R, Chen B, Higgins TE, Barry, D. J., et al. Ena/VASP proteins cooperate with the WAVE complex to regulate the actin cytoskeleton. Dev. Cell. 2014; 30 (5): 569–584. https://pubmed.ncbi.nlm.nih.gov/25203209/. DOI: https://doi.org/10.1016/j.devcel.2014.08.001
37. Naj X, Hoffmann AK, Himmel M, Linder S. The formins FMNL1 and mDia1 regulate coiling phagocytosis of Borrelia burgdorferi by primary human macrophages. Infect Immun. 2013; 81 (5): 1683-1695. https://pubmed.ncbi.nlm.nih.gov/23460512/. DOI: https://doi.org/10.1128/IAI.01411-12
38. Miller MR, Blystone SD. Human Macrophages Utilize the Podosome Formin FMNL1 for Adhesion and Migration. Cellbio (Irvine, Calif). 2015; 4 (1): 1-11. https://pubmed.ncbi.nlm.nih.gov/26942206/. DOI: https://doi.org/10.4236/cellbio.2015.41001
39. Williams SK, Weiner ZP, Gilmore RD. Human neuroglial cells internalize Borrelia burgdorferi by coiling phagocytosis mediated by Daam1. PLoS One. 2018; 13 (5): e0197413. https://pubmed.ncbi.nlm.nih.gov/29746581/. DOI: https://doi.org/10.1371/journal.pone.0197413
Downloads
Publicado
Edição
Seção
Licença
O(s) autor(es) mantém(êm) os direitos sobre o material publicado. Todavia, a publicação implica automaticamente, a cessão dos direitos autorais, sem pagamento por parte do periódico. O (s) autor (es) transfere (m) seus direitos patrimoniais (o direito de publicar, reproduzir, distribuir) para a revista. O (s) autor (es) não recebe (m) remuneração financeira da Revista Acta Biologica Brasiliensia para publicar, sendo a contrapartida a divulgação de seu trabalho.
